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VOLUME NINETY

ADVANCES IN
PARASITOLOGY
Fossil Parasites
SERIES EDITOR
D. ROLLINSON J. R. STOTHARD
Life Sciences Department Department of Parasitology
The Natural History Museum, Liverpool School of Tropical
London, UK Medicine Liverpool, UK
d.rollinson@nhm.ac.uk russell.stothard@lstmed.ac.uk

EDITORIAL BOARD
T. J. C. ANDERSON R. C. OLIVEIRA
Department of Genetics, Texas Centro de Pesquisas Rene Rachou/
Biomedical Research Institute, CPqRR - A FIOCRUZ em Minas
San Antonio, TX, USA Gerais, Rene Rachou Research
Center/CPqRR - The Oswaldo Cruz
M. G. BASÁÑEZ Foundation in the State of Minas
Professor of Neglected Tropical Gerais-Brazil, Brazil
Diseases, Department of Infectious
Disease Epidemiology, Faculty of R. E. SINDEN
Medicine (St Mary’s Campus), Immunology and Infection
Imperial College London, Section, Department of Biological
London, UK Sciences, Sir Alexander Fleming
Building, Imperial College of
Science, Technology and
S. BROOKER Medicine, London, UK
Wellcome Trust Research Fellow
and Professor, London School of D. L. SMITH
Hygiene and Tropical Medicine, Johns Hopkins Malaria Research
Faculty of Infectious and Tropical, Institute & Department of
Diseases, London, UK Epidemiology, Johns Hopkins
Bloomberg School of Public Health,
R. B. GASSER Baltimore, MD, USA
Department of Veterinary Science,
The University of Melbourne, R. C. A. THOMPSON
Parkville, Victoria, Australia Head, WHO Collaborating Centre
for the Molecular Epidemiology
of Parasitic Infections, Principal
N. HALL Investigator, Environmental
School of Biological Sciences, Biotechnology CRC (EBCRC), School
Biosciences Building, University of of Veterinary and Biomedical
Liverpool, Liverpool, UK Sciences, Murdoch University,
Murdoch, WA, Australia
J. KEISER
Head, Helminth Drug X.-N. ZHOU
Development Unit, Department Professor, Director, National
of Medical Parasitology and Institute of Parasitic Diseases,
Infection Biology, Swiss Tropical Chinese Center for Disease Control
and Public Health Institute, Basel, and Prevention, Shanghai, People’s
Switzerland Republic of China
VOLUME NINETY

ADVANCES IN
PARASITOLOGY
Fossil Parasites
Edited by

KENNETH DE BAETS
GeoZentrum Nordbayern,
Friedrich-Alexander-Universit€
at
Erlangen-N€ urnberg, Erlangen, Germany

D. TIMOTHY J. LITTLEWOOD
Department of Life Sciences, Natural History Museum,
London, UK

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CONTRIBUTORS

Adauto Ara ujo


Fundaç~ao Oswaldo Cruz, Laborat
orio de Paleoparasitologia, Rio de Janeiro, RJ, Brazil
Geoff A. Boxshall
Department of Life Sciences, Natural History Museum, London, UK
Kenneth De Baets
Fachgruppe Pal€aoUmwelt, GeoZentrum Nordbayern, Friedrich-Alexander-Universit€at
Erlangen-N€
urnberg, Erlangen, Germany
Paula Dentzien-Dias
N
ucleo de Oceanografia Geologica, Instituto de Oceanografia, Universidade Federal do Rio
Grande, Rio Grande, Brazil
Philip C.J. Donoghue
School of Earth Sciences, University of Bristol, Life Science Building, Bristol, UK
Stephen K. Donovan
Department of Geology, Naturalis Biodiversity Center, Leiden, The Netherlands
Luiz Fernando Ferreira
Fundaç~ao Oswaldo Cruz, Laborat
orio de Paleoparasitologia, Rio de Janeiro, RJ, Brazil
Joachim T. Haug
Department of Biology II, Functional Morphology Group, University of Munich (LMU),
Planegg-Martinsried, Germany
John Warren Huntley
Department of Geological Sciences, University of Missouri, Columbia, MO, USA
Adiël A. Klompmaker
Florida Museum of Natural History, University of Florida, Gainesville, FL, USA
D. Timothy J. Littlewood
Department of Life Sciences, Natural History Museum, London, UK
Piers D. Mitchell
Department of Archaeology and Anthropology, University of Cambridge, Cambridge,
United Kingdom
Christina Nagler
Department of Biology II, Functional Morphology Group, University of Munich (LMU),
Planegg-Martinsried, Germany
George O. Poinar, Jr.
Department of Integrative Biology, Oregon State University, Corvallis, OR 97331, USA
Karl Reinhard
School of Natural Resources, University of Nebraska, Lincoln, NE, USA

ix j
x Contributors

Paul D. Taylor
Department of Earth Sciences, Natural History Museum, London, UK
Ieva Upeniece
Department of Geology, University of Latvia, Riga, Latvia
Olivier Verneau
CNRS, Centre de Formation et de Recherche sur les Environnements Méditerranéens,
University of Perpignan Via Domitia, Perpignan, France; Unit for Environmental Sciences
and Management, North-West University, Potchefstroom, South Africa
PREFACE

Parasites are ubiquitous, numerous and diverse, and it is widely considered


that this must have been the situation for much of the history of life.
However, understanding the evolutionary history of parasites and their
impact on hosts and ecology through time has relied almost exclusively on
inferences extrapolated from the diversity and nature of parasite species
living today. To a large extent the fossil record of parasites has been over-
looked. Consequently, the role and potential of fossil parasites in the field of
evolutionary biology, and indeed parasitology more generally, has been
difficult to assess. Almost 25 years ago Simon Conway Morris published a
review of fossil parasites in the Journal of Parasitology (82:489–509), consid-
ering their importance in an evolutionary context and providing a com-
prehensive singular resource amenable to parasitologists and palaeontologists
alike. Subsequent reviews on this topic have focused on particular groups of
marine or terrestrial parasites, whilst consideration of fossil parasites more
generally has been invoked through palaeoecological interpretations of
behaviour, coevolution and the nature of trace fossils. This new knowledge
on fossil parasites is mostly scattered in the literature, making it harder to get
an overview of their usefulness and potential for illuminating or framing
their evolutionary history. Newly discovered fossils, the development of
sensitive techniques that enable fossils to be better visualized, manipulated
digitally, and analyzed chemically, and the need to integrate palae-
ontological data into time-calibrated phylogenies, have provided a wealth of
new opportunities to consider fossil parasites again. The combination of
frustrations balanced by advances and opportunities provided the impetus for
this volume. Fortuitously there are also currently many active researchers
considering fossil parasites and their role in better understanding the nature
of parasitism in evolution, disease and ecology. The sheer diversity of
approaches and innovations further merits a renewed perspective, not least
to demonstrate how much more integrative the study of parasitology has
become.
This volume aims to demonstrate that direct and indirect evidence from
the fossil record can be crucial in a variety of ways, providing empirical,
complementary and supplementary evidence in testing and developing
hypotheses on the nature of parasite diversity, phylogeny and host associa-
tions through space and time. In the first chapter, Kenneth De Baets and
Tim Littlewood review recent discoveries of fossil parasites and vectors and

xi j
xii Preface

consider them in their phylogenetic context, highlighting emerging tech-


niques and pathways for further progress. The fossil record of soft-bodied
parasites is understandably poor, but George Poinar’s contribution and that
of De Baets and co-workers, each explore how the fossil record of parasitic
helminths might be richer, or at least ‘less poor’, than that of their free-living
relatives. Poinar concisely discusses the evolutionary history of nematode
parasites of invertebrates, vertebrates and plants based on fossil remains in
amber, rock and coprolites ranging from the Palaeozoic to the Holocene
drawing from his long personal research on this topic. De Baets and co-
workers review the fossil record of parasitic flatworms for the first time and
illustrate how fossil and geological evidence may be used to calibrate
molecular clocks. Christina Nagler and Joachim Haug comprehensively
review the fossil record of insects, which includes some of the most
important terrestrial parasites, parasitoids and vectors today.
In reviewing the fossil record of crustacean parasites and hosts, Adiël
Klompmaker and Geoff Boxshall demonstrate that characteristic pathologies
and traces in hosts with fossilizable skeletons can provide a less patchy record
of parasitism compared with the body fossil record, thus demonstrating the
need to better understand and detect such traces. Pathologies in several other
groups of hosts with hard parts can be linked with parasitism, particularly in
bivalve molluscs, echinoderms and colonial organisms. John Huntley and
Kenneth De Baets discuss the indirect record of trematode flatworms in
bivalve shells. Stephen Donovan adds a new take on evidence for ecto-
parasitism on echinoderms, a group with a remarkable fossil record and one
that has captured numerous lesions, traces, burrows and attachments since
their appearance in deep time. Paul Taylor reviews for the first time the fossil
evidence for parasitism in fossil colonial organisms including sponges,
bryozoans, corals and graptolites and reveals a number of questions and
conundrums. In spite of this wealth of damage and evidence of association,
the identity of the perpetrators and the true nature of their associations
remain open to interpretation and speculation. For these predominantly
marine taxa, it seems that modern studies of parasite ecology in marine
environments may yet reveal more about ancient associations, and the
nature of traces caused by species (likely extinct) in other organisms also
extinct. The systematic review of fossil evidence at least provides focus for a
renewed search amongst modern marine assemblages.
Last but not least, the field of palaeoparasitology is drawn considerably
from techniques and methods introduced and still being developed rapidly
in the study of human parasites at archaeological sites. Drawing from a
Preface xiii

lifetime of experience Adauto Ara ujo and co-workers illustrate the impor-
tance of ancient parasitic remains and review the methods to study human
parasites. Considering the links between human health, medical practice and
parasites, Piers Mitchell provides the final chapter with a focus specifically on
Medieval European parasite remains. Fascinating personal natural histories of
the rich, famous and simple peasantry provide insights into archaeology as
well as anthropology. The constraints of parasitic infections on lifestyle,
sanitation and medical treatment of humans in early Europe resonates with
much of modern parasitology today and brings into focus our own ongoing
struggles with infection and parasite-mediated disease worldwide.
We take this opportunity to thank all of the authors for their con-
tributions and to the editorial team for their support in making this volume
possible.

Kenneth De Baets and D. Timothy J. Littlewood


October 2015
CHAPTER ONE

The Importance of Fossils in


Understanding the Evolution of
Parasites and Their Vectors
Kenneth De Baets*, 1, D. Timothy J. Littlewoodx, 1
*Fachgruppe Pal€aoUmwelt, GeoZentrum Nordbayern, Friedrich-Alexander-Universit€at
Erlangen-N€urnberg, Erlangen, Germany
x
Department of Life Sciences, Natural History Museum, London, UK
1
Corresponding authors: E-mail: kenneth.debaets@gmail.com; t.littlewood@nhm.ac.uk

Contents
1. Introduction 2
2. Techniques for Ancient Parasite Discovery 4
2.1 Thin sections and computed tomography 5
2.2 Ancient biomolecules 6
2.2.1 Ancient DNA 6
2.2.2 Palaeoproteomics 7
3. The Parasite Fossil Record 8
3.1 Body fossils 14
3.2 Trace fossils and pathologies 18
3.3 Coprolites 22
4. Molecular Perspectives on Parasite Phylogeny and Evolution 26
4.1 Molecular clocks 29
4.2 HGT and ‘parasitic DNA’ 34
5. Future Perspectives 35
Acknowledgements 36
References 36

Abstract
Knowledge concerning the diversity of parasitism and its reach across our current
understanding of the tree of life has benefitted considerably from novel molecular
phylogenetic methods. However, the timing of events and the resolution of the nature
of the intimate relationships between parasites and their hosts in deep time remain
problematic. Despite its vagaries, the fossil record provides the only direct evidence
of parasites and parasitism in the fossil record of extant and extinct lineages. Here,
we demonstrate the potential of the fossil record and other lines of geological evi-
dence to calibrate the origin and evolution of parasitism by combining different kinds
of dating evidence with novel molecular clock methodologies. Other novel methods
promise to provide additional evidence for the presence or the life habit of pathogens
Advances in Parasitology, Volume 90
© 2015 Elsevier Ltd.
j
ISSN 0065-308X
http://dx.doi.org/10.1016/bs.apar.2015.07.001 All rights reserved. 1
2 Kenneth De Baets and D. Timothy J. Littlewood

and their vectors, including the discovery and analysis of ancient DNA and other bio-
molecules, as well as computed tomographic methods.

1. INTRODUCTION
Parasitism is one of the most successful modes of life, as evidenced by
its convergent appearance in numerous lineages and its sheer absolute and
relative abundance among extant biodiversity (Poulin and Morand, 2000).
Antagonistic interactions, in the form of arms races between parasites and
their hosts, have been considered important drivers of evolution (Zaman
et al., 2014) and might also have contributed to the origin of sexual repro-
duction (Mostowy and Engelst€adter, 2012). Because parasitism also has an
obvious societal importance with many parasitic taxa being of significant
biomedical, veterinary or economic importance (Bush et al., 2001), it is
here that most of the research effort is focused. This focus is narrow and fails
to provide the wider evolutionary picture or an appreciation of the influence
of parasitism on, and as part of, biodiversity. Indeed, despite their importance
and ubiquity, the evolutionary history of parasites is still poorly known, a
phenomenon not helped by their inadequate, or rather inadequately
explored, fossil record (Littlewood and Donovan, 2003).
Establishing time-calibrated evolutionary frameworks to test the origins
and radiations of parasites in parallel with studies on environmental param-
eters, or the degree of coevolution between parasites and hosts, is a difficult
but as yet a largely unexplored means by which ancient associations may be
revealed. Parasitologists have often resorted to more circular lines of evi-
dence, such as extrapolating from current host associations or distributions
to put time constraints on the origins and evolution of parasites. For instance,
where extant hosteparasite associations appear to be combinations of early
divergent hosts and early divergent parasites, it is tempting and compelling to
assume a long and ancient association; for example, early divergent gyroco-
tylidean cestodes found only parasitizing early divergent ‘primitive’ holoce-
phalan fishes (Xylander, 2001). In these cases, when the timing of a host’s
divergence can be estimated from molecular or preferably fossil evidence,
a calibration point for the parasite’s association also appears tractable, at least
as a working hypothesis. Assumptions of cophylogeny are common but
bring their own suites of problems, not in the least because of the traps set
by multiple assumptions (Page, 2003). To reveal coevolutionary patterns,
phylogenies of hosts and parasites need to be untangled to better understand
The Importance of Fossils in the Evolution of Parasites 3

historical relationships, but the task is complex. Accurate estimates of histor-


ical events such as co-divergence, duplication or loss of an association require
complex mathematics and computationally demanding algorithms, and any
estimate is contingent upon adequate sampling (Charleston and Perkins,
2006). Usually such sampling relies on phylogenies determined from extant
organisms and pays little heed to loss of lineages through extinction. Whilst
these studies can be profitable, direct evidence from the fossil record remains
the most compelling evidence for past historical and deep evolutionary
associations, as well as extinctions. Palaeontological data could also have a
bearing on testing of how parasiteehost associations respond to environ-
mental changes across longer time-scales and to what extent parasites could
be prone to (co)extinction (Dunn et al., 2009).
The past decades have seen a wealth of new discoveries, ranging from
exceptionally preserved parasites and eggs assignable to modern (even family
level) lineages (Cressey and Boxshall, 1989; Da Silva et al., 2014; Hugot
et al., 2014), to characteristic traces of preserved biomolecules in host
remains (Dittmar, 2009; Greenwalt et al., 2013; Wood et al., 2013b). Of
particular note have been advances in X-ray, ion, electron and laser-beam
techniques, serial grinding/imaging techniques and magnetic resonance
tomography characterizing fine structures, textures and underlying chemis-
tries (Mietchen et al., 2008; Sutton, 2008; Schiffbauer and Xiao, 2011;
Dunlop et al., 2012; Cunningham et al., 2014a,b; Sutton et al., 2014). Addi-
tionally, advances in mass spectrometry have allowed the detection and
characterization of amino acid traces, particularly collagen within bone, to
a remarkable level of detail and resolution (Cappellini et al., 2014). Such
techniques open up the prospect of detecting traces of parasites and para-
sitism more frequently and revealing key systematic features and morpho-
logical characters indicative of a parasitic way of life.
Another facet of palaeoparasitology, although perhaps not widely
considered as such, is the study of horizontally (laterally) transferred
DNA including transposable elements, where DNA from one organism
can be detected buried within the genome of another. These so-called
‘genomic fossils’ offer clues as to the origins and nature of ancient associa-
tions (Gilbert and Feschotte, 2010; Gilbert et al., 2010; Katzourakis and
Gifford, 2010; Katzourakis, 2013; Koutsovoulos et al., 2014). Indeed,
Ford Doolittle considers horizontally transferred DNA fragments as
‘basically parasites’ (p. 8; Gitschier, 2015) that have been parts of their
host genomes for a considerable length of time. The rise in genome studies
has provided ever-increasing evidence for horizontal gene transfers, HGTs
4 Kenneth De Baets and D. Timothy J. Littlewood

(e.g. see Scholl et al., 2003), although such events detected among Metazoa
appear to be more common in some groups (e.g. bdelloid rotifers:
Gladyshev et al., 2008) than in others. Whereas palaeontology looks
towards the earth’s fossil and subfossil record for ancient biotic interactions,
it is clear that genomes may also be gleaned for evidence of relictual genetic
elements of nonhost (“parasitic”) origin.
Regardless of approach, time points gathered directly from fossils or
inferred from calibrated phylogenies remain critical in understanding
when, where and to some extent how hosteparasite interactions took place
and how they might respond in the future; for example, the exchange of
genes from parasitic to host plants of the genus Plantago has been shown
to be a result of their direct physical contact with one another (Mower
et al., 2004). Parasitic plants offer a particularly rich resource for understand-
ing HGT (Davis and Xi, 2015).
Morphologically based classifications of parasites have proved chal-
lenging due to frequent apparent simplifications, convergence or specializa-
tions in their morphology that make homology assessment difficult.
However, novel molecular methods, used with caution, may form the basis
for more robust phylogenetic assignments of extant and subfossil parasitic
remains, and thus more comprehensive understanding of the origin and
evolution of parasitism within single lineages (Near, 2002; Lockyer et al.,
2003; Littlewood, 2011; Wood et al., 2013b; Hartikainen et al., 2014; Sum-
mers and Rouse, 2014; Blaxter and Koutsovoulos, 2015; Littlewood and
Waeschenbach, 2015; Okamura and Gruhl, 2015). Here we provide an
updated perspective on the merits, further possibilities and frustrations
associated with using the fossil record in constraining the origins and evolu-
tion of parasitism. We highlight novel methods, which make it possible to
more fully exploit information buried in fossil or genomic sequences of their
hosts.

2. TECHNIQUES FOR ANCIENT PARASITE DISCOVERY


Various destructive methods (thin sections, rehydratation or resedi-
mentation techniques, and grinding tomography) and nondestructive
methods (e.g. phase contrast synchrotron or microcomputed tomography,
mCT) are particularly relevant to discovering and characterizing the
morphology of parasitic remains or host responses in older (fossil) samples.
Increasingly these can be supplemented with analyses of ancient
The Importance of Fossils in the Evolution of Parasites 5

biomolecules, including ancient DNA (aDNA) in younger (archaeological)


samples, or analyses of more resistant biomolecules in older, exceptionally
preserved fossil samples (Briggs and Summons, 2014).

2.1 Thin sections and computed tomography


Various studies have demonstrated the merit of conventional preparation
and imaging methods used for archaeological samples (Araujo et al., 2008;
Ara ujo et al., 2015) to provide evidence for helminth eggs or other parasitic
remains in fossil coprolites (Poinar and Boucot, 2006; Dentzien-Dias et al.,
2013; Da Silva et al., 2014). Such investigations typically rely on thin
sectioning and various dissolution/rehydration/resedimentation methods,
which destroy the original 3D structure and/or association of the parasites
and may lose less-resistant parasite remains (Dufour and Le Bailly, 2013;
Wood et al., 2013b; Ara ujo et al., 2015).
Computed tomography (Sutton et al., 2014), whereby 3D reconstruc-
tions of serially sectioned material are rendered and visualized by computer,
is developing rapidly as a means by which high resolution differentiation can
be achieved from the fossilized remains of small and even soft-bodied organ-
isms. However, the resolution of parasites and evidence of parasitism often
remains a serendipitous by-product of investigating fossil microstructures.
One such case has recently revealed the remarkable discovery of a putative
fossil pentastomid found in association with its ostracod host entombed for
425 Ma (Siveter et al., 2015). Not only did this discovery reveal the first fos-
sil occurrence of an adult pentastomid but also its host association, which had
been the subject of some considerable speculation in the literature
(Waloszek et al., 2005). Today, pentastomids mostly parasitize terrestrial ver-
tebrates exclusively as endoparasites, and although extinct representatives
have been identified in Cambrian marine sediments at a time before these
terrestrial hosts existed, it has been suggested that these forms were parasitic
on marine vertebrates (Sanders and Lee, 2010). The new Silurian record by
Siveter et al. (2015) not only reveals a new host association but also shows
the parasite as ectoparasitic. Unfortunately, because of the destructive nature
of the grinding technique, the fossil now exists only as an image. Although
many reports for terrestrial parasites or vectors come from amber (Poinar,
2014a), computed tomography has only been rarely used to test such
assertions (Dittmar et al., 2011; Dunlop et al., 2012), which have been
largely based on microscopic methods. Phase contrast tomography and other
tomographic methods are however ideally suited to characterize fossils in
three dimensions (even in nontransparent amber) and corroborate
6 Kenneth De Baets and D. Timothy J. Littlewood

parasite/vector interpretations as it has been used for phoretic associations


(Dunlop et al., 2012; Penney et al., 2012).

2.2 Ancient biomolecules


Novel techniques make it possible to identify biomolecules (Greenwalt
et al., 2013; Briggs and Summons, 2014; Yao et al., 2014) in ancient remains
and samples. The most familiar one is probably aDNA, which has been
applied to various parasitic (sub)fossils (Dittmar, 2009; Dittmar et al.,
2011; Wood et al., 2013b), although it can only be detected and character-
ized reliably in exceptionally well-preserved material up to 1 Ma (Hebsgaard
et al., 2005; Briggs and Summons, 2014). Large and fragile molecules such as
DNA cannot survive fossilization (Briggs and Summons, 2014), but other
complex organic structures such as iron-stabilized haem, can survive for
longer, at least under certain conditions (Briggs, 2013; Greenwalt et al.,
2013; Yao et al., 2014), opening up the prospects for protein-based detec-
tion methods (Cappellini et al., 2014). This can be used as an extension to
the analysis of gut contents of isolated parasite or vector remains to get an
indication of the trophic targets and, therefore, the possible identity of the
hosts. Preservation of feather remnants in a louse specimen’s foregut, for
example, confirmed its association to a waterbird ectoparasite (Wappler
et al., 2004).
Advances in chemical analysis at the nanoscale, and as applied to fossils,
opens up a whole new world in revealing ancient colours, pigments,
microbiomes, and the hidden remnants of soft-bodied organisms (Briggs
and Summons, 2014; Bertazzo et al., 2015; Vinther, 2015). A better
understanding of taphonomy (Briggs, 2013), as applied to parasitic groups,
may provide the tools to improve and apply these techniques in recognizing
parasites and their influence on hosts in the fossil record. Certainly there
seems room for developing and applying these techniques to subfossil
(unmineralized) remains where eggs are found intact without DNA and
without clear morphological identity (see also Linseele et al., 2013 and
Cano et al., 2014).

2.2.1 Ancient DNA


Earlier aDNA studies focused on PCR to amplify specific short gene
sequences targeted for particular parasite groups or species from single sam-
ples (reviewed in Dittmar, 2009; Dittmar et al., 2011; Dittmar, 2014). Novel
approaches (Wood et al., 2013b) focus on the amplification of total DNA of
whole samples followed by the application of next generation sequencing
The Importance of Fossils in the Evolution of Parasites 7

platforms for shotgun sequencing. Subsequent bioinformatic interrogation


of the data for various groups of parasites has been established in the field
of metagenomics and environmental samples (Dittmar, 2009; Wood et al.,
2013b). In spite of remarkable progress, aDNA techniques will always be
constrained by the rapid deterioration of DNA.

2.2.2 Palaeoproteomics
DNA is not believed to survive in sufficiently long lengths for sequencing
over longer geological timescales (>1 Ma) (Hebsgaard et al., 2005; Briggs
and Summons, 2014) and is rarely found well preserved. However, the
study of fossilized bone, which has been crudely defined as a composite
of collagen (protein) and hydroxyapatite (mineral) (see Hill et al., 2015),
has shown that, for vertebrates at least, palaeoproteomics can be a
rewarding insight into ancient proteins, providing evidence for phyloge-
netics and an understanding of bone biochemistry (Wadsworth and
Buckley, 2014). Collagen, in particular, has been isolated from vertebrate
fossils of considerable age, including an 80 million year (my)-old Campa-
nian hadrosaur, Brachylophosaurus canadensis (Schweitzer et al., 2009) and a
68-my-old Tyrannosaurus rex (Asara et al., 2007); some of these studies have
attracted some criticism (Pevzner et al., 2008). The characterization of the
constituent peptides of fossil bone proteins, requiring mass spectrometry,
suggests that collagen (the most abundant protein) can survive up to
340 ky at 20  C, and the second most abundant protein, osteocalcin, can
persist for w45 ky; see Ostrom et al. (2000), Hofreiter et al. (2012) and
Collins et al. (2000). There are many other bone proteins that can be iso-
lated and identified depending on the nature of preservation and the age of
the fossil (Cappellini et al., 2012), but recent studies focusing on collagen
have provided opportunities to push timescales back further in the charac-
terization of ancient biomolecules useful for phylogenetics (Welker et al.,
2015). Recently, even putative erythrocyte remains were reported in dino-
saur bones (Bertazzo et al., 2015).
The application of palaeoproteomics more broadly to parasites or to
other fossil remains, in the hope of finding evidence for parasitism, is in its
infancy, but analysis of more resistant biomolecules than DNA might
make it possible to test other hypotheses associated with parasites or host-
related biomolecules. Certainly, the prospect of verifying the presence of
porphyrins in fossilized haematophagous insects (Greenwalt et al., 2013;
Yao et al., 2014) seems a tractable goal.
8 Kenneth De Baets and D. Timothy J. Littlewood

3. THE PARASITE FOSSIL RECORD


The fossil record of parasites or other pathogens is usually poor
because they often reside within their hosts or vectors, may go through
some life cycle stages away from their hosts, are small, and lack hard tissues
(Conway Morris, 1981; Baumiller and Gahn, 2002; Labandeira, 2002;
Littlewood and Donovan, 2003; De Baets et al., 2011). This is particularly
true not only for viruses, bacteria and protozoa (Poinar, 2014a), but also
for various soft-bodied metazoan parasites such as helminths (Littlewood
and Donovan, 2003; De Baets et al., 2015a; Huntley and De Baets, 2015;
Poinar, 2015a) or weakly sclerotized arthropods (Cressey and Boxshall,
1989; Castellani et al., 2011; Klompmaker and Boxshall, 2015; Nagler
and Haug, 2015). Body fossils of parasites are rare and usually restricted to
sites of exceptional fossil preservation (KonservateLagerst€atten), particularly
those still associated with the remains of their hosts providing direct evidence
of parasitism. Characteristic traces or pathologies in the skeletons of their
hosts are more common and can be traced more continuously over longer
timescales, but the taxonomic affinity of the culprits is not always easy to
disentangle (Donovan, 2015; Huntley and De Baets, 2015; Klompmaker
and Boxshall, 2015; Taylor, 2015). The fossil record of parasitism has
been reviewed on various occasions (Conway Morris, 1981; Boucot,
1990; Littlewood and Donovan, 2003; Boucot and Poinar, 2010; Dittmar,
2010) with some others focusing particularly on marine parasites (Baumiller
and Gahn, 2002; Rouse, 2005a) or terrestrial pathogens (Labandeira, 2002;
Poinar, 2014a). The fossil record can also provide direct evidence for pres-
ence of parasiteehost associations e some of which might now be extinct, as
well as the impact of parasitism on their hosts in the geological past. We will
discuss the different sources of fossil evidence, their merits, limitations and
associated frustrations.
Major important fossil discoveries of metazoan parasites and pathogens
distributed by vectors underpinning our understanding of the ancient history
of hosteparasite associations are detailed in Table 1. The table reveals
considerable diversity of hosts and parasites, and hosteparasite interactions.
New finds also highlight the potential of finding evidence in coprolites for
parasitic remains in both marine and terrestrial realms, and amber as sources
for haematophagous vectors. Fossil pentastomids were long thought to be
rare and restricted to the CambrianeOrdovician sites with Orsten preserva-
tion, but new discoveries highlight they might be more common than
Table 1 Ancient history of hosteparasite associations
Higher taxon Taxon Fossil evidence Age Source Host References Environment
Bacteria
Spirochaetes Palaeoborrelia Direct: spirochaete- Miocene Amber Amblyomma sp. Poinar (2014b) T
dominicana like cells
Rickettsiales Palaeorickettsia Direct: rickettsial-like Early Cretaceous Amber Cornupalpatum Poinar (2015b) T
protera cells burmanicum

Eukaryota
Metamonada Parabasalia: Indirect: lesions Cretaceous Skeletal Tyrannosaurus rex Wolff et al. (2009) T
Trichomonadida deformation
Amoebozoa? Entamoebites antiquus Direct: cyst Cretaceous Coprolite Archosaur Poinar and Boucot T
(?dinosaur) (2006)

Phylum Apicomplexa
Gregarinasina Primigregarina Direct: in amber CretaceouseMiocene Amber Cockroaches Poinar (2012) T
burmanica
Coccidia Cryptosporidium, Direct: aDNA in Holocene Coprolite Moas Wood et al. (2013b) T
Eimeriorina coprolite
Eimeria lobatoi Indirect: oocysts Holocene Coprolite Deer Ferreira et al. (1992)
Archeococcidia antiquus; Indirect: oocysts Pleistocene Coprolite Ground sloth Schmidt et al. (1992)
A. nothrotheriopsae
Haemospororida Plasmodium dominicana Direct: erythocytes Miocene Amber Culex malariager Poinar (2005b) T
Vetufebrus ovatus Direct: erythocytes Miocene Amber Enischnomyia stegosoma Poinar (2011b) T
Paleohaemoproteus Direct: erythocytes Early Cretaceous Amber Proticulicoides sp. Poinar and Telford T
burmacis (2005)

Phylum Euglenozoa
Trypanosomatida Palaeotrypanosoma Direct: erythocytes Early Cretaceous Amber Leptoconops nosopheris Poinar (2008a) T
burmanicus
Trypanosoma Direct: erythocytes Miocene Amber Triatoma dominicana Poinar (2005b) T
antiquus
(Continued)
Table 1 Ancient history of hosteparasite associationsdcont'd
Higher taxon Taxon Fossil evidence Age Source Host References Environment
Palaeoleishmania Direct: erythocytes Early Cretaceous Amber Palaeomyia burmitis Poinar and Poinar T
proterus (2004a,b)
Paleoleishmania Direct: erythocytes Miocene Amber Lutzomyia adiketis Poinar (2008b) T
neotropicum

Phylum Arthropoda
Copepoda ? Indirect: exocysts Jurassic Skeletal Crinoids, echinoids Mercier (1936),
deformation Radwa nska and
Radwa nska (2005),
Radwanska and
Poirot (2010)
Kabatarina pattersoni Direct: Early Cretaceous Calcareous Fish Cressey and Patterson M
nodules (1973), Cressey and
Boxshall (1989)
Isopoda ?Bopyridae Indirect: swellings ?Early Jurassic; Middle Skeletal Crustacea Klompmaker et al. M
JurassiceRecent deformation (2014),
Klompmaker and
Boxshall (2015)
Pentastomida 5 genera; 10 species Direct: phosphatized Cambrian Calcareous ? early chordates; Waloszek and M€ uller M
remains isolated eOrdovician; nodules ostracod (1994), Waloszek
from host Silurian? et al. (1994),
Waloszek et al.
(2005a,b),
Castellani et al.
(2011), Siveter et al.
(2015)
Acari Cornupalpatum Direct: larva stage Early Cretaceous Amber ? Poinar and Brown T
burmanicum (2003)
(Ixodidae)
Compluriscutula Direct: larva stage Early Cretaceous Amber ? Poinar and Buckley T
vetulum (Ixodidae) (2008)
Thecostraca ?Ascothoracida Indirect: borings Cretaceous Skeletal Echinoidea Madsen and Wolff M
deformation (1965)
?Ascothoracida Indirect: borings Cretaceous Skeletal Octocorallia Voigt (1959), (1967) M
deformation

Insecta
Siphonaptera s.l. Pseudoculidae Direct: isolated from JurassiceCretaceous Lacustrine ?pterosaurs, dinosaurs Gao et al. (2012), T
host deposits and/or small Huang et al. (2012),
mammals Gao et al. (2013),
Huang et al. (2013),
Gao et al. (2014),
Huang (2014)
Siphonaptera s.s. Paleopsylla: 4 species Direct: isolated from Eocene Amber ?mammals Dampf (1911), T
host Beaucournu and
Wunderlich
(2001),
Beaucournu (2003)
Phthiraptera Megamenopon rasnitsyni Direct: isolated from Eocene Lacustrine ?water birds Wappler et al. (2004) F
host deposits
? Indirect: nits Eocene Baltic amber Mammals Voigt (1952) T
Diptera Qiya jurassica Direct: parasitic larvae Jurassic Lacustrine ?salamanders Chen et al. (2014) F
(Athericidae) deposits

Phylum Nematoda
Ascaridida Ascarites rufferi Indirect: eggs Upper Triassic Coprolite Cynodont Da Silva et al. (2014) T
(Ascarididae)
Ascarites gerus Direct: egg with Early Cretaceous Coprolite Archosaur Poinar and Boucot T
(Ascarididae) developing juvenile (2006)
Toxocara canis Direct: eggs Pleistocene Cave deposits Canid Bouchet et al. (2003)
(Ascarididae) (?Crocuta spelaea)
Oxyurida Paleoxyuris cockburni Indirect: eggs Upper Triassic Coprolite Cynodont Hugot et al. (2014) T
(Heteroxyne-
matidae)
(Continued)
Table 1 Ancient history of hosteparasite associationsdcont'd
Higher taxon Taxon Fossil evidence Age Source Host References Environment
Mermithida Cretacimermis libani Direct Early Cretaceous Amber Midge Poinar et al. (1994) T
(Mermithidae) (Chironomidae:
Diptera)
?Enoplida Palaeonema phyticum Direct Early Devonian Silicified plant Early land plant Poinar et al. (2008) T
(Palaeonematidae) material

Phylum Nematomorpha
Chordodidae Cretachordodes burmitis Direct Early Cretaceous Amber Poinar and Buckley T
(2006)

Phylum Platyhelminthes
Cestoda Permian Direct: eggs with Coprolite Sharks Dentzien-Dias et al. M
developing embryo (2013), De Baets
et al. (2015a)
Trematoda Digenites proterus Early Cretaceous Indirect: eggs Coprolite Archosaurs Poinar and Boucot T
(2006)
Dicrocoelidae Pleistocene Indirect: eggs Coprolite ?bear Jouy-Avantin et al. T
(1999)
?Gymnophallidae Early Eocene Indirect: characteristic Skeletal Ruiz and Lindberg M
pits in bivalve shells deformation (1989), Todd and
Harper (2011),
Huntley and De
Baets (2015)
?Monogenea Middle Devonian Direct: attachment Fine-grained Placoderms, Upeniece (2001,
structure sediments acanthodians 2011), De Baets
et al. (2015a)
Phylum Acanthocephala
? ? Holocene Indirect: eggs Coprolite Mammals (canids, Fry and Hall (1969), T
humans) Noronha et al.
(1994)

Phylum Annelida
Myzostomida ? Carboniferous Indirect: skeletal Crinoids Welch (1976), M
eJurassic deformations (galls) Hess (2010)
Clitellata ?Hirudinae Triassic Indirect: cocoons Freshwater ? Manum et al. (1991), F
deposits Bomfleur et al.
(2012), Parry et al.
(2014)

Phylum Mollusca
Eulimidae Eulima Upper Cretaceous Direct: isolated shells Marine deposit ? Sohl (1964) M
? Upper Cretaceous Indirect: trace on Skeletal Echinoids Neumann and M
echinoid hosts deformation Wisshak (2009)
Coriaphyllidae Coralliophila (Timothia) Eocene Direct: isolated shells Marine deposit ? Dockery (1980) M
aldrichi
Leptoconchus: 2 species; OligoceneeMiocene Direct: shells associated Skeletal Corals (Cladocera, Lozouet and Renard M
Coralliophila: with coral host deformation Thegioastraea, (1998)
1 species; Galeropsis: Pocillopora)
1 species
Unionidae Unio, Anodonta Quaternary Direct: glochidium Freshwater ?fish Brodniewicz (1968) F
larvae deposits
14 Kenneth De Baets and D. Timothy J. Littlewood

expected even during different ages. Such fossil Lagerst€atte should therefore
be systematically screened for parasites. Further work needs to be done on
establishing characteristic trace fossils and pathologies, particularly in verte-
brates, back in time.

3.1 Body fossils


Body fossils are usually defined as remains or representations of the whole or
actual parts of organisms (Goldring 1999; Foote and Miller, 2007). In rare
cases, parasites are so well and completely preserved that they can be accu-
rately assigned to modern taxa (Cressey and Boxshall, 1989; Siveter et al.,
2015). Often, only sclerotized attachment organs, eggs or cysts are known,
which can still be characterized sufficiently to assign them to particular taxa
(De Baets et al., 2015a). In other cases, body fossils of nonparasitic life stages
of extant parasites hint that their parasitic life stages might potentially also be
present (e.g. parasitic stages of arthropods or unionids), but this can only be
confirmed by future discoveries (Skawina and Dzik, 2011; Nagler and Haug,
2015). All extant members of Unionida have parasitic larvae, which suggests
that this is a synapomorphic trait for this group, which goes as far back as the
middle Triassic (Skawina and Dzik, 2011). Unfortunately, the oldest fossil
glochidia cannot be used to test this hypothesis as they are only found as
late as the Pleistocene (Brodniewicz, 1968). In exceptional cases, parasite
body fossils are still associated with host remains, while in other cases they
are isolated, making it difficult to identify the hosts or even decide if these
forms were parasitic or not. Establishing them as parasites is usually achieved
by comparing them with the morphology of modern relatives or analogues,
but in some cases it can only be corroborated by finding the parasite in situ
parasitizing its host. Labandeira (2002), for example, claims that Cambrian
tardigrades (Muller et al., 1995) have certain resemblances to extant parasitic
forms, which indicates at least a possible phylogenetic relationship and
potentially a mode of life, but this still needs to be further corroborated.
The body fossil record is restricted to sites of exceptional preservation.
One of the most important types of preservation is found in fossil ambers
which have preserved the remains of unicellular pathogens from a variety
of terrestrial parasitic arthropods (Nagler and Haug, 2015), to nematodes
exiting their dying hosts (Poinar, 2014a, 2015a). Other important Konservat
Lagerst€atten for the preservation of parasites include phosphatized remains of
arthropods (Cressey and Patterson, 1973; Cressey and Boxshall, 1989; Maas
and Waloszek, 2001; Maas et al., 2006) in carbonate nodules (the so-called
Orsten preservation), silicified nematodes (Poinar et al., 2008) in
The Importance of Fossils in the Evolution of Parasites 15

hydrothermal vent environments (the so-called Rhynie Chert preservation),


fine-grained lacustrine or marine deposits where the remains were quickly
buried and/or anoxic environments contributed to fossilization. The latter
includes oil shales deposited not only in maars or other lacustrine environ-
ments (Wappler et al., 2004; Hughes et al., 2010; Greenwalt et al., 2013),
but also in low energetic, marginal marine or deeper marine environments.
In some cases, ectoparasites are still attached or associated with their hosts,
while endoparasites are still found in situ within their hosts or escaping their
dead hosts. Cysts, eggs including those with developing embryos, larvae
(Ferreira et al., 1993) or remains of juveniles, are sometimes also recovered
from coprolites, one of the many types of trace fossils (see Section 3.2).
Protozoan parasites or other pathogens like viruses and bacteria are usu-
ally hard to verify in the fossil record (Frías et al., 2013; Poinar, 2014a), but
are known to be transmitted by various vectors, which might themselves
fossilize. Most common vectors are arthropods which feed on blood,
although forms feeding on feathers or hairs might also be involved. Direct
fossil evidence for vector feeding behaviour is even rarer than parasitism
(Table 2). Possible exceptions include the recent discovery of haemoglo-
bin-derived porphyrins in the stomach content of an Eocene mosquito
(Greenwalt et al., 2013) as well as higher Fe contents in fossilized true
bugs, Hemiptera (Yao et al., 2014). Direct evidence for vector behaviour
of haematophagous taxa has been restricted so far to amber deposits (Poinar
and Poinar, 2004b; Poinar, 2005a,b,c; Poinar and Telford, 2005; Poinar,
2011b, 2014b, 2015b). Some unicellular pathogens have also been reported
from fossil and subfossil archosaur coprolites, although microscopic taxa are
harder to identify in older occurrences than in more recent occurrences
where aDNA is available (Poinar and Boucot, 2006; Wood et al., 2013b).
Our ability to identify parasitic and haematophagous insects is mostly based
on their possible taxonomic affinities and morphological adaptions of their
mouth parts or other structures similar to extant taxa (Lukashevich and
Mostovski, 2003; Greenwalt et al., 2013; Pe~ nalver and Pérez-De la Fuente,
2014; Nagler and Haug, 2015). Such morphological adaptations have even
been used to suggest ectoparasitic behaviour in lineages where larvae are no
longer parasitic (Chen et al., 2014).
Modern-type lice can be traced back to the Eocene (Wappler et al., 2004),
while earlier reports are most likely erroneous determinations of mites
(Dalgleish et al., 2006), so that Phthiraptera, which are mainly specialized
on mammals, probably evolved later than did fleas (Nagler and Haug,
2015). Fossils of modern-type fleas can be traced back to the Eocene at least
16
Table 2 Body fossils of haematophagous vectors
Taxonomy Species Haematophagy Parasite Source References
Arachnida
Ixodidae Cornupalpatum burmanicum Indirect Rickettsial-like cells Burmese amber Poinar (2015b)
Amblyomma sp. Indirect Spirochaete-like cells Dominican amber Poinar (2014b)

Diptera
Ceratopogonidae Proticulicoides sp. Indirect Plasmodiidae Burmese amber Poinar and Telford (2005),
Boucot and Poinar (2010)
Leptoconops nosopheris Indirect Trypanosomatidae Burmese amber Poinar (2008a)
Culicidae Culiseta sp. Direct Fe ? Kishenehn Formation Greenwalt et al. (2013)
concentrations,

Kenneth De Baets and D. Timothy J. Littlewood


porphyrins
Culex malariager Indirect Plasmodiidae Dominican amber Poinar (2005a,b)
Phlebotomidae Palaeomyia burmitis Indirect Trypanosomatidae Burmese amber Poinar and Poinar (2004a,b)
Lutzomyia adiketis Indirect Trypanosomatidae Dominican amber Poinar (2008b)
Streblidae Enischnomyia stegosoma Indirect Plasmodiidae Dominican amber Poinar (2011b),
Poinar and Brown (2012)

Hemiptera
Reduviidae Triatoma dominicana Indirect Trypanosomatidae Dominicsssan amber Poinar (2005c)
Torirostratidae Torirostratus pilosus Direct Fe concentrations ? Yixian Formation Yao et al. (2014)
Torirostratidae Flexicorpus acutirostratus Direct Fe concentrations ? Yixian Formation Yao et al. (2014)
The Importance of Fossils in the Evolution of Parasites 17

(Perrichot et al., 2012), although several extinct families of putative stem-


group Siphonaptera have been reported from the Jurassic and Cretaceous pe-
riods (Gao et al., 2012, 2013, 2014; Huang et al., 2012, 2013; Huang, 2014,
2015). Host associations with dinosaurs and pterosaurs have been suggested
for stem-group fleas (Huang, 2014), but a novel molecular study suggests
that the earliest fleas appeared in the early Cretaceous era and had a strong as-
sociation with mammals, whereas the Jurassic stem-group forms are only
distantly related (Zhu et al., 2015). Finding direct evidence of Jurassic or
Cretaceous fleas associated with host remains would be the smoking gun to
resolve this issue. The relationship between hosts and other haematophagous
insects, which are also important vectors, is less strict. Bed bugs and their close
relatives can probably be traced back to the Eocene (Engel, 2008). Diptera can
be traced back to the PermianeTriassic. Blood-sucking is inferred to be
ancestral in this group and members of various lineages are important vectors
(Poinar, 2014a; Nagler and Haug, 2015), including blackflies (Simulidae),
sandflies (Phlebotominae, Psychodidae) and mosquitoes (Culicidae). Direct
evidence for both haematophagy and their vectors is only known from
Diptera (Greenwalt et al., 2013; compare Table 2). Ticks are also important
vectors for Spirochaetes and Ricketsiales, which might have been already the
case since the Cretaceous period (Poinar, 2014b, 2015b).
Even when isolated from their hosts, gut contents or coprolites of fossil
parasitic invertebrates (Wappler et al., 2004; Greenwalt et al., 2013) or verte-
brate hosts (McConnell and Zavada, 2013), as well as other remains found
alongside, have allowed parasite remains to be confidently attributed to
major host groups, at least at higher taxonomic levels (Dentzien-Dias
et al., 2013; Da Silva et al., 2014; Hugot et al., 2014). Archaeological exam-
ples frequently allow species level identifications of helminth eggs (Dittmar
et al., 2011).
The earliest evidence for Metazoa parasitizing a plant is nematodes found
within early land plants (Poinar et al., 2008). Nevertheless, fungi can also be
vicious pathogens of animals and plants (Sexton and Howlett, 2006). The
oldest evidence for the presence of fungi parasitic on animals derives from
the Cretaceous period (Sung et al., 2008). Sometimes, the characteristic
response of the host to a fungal parasite can also be preserved (see Section
4.2). Fossilized galls can also be important sources of information on
planteparasite interactions (Knor et al., 2013; Labandeira and Currano,
2013; Leckey and Smith, 2015). Note that galls are often caused by parasitic
insects, but can also be induced by viruses, bacteria, fungi, nematodes and
mites (Knor et al., 2013).
18 Kenneth De Baets and D. Timothy J. Littlewood

3.2 Trace fossils and pathologies


Various invertebrate hosts including arthropods, molluscs, echinoderms and
various colonial organisms can contain traces or pathologies in their
skeleton, which is evidence of an infestation or association with parasites
(Boucot and Poinar, 2010; Donovan, 2015; Huntley and De Baets, 2015;
Taylor, 2015).
In some cases, these traces or pathologies are believed to be so character-
istic that they are interpreted to represent the oldest fossil evidence for
particular lineages in the fossil record; including castration of fossil decapods
by rhizocephalan barnacles (Feldmann, 1998, 2003; compare Klompmaker
and Boxshall, 2015), deformations in echinoderms attributed to myzostomid
annelids (Welch, 1976; Hess, 2010; Parry et al., 2014), crustacean arthropods
(Madsen and Wolff, 1965; Radwa nska and Radwa nska, 2005; Radwanska
and Poirot, 2010) or eulimid gastropods (Neumann and Wisshak, 2009) as
well as borings in octocorals related to the presence of ascothoracid barnacles
(Voigt, 1959, 1967). The most convincing palaeontological model systems
are those where both extant and fossil parasiteehost interactions are compa-
rably well studied such as the gymnophallid-induced pits and igloo-shaped
shell concretions in bivalves (Campbell, 1985; Ruiz and Lindberg, 1989;
Ituarte et al., 2001, 2005; Huntley, 2007; Todd and Harper, 2011; De Baets
et al., 2015a; Huntley and De Baets, 2015) and (?bopyrid) isopod swellings
in decapods (Weinberg Rasmussen et al., 2008; Boyko and Williams, 2009;
Williams and Boyko, 2012; Klompmaker et al., 2014; Klompmaker and
Boxshall, 2015). Particularly in such cases, trace fossils and associated pathol-
ogies can not only provide direct information on the behaviour of the par-
asites but also the response of the host, which makes it possible to interpret
the type of relationship between them. However, even in the case of such
model systems, it cannot be ruled out that they were made by another
type of closely related parasite or organism with similar behaviour in the
geological past, which are now extinct or where pathological reactions are
not yet documented in extant hosts. Other (now extinct) culprits can be sus-
pected when the record of these structures is not so continuous and shows
major stratigraphic gaps (Boucot and Poinar, 2010). For example: shell pits
have been confidently linked with gymnophallid flatworms in extant
bivalves, and can be confidently traced into the Eocene (Ruiz and Lindberg,
1989; Todd and Harper, 2011; De Baets et al., 2015a; Huntley and De Baets,
2015), which is more or less consistent with the origin of their final hosts
(extant shorebirds). However, igloo-shaped concretions e attributed to
The Importance of Fossils in the Evolution of Parasites 19

gymnophallids in extant bivalves (Ituarte et al., 2001, 2005), have also been
reported from the Silurian (Liljedahl, 1985), which is not consistent with
extant parasiteehost associations (De Baets et al., 2015a) as shorebirds (Char-
adriiformes), their present day definitive hosts, are believed to have radiated
sometime between the Cretaceous and Eocene periods (Smith, 2015).
Pathologies, therefore, offer less confident evidence for the presence of
parasitic lineages in the fossil record than in body fossils, when no parasitic
remains are found associated with these traces. Direct evidence for the par-
asites associated with such pathologies is mostly restricted to parasitic organ-
isms with mineralized skeletons such as gastropods (Hayami and Kanie,
1980; Lozouet and Renard, 1998; Baumiller and Gahn, 2002). Such traces
are usually compared with known responses to parasites by extant hosts,
which are sometimes not that well-investigated, and by extrapolation it
has been assumed that the same culprits were responsible in the past. This
can be further complicated by the fact that extant phylogenies indicate
that pathology-inducing lineages might have evolved more than once
(e.g. gall- and cyst-forming myzostomids: Summers and Rouse, 2014).
Parasite-induced pathologies have also been reported from hosts that are
now extinct or no longer affected; although their interpretation becomes
more difficult if no modern analogues are available (Owen, 1985; Babcock,
2007; De Baets et al., 2011; De Baets et al., 2015b). Traces which are
reminiscent of nematode borings in foraminifer tests (Sliter, 1971) have
been reported from Cambrian and Ordovician trilobites (Babcock, 2007),
but no conclusive assignment to nematodes as culprits can be made without
direct fossil evidence for associated nematodes. Furthermore, it is still
debated whether these traces in trilobites were made during life or post-
mortem (Owen, 1985). Various pathological reactions in ammonoids (an
extinct group of externally shelled cephalopods) have been attributed to
parasitic flatworms based on their prevalence and similar pathologies in
extant shelled molluscs (De Baets et al., 2011), but as long as no parasite
remains are found associated with them, their attribution to parasitic flat-
worms remains highly speculative at best (De Baets et al., 2015b).
Many palaeontologists also point out the difficulty of defining an inter-
action as being parasitic, although this might be more a problem concerning
the definition of parasitism rather than its recognition (Tapanila, 2008;
Zapalski, 2011), which is not restricted to fossil associations. Some authors
like Tapanila (2008) have suggested that fossil studies should assume that a
symbiosis is neutral (commensal), unless demonstrated otherwise. Other au-
thors have argued that a neutral interaction is absence of an interaction,
20 Kenneth De Baets and D. Timothy J. Littlewood

which cannot be proven, and is therefore unfit for empirical science. The
detection of commensalism is difficult and rather subjective in recent asso-
ciations (usually it is understood as a weak positive or negative interaction)
and as such it seems impossible to detect in the fossil record. Zapalski (2011)
has, therefore, argued avoiding commensalism as a null hypothesis in palae-
oecology, because the possibility of making a type II error is very high. Pos-
itive or negative effects can be detected or inferred based on comparisons
with extant interactions. Identifying traces or pathologies of fossil parasites
can potentially also be performed by demonstrating a negative influence
or effect on growth, body size and/or morphology of their hosts, while a
certain positive effect for the parasite can be inferred. Of course, such inter-
pretations rely on identifying the traces (e.g. borings) or structures as being
made in vivo. This can be most convincingly demonstrated when a host
response (e.g. growth deformation or pathology) can be shown to be asso-
ciated with these structures, often most readily recognized in specimens with
sparse traces or pathologies (De Baets et al., 2011; Donovan, 2015).
Studies have focused particularly on invertebrate hosts, and especially on
those with external shells or exoskeletons, but such pathologies which could
potentially be tracked in the fossil record are also found in vertebrates
including characteristic limb malformations in amphibians (Johnson et al.,
2001, 2002, 2003; Johnson and Sutherland, 2003) or cavities in the mastoid
bone of humans (Oyediran et al., 1975) caused by digenetic trematodes or
trabecula-like bone lesions in cetacean whales (Littlewood and Donovan,
2003) and enlargement of the frontal sinuses accompanied by bone lesions
in mustelids (Rothschild and Martin, 2006) caused by cestodes. Character-
istic skeletal pathologies in terrestrial vertebrates (e.g. mammals) induced by
helminths with resistant eggs have the potential for comparison of preva-
lence of skeletal deformations directly with parasite load or prevalence in
coprolites effectively linking palaeoparasitology and palaeopathology
(compare Dutour, 2013). Some parasitic unicellular pathogens might leave
characteristic traces or pathologies in their hosts. Wolff et al. (2009) studied
erosive lesions in tyrannosaurs and attributed them to Trichomonas gallinae-
like protozoans, because they are reminiscent of similar pathologies in extant
birds caused by this parasite. Unicellular eukaryotes can also leave character-
istic traces in their hosts; for example, borings by foraminifera in marine
echinoderms and bivalves (Neumann and Wisshak, 2006; Beuck et al.,
2007, 2008). In some cases, the host performs activities or exhibits behaviour
induced by the parasites, which can occasionally also be found in the fossil
record. One spectacular example is the death-grip scars found on Eocene
The Importance of Fossils in the Evolution of Parasites 21

leaves, interpreted to have been made by ‘zombie’ ants infested by fungi


(Hughes et al., 2010); the fungal infection Ophiocordyceps forces ants to
hold onto tips of leaves so that after the death of the ant, emerging fungal
spores can be released into the wind from an elevated position. Trace fossils
can give unique information on the behaviour and prevalence of the
parasites and track the response of their host through geological time, as their
record can be more continuous (less patchy) than that of body fossils which
only fossilize in exceptional conditions.
Pathologies have their own problems as they are sometimes hard to
assign to a certain lineage of culprits, although there are some pathologies
which are believed to be diagnostic, or at least characteristic, for parasitism.
Irrespective of this problem, the temporal and spatial record of parasite-
induced pathologies in their hosts can be much more continuous than the
parasite body fossil record, particularly in molluscs, echinoderms, colonial
organisms and others with fossilizable skeletons (Donovan, 2015; Huntley
and De Baets, 2015; Klompmaker and Boxshall, 2015; Taylor, 2015).
This can provide valuable quantitative data on various aspects of parasitee
host interactions, which can be tracked over millions of years (Brett,
1978; Ruiz and Lindberg, 1989; Baumiller and Gahn, 2002; De Baets
et al., 2011; Klompmaker et al., 2014; De Baets et al., 2015b; Huntley
and De Baets, 2015; Klompmaker and Boxshall, 2015). Such data can
only rarely be obtained by looking at body fossil records of parasiteehost as-
sociations, with some rare exceptions where both the host and the parasite
have fossilizable skeletons (Lozouet and Renard, 1998; Baumiller and Gahn,
2002) or where multiple similar taphonomic windows (e.g. amber) exist.
This includes direct information concerning prevalence and virulence of
this relationship, and their possible relationship with host evolution
including diversity (Klompmaker et al., 2014) and body size (Ruiz, 1991;
Huntley and De Baets, 2015), as well as environmental factors such as
sea-level and climate change (Huntley et al., 2014). This can be particularly
relevant to predict the future response of parasiteehost systems to global
change, where studies have suggested that parasites might be more prone
to (co)extinction (Dunn et al., 2009).
The link between the prevalence of parasites and pathologies, within pop-
ulations and particularly individual hosts, might not be straightforward and has
only rarely been investigated in extant hosts. Furthermore, the nature of the
relationship and their effects might be context dependent (Bronstein, 1994;
Daskin and Alford, 2012). Various preservation, collection and taxonomic
biases can and should be accounted for in quantitative analyses of fossil
22 Kenneth De Baets and D. Timothy J. Littlewood

antagonistic interactions (Huntley and De Baets, 2015; Klompmaker and


Boxshall, 2015), which have so far mainly focused on less specific (pred-
atoreprey) interactions (Kelley et al., 2003; Huntley and Kowalewski,
2007) rather than parasiteehost interactions. Various environmental factors
can, for example, influence the invasion of molluscs by parasites on various
organizational levels (Cheng and Combes, 1990). To further progress in
the field of quantitative palaeopathology in deep time, more quantitative
data and analyses on existing model systems are required, as well as the
need to identify additional modern and/or fossil analogues of already identi-
fied parasite-related pathologies. Palaeopathologies with a more continuous
fossil record have the potential to be used to model the influence of parasite
prevalence and virulence on the evolution of their hosts and how they are
modulated by environmental parameters on longer time-scales.

3.3 Coprolites
Coprolites are usually defined as fossilized (permineralized) faeces, although
the term is often also used for desiccated, more recent faeces from archaeo-
logical sites (Ferreira et al., 1991; Reinhard and Bryant, 1992; Hunt et al.,
2012). Coprolites have yielded fossil and archaeological evidence for para-
sitic organisms (Table 3) ranging from coccidia or other protozoans (Ferreira
et al., 1992; Schmidt et al., 1992; Poinar and Boucot, 2006; Frías et al., 2013;
Wood et al., 2013b), to parasitic fungi and plant remains (Sharma et al.,
2005; Wood et al., 2012), to helminths (Gonçalves et al., 2003; Savinetsky
and Khrustalev, 2013), including acanthocephalans (Noronha et al., 1994),
but particularly nematodes (Ferreira et al., 1991, 1993; Poinar and Boucot,
2006; Leles et al., 2010; Da Silva et al., 2014; Hugot et al., 2014) and various
groups of parasitic flatworms (Schmidt et al., 1992; Jouy-Avantin et al.,
1999; Dentzien-Dias et al., 2013). Coprolites can therefore be an important
additional source of ancient parasitism supplementary to amber, where the
record is heavily biased towards arthropods and their terrestrial parasites.
In ideal cases, coprolites are still associated with their producer, which
makes it possible to confidently identify their origin and therefore the
host taxon of the fossil parasites. The coprolite producer may correspond
with the host of the parasite or more rarely as the one who ingested the para-
site and/or host. However, most frequently, coprolites are found in isola-
tion, where the identity of the producer can only be inferred from their
morphology and content (Poinar and Boucot, 2006; Dentzien-Dias et al.,
2013), and, in the case of more recent specimens, by aDNA analysis
(Wood and Wilmshurst, 2014). Invertebrate coprolites might also have
The Importance of Fossils in the Evolution of Parasites
Table 3 Coprolites depicting fossil and archaeological evidence for parasitic organisms
Taxonomic affinity Fossil evidence Age Host References
Protozoa
Coccidia
Eimeriorina Oocyst Holocene Ground sloth Schmidt et al. (1992)
(Nothrotheriops
shastensis)
Eimeridae Oocysts (Eimera) Holocene Deer Ferreira et al. (1992)
Cryptosporidiidae aDNA (Cryptosporidium) Holocene Moas (Dinomis robustus, Wood et al. (2013b)
Pachyornis
elephantopus)
Helminths
Platyhelminthes
Cestoda Egg þ developing Permian ?elasmobranchs Dentzien-Dias et al. (2013)
embryo
Trematoda Eggs Cretaceous Archosaur (?dinosaur) Poinar and Boucot (2006)
Dicrocoelidae Eggs Pleistocene Mammal (?bear) Jouy-Avantin et al. (1999)
Schistosomatidae Schistosome-like eggs Holocene Ground sloth Schmidt et al. (1992)
(Nothrotheriops
shastensis)
Nematoda
? Larvae Pleistocene Hyenid Ferreira et al. (1993)
Ascaridomorpha Eggs Triassic Cynodont Da Silva et al. (2014)
Oxyurida Eggs Triassic Cynodont Hugot et al. (2014)
(Continued)

23
Table 3 Coprolites depicting fossil and archaeological evidence for parasitic organismsdcont'd

24
Taxonomic affinity Fossil evidence Age Host References
Ascaridomorpha Egg þ developing Cretaceous Archosaur (?dinosaur) Poinar and Boucot (2006)
larvae
Heterakoidea aDNA Holocene Archosaur Wood et al. (2013b)
(Anomalopteryx,
Dinornis, Pachyornis,
Megalapteryx)
Trichocephalida Eggs (Trichuris) Pleistocene Hyenid Ferreira et al. (1991)
Acanthocephala
? Eggs Holocene Humans Fry and Hall (1969)
Eggs (Echinopardalis) Holocene Felidae Noronha et al. (1994)
Arthropods
Ticks Body remains Holocene Humans Johnson et al. (2008)

Kenneth De Baets and D. Timothy J. Littlewood


Lice Body remains Holocene Humans Fry (1977)
Fungi
Plant-parasitic fungi Spores Cretaceous Archosaur (?dinosaur) Sharma et al. (2005)
Plants
Root-parasite Pollen (Dactylanthus Holocene Kakapo (Strigops Wood et al. (2012)
taylorii) habroptilus)
The Importance of Fossils in the Evolution of Parasites 25

the potential to reveal past parasite infections, as demonstrated by reports of a


putative trypanosome from faecal droplets found in association with a fossil
triatomine in Dominican amber (Poinar, 2005c). Protozoa remains have also
been reported from the abdominal region of Miocene Tapir remains
(McConnell and Zavada, 2013) as well as in termites preserved in amber
(Poinar, 2009).
Egg remains are usually considered trace fossils, but they can occasionally
contain remains of developing embryos (Poinar and Boucot, 2006;
Dentzien-Dias et al., 2013), which are body fossils. Interestingly, parasite
eggs have often been found in coprolites or fossilized faeces, which are trace
fossils themselves. Some of these coprolites range back to the Palaeozoic
(Zangerl and Case, 1976; Dentzien-Dias et al., 2013) or Mesozoic periods
(Poinar and Boucot, 2006; Da Silva et al., 2014; Hugot et al., 2014),
although most are known from the Cenozoic, particularly the Quaternary
era (Ferreira et al., 1991; Jouy-Avantin et al., 1999; Gonçalves et al.,
2003). As some of these eggs can be quite resistant to decay, they can also
be found in Quaternary sediments, particularly in archaeological sites
(Bouchet et al., 2003; Gonçalves et al., 2003; Ara ujo et al., 2015). In other
cases, parasite eggs have been reported associated with Cretaceous fossil
feathers (Martill and Davis, 1998) or Eocene mammal hair in Baltic amber
(Voigt, 1952; Nagler and Haug, 2015).
Remains of fossil parasites have typically been revealed through destruc-
tive preparation (e.g. thin sectioning, dissolution/rehydration methods) and
classical imaging methods leaving little chance for further study, or have
been missed or destroyed because of techniques designed to reveal structures
of the hosts to which they are associated. Traditional methods of parasite
recovery from coprolites, or other ancient samples, can be combined with
aDNA techniques (Wood et al., 2013b; Ara ujo et al., 2015) or computed
tomography.
Sequencing of aDNA might successfully detect very small and/or fragile
parasites that may not preserve intact in coprolites, or can be destroyed dur-
ing the extraction or preparation methods. This method is however also
destructive (e.g. samples need to be rehydrated to extract DNA) and
restricted to younger (archaeological) samples due to the rapid deterioration
of DNA/RNA, making computer tomography particularly important to
identify parasites for older (fossil) samples.
Tomographic methods might help to reveal additional details of fossils
trapped in amber as well as help to discover parasites in coprolites or other
ancient remains which can be destroyed during the traditional destructive
26 Kenneth De Baets and D. Timothy J. Littlewood

preparation processes. The potential of these windows into parasite evolu-


tion has become clear in the last two decades by multiple new discoveries,
particularly in marine and terrestrial coprolites (Table 3) as well as in amber
fossils (Tables 1, 2). Parasitic remains in fossil coprolites have been reported
for a long time (Zangerl and Case, 1976), but were usually received with a
certain degree of scepticism (Boucot, 1990; Poinar, 2003). Various methods
can yield high-resolution reconstructions of microscopic remains or struc-
tures in larger fossils including mCT-scanning or phase-contrast synchrotron
tomography (Donoghue et al., 2006; Sutton et al., 2014), but their useful-
ness depends on the contrast between the fossils and the matrix. Computed
tomography can not only be relevant to identify and characterize parasite re-
mains, perhaps to place them in extant phylogenies (Faulwetter et al., 2013;
Garwood and Dunlop, 2014), but also to quantify their original position, 3D
structure and morphology or association in coprolites or other ancient re-
mains (Dunlop et al., 2012; Siveter et al., 2015). It could potentially be
used to study the presence of developing embryos (Donoghue and Dong,
2005; Donoghue et al., 2006; Duan et al., 2012), which have been suggested
to be present in some fossil eggs attributed to helminths based on traditional
imaging methods (Poinar and Boucot, 2006; Dentzien-Dias et al., 2013).
These could even provide supplementary information on the morphology
and content of the coprolites, which could make it possible to more confi-
dently identify their host, the coprolite producers, as well as give indications
about possible predatoreprey relationships and parasite load. In archaeolog-
ical studies, coprolites can be quantitatively studied to establish changes in
biogeographic distributions and habits of their hosts (Ara ujo et al., 2015;
Mitchell, 2015) as well as on parasite body size changes (Fugassa et al.,
2008). Additional data are required to quantitatively study these aspects
on longer (palaeontological) timescales as the parasitological coprolite studies
are still quite patchy in space and time.

4. MOLECULAR PERSPECTIVES ON PARASITE


PHYLOGENY AND EVOLUTION
Historically, for many taxonomic groups of parasites, morphologically
based systematic schemes and phylogenies have been difficult to resolve
even in the light of additional sampling or analysis. Parasites often demonstrate
high degrees of specialization compared with their free-living relatives, high
degrees of reduction or apparent simplification, specialization and/or conver-
gence in morphology related to their parasitic lifestyle. Complex life cycles
The Importance of Fossils in the Evolution of Parasites 27

involving multiple hosts or even a single host can consist of morphologically


distinct ontogenetic stages making homology assessment and the identifica-
tion of shared features even more difficult (Brooks and McLennan, 1993).
Molecular methods have the potential to resolve many problems where
morphology has been problematic, as long as one can properly deal with
biases and spurious signal related to long-branch attraction, sampling,
(host) contamination and other issues arising from a purely molecular
approach (Edgecombe et al., 2011). Contamination is not only relevant
for aDNA (Shapiro and Hofreiter, 2014), but might also be responsible
for wrong assignment of various groups of extant parasites. Previously erro-
neous assignment of Myxozoa, including the vermiform Buddenbrockia, with
other taxa has been attributed to host contamination (Jiménez-Guri et al.,
2007). On the other hand, molecular studies have had a considerable impact
on the assignment of some parasite groups within the broader context of
metazoan evolution (Zrzavý, 2001; Edgecombe et al., 2011). For example,
pentastomids, long considered to be a separate phylum, are now considered
to be closely related to fish lice based on molecular evidence (Sanders and
Lee, 2010; Oakley et al., 2012). Also, Myxozoa are now considered to be
cnidarians based on molecular evidence (Jiménez-Guri et al., 2007;
Hartikainen et al., 2014; Okamura and Gruhl, 2015; Okamura et al.,
2015). The phylogenetic position of myzostomids has also been long
debated, but most authors now agree that they belong within the Annelida
based on molecular analyses (Parry et al., 2014; Summers and Rouse, 2014).
The discovery of Chromera velia, the first photosynthetic apicomplexan
with a fully functional plastid, might also provide a powerful model to study
the evolution of parasitism in Apicomplexa. Molecular analyses indicate that
it is the closest relative to apicomplexan parasites, indicating that the plastid
of this coral symbiont shares its origin with the apicoplasts (Moore et al.,
2008; Okamoto and McFadden, 2008).
Acanthocephala (thorny-headed worms) were occasionally compared to
priapulids (penis worms) based on morphological evidence (Conway Morris
and Crompton, 1982), but are now aligned with Rotifera within the
Syndermata (Weber et al., 2013; Wey-Fabrizius et al., 2013). Most recent
molecular studies with greater coverage indicate a particular route to para-
sitism within Platyhelminthes and a closer relationship between cestodes
and trematodes (Lockyer et al., 2003; De Baets et al., 2015a; Egger et al.,
2015; see Littlewood and Waeschenbach, 2015 for a review), although there
are some exceptions (Laumer et al., 2015), which illustrate that the relative
importance of particular gene regions needed to disentangle phylogenetic
28 Kenneth De Baets and D. Timothy J. Littlewood

relationships still need to be better understood. A recent molecular study


(Struck et al., 2014) also indicates that the Platyzoa, which groups Acantho-
cephala and Platyhelminthes among various free-living taxa, is probably an
artefact of long-branch attraction, whereby distantly related lineages are
incorrectly inferred to be closely related because both lineages have under-
gone a considerable amount of change. This theory has since been
confirmed by Egger et al. (2015), who demonstrated that only the fast-
evolving quartile of their transcriptomic dataset supported the Platyzoa.
Importantly, in the absence of phylogenetic artifacts, molecular studies
can be used to investigate the origins and radiations of parasitic lineages.
This has been shown for acanthocephalans (Near, 2002; Wey-Fabrizius
et al., 2014), parasitic flatworms (Lockyer et al., 2003), myzostomid annelids
(Summers and Rouse, 2014) and nematodes (Dorris et al., 1999; Blaxter,
2003; Blaxter and Koutsovoulos, 2015). Sister-group relationships within
and between parasite lineages, the determination of free-living sister groups
and the inference of ancestral life history strategies are key to determine the
origins of parasitism and the evolution of complex life cycles. The evolution
of complex life cycles is a major research question, with two main mecha-
nisms proposed (Parker et al., 2015): upward incorporation by terminal
addition of hosts, or downward incorporation by addition of intermediate
hosts. Cladistic studies, or the application of parsimony principles to infer
ancestral life cycles, have yielded some controversial hypotheses as to the or-
igins and development of ontogenetic sequences (O’Grady, 1985). In para-
sitic flatworms (Neodermata), complex parasite life cycles appear to have
initially evolved by the addition of intermediate hosts, with vertebrate defin-
itive hosts argued to be the plesiomorphic condition for stem group neoder-
matans (Littlewood et al., 1999); the scenarios are inferred from molecular
phylogenies of extant taxa; however, fossil vertebrates may yet hold the
key to verifying or at least supporting this claim.
Since their initial application, molecular clock methodologies have
undergone major developments (Bromham and Penny, 2003; W€ orheide
et al., 2015), with ever more sophisticated models accommodating large
genomic datasets, rate variation and the uncertainties of multiple types of
calibration points (Parham et al., 2012; Ho, 2014). Nevertheless, molecular
clocks still need age constraints from the fossil record or other lines of
evidence to provide calibration points for at least one or more nodes in a
calibrated phylogeny (Ho and Phillips, 2009; Hipsley and M€ uller, 2014;
Warnock, 2014). The use of fossils in molecular clocks has changed in the
last decades (Parham et al., 2012; Ho, 2014; W€ orheide et al., 2015)
The Importance of Fossils in the Evolution of Parasites 29

including their implementation as probabilistic time priors (Ho and Phillips,


2009; Warnock et al., 2015) and tip calibrations integrated among their
living relatives by combing molecular and morphological evidence (Pyron,
2011; Ronquist et al., 2012; Wood et al., 2013a; Arcila et al., 2015). How-
ever, methods using other types of age evidence like geological calibrations
(e.g. vicariance events) or host calibrations lag behind in their development
and leave them heavily scrutinized (Goswami and Upchurch, 2010; Kodan-
daramaiah, 2011; Hipsley and M€ uller, 2014).
Finally, advances in molecular techniques have provided additional
advances in unravelling past events. aDNA techniques have made it possible
to obtain pathogen DNA from dated ancient parasites or host remains
(Dittmar, 2009; Bos et al., 2015; Hofreiter et al., 2015). Although many
of these studies have been targeted in their approach, there are also those
that have characterized complete biomes (Rawlence et al., 2014); for
example, detection and characterization of bacteria entombed in dental
calculus (Warinner et al., 2015), and the discovery of subfossil coprolites
(Santiago-Rodriguez et al., 2013; Wood et al., 2013b; Cano et al., 2014)
has opened up new avenues in palaeomicrobiology.

4.1 Molecular clocks


The ancient origin of parasitism is suggested by the deep-branching position
of various parasitic lineages within the tree of life as well as the extrapolation
of extant parasite host associations. In prokaryote and unicellular eukaryote,
parasitic relationships might have already existed in the Precambrian,
although so far no direct fossil evidence has been found. For metazoan par-
asites, for which the fossil constraints are better than they are for unicellular
organisms, parasitism must have evolved at least for some groups during or
slightly before the Cambrian explosion in the marine realm. This is corrob-
orated by the earliest sign of parasitism by an unknown metazoan parasite in
Cambrian brachiopods (Bassett et al., 2004) and body fossil remains of
various pentastomid taxa from the CambrianeOrdovician (Castellani
et al., 2011). Additional indications for parasitism are also found in other
Lower Palaeozoic groups like Ordovician graptoloids (hemichordates)
(Bates and Loydell, 2000) as well as in Silurian echinoderms (Franzen,
1974) and bivalves (De Baets et al., 2015a), although the exact identity of
the culprits is unknown. Based on extrapolation of extant host-associations,
the origin of parasitic flatworms and some lineages of parasitic nematodes
have also been estimated to lie in the CambrianeOrdovician (Littlewood,
2006; Poinar, 2011a, 2015a). Since the assignment of Cambrian
30 Kenneth De Baets and D. Timothy J. Littlewood

Cambroclavida (a group of enigmatic, phosphatized, hollow spine-shaped


sclerites) to Acanthocephala (Qian and Yin, 1984) is unsubstantiated (Kou-
chinsky et al., 2012), the earliest confidently assigned ancient acanthoceph-
alan remains are eggs derived from Quaternary archaeological sites (Fry and
Hall, 1969; Noronha et al., 1994). The earliest metazoan helminth remains
are circlets of hooks from Middle Devonian fishes (Upeniece, 2001),
although their systematic affinity is still unclear (Littlewood and Donovan,
2003; De Baets et al., 2015a). So far no direct unequivocal evidence for
metazoan parasites has been discovered in the Precambrian. Ediacaran fossils
like Dickinsonia have occasionally been compared with Spinther (Wade,
1972; Conway Morris, 1981), an annelid parasite of sponges (Rouse,
2005b). This comparison proved to be superficial at best and they are
now often interpreted to be more basal metazoans (Xingliang and Reitner,
2006; Sperling and Vinther, 2010), although the exact systematic position of
Dickinsonia remains highly controversial (Retallack, 2007; Brasier and Ant-
cliffe, 2008). More importantly, no evidence for a parasitic relationship of
Dickinsonia with other taxa could be evidenced. A parasitic mode of life of
Dickinsonia would be rather absurd too as it would mean the presence of
hosts which would have to be considerably larger than Dickinsonia, which
have remained unnoticed in the fossil record.
Considering that bacteria, viruses and various other unicellular to multi-
cellular eukaryotes have evolved before this time, many could have already
evolved towards parasitism in the Precambrian. The discovery that the
closest relative of parasitic apicomplexans is a coral symbiont might suggest
that modern parasites may have started out as mutualistic metazoan symbi-
onts before turning to parasitism (Moore et al., 2008). It has, therefore, been
suggested that symbiotic/parasitic relationships in dinoflagellates and Api-
complexa might have extended back in evolutionary time to the earliest or-
igins of Metazoa, which means that either as parasites or symbionts, these
protists have been interacting with the metazoan immune system since their
inception (Okamoto and McFadden, 2008). However, calibrating molecu-
lar clocks to test such hypotheses remains a challenge (Bensch et al., 2013).
Parasitism-like life history patterns probably first evolved in the sea, but it
is unclear if parasites closely tracked the terrestrialization of their hosts. In
some cases this might have been true, as indicated by nematode remains
in early diverging land plants from the Early Devonian (Poinar et al.,
2008), although both plants and nematodes might have colonized the
land considerably earlier based on molecular clock estimates (Clarke et al.,
2011; Rota-Stabelli et al., 2013). In other cases it is less clear as the earliest
The Importance of Fossils in the Evolution of Parasites 31

fossil evidence for terrestrial parasitism in these lineages considerably predates


the presumed origin of their host taxa (e.g. vertebrates or arthropods). How-
ever, various groups of terrestrial vertebrates (archosaurs, synapsids) were
already parasitized in now extinct lineages leading up to currently infested
host taxa (Poinar and Boucot, 2006; Da Silva et al., 2014). Although para-
sitism evolved in the sea, using this premise to constrain molecular clocks
might be dangerous in particular cases; as is the case for various groups of
nematodes parasitizing shallow marine to intertidal taxa, which have evolved
convergently from terrestrial ancestors (Sudhaus, 2010).
The fossil record can only provide minimum constraints on the origin of
parasitism, but molecular clocks might be an alternative to dating important
events without relying on recent evidence of parasiteehost associations or
the evolutionary history of their hosts. The calibration of molecular clocks
in pathogens with a poor fossil record like viruses, bacteria, protozoa (Bensch
et al., 2013; Frías et al., 2013) or soft-bodied helminths (De Baets et al., 2015a)
is not straightforward. The direct record is largely restricted to more recent
Quaternary sites, particularly archaeological sites (Ara ujo et al., 2015;
Mitchell, 2015) which can put important constraints on shallower nodes in
phylogenies, although deeper nodes, particularly the root, in phylogenies
are more crucial for dating (Warnock et al., 2012; Mello et al., 2014). Further-
more, most authors agree that multiple calibration points implemented faith-
fully across a phylogeny are ideal in achieving accurate and precise divergence
estimates. However, these calibration points should be screened and selected a
priori, rather than using posteriori selections methods, which evaluate
congruence through cross-validation, as the latter can lead to selection of
congruent, erroneous calibrations (Warnock et al., 2015).
Nevertheless, the summary above shows that the body fossil record offers
confident minimum constraints for various lineages of parasites, when crit-
ically evaluated. Various methods have been developed to estimate diver-
gence times based on the stratigraphic distribution of fossil data
(Wilkinson et al., 2011; Nowak et al., 2013; Heath et al., 2014), but most
studies apply phylogenetic bracketing (M€ uller and Reisz, 2005; Benton
and Donoghue, 2007) or probability functions that express some predefined
perception of the degree to which fossil minima approximate the true time
of divergence (Ho and Phillips, 2009). The latest tip-calibration or total ev-
idence dating methods (Pyron, 2011; Ronquist et al., 2012; Wood et al.,
2013a) allow fossils to be integrated into divergence time studies among
their living relatives, using combined morphological and molecular datasets
and evolutionary models. These have been shown, however, to yield
32 Kenneth De Baets and D. Timothy J. Littlewood

unexpectedly old age estimates of clades (Arcila et al., 2015) and their per-
formance needs to be more extensively tested. Furthermore, such methods
might be difficult to apply to soft-bodied taxa as crucial morphological char-
acters required to confidently place them in extant phylogenies might be ab-
sent or limited in fossil parasite specimens.
Computed tomography will be important to reveal additional details of
the morphology and structure of putative body fossils, which will make it
possible to assign them more accurately to extant lineages. In some cases,
the nearest free-living relatives have a good fossil record, which can be
used to put constraints on early nodes in molecular clocks. Interestingly,
this is not always the case. In some soft-bodied helminths, the body fossil
record of parasitic forms is even richer (at least less poor) than that in their
free-living relatives, such as amongst Platyhelminthes (Poinar, 2003; De
Baets et al., 2015a) and Nematoda (Poinar, 2011a, 2015a). Their fossil re-
cord remains are rare in time and space due to their restriction to sites of
exceptional preservation, but can potentially still be valuable to place con-
straints on the evolution of these groups as a whole. In the absence of reliable
body fossils, characteristic traces or pathologies could potentially also be used
to put constraints on certain nodes and computed tomography could also be
possibly used to characterize those (Dittmar et al., 2011). Unfortunately,
skeletal responses to parasitism are still comparatively poorly studied, partic-
ularly in extant taxa (Zibrowius, 1981; Ituarte et al., 2001, 2005; Keupp,
2012; Klompmaker et al., 2014). This makes interpretation of fossil traces
even more open to interpretation as they could also have been made by a
different group of organisms with a similar behaviour, but not necessarily
closely related. It therefore probably makes more sense to avoid using
them to constrain molecular clocks directly. Molecular clocks constrained
by other types of evidence (e.g. body fossils or geological events) could how-
ever be used to test the appearances of these skeletal responses.
Problematically, the fossil record does not yield body fossils or other re-
mains for multiple lineages of unicellular pathogens or soft-bodied metazoan
parasites (e.g. Myxozoa, Argulidae). In these cases, it is therefore necessary to
look for and select suitable alternatives, or supplementary ways, to constrain
the molecular clock (Bensch et al., 2013; De Baets et al., 2015a; Héritier
et al., 2015). Such solutions potentially lie in the host fossil record or biogeo-
graphic events, which have left a footprint of divergence among
evolutionary lineages. Unfortunately, host or biogeographic calibrations
have not received the same scrutiny and refinement as fossil calibrations
(Kodandaramaiah, 2011; De Baets and Donoghue, 2012; Parham et al.,
The Importance of Fossils in the Evolution of Parasites 33

2012; Hipsley and M€ uller, 2014). Biogeographic dating often relies on


geochronologically or otherwise geologically dated events. As they are
currently implemented, biogeographic calibrations and their age evidence
are rarely if ever justified; they often assume the biogeography of living or-
ganisms is a faithful reflection of ancestral distribution, which is not always,
or even rarely, the case as they might have been modified or even reset by
subsequent events. Some exceptions have been suggested in parasites but
these still need to be tested; for example, the cestode Nesolecithus and the
nematode Nilonema have an apparent Gondwanaland origin with their
present day distribution in Africa and South America (Gibson et al., 1987;
Santos and Gibson, 2007). Furthermore, tectonic episodes are protracted
and might have different impacts on lineages depending on their ecology.
These limitations can be partially overcome or at least controlled like fossil
calibrations, by implementing them in the most conservative way as proba-
bilistic constraints that span an interval of time, which takes into account
these factors (Warnock, 2014). Parasitologists often extrapolate extant
parasiteehost or biogeographic relationships to estimate the evolutionary
origin of parasites (Mejía-Madrid, 2013 for a review) or more rarely to cali-
brate molecular clocks, which can introduce a factor of circularity when
testing hypotheses of evolutionary changes in parasiteehost associations or
biogeographic distribution (Trewick and Gibb, 2010; Crisp et al., 2011;
Kodandaramaiah, 2011; Hipsley and M€ uller, 2014). Although some of these
hypotheses do stand the test of additional sampling of extant or fossil forms,
others do not if quite different host associations or biogeographic distribu-
tions are recovered. Caution should be always taken as the fossil record
also yields evidence of parasitic lineages and parasiteehost associations which
are now clearly extinct (Upeniece, 2001; Poinar and Boucot, 2006;
Castellani et al., 2011; Upeniece, 2011; Chen et al., 2014). Biogeographic
distributions of their hosts and potentially that of their parasites might also
have differed considerably in the past. Therefore, assumptions should be
at least consistent with the fossil evidence and robust molecular clock
estimates of their hosts. Not only does the fossil record provide direct and
indirect evidence for the presence of certain parasite lineages, but it can
also provide evidence for infection intensity, host response (developmental,
pathological), novel (potentially extinct) host associations and parasite life
cycles. Likewise, ancestral state reconstruction of host associations and life
cycles (host use and complexity) from phylogenies, combined with calibra-
tions can inform the interpretation of body fossils and inferred chronologies
(Zhu et al., 2015). All factors considered, we should prefer to have an
34 Kenneth De Baets and D. Timothy J. Littlewood

accurate timescale that might lack precision, than a precise timescale that
lacks the necessary accuracy (De Baets et al., 2015a). Even if no suitable cali-
bration points can be found, methods have been developed, which can
compare the relative molecular rates of groups to test the hypotheses of
co-divergences (Loader et al., 2007; Hibbett and Matheny, 2009; Loss-Oli-
veira et al., 2012; Silva et al., 2015).

4.2 HGT and ‘parasitic DNA’


Even for groups where no fossil biomolecules have been found, for example,
viruses or symbionts, parasites can leave footprints in their hosts’ genomes
(Gilbert and Feschotte, 2010; Thézé et al., 2011; Katzourakis, 2013;
Koutsovoulos et al., 2014). Interrogation of genomes has made it possible
to identify horizontal transfers of genetic elements (HGTs) in the deep
history of living organisms. HGTs are the transfer of DNA between two
nonvertically related individuals belonging to the same or different species
(Sj€
ostrand et al., 2014). Some of these transfers retain an apparent parasitic
role (Kidwell and Lisch, 2001) or become integrated into biochemical
pathways that are functionally important in lineages that become parasitic
(Alsmark et al., 2013).
Comparison of such genomic signatures between species provides a
means of determining their origins, diversification and change through
time. Studies have focused particularly on ancient viruses (Gilbert and
Feschotte, 2010; Thézé et al., 2011; Gifford, 2012; Herniou et al., 2013;
Lee et al., 2013), typically revealing ‘hosteparasite’ interactions over
prehistoric or geological timescales. There is increasing evidence that
HGTs have left genomic signatures of other more highly organized symbi-
onts like bacteria in their metazoan host genomes, too (Cerveau et al., 2011;
Koutsovoulos et al., 2014). Things may be even more complicated as evi-
dence of HGT may have occurred between various types of endosymbiotic
bacteria (Duron, 2013) or viruses within their hosts (Niewiadomska and
Gifford, 2013). There is no physical ‘fossil record’ of these viruses or signa-
tures (Katzourakis and Gifford, 2010; Katzourakis, 2013), and their long
unchanged history is inferred such that they cannot be referred to as
genomic ‘fossils’ as such. However, further evidence of historical hoste
parasite interactions will undoubtedly arise from future genomic studies of
both hosts and parasites, although an understanding of the role of HGT in
eukaryotes is still in its infancy (Hirt et al., 2015).
HGT events are common in prokaryotes and many microbial eukary-
otes, but are expected to become more commonly detected in multicellular
The Importance of Fossils in the Evolution of Parasites 35

eukaryotes as more is known about their genomes (Andersson, 2005). With


microbial phylogenies, HGTs are important in revealing which evolutionary
lineages were concurrent and when speciation (or broader divergence)
events took place. By explicitly modelling the evolution of genes present
in genomes, Sz€ ollTsi et al. (2012) provided a chronologically ordered
phylogeny for cyanobacteria, validated against the groups’ good microfossil
record, thus showing that their methods can reveal and use HGTs as a source
of information on timing (or at least chronology) of evolutionary events.
Focusing on microbial eukaryotes, Alsmark et al. (2013) showed the pattern
of HGTs retained after parasite diversification are likely to be functionally
important for the parasites (e.g. in kinetoplastids and apicomplexans).
Similarly, there is strong evidence that multiple HGT events have promoted
the plant parasitism ability in some nematodes (Danchin et al., 2010).
There is increasing evidence that the role of HGTs in eukaryote evolution
is important, particularly in the evolution of resistance, and it does not seem
overly speculative to predict that signatures from hosteparasite interactions
will be found in more genomes. Further interrogation will reveal lineages
of parasites with genomic signatures of their long-associated histories with
their host groups, and vice versa; for example, Richards et al. (2011);
Wijayawardena et al. (2013); Davis and Xi (2015). In turn, this evidence
will provide indications as to when particular lineages came into contact
with one another, but the success of these leads in revealing accurate records
of historical interactions depends on greater study. Some recent claims of
HGT in multicellular parasites (e.g. schistosomes) have been discredited,
revealing the need to be wary of technical artifacts and gene conservation is-
sues before claims of HGT can be verified (Wijayawardena et al., 2015).

5. FUTURE PERSPECTIVES
Various new advances in ancient biomolecule detection and charac-
terization (Briggs and Summons, 2014) including aDNA (Dittmar, 2009,
2014; Wood et al., 2013b; Dittmar, 2014; Shapiro and Hofreiter, 2014;
Hofreiter et al., 2015), palaeoproteomics (Hofreiter et al., 2012), novel
development in molecular clock methodologies (Parham et al., 2012; Ho,
2014; W€ orheide et al., 2015) and new possibilities for the critical evaluation
and nondestructive analysis of 3D fossil structures by computed tomography
(Cunningham et al., 2014a,b; Sutton et al., 2014) offer many new prospects
and perspectives in palaeoparasitology.
36 Kenneth De Baets and D. Timothy J. Littlewood

ACKNOWLEDGEMENTS
We are very grateful to Andrea Waeschenbach and Rod Bray for constructive comments on
an earlier draft of the manuscript. The initial research leading to this article was partially
funded by an SNF-grant for Prospective Researchers to KDB (141438).

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CHAPTER TWO

The Geological Record of


Parasitic Nematode Evolution
George O. Poinar, Jr.
Department of Integrative Biology, Oregon State University, Corvallis, OR 97331, USA
E-mail: poinarg@science.oregonstate.edu

Contents
1. Introduction 54
2. Media for the Study of Fossil Nematodes 54
2.1 Amber 54
2.2 Rock fossils 54
2.3 Coprolites 55
3. Palaeozoic Parasitic Nematodes 55
4. Parasitic Nematode Body Fossils from the Mesozoic 55
5. Nematode Parasites from the Early Cenozoic 60
5.1 Baltic amber 60
6. Nematode Parasites from the OligoceneeMiocene 65
6.1 Dominican amber nematodes 65
6.2 Mexican amber nematodes 75
7. Nematode Parasites from the Pliocene 77
8. Nematode Parasites from the Pleistocene and Holocene 77
8.1 Nematode parasites of humans from the Pleistocene and Holocene 78
9. Stages in the Evolution of Nematode Parasites of Invertebrates 79
10. Origin of Nematode Parasites of Vertebrates 81
11. Origin of Nematode Parasites of Plants 83
12. Summary 83
Acknowledgements 86
References 86

Abstract
This chapter discusses the evolutionary history of nematode parasites of invertebrates,
vertebrates and plants based on fossil remains in amber, stone and coprolites dating
from the Palaeozoic to the Holocene. The earliest parasitic nematode is a primitive plant
parasite from the Devonian. Fossil invertebrate-parasitic nematodes first appeared in
the Early Cretaceous, while the earliest fossil vertebrate-parasitic nematodes are from
Upper Triassic coprolites. Specific examples of fossil nematode parasites over time
are presented, along with views on the origin and evolution of nematodes and their
hosts.
Advances in Parasitology, Volume 90
© 2015 Elsevier Ltd.
j
ISSN 0065-308X
http://dx.doi.org/10.1016/bs.apar.2015.03.002 All rights reserved. 53
54 George O. Poinar, Jr.

1. INTRODUCTION
The body fossil record of parasitic nematodes is limited by their small
size and soft bodies (Littlewood and Donovan, 2003). While parasitic forms
can reach up to several metres in length (Yeates and Boag, 2006), decompo-
sition after death is quite rapid, and sclerotized structures that could be fossil-
ized are microscopic, which makes them extremely difficult to locate. While
some nematodes have been preserved in fine-grained cherts dating back to
the Devonian, fossilized resin (amber) and coprolites have been the most use-
ful media for studying the evolution and early hosts of parasitic nematodes.

2. MEDIA FOR THE STUDY OF FOSSIL NEMATODES


2.1 Amber
Amber is fossilized tree resin that preserves a wide range of organisms,
from microbes to vertebrates (Poinar, 1992). Preservation appears to be the
result of inert dehydration and fixation by natural plant products in the orig-
inal resin. The occurrence of parasitic nematodes in fossilized resin is
frequently associated with the habits of their hosts, the great majority of
which are forest living arthropods (cf. Poinar, 2011). The urge of parasitic
nematodes to escape from hosts that become entrapped in tree resin, even
if they have not completely finished their development, provides most of
our fossil records of parasitic nematodes.
Amber-containing parasitic nematodes extend from the early Cretaceous
(130e135 mya) to the Miocene (15e20 mya). Dating of amber deposits is
usually based on fossils in the surrounding bedrock. Using this method,
Dominican amber has been dated at 20e45 mya (Cepek in Schlee, 1990;
Iturralde-Vincent and MacPhee, 1996; Iturralde-Vinent, 2001), Mexican
amber at 22e26 mya (Poinar, 1992), Baltic amber, 40e50 mya (Larsson,
1978), Burmese amber, 97e110 mya (Cruickshank and Ko, 2003) and Leb-
anese amber, 130e135 mya (Poinar and Milki, 2001). Geological ages
mentioned here are based on Gradstein et al. (2012). Taxonomic groupings
of nematode categories follow treatments of De Ley and Blaxter (2004),
Eyualim-Abebe et al. (2006) and Poinar (2011).

2.2 Rock fossils


Nematode remains in sedimentary deposits mostly occur as compression fos-
sils with only the body outline and external ornamentation evident.
The Geological Record of Parasitic Nematode Evolution 55

However, in some fine-grained sedimentary deposits known as Lagerst€atten,


sclerotized parts such as onchia and spicules, and occasionally even portions
of the alimentary and reproductive systems (Poinar, 2011) can be found.
In some rare instances where silica and other dissolved minerals impreg-
nate rocks, nematodes inside can be preserved in amazing detail. This type of
permineralization has provided us with the earliest record of parasitic nem-
atodes from the Early Devonian Rhynie Chert (Poinar et al., 2008).

2.3 Coprolites
Analysis of lithified coprolites dating back millions of years (e.g. Poinar and
Boucot, 2006; Da Silva et al., 2014; Hugot et al., 2014) and desiccated dung
of more recent ages (Poinar, 2014) can reveal the presence of vertebrate-
parasitic nematodes. Ancient dung samples also are one of the best resources
for establishing early records of human nematode parasites (Gonçalves et al.,
2003). However, it can be difficult to distinguish between actual nematode
parasites and microbotrophic nematodes that entered the dung after it was
deposited (Poinar, 1983).

3. PALAEOZOIC PARASITIC NEMATODES


The only Palaeozoic body fossil of a parasitic nematode is the Early
Devonian Rhynie Chert plant-parasitic nematode, Palaeonema phyticum
Poinar et al. (2008) (Figure 1). Eggs, juveniles and adults were present in
the stomatal chambers of the Early Devonian (396 mya) land plant, Aglao-
phyton major Kidson & Lang. Their presence provides the earliest evidence
of a symbiotic association between terrestrial plants and animals and repre-
sents an early stage in the evolution of plant parasitism by nematodes and
their presence on land.

4. PARASITIC NEMATODE BODY FOSSILS FROM THE


MESOZOIC
The oldest animal-parasitic nematodes have recently been found in
Triassic cynodont coprolites in Brazil. These include a 240 mya ascarid,
Ascarites rufferi Da Silva et al. (2014) and a 240 mya old oxyurid, Paleoxyuris
cockburni Hugot et al. (2014). The next oldest member of this group is the
130 mya mermithid, Cretacimermis libani Poinar et al. (1994) from Early
Cretaceous Lebanese amber. The single specimen was coiled up in the
body cavity of an adult midge (Chironomidae: Diptera) (Figure 2).
56 George O. Poinar, Jr.

Figure 1 Palaeonema phyticum Poinar et al., 2008 surrounded by cortical cells of Aglao-
phyton major in Devonian Rhynie Chert, Aberdeen, Scotland (Scale bar ¼ 59 mm).

Figure 2 The mermithid, Cretacimermis protus Poinar and Buckley, 2006 emerging from
a biting midge in Early Cretaceous Burmese amber (Ron Buckley amber collection)
(Scale bar ¼ 1 mm).
The Geological Record of Parasitic Nematode Evolution 57

Infection was probably initiated in the larval stage of the midge and the
parasite was carried through the pupal and into the adult stage. Such hoste
parasite associations still occur today (Poinar and Poinar, 2003).
Mid-Cretaceous Burmese amber contains both plant and animal nema-
tode parasites. A small population of the fungal-feeding aphelenchoidid,
Cretaciaphelenchoides burmensis Poinar (2011), together with mycelium, pro-
vides the earliest record of mycetophagous nematodes. Adult males and
females, as well as resistant juvenile stages were present. The nematodes
could have been carried to the site by wood-boring insects, as occurs in
extant members of the family (Hunt, 1993).
A snail in Burmese amber with juveniles of Palaeocosmocerca burmanicum
Poinar (2011) adjacent to its mantle cavity provide early evidence of the
family Cosmocercidae. Features of the fossil nematodes resemble those of
the extant snail parasite, Cosmocercoides dukae (Anderson, 1960). The adults
of C. dukae live in the intestinal tract of the snail, and second stage juveniles
and third stage infectives occur in the mantle cavity. A sibling species of C.
dukae occurs in the rectum of frogs and toads (Harwood, 1930; Vanderburgh
and Anderson, 1987), but it is likely that molluscs were the original host of
Cosmocercoides spp.
Oxyurids may be the first nematodes to form parasitic associations with
terrestrial animals, beginning with invertebrates and then expanding their
host range to vertebrates. While the origin of oxyurids could extend back to
the Silurian based on the earliest fossils of their millipede hosts (Wilson and
Anderson, 2004), when they first invaded insects is unknown. The thelasto-
matid, Paleothelastoma tipulae Poinar (2011) adjacent to a cranefly in Burmese
amber (Figure 3) establishes the earliest fossil record of this group in inverte-
brates. Extant craneflies are common hosts of thelastomatids (Poinar, 1975).

Figure 3 The thelastomatid, Paleothelostoma tipulae Poinar (2011) (arrow) adjacent to


its tipulid host in Early Cretaceous Burmese amber (Scale bar ¼ 251 mm).
58 George O. Poinar, Jr.

Figure 4 Proheterorhabditis burmanicus Poinar (2011) (arrow) adjacent to its beetle host
in Early Cretaceous Burmese amber (Scale bar ¼ 152 mm).

Entomopathogenic nematodes, for example those whose infective stages


carry symbiotic bacteria in their gut and release them in a potential host, date
back to the Early Cretaceous with Proheterorhabditis burmanica Poinar (2011)
and its rove beetle (Staphylinidae) host in Burmese amber (Figure 4). Rod-
shaped bacteria similar to those associated with extant species of Heterorhab-
ditis occurred in the fossil rove beetle.
Mermithid nematodes emerging from insects also occur in Burmese
amber. Two specimens of Cretacimermis chironomae Poinar (2011) were asso-
ciated with an adult chironomid midge. These specimens, as well as Creta-
cimermis lebani from Lebanese amber, show that mermithid parasitism of
the Chironomidae occurred in Laurasia and Gondwanaland in the Early
Cretaceous.
The Burmese amber mermithid, Cretacimermis protus Poinar and
Buckley (2006) parasitized biting midges (Ceratopogonidae) of the genera
Atriculoides Remm and Leptoconops Skuse (Poinar and Monteys, 2008)
(Figure 5).
Extant species of Leptoconops feed on the blood of mammals, birds and
reptiles. While the genus Articulicoides is now extinct, it is likely that the
females also fed on vertebrate blood (Szadziewski and Poinar, 2005).
An analysis of an dinosaur coprolite from the Early Cretaceous Iguan-
odon shaft in Belgium revealed ascarid eggs. The egg of Ascarites priscus
Poinar and Boucot (2006) (Figure 6) still had its outer mammillated surface
and contained a developing juvenile nematode.
The Geological Record of Parasitic Nematode Evolution 59

Figure 5 The mermithid, Cretacimermis protus Poinar and Buckley, 2006 emerging from
a biting midge in Early Cretaceous Burmese amber (Scale bar ¼ 1 mm).

Figure 6 Egg of the early Cretaceous Ascarites priscus Poinar and Boucot, 2006 in a
coprolite of the predatory dinosaur, Megalosaurus from the Bernissant Wealden Iguan-
odon locality in Belgium (Scale bar ¼ 11 mm).
60 George O. Poinar, Jr.

Nematodes that occur in extant foraminifera tests provide a challenge to


both biologists and paleontologists. Sliter (1971) found nematodes living
within borings in the tests of the foraminifera Rosalina globularis d’Orbigny
and Bolivlina doniezi Cushman and Widkenden off Southern California
and felt that the borings were made by the nematodes rather than by
some other invertebrate. Later, other nematodes recovered from forami-
nifera tests were identified as Syringonomous typicus Hope and Murphy
(1969), Smithsoninema inaequale Hope and Tchesunov (1999) and an unde-
scribed species (Myers, 1943). Sliter (1971) used identical borings in bathyal
and neritic Cretaceous foraminifera to determine the distribution and abun-
dance of marine nematodes. Additional studies are needed to verify the abil-
ity of specialized groups of nematodes to bore through the shells of
foraminifera before fossil tests with bore holes can be used to establish the
presence of marine nematodes.

5. NEMATODE PARASITES FROM THE EARLY


CENOZOIC
5.1 Baltic amber
A wide range of parasitic nematodes occur in Baltic amber. Myce-
tophagous parasites include a reproducing population of the aphelenchoidid,
Palaeoaphelenchoides balticus Poinar (2011) that were probably feeding on
fungi on the resin-producing tree. There are many extant nematodes that
live in the tunnels of bark beetles and develop on fungi in the insect galleries.
A number of mermithids occur in Baltic amber, especially as parasites of
the family Chironomidae. The first one described in 1866, Heydenius matu-
tinus (Menge, 1866) is now considered a collective species for all mermithids
parasitizing chironomid midges in Baltic amber (Figure 7). While there may
be several genera and species involved, the absence of diagnostic characters
prohibits further identification.
It is unusual to find nematodes in coal deposits, but Heydenius antiqua
(von Heyden) was found protruding from the body of a long-horned beetle
(Coleoptera: Cerambycidae) in German brown coal strata (von Heyden,
1860), showing that mermithid lineages were parasitizing Coleoptera by
the Eocene.
Extant ants are known to host a number of mermithids and this parasitic
association dates back at least to the Eocene, as shown by Heydenius formicinus
Poinar (2002) emerging from a winged male of Prenolepis henschei Mayr in
Baltic amber (Figure 8).
The Geological Record of Parasitic Nematode Evolution 61

Figure 7 Two specimens of Heydenius matutinus (Menge, 1866): one completely


emerged and the second still in the body cavity of their chironomid midge host in Baltic
amber (Scale bar ¼ 53 mm).

Also, in Baltic amber the first fossil record of a mermithid parasite of a


hemipteran, Heydenius brownii Poinar (2001), was found protruding from
the body of a planthopper (Fulgoroidea) (Figure 9). Hemipteran hosts of
mermithids are rare today, with the only records coming from Ireland
(Helden, 2008). With a fossil record extending back to the Early Permian

Figure 8 The mermithid, Heydenius formicinus Poinar, 2002 emerging from a male
winged ant (Prenolepis henschei Mayr) in Baltic amber (Scale bar ¼ 640 mm).
62 George O. Poinar, Jr.

Figure 9 The mermithid, Heydenius brownii, Poinar, 2001, emerging from an achiliid
planthopper in Baltic amber (Scale bar ¼ 2.6 mm).

(Rasnitsyn and Quicke, 2002), hemipterans could have been ancient terres-
trial hosts for mermithids.
Several different lineages of parasitic nematodes have been found to
attack sciarid fungus gnats (Diptera: Sciaridae) in Baltic amber. One was a
mermithid, Heydenius sciarophilus Poinar (2011) (Figure 10) and another a
tetradonematid, Palaeotetradonema sciarae Poinar (2011). A third parasite line-
age was represented by Tripius balticus Poinar (2011) of the family Sphaeru-
lariidae. Several nematodes were still inside the body cavity of the adult host
while others had emerged (Figure 11). The life cycle of the fossil was prob-
ably similar to that of the extant species, Tripius sciarae (Bovien).
Other dipterous hosts of mermithids in Baltic amber were gall gnats
(Cecidomyiidae). One specimen of Heydenius cecidomyae Poinar (2011)
had completely emerged from the gall gnat while the second was only partly

Figure 10 Heydenius sciarophilus Poinar (2011) emerging from a sciarid fungus gnat in
Baltic amber (Scale bar ¼ 207 mm).
The Geological Record of Parasitic Nematode Evolution 63

Figure 11 Parasitic juveniles of Tripius balticus Poinar (2011) (arrow) that emerged from
a sciarid fungus gnat in Baltic amber (Scale bar ¼ 322 mm).

emerged (Figure 12). There are no reports of extant gall gnats parasitized by
mermithids.
Another parasite lineage of Diptera was represented by the allantonematid,
Howardula helenoschini Poinar (2003) that parasitized scuttle flies (Phoridae).

Figure 12 Two specimens of Heydenius cecidiomyae Poinar (2011), a parasite of a gall


gnat in Baltic amber (Scale bar ¼ 575 mm).
64 George O. Poinar, Jr.

Figure 13 Specimens of the allantonematid, Howardula helenoschini Poinar (2003)


(arrow) emerging from a phorid fly, Triphleba sp., in Baltic amber (Scale bar ¼ 347 mm).

Five specimens of H. helenoschini were clustered at the posterior tip of the fly’s
abdomen, obviously having just exited from the host’s body cavity (Figure 13).
The lemon-shaped parasitic female of H. helenoschini could be detected
through the host’s abdomen. Extant phorid flies are parasitized by Howardula
nematodes globally (Richardson et al., 1977; Poinar, 1975; Disney, 1994).
The nematodes normally leave the fly host via the intestine or reproductive
system (Richardson et al., 1977) and that is probably the route used by the
five fossil nematodes.
Another Baltic amber nematode in the allantonematid lineage was Palae-
oallantonema baltica Poinar (2011) that was parasitizing a rove beetle (Staph-
ylinidae). A number of last stage juveniles that had exited the host consisted
of two morphotypes: females of the first generation and pre-adults of the
second generation.
Hematophagous flies in Baltic amber also were associated with vertebrate
nematode parasitic lineages. Blackflies (Simuliidae) and biting midges (Cera-
topogonidae) are the most common biting insects in Baltic amber. A micro-
filaria of Cascofilaria baltica Poinar (2011, 2012) was adjacent to a blackfly with
a swollen abdomen, suggesting that the fly had taken a blood meal shortly
before falling in the resin. The microfilaria falls within the size range of those
of extant Onchocerca spp., a worldwide genus infecting mammals and vectored
by blackflies. This represents the oldest fossil record of a filarial nematode.
Still additional insect hosts of mermithid nematodes in Baltic amber
include a moth (Lepidoptera) parasitized by Heydenius podenasae Poinar
The Geological Record of Parasitic Nematode Evolution 65

Figure 14 Adult caddis fly (Triaenodes balticus Wichard and Barnard, 2005) parasitized
by Heydenius trichorosus Poinar (2012) in Baltic amber (Scale bar ¼ 1.4 mm).

(2012), an adult caddis fly, Triaenodes balticus Wichard and Barnard, 2005
(Trichoptera) parasitized by Heydenius trichorosus Poinar (2012) (Figure 14)
and a phasmatid, Balticophasma sp. (Phasmatodea: Phasmatidae) parasitized
by Heydenius phasmatophilus Poinar (2012) (Figure 15).
Spiders were also parasitized by mermithid nematodes in the Baltic
amber forest, and Heydenius araneus Poinar (2000) from a crab spider (Tho-
misidae) (Figure 16) is the earliest record of nematode parasitism of spiders.

6. NEMATODE PARASITES FROM THE


OLIGOCENEeMIOCENE
6.1 Dominican amber nematodes
One of the major host groups of nematode parasites in amber from the
Dominican Republic is ants and there is evidence that three lineages of para-
sitic nematodes were involved.
A mermithid lineage is represented by Heydenius myrmecophilia Poinar
et al. (2006) that had recently emerged from a species of the ant genus Line-
pithema Mayr.
A second lineage was a member of the family Tetradonematidae, Myr-
meconema antiqua Poinar (2011). This species was represented by a mass of
66 George O. Poinar, Jr.

Figure 15 A phasmatid, Balticophasma sp. (Phasmatodea: Phasmatidae) parasitized by


Heydenius phasmatophilus Poinar (2012) in Baltic amber (Scale bar ¼ 2.1 mm).

eggs (Figure 17) that had escaped through a hole in the gaster (abdomen) of
a species of Cephalotes Latreille, 1803. The fossil probably had a life cycle
similar to the extant Myrmeconema neotropicum Poinar and Yanoviak
(2008), a parasite of Cephalotes atratus (L.). The life cycle of this group is
especially fascinating and unique. When females of M. neotropicum have
matured and the body cavity of the ant is filled with eggs, the color of

Figure 16 The spider mermithid, Heydenius araneus Poinar (2000) adjacent to its clu-
bionid spider host in Baltic amber (Scale bar ¼ 2 mm).
The Geological Record of Parasitic Nematode Evolution 67

Figure 17 Eggs of Myrmeconema antiqua Poinar (2011) from an ant of the genus Ceph-
alotes Latreille in Dominican amber (Scale bar ¼ 360 mm).

the host’s gaster changes from black to a shiny red. The bright red abdomen
resembles ripe berries that are relished by birds. The infected ants stand on
stems and raise their abdomens high in the air. When a bird ingests an
infected ant, the eggs of M. neotropicum pass thought the bird’s digestive tract
and are deposited in the droppings. Worker ants collect and feed the
infested bird droppings to their brood. The ingested nematode eggs hatch
in the larval guts and the juveniles penetrate into the insect’s body cavity. It
appears that this complicated life cycle was established already some 20e30
million years ago.
Cephalotes ants are also hosts to a third parasite lineage, the Allantonema-
tidae. Mature juveniles of Palaeoallantonema cephalotae Poinar (2011) were
emerging from a worker of Cephalotes serratus in a piece of amber (Figure 18).
A similar hosteparasite association occurs with an undescribed allantonema-
tid and workers of Cephalotes christopherseni in Peru.
A separate lineage of allantonematids, represented by Palaeoparasitylenchus
dominicana Poinar (2011) parasitized drosophilid fruit flies in the Dominican
amber forest. A female fly was heavily infected and large numbers of juve-
niles and second-generation female nematodes were adjacent to the host
(Figure 19). The life cycle of P. dominicanus was probably similar to that
68 George O. Poinar, Jr.

Figure 18 Detail of a specimen of Palaeoallantonema cephalotae Poinar (2011)


from the ant, Cephalotes serratus Vierbergen & Scheve, in Dominican amber (Scale
bar ¼ 24 mm).

of the extant species, Parasitylenchus nearcticus Poinar et al. (1997) from


Eastern North America.
Moth flies (Diptera: Psychodidae) were also attacked by mermithid
nematodes in the Dominican amber forest. Two juvenile specimens of
Heydenius psychodae Poinar (2011) had completely emerged from an adult
moth fly (Figure 20). There appears to be no record of mermithids parasit-
izing extant moth flies. Another mermithid lineage attacked scavenger flies

Figure 19 Parasitic juveniles of Palaeoparasitylenchus dominicanus Poinar (2011)


emerging from a drosophilid fly in Dominican amber (Scale bar ¼ 432 mm).
The Geological Record of Parasitic Nematode Evolution 69

Figure 20 Two specimens of the mermithid, Heydenius psychodae Poinar (2011), with
their moth fly host in Dominican amber (Scale bar ¼ 800 mm).

(Diptera: Scatopsidae). Five specimens of Heydenius scatophilus Poinar


(2011) were adjacent to their scatopsid host in Dominican amber. There
appears to be no report of mermithids infecting extant scavenger flies.
Another fly group in the Dominican amber that was parasitized by mer-
mithid nematodes was milichids (Diptera: Milichidae). The mermithid, Hey-
denius dipterophilus Poinar (2011) had completely emerged from its milichid
host in Dominican amber. There are no extant records of mermithids from
this family of flies.
Fungus gnats of the family Mycetophilidae are common in Dominican
amber, and one representative was parasitized by a member of the Iotonchi-
dae lineage. Iotonchid nematodes have evolved a complex life cycle alter-
nating between insects and fungi. The Dominican amber Paleoiotonchium
dominicanum Poinar (2011) probably had a similar dual host life cycle. The
swollen female nematode and a number of juveniles remain in the body
cavity of the fossil fly, while additional juveniles are in the amber surround-
ing the host (Figure 21). The life cycle of P. dominicanum may have been
similar to that of the extant Iotonchium californicum Poinar (1991). The latter
has a mycetophagous cycle that occurs in mushrooms also invaded by fungus
gnats, which become a secondary host. The fossil shows that life cycles
70 George O. Poinar, Jr.

Figure 21 Parasitic juveniles of Paleoiotonchium dominicanum Poinar (2011) inside the


body cavity of a mycetophilid fungus gnat in Dominican amber (Scale bar ¼ 75 mm).

alternating between insects and fungi are ancient and provides an evolu-
tionary scenario that insect parasitism by tylenchoid nematodes may have
evolved from mycetophagous lineages.
Strictly mycetophagous nematodes of aphelenchoidid lineages have also
been described from Dominican amber. The stylet-bearing Bursaphelenchus
similus Poinar (2011) probably originated from a gallery belonging to an
adjacent platypodid beetle. Some 60 specimens of the aphelenchoidid Crypt-
aphelenchus dominicus Poinar (2011) were associated with an adult platypodid
beetle. Many of them were dauer (resistant) juveniles, which is a phoretic
stage. A third lineage was represented by numerous individuals of Oligaphe-
lenchoides dominicanus Poinar (2011) feeding on a large mat of adjacent fungal
hyphae.
Also in Dominican amber are nematode parasites of herbivorous insects.
The allantonematid, Palaeoallantonema apionae Poinar (2011) was parasitizing
an apionid weevil, and numerous individuals of the diplogastrid, Synconema
dominicana Poinar (2011) were adjacent to a fig wasp (Hymenoptera: Agao-
nidae) (Figure 22), thus providing indirect evidence of fig trees in the ancient
forest. Based on their attenuated head, lack of a stylet, rounded lip region
and elongate tail, S. dominicana was placed in the Parasitodiplogaster clade,
an extant genus that parasitizes figs wasps in Africa and Mesoamerica (Poinar,
1979; Poinar and Herre, 1991).
Fossil-parasitic nematodes of higher plants are extremely rare; however,
numerous specimens of Oligaphelenchoides maximus Poinar (2011) in all
developmental stages were found in a section of a monocot rootlet in
Dominican amber (Figure 23). The long, slender, stylet-bearing adults
The Geological Record of Parasitic Nematode Evolution 71

Figure 22 Parasitic stages of Synconema dominicana Poinar (2011) emerging from a fig


wasp in Dominican amber (Scale bar ¼ 545 mm).

and males with a C-shaped terminus align the species with members of the
Aphelenchoididae.
Another species of stylet-bearing plant-parasitic nematode in Dominican
amber was the anguinid, Palaeoanguina dominicana Poinar (2011) (Figure 24).
It apparently had been feeding within and then attempted to escape from a
seed that fell in the resin. Extant anguinids can withstand desiccation and
survive for years in dried seeds.
One interesting lineage of aphelenchoidids in Dominican amber is the
Acugutturidae Hunt (1993). Extant representatives are ectoparasites on
the external surface of insects, especially moths. Several specimens of Seto-
nema protera Poinar (2011) belong to this family. One large specimen is adja-
cent to its moth host (Figure 25), while another is some distance away.

Figure 23 Population of the plant nematode, Oligaphelenchoides maximus Poinar


(2011) in Dominican amber (Scale bar ¼ 857 mm).
72 George O. Poinar, Jr.

Figure 24 Juvenile female of Palaeoanguina dominicana Poinar (2011) in Dominican


amber (Scale bar ¼ 128 mm).

Several additional specimens are attached to the moth’s abdomen. Extant


species of this family occur on six families of moths, especially noctuids,
and apparently transfer from moth to moth during mating.
While the high rate of mermithid parasitism of chironomid midges in
Eocene Baltic amber was previously noted, mermithid parasitism of this
host group also occurs in Dominican amber as exemplified by Heydenius

Figure 25 The ectoparasitic nematode Setonema protera Poinar (2011) (arrow) adja-
cent to its moth host in Dominican amber (Scale bar ¼ 245 mm).
The Geological Record of Parasitic Nematode Evolution 73

Figure 26 A specimen of Heydenius dominicus Poinar, 1984 inside the body cavity of a
Culex mosquito in Dominican amber (Scale bar ¼ 348 mm).

neotropicus Poinar (2011). Other mermithid lineages, such as Heydenius dom-


inicus Poinar (1984) (Figure 26) parasitized mosquitoes.
A few fossil blood-sucking flies were found vectoring filarial parasites in
Dominican amber. One female mosquito was adjacent to an infective and
pre-infective stage of the filarial nematode, Cascofilaria dominicana Poinar
(2011). The nematodes resemble the infective stages of the extant frog para-
site, Foleyella duboisi (Witenberg and Gerichter, 1944). Members of Foleyella
infect tree frogs (Leptodactylus spp.) in South America and Eleutherodactylus
tree frogs have been found in Dominican amber (Poinar and Poinar, 1999).
A second filarial nematode adjacent to another adult mosquito was
described as Cascofilaria parvus Poinar (2011). It is thought to represent an
infective stage juvenile but could not be further identified.
Nematodes also parasitized sand flies, another group of bloodsuckers in
the Dominican amber forest. A female sand fly of the genus Lutzomyia was
parasitized by Palaeoallantonema phlebotomae Poinar (2011). Aside from those
adjacent to the sand fly, nematode parasites also occurred inside the host.
Saprophagous flies were also attacked by mermithids in Dominican
amber. Heydenius saprophilus Poinar (2011) had been parasitizing a wood
gnat (Anisopodidae) (Figure 27).
The host range of mermithid nematodes in Dominican amber is
amazingly broad and also includes predatory beetles. Heydenius lamprophilus
Poinar (2011) was parasitizing an adult firefly (Coleoptera: Lampyridae) in
Dominican amber (Figure 28), and a rove beetle (Staphylinidae) was sur-
rounded by 44 juveniles of the allantonematid parasite, Palaeoallantonema
dominicana Poinar (2011) (Figure 29).
74 George O. Poinar, Jr.

Figure 27 Parasitic juvenile of Heydenius saprophilus Poinar (2011) adjacent to its wood
gnat host (Diptera: Anisopodidae) in Dominican amber (Scale bar ¼ 971 mm).

One interesting record of parasitism unknown today involved several


nematodes that had emerged from a parasitic wasp (Hymenoptera: Pteroma-
lidae). Two individuals were projecting from the body of the wasp and one
was still inside the wasp. The nematodes, described as Chalcidonema paradoxa
Poinar (2011) were tentatively placed in the Aphelenchoididae (Figure 30).

Figure 28 Heydenius lamprophilus Poinar (2011) from a lampyrid beetle in Dominican


amber (Scale bar ¼ 914 mm).
The Geological Record of Parasitic Nematode Evolution 75

Figure 29 A group of parasitic juveniles of Palaeoallantonema dominicana Poinar


(2011) adjacent to their rove beetle host in Dominican amber (Scale bar ¼ 233 mm).

Since the wasp larvae develop as internal insect parasites, it is possible that the
nematodes were also parasitizing the same host and entered the wasp larva.

6.2 Mexican amber nematodes


The Mexican amber forest was in large part similar to that of the Dominican
amber forest with similar insect genera but different species, showing that the
forests were separated long enough for speciation to occur.
One of the most spectacular nematode parasites in Mexican amber was a
population of the aphelenchoidid, Oligaphelenchoides atrebora Poinar (1977).
Males, females, eggs and juveniles were present, along with fungal hyphae

Figure 30 Stages of Chalcidonema paradoxa Poinar (2011) (arrows) associated with a


chalcidoid wasp in Dominican amber (Scale bar ¼ 471 mm).
76 George O. Poinar, Jr.

Figure 31 A reproducing population of Oligaphelenchoides atrebora Poinar, 1977 in


Mexican amber (Scale bar ¼ 176 mm).

that served as their food source (Figure 31). Also present were nematopha-
gous fungi that had parasitized several individuals of O. atrebora (Jansson and
Poinar, 1986) (Figure 32).
Few parasitic nematodes have been recovered from Mexican amber;
however, one interesting species was the tetratonematid, Palaeotetradonema

Figure 32 Thick hyphae of a nematophagous fungus inside a specimen of Oligaphelen-


choides atrebora Poinar, 1977 in Mexican amber (Scale bar ¼ 9 mm).
The Geological Record of Parasitic Nematode Evolution 77

phlebotomae Poinar (2011) that attacked a phlebotomine sand fly. Placement


in the Tetradonematidae was based on the structure of developing ova in
one specimen that was similar in size to ova in the extant sand fly tetrado-
nematid, Didilea ooglypta Tang et al. (1993).

7. NEMATODE PARASITES FROM THE PLIOCENE


An interesting Pliocene nematode parasite is the mermithid, Heydenius
tabanae Poinar (2011) emerging from an adult horsefly (Diptera: Tabanidae)
in sedimentary deposits in Germany dated at about 2.5 million years
(Grabenhorst, 1985). The horsefly was identified as the extant Tabanus sude-
ticus Zeller. It is interesting that H. tabanae was emerging from an adult
horsefly, while all extant cases of horsefly parasitism by mermithids are in
larvae (Poinar, 1985; Poinar and Lane, 1978).

8. NEMATODE PARASITES FROM THE PLEISTOCENE


AND HOLOCENE
Several vertebrate-parasitic nematodes have been reported from
deposits in the Pleistocene that extends from 1.81 mya to 11,500 BP and
the Holocene from 11,500 BP to 3300 BC. The oldest records of various
vertebrate parasite lineages are presented below. In most cases, the hosts
are still extant.
Palisade worms, Strongylus edentatus (Looss, 1900), were recovered from
the intestine of a mummified Late Pleistocene horse (Dubinina, 1972).
These nematodes are widespread and reproduce in the caecum and colon
of horses today (Anderson, 2000). Horse pinworm eggs (Oxyuris equi
Schrank) can be used to place horses at ancient locations (Jansen and
Over, 1962, 1966).
Pinworms of the genus Syphacia Seurat were recovered from fossilized
remains of a 10,000e12,000-year-old ground squirrel (Citellus sp.) (Dubinin,
1948). The fossil worms closely resemble the extant species Syphacia obvetata
(Rudolphi), which occurs in the intestine of rodents worldwide.
Whipworm (Trichuris Roederer) remains date from 30,000-year-old
eggs in coprolites of the caviid rodent, Kerodon rupestris, in Brazil. The
authors suggested that climate change was responsible for the disappearance
of Trichuris sp. in extant populations of K. rupestris at the same location
(Ferreira et al., 1991).
78 George O. Poinar, Jr.

Nine-thousand-year-old coprolites from a Brazilian iguaniid, Tropidarus


sp., contained eggs of an oxyurid considered to be Parapharyngodon sceleratus
(Travassos, 1923) that infects the extant lizard, Tropidarus torquatus (Ara
ujo
et al., 1982).
Some rare fossil nematodes have been obtained from remains of extinct
animals such as coprolites from a 1.5-million-year-old extinct Hyaena Bris-
son, 1762. The nematode juveniles could not be identified, but they could
have belonged to either Ancyclostoma or Toxascaris since both genera para-
sitize extant hyaenids (Ferreira et al., 1993).
An analysis of dried 10,000-year-old boluses of the extinct ground sloth,
Mylodon listai Ameghino, 1889, in Argentina produced elliptical bodies that
are thought to be nematode eggs (Ringuelet, 1957). Shasta Ground Sloth
(Nothrotheriops shastensis) boluses dated at 10,000  180 years from Rampart
Cave, Arizona contained first stage juveniles of the oxyurid, Agamofilaria oxy-
ura Schmidt et al. (1992) and a strongyloid, Strongyloides shastensis Schmidt
et al. (1992).
Rarely it is possible to obtain molecular evidence of parasites from sub-
fossilized remains. Wood et al. (2013) reported extracting ancient nematode
DNA from four moa species in New Zealand. Using these markers and
microscopic analysis, nematode representatives of the Heterakoidea, Tri-
chostrongylidae and Trichinellidae were identified in the moa coprolites.

8.1 Nematode parasites of humans from the Pleistocene and


Holocene
The search for human nematode parasites by anthropologists and archaeol-
ogists falls under the discipline of paleoparasitology or archaeoparasitology
(Taylor, 1955; Klicks, 1990; Reinhard, 1992; Reinhard and Ara ujo,
2008). Eggs and larvae of most gastrointestinal parasites have been obtained
from coprolites, cesspits, latrines and mummies (Gonçalves et al., 2003;
Sandison and Tapp, 1998). While the earliest evidence of human nematode
parasites are 30,000e24,000-year-old ascarid eggs from the Pleistocene
(Bouchet et al., 1996), these records are not old enough to shed light on
the origin of nematode lineages in humans. However, they do provide
important information on the types and geographical distribution of human
nematode parasites.
We know very little about how humans acquired their 138 species of
nematode parasites (Crompton, 1999). Egyptian mummies have been an
excellent source of human nematodes, especially those ‘natural mummies’
that were preserved with all their organs intact. Pages from the Papyrus Ebers
The Geological Record of Parasitic Nematode Evolution 79

dating from 3553 to 3550 BC, include treatments for ascarids (Ascaris lumbri-
coides L.), hookworms (Ancyclostoma duodenale Dubini) and Guinea worms
(Dracunculus medinensis L.) (Bryan, 1931; Ebbell, 1937).
Additional nematodes found in Egyptian mummies, but not mentioned
in the Papyrus Ebers, were whipworms (Trichuris trichiura L.), filarial nema-
todes (probably Wuchereria Silvo Araujo or Brugia spp.), and Trichinella spiralis
Owen and Stronglyoides stercoralis Bavay. Mummies show that Egyptians
were parasitized by ascarids some 2200 years ago (Cockburn et al., 1975),
infections of D. medinensis 3991e3786 years ago (Tapp and Wildsmith,
1993) and scrotal filarial nematodes (Tapp and Wildsmith, 1993).
It is curious that pinworms (Enterobius vermicularis L.) have only been
rarely recovered from ancient Egyptian mummies (Horne, 2002) and are
not mentioned in the Papyrus Ebers. Since the earliest record of pinworms
is from the New World, perhaps this species originated in the Americas,
although this might be a sampling bias.
The oldest records of human hookworms are 7230-year-old eggs recov-
ered from coprolites in Brazil (Montenegro et al., 2006; Ferreira et al.,
1987), showing that the parasites were present in South America well before
the Spanish invasion.
The whipworm, T. trichiura, infects slightly over 1000 million humans
worldwide today (Crompton, 1999). The oldest record of human parasitism
by this species dates back between 7000 and 8000 BP based on eggs from
human remains in a pre-Colombian bog in Chile, suggesting that this species
is endemic to the New World although Klicks (1990) concluded that both
T. trichiura and E. vermicularis were introduced to the New World by people
migrating across the Bering strait from Siberia.
When parasitic nematodes were originally acquired by humans is
unknown. Recent studies on nematode parasites of nonhuman primates
suggest that at least all human intestinal nematodes could have been acquired
from other primates (Dupain et al., 2009; Kaur and Singh, 2009). In fact, it is
likely that most, if not all, nematode parasites that plague humans today were
obtained through their distant ancestors and domesticated animals.

9. STAGES IN THE EVOLUTION OF NEMATODE


PARASITES OF INVERTEBRATES
Nematode parasitism of animals probably first originated in invertebrate
marine hosts with the ‘aphasmidians’ and later on land with the ‘phasmidians’.
It is likely that nematodes arose in the sea as free-living microbotrophs in the
80 George O. Poinar, Jr.

Precambrian, even earlier than has been proposed using relaxed molecular
clock methodologies (Rota-Stabelli et al., 2013), and were parasitizing marine
invertebrates by the Cambrian and terrestrial invertebrates by the Ordovician
based on extrapolations from extant parasiteehost relationships and the fossil
record of the hosts of nematode parasites (Poinar, 2011).
Early hosts of nematode parasites of invertebrates were probably repre-
sentatives of Tetradonematidae, Marimermithidae, Echinomermellidae,
Benthimermithidae, Monhysteridae and Leptolaimidae (see Poinar (2011)
for the systematic placement of these groups) that today parasitize marine
ostracods, copepods, shrimp, amphipods and isopods (Petter, 1980; Poinar
et al., 2002, 2009), starfish (Asteroidea) (Rubtsov and Platonova, 1974;
Rubtsov, 1977), brittle stars (Ophiuroidea) (Ward, 1933), sea urchins
(Echinoidea) (Gemmill and Von Linstow, 1902; Jones and Hagen, 1987),
priapulids (Rubtsov, 1980), polychaetes (Petter, 1983), tubicifid oligo-
chaetes (Hallett et al., 2001), foraminifera (Hope and Tchesunov, 1999)
and marine nematodes (Chesunov, 1988; Tchesunov and Spiridonov,
1993). Some of these host groups, such as polychaetes, ostracods and fora-
minifera, have fossil records extending back to the Cambrian (Lehmann and
Hillmer, 1983).
Today, members of the Mermithidae parasitize invertebrates in the
marine and terrestrial habitat. When mermithids shifted towards land,
marine amphipods and intertidal chironomid midges could have served as
hosts (Poinar, 1975; Schlinger, 1975; Poinar et al., 2002). Chironomid
midges have a fossil record extending back to the Late Triassic (Rasnitsyn
and Quick, 2002) and Cretacimermis and Heydenius show that mermithid
parasitism of these flies was present in the Early Cretaceous.
Later, mermithids selected freshwater aquatic or semiaquatic Diptera as
hosts, such as biting midges (Ceratopogonidae), scavenger flies (Scatopsi-
dae), gall gnats (Cecidiomyiidae), moth flies (Psychodidae), wood gnats
(Anisopodidae), scuttle flies (Phoridae), fruit flies (Drosophilidae) and
fungus gnats (Sciaridae and Mycetophilidae). These insect families all
have fossil records dating back to the Jurassic (Rasnitsyn and Quicke,
2002).
Three terrestrial groups of invertebrate-parasitic nematodes, the oxy-
urids, drilonematids and cosmocercoids, are particularly primitive and
were the possible first terrestrial parasites of invertebrates (Osche, 1963;
Inglis, 1965). Oxyurids probably parasitized invertebrates before verte-
brates and while P. tipulae) establishes the oxyurids as parasites of Diptera
in the Early Cretaceous, pinworms could have potentially already occurred
The Geological Record of Parasitic Nematode Evolution 81

in earliest known (Silurian) millipedes. Other early hosts for oxyurids could
have been isopods (Schwenk, 1927) and annelids (Poinar, 1978b; Yeates
et al., 1998). The drilonematids represent a primitive, but highly special-
ized lineage now confined to the coelom of earthworms. The discovery
of Mesidionema praecomasculatis Poinar (1978a), an earthworm parasite that
has morphological and biological features of both oxyurids and drilonema-
tids, suggests that drilonematids could have evolved as a specialized clade
from oxyurids.
The Cosmocercoids may have evolved in gastropods Anderson, 2000;
McClelland, 2005), and P. burmanicum shows that a snail-infecting lineage
was already in existence by the Early Cretaceous (Poinar, 2011). Infected
snails eaten by amphibians could have initiated the vertebrate-parasitic
taxa, although it has been suggested that amphibians may have been the
original hosts (Vanderburgh and Anderson, 1987).
The first fossil record of parasitic rhabditids is the Early Cretaceous Pro-
heterorhabdites burmanicus parasitizing a rove beetle. Heterorhabditids are
thought to have evolved from free-living, intertidal rhabditids (Poinar,
1993) and their early hosts could have been beach dwelling crustaceans (iso-
pods, amphipods, etc.) and intertidial insects.
Insect-parasitic tylenchs and aphelenchs probably evolved from myce-
tophagous lineages like Cryptaphylenchus dominicus that were associated
with platypodid beetles. This could lead to dual fungal and insect parasitism
as seen in the Dominican amber Paleoiotonchium dominicanum that probably
had a life cycle alternating between mushrooms and fungus gnats. While
there is no evidence of fungal fruiting bodies in the amber piece with Pale-
oiotonchium, mushrooms and other fungi occur in Dominican amber (Poinar
and Poinar, 1999; Boucot and Poinar, 2010). The fossil representatives of
Howardula, Palaeoallantonema, Palaeoparasitylenchus and Tripius show that the
typical allantonematidesphaerularid life cycle involving only insect hosts
existed by the beginning of the Cenozoic.

10. ORIGIN OF NEMATODE PARASITES OF


VERTEBRATES
The earliest fossil vertebrates were in shallow, near shore Cambrian
and Ordovician deposits. There is no evidence of their presence in fresh-
water deposits prior to the Early Devonian (Carroll, 1988). In the Silurian
seas, nematodes probably parasitized the primitive-jawed acanthodians
82 George O. Poinar, Jr.

as well as elasmobranchs and the ancestors of coelacanths based on present-


day host records (Poinar, 2011).
It is likely that oxyurids were the earliest nematode parasites of terrestrial
vertebrates, and their antiquity has recently been demonstrated with the dis-
covery of P. cockburni Hugot et al. (2014) in a 240-million-year-old cyno-
dont coprolite (Hugot et al., 2014). There is quite a time lapse to the
next oldest record of vertebrate pinworms in Holocene and Pleistocene de-
posits (Jansen and Over, 1962, 1966; Poinar, 2014).
However, the ascarid lineage may be just as ancient since the Triassic fos-
sil, A. rufferi Da Silva et al. (2014) dates from the same time period and same
host as P. cockburni (Da Silva et al., 2014). The next oldest fossil ascarid par-
asites are the Early Cretaceous A. priscus and A. gerus recovered from an
dinosaur coprolite (Poinar and Boucot, 2006).
The three records of filarial nematodes in amber establish this nematode
lineage in the Cenozoic and show what types of insect vectors were trans-
mitting these parasites. The next oldest records of vertebrate parasitism are
30,000-year-old eggs of A. lumbricoides from human coprolites (Patrucco
et al., 1983) and 30,000-year-old whipworm eggs from coprolites of a caviid
rodent (Ferreira et al., 1991).
The question regarding the original host of heteroxenous parasites (those
using an invertebrate as an intermediate host and a vertebrate as a final,
developmental host) has been debated for years. These nematodes, exempli-
fied by the Spirurida, actually have two infective stages, one for the inver-
tebrate and the other for the vertebrate. Did these heteroxenous
nematodes evolve first in vertebrates with invertebrates becoming second-
arily infected by ingesting eggs in faecal material? Or were invertebrates
parasitized first and the vertebrate cycle was established when the latter hosts
were eaten? Evidence for the invertebrate first theory is that (1) some of
these parasites can complete their entire development in the invertebrate
host and (2) invertebrate hosts appeared in the fossil record before those
of vertebrates.
Unfortunately, the fossil record of nematodes is too sparse to answer this
question; however, estimated dates of the origin of vertebrate- and inverte-
brate-parasitic nematode families can be inferred from the earliest fossil re-
cord of their host group or molecular clock estimates. Regarding the
family Spiruridae Railliet and Henry, 1915, the earliest vertebrate host
group appears in the Cretaceous while the earliest fossil record of an inver-
tebrate host group is in the Carboniferous (Poinar, 2011).
The Geological Record of Parasitic Nematode Evolution 83

11. ORIGIN OF NEMATODE PARASITES OF PLANTS


Plant parasitism evolved independently in at least four terrestrial line-
ages, the Enoplida, Triplonchia, Dorylaimia and Rhabditida (Poinar, 2011).
Plant-parasitic nematodes may have existed in the Silurian or even Ordovi-
cian since the earliest known fossils are from the Devonian (Poinar et al.,
2008). There is no evidence yet of any marine lineage of plant-parasitic
nematodes. Those plant-parasitic nematodes found in the sea are terrestrial
lineages that invaded littoral and sublittoral habitats. These include the
tylench genera Halenchus Cobb (Fortuner and Maggenti, 1987), Hirschma-
niella Luc & Goodey (Luc, 1987) and the aphelench species Aphelenchoides
marinus Timm & Franklin and A. gynotylurus Timm & Franklin (Timm
and Franklin, 1969).
The most primitive higher plant parasites are members of Aphelenchi-
dae, Tylenchidae, Paraphelenchidae, Neotylenchidae and Paurodontidae,
whose lineages could well extend back to the Silurian with early fossil
records of fungi (Taylor et al., 2015). Siddiqi (1983) supposed that tylenchid
plant parasites originated from algal-feeding lineages while Paramonov
(1962) and Maggenti (1971) felt they developed from mycetophagous
lineages.
The oldest aphelench fossil is the Early Cretaceous C. burmensis followed
by the Eocene P. balticus (Poinar, 2011). The above species represent free-
living mycetophages that are probably the primitive aphelench trophic stage.
Just when aphelenchs shifted their diet to higher plants is not known, but the
Dominican amber Oligaphelenchoides maxima is considered to represent an
aerial parasite with a biology similar to some extant Aphelenchoides spp.
The fossil Palaeoanguina dominicana that was developing in a seed in Domin-
ican amber is further evidence of obligate parasitism of aerial portions of
plants. This species probably had a life cycle similar to some extant members
of the genus Anguina Scopoli (Fortuner and Maggenti, 1987).

12. SUMMARY
Since nematodes most likely evolved in the sea (Poinar, 2011), it is
highly likely that the earliest animal parasites already lived in trilobites,
eurypterids and other marine invertebrates, although so far no direct fossil
evidence has become known. The first vertebrate parasites might have used
84 George O. Poinar, Jr.

elasmobranchs and primitive marine fish as hosts based on extant parasitee


host associations (Poinar, 2011). Since their fossil record is so sparse, deter-
mining the evolutionary clocks of the many lineages of parasitic
nematodes, each of which evolved independently, is difficult. However,
the minimum longevity of some nematode orders and infraorders can be
determined by body fossils (Figure 33), and time constraints on other lin-
eages can be inferred with molecular clock methodologies. However,
morphology and molecular methods do not always match. For instance,
some molecular clock studies place the origin of ascarids in the Jurassic
(Blaxter, 2009), but this is clearly incorrect since ascarid body fossils occur
in the Triassic (Da Silva et al., 2014). Since most nematode families have
multiple hosts, the earliest fossil of the most primitive host can be used
to estimate the possible date of origin for various nematode groups (see
Poinar (2011)). Using fossil host records, the earliest animal-parasitic nem-
atodes would have been members of the marine families Benthimermithi-
dae, Tetradonematidae and Leptolaimidae, whose invertebrate host groups
extend back to the Cambrian. The earliest terrestrial animal parasites would
be Thelastomatoidea, Rhigonematoidea and Ransomnematoidea that
parasitized millipedes, which have a body fossil record dating back to the
Silurian (Wilson and Anderson, 2004). The first vertebrate parasites would
have used elasmobranchs and primitive marine fish as hosts (Poinar et al.,
2014). The earliest higher plant parasites, which could have evolved
from mycetophagous lineages as far back as the Silurian could have been
lineages of Aphelenchidae, Paraphelenchidae, Neotylenchidae, Paurodon-
tidae and Tylenchidae (Poinar, 2011). With so many different lineages of
nematode parasites, it is only natural to assume that parasitism has evolved
convergently and independently in multiple lineages of nematodes. Ac-
cording to recent molecular studies (e.g. Blaxter and Koutsovoulos,
2015), plant parasitism has evolved at least three times, animal parasitism
has arisen at least ten times across a wide range of invertebrates and five
times in vertebrates hosts within the three nematodes subclasses. However,
many additional origins of parasitism could be proposed based on firm
morphological data. Sudhaus (2008, 2010) used morphological characters
to show that there are at least 20 independent origins of insect parasitism
by nematodes.
We look forward to the discovery of additional nematode fossils associ-
ated with identifiable host remains (including coprolites) that will help us to
better understand the origin and evolution of nematode parasitism of verte-
brates, invertebrates and plants.
The Geological Record of Parasitic Nematode Evolution
Figure 33 Minimum longevity of nematode orders and infraorders based on body fossils. Numbers refer to mya (million years ago).

85
86 George O. Poinar, Jr.

Molecular clock methodologies are extremely important, and together


with morphology, the two disciplines complement each other very well.
Together they can show relationships between extant lineages, perform
ancestral host reconstruction with phylogenetic dating analyses and deter-
mine when various lineages might have appeared in geological time (Sung
et al., 2008; Poinar et al., 2011).

ACKNOWLEDGEMENTS
The author would like to acknowledge E. J. Brill and ‘Nematology’ for previously having
published many of the figures used in the present work.

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CHAPTER THREE

Constraining the Deep Origin of


Parasitic Flatworms and Host-
Interactions with Fossil Evidence
Kenneth De Baets*, 1, Paula Dentzien-Diasx, Ieva Upeniece{,
Olivier Verneaujj, #, **, Philip C.J. Donoghuexx
*Fachgruppe Pal€aoUmwelt, GeoZentrum Nordbayern, Friedrich-Alexander-Universit€at
Erlangen-N€ urnberg, Erlangen, Germany
x
Nucleo de Oceanografia Geol ogica, Instituto de Oceanografia, Universidade Federal do Rio Grande,
Rio Grande, Brazil
{
Department of Geology, University of Latvia, Riga, Latvia
jj
Centre de Formation et de Recherche sur les Environnements Méditerranéens, University of Perpignan Via
Domitia, Perpignan, France
#
CNRS, Centre de Formation et de Recherche sur les Environnements Méditerranéens, Perpignan, France
**Unit for Environmental Sciences and Management, North-West University, Potchefstroom, South Africa
xx
School of Earth Sciences, University of Bristol, Life Science Building, Bristol, UK
1
Corresponding author: E-mail: kenneth.debaets@fau.de

Contents
1. Introduction 94
2. Assessment of the Flatworm Fossil Record 96
2.1 Devonian fossil hook circlets 97
2.2 Silurian blister pearls and calcareous concretions in bivalve shells 101
2.3 Permo-Carboniferous egg remains in shark coprolites 103
2.4 Cretaceous egg remains in terrestrial archosaur coprolites 105
2.5 Eocene shell pits in intermediate bivalve hosts 106
2.6 Eggs remains in a Pleistocene mammal coprolite 107
2.7 Holocene evidence for parasitic flatworms from ancient remains 107
2.8 Free-living flatworms 108
3. Interpolating or Extrapolating Extant ParasiteeHost Relationships and the 110
Assumption of ParasiteeHost Coevolution
4. Molecular Clock Studies 113
5. Conclusions and Future Prospects 119
Acknowledgements 121
References 122

Abstract
Novel fossil discoveries have contributed to our understanding of the evolutionary
appearance of parasitism in flatworms. Furthermore, genetic analyses with greater
coverage have shifted our views on the coevolution of parasitic flatworms and their
hosts. The putative record of parasitic flatworms is consistent with extant host
Advances in Parasitology, Volume 90
© 2015 Elsevier Ltd.
j
ISSN 0065-308X
http://dx.doi.org/10.1016/bs.apar.2015.06.002 All rights reserved. 93
94 Kenneth De Baets et al.

associations and so can be used to put constraints on the evolutionary origin of the par-
asites themselves. The future lies in new molecular clock analyses combined with addi-
tional discoveries of exceptionally preserved flatworms associated with hosts and
coprolites. Besides direct evidence, the host fossil record and biogeography have the
potential to constrain their evolutionary history, albeit with caution needed to avoid
circularity, and a need for calibrations to be implemented in the most conservative
way. This might result in imprecise, but accurate divergence estimates for the evolution
of parasitic flatworms.

1. INTRODUCTION
Parasitic flatworms (Platyhelminthes: Neodermata) are a highly
diverse group containing many parasites of biomedical, veterinary and eco-
nomic importance (Olson and Tkach, 2005; Littlewood, 2006). Time con-
straints on the origin and evolution of parasitism in this group are still poorly
resolved due to their patchy and largely overlooked fossil record (Littlewood
and Donovan, 2003; Littlewood, 2006). The fossil record of parasitic
flatworms is often disregarded by parasitologists (Combes, 2001; Littlewood,
2006; Verneau et al., 2009a; Badets et al., 2011) and evolutionary (paleo)bi-
ologists (Labandeira, 2002; Erwin et al., 2011; Wey-Fabrizius et al., 2013)
alike. Most parasitologists have therefore focused on extrapolating or inter-
polating extant parasiteehost associations to infer information on the
evolution history of parasitic flatworms (Llewellyn, 1987; Brooks, 1989;
Brooks and McLennan, 1993; Boeger and Kritsky, 1997; Hoberg, 1999;
Hoberg et al., 1999; Littlewood et al., 1999a). Nevertheless, the last two
decades have seen several new fossil discoveries, which have extended the
record from certain lineages of parasitic flatworms deeper into the Cenozoic
( Jouy-Avantin et al., 1999; Todd and Harper, 2011) or from the Cenozoic
to the Mesozoic (Poinar and Boucot, 2006) or even the Paleozoic
(Upeniece, 2001, 2011; Dentzien-Dias et al., 2013).
Furthermore, molecular analyses have considerably shifted our views on
flatworm phylogeny (Lockyer et al., 2003a; Olson and Tkach, 2005;
Littlewood, 2008; Perkins et al., 2010; Laumer and Giribet, 2014) with
implications for older hypotheses of parasiteehost coevolution. Due to
the patchy fossil record, establishing the phylogeny of flatworms is particu-
larly important for establishing a timeline for the group. Traditionally, Mon-
ogenea (ectoparasitic with simple life cycles) and Cestoda (endoparasitic with
complex, trophically transmitted, life cycles) were often grouped based on
morphological similarities of their larval stages (Bychowsky, 1937; Brooks,
Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence 95

1989), sometimes referred to as the cercomer theory (Lockyer et al., 2003a).


However, most recent molecular-based analyses (Mollaret et al., 1997;
Lockyer et al., 2003a; Park et al., 2007; Perkins et al., 2010; Wey-Fabrizius
et al., 2013; Hahn et al., 2014; Egger et al., 2015) and those including alter-
native data such as microRNAs (Fromm et al., 2013) indicate a sister-group
relationship between cestodes and trematodes (rather than between Mono-
genea and Cestoda) with one possible exception (Laumer and Giribet, 2014;
Laumer et al., 2015), although no clear morphological characters support
this arrangement. Interestingly, the monophyly of Monogenea i.e. the sis-
ter-group relationship between Monopisthocotylea and Polyopisthocotylea
based on morphological data (Boeger and Kritsky, 2001), is not always sup-
ported by molecular phylogenetics (Mollaret et al., 1997; Justine, 1998;
Lockyer et al., 2003a) either. Based on recent results employing mitoge-
nomic data, primitive parasitic flatworms (Neodermata) were probably ecto-
parasitic with a simple life cycle on vertebrates (Park et al., 2007) and
engaged in epithelial feeding (Perkins et al., 2010). Subsequently, it has
been proposed they added an intermediate host to their life cycle, probably
first a crustacean intermediate host in Cestoda and a mollusc intermediate
host in Trematoda (Park et al., 2007) before switching to a blood diet
(Perkins et al., 2010). This differs from previous hypotheses (Brooks,
1989; Littlewood et al., 1999a), where a sister-group relation between Mon-
ogenea and Cestoda, and between these taxa and Trematoda was postulated.
This led to two now probably outdated hypotheses of interpreting the life
cycle evolution of Neodermata (Park et al., 2007). One hypothesis
(Littlewood et al., 1999a) suggested that proto-neodermatan first acquired
an endoparasitic association with vertebrates and that independent adoptions
of invertebrates by the Trematoda (molluscs) and Cestoda (crustaceans) as
well as ectoparasitism in Monogenea were subsequent acquisitions (verte-
brate first hypothesis). Another hypothesis (Cribb et al., 2001) suggested
that the association of common ancestor of the Trematoda with molluscan
hosts was primitive (acquiring its subsequent vertebrate hosts indepen-
dently), and that the vertebrates were involved in the life cycle of the
common ancestor of the Monogenea þ Cestoda clade as independent initial
hosts apart from that of trematodes, with the crustaceans as subsequent inter-
mediate hosts adopted by the Cestoda groups after the ancestral cestode
diverged from the monogeneans (mollusk first hypothesis).
The closest free-living relatives of helminths are also important in con-
straining divergence times in their evolutionary history (Littlewood et al.,
1999b; Near, 2002; Littlewood, 2006). However, the phylogeny of
96 Kenneth De Baets et al.

free-living flatworms has proven even more problematic (but see Littlewood
and Waeschenbach, 2015 for a review of recent advances) and has been
further complicated by the fact that some extant forms traditionally included
in Platyhelminthes have been excluded from the phylum based on molec-
ular analyses (Jondelius et al., 2002; Telford et al., 2003; Willems et al.,
2006; Wallberg et al., 2007; Hejnol et al., 2009) such as the Acoela
(Ruiz-Trillo et al., 1999; Mwinyi et al., 2010; Philippe et al., 2011) and Xen-
oturbella (Bourlat et al., 2003). Furthermore, platyhelminths have often been
grouped in the Platyzoa (Cavalier-Smith, 1998) together with various other
taxa including Acanthocephala, which have convergently evolved a parasitic
lifestyle with larval stages and have been shown to be closely related with
free-living Rotifera (Near, 2002; Weber et al., 2013). It remains unclear
whether Platyzoa is a clade or an artificial grouping generated by systematic
error and long-branch attraction artefacts (Edgecombe et al., 2011; Wey-
Fabrizius et al., 2013; Struck et al., 2014), since subsequent studies have
not only disagreed on the membership of the phyla, but also on the relation-
ships within this grouping. This makes new fossil discoveries of parasitic flat-
worms not only relevant in constraining the evolutionary origin of
flatworms, but also that of the Platyzoa as a whole.
Here we review the potential of fossil flatworm evidence with a view to
using these data to constrain the timescale for the evolutionary history of this
group and outline how they can be used to improve our understanding of
the evolutionary radiation of the Neodermata. We consider whether these
rare fossil finds are at least consistent with coevolution of parasitic flatworms
and their hosts, as well as how fossil finds and other geological evidence in
combination with molecular clock methodology can be best used to
constrain the temporal framework for the evolution of parasitic flatworms.
Such a temporal framework is a key to test evolutionary hypotheses
regarding the origin and diversification of parasitism and its coincidence
with certain biogeographic events, major environmental changes or key
ecological or evolutionary events in the evolution of their hosts.

2. ASSESSMENT OF THE FLATWORM FOSSIL RECORD


Fossil evidence for parasitic flatworms can be derived from (1) rare
exceptionally preserved body fossils, which can be isolated (Poinar and
Boucot, 2006; Dentzien-Dias et al., 2013) or remain associated with their
hosts (Upeniece, 2001, 2011) or (2) more commonly occur as characteristic
Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence 97

traces or skeletal pathologies in their (intermediate) hosts, which have the


potential to be traced back in the fossil record (Ruiz and Lindberg, 1989;
Ruiz, 1991; Ituarte et al., 2001, 2005; Huntley, 2007; Todd and Harper,
2011; Huntley and Scarponi, 2012; Huntley et al., 2014; Huntley and Scar-
poni, 2015; Huntley and De Baets, 2015). Parasite body fossils are scarce due
to their small size, lack of hard parts and the residence within the host and/or
isolation from their hosts (Conway Morris, 1981; Littlewood and Donovan,
2003; De Baets et al., 2011). The rarity of fossilized parasiteehost associa-
tions and the fact that culprits of traces or pathologies in the skeletons of their
hosts are often hard to identify can make it difficult to infer parasiteehost
associations from the fossil record. Nevertheless, it is the only direct evidence
for the presence of such associations in the geological past.

2.1 Devonian fossil hook circlets


Circlets of fossil hooks described from the Devonian of Latvia (Upeniece,
1996, 1998, 1999, 2001, 2011) are the oldest potential body fossil evidence
for parasitic flatworms. Upeniece (2001, 2011) discovered about 77 cir-
clets, which were mostly attached or closely associated with fossil gnathos-
tomes (16 juveniles of the antiarch placoderm Asterolepis ornata; 27
specimens of the acanthodian Lodeacanthus gaujicus: Figures 1(b, c, e, f)).
However, one isolated circlet was found close to a specimen of a clam
shrimp (Figure 1(g)) and two other circlets were found associated with
another crustacean arthropod (Mysidacea: Figure 1(e)), but the hooks are
too large to indicate parasitism based on the size of the crustaceans.
The location of these remains in fossils of their vertebrate hosts (Figure 1(b)
and (c)) and their similarity to the hooks of parasitic helminths, strongly sug-
gest a parasitic nature (Upeniece, 2011). In acanthodians (L. gaujicus), they
are associated with the gill regions, near the fin spines, and in the abdominal
region near the scapula (Figure 1(d) and (f)), while in placoderms (A. ornata)
their location is not so well determined (see Figure 1(a)). The length of
infested fishes varies between 1 and 4 cm (Figure 1(a) and (d)). Several of
them were infested with 2e9 parasites (7 hook circlets can be counted in
the specimen figured in Figure 1(b)). Most authors agree that they are the
remains of parasitic helminths, although their exact affinity remains the sub-
ject of debate (Upeniece, 2001; Littlewood and Donovan, 2003; Upeniece,
2011). These are reminiscent of hooks which are used by Neodermata
(Monogenea, Cestoda) and Acanthocephala to attach themselves to their
hosts. Differences in morphology and their location on the host body
(Upeniece, 2011) might even indicate that they belong to different groups
98 Kenneth De Baets et al.

(a) (b) (c)

(d)

(e)

(f) (g)
Figure 1 Fossil helminth remains in Middle Devonian gnathostomes (Upeniece, 2001,
2011) (Modified from Upeniece (2011) unless otherwise stated.): (a) Locations where hel-
minth remains were found on juveniles of the placoderm Asterolepis ornata. (b) Multiple
fossil circlets of parasitic helminth hooks (marked with ellipses in (a)) found inside the
acanthodian Lodeacanthus gaujicus, LDM 270/18c (Upeniece, 2001, Pl. 3, Figure 2); (c)
Close-up on the hook circlet found associated with L. gaujicus, specimen LDM 270/
33; (d) Locations where helminth remains were found in juvenile and adults of the
Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence 99

of parasites (Upeniece, 2001), including ectoparasites (e.g. monogeneans)


and endoparasites (e.g. cestodes and acanthocephalans).
The circular arrangement of the bilaterally symmetrically located hooks,
traces of cuticular disc as well as the maximum number of 16 hooks, which is
characteristic for early divergent monogeneans (Boeger and Kritsky, 1993),
indicates that at least some of them represent Monogenea (Combes, 2001;
Upeniece, 2011), although the larvae of Cestoda can also have radially
arranged chitinous hooks for attachment. The hooks are also considerably
larger (length: 0.02e0.40 mm) than those of extant flatworms, but this
does not necessarily rule out a monogenean affinity. Poulin (2005), for ex-
ample, could demonstrate an evolutionary trend towards decreasing body
size in extant ectoparasitic Monogenea, while this was less clear for derived
endoparasitic flatworms (Digenea). Interestingly, Upeniece (2011) observed
that small-sized acanthodians possessed small hook systems, while larger
acanthodians exhibited the greatest range in size of the hook systems. These
might indicate that parasites might have spent all their life in one host, which
might further corroborate a similarity to early divergent parasitic flatworms.
The lack of fossilized soft body parts, with the exception of traces of the disc
outline, further hampers a more precise taxonomic assignment. Upeniece
(1999, 2011) suggested that at least two morphological groups are presented
in both species of fish: hooks with a ‘handle’ and hooks without a ‘handle’.
She noticed that the hooks with ‘handles’ typically occur in the abdominal
region of acanthodians and placoderms, suggestive of a close affinity with
endoparasites such as Acanthocephala or Cestoda. The elongated tube-
like body of acanthocephalans typically possesses a thorny proboscis, which
is an anterior retractile organ bearing a large number of hooks (Bush et al.,
2001). This holdfast organ is only fully evaginated after death and resembles
the ‘introvert’ of Rotatoria, Priapulida, Kinorhyncha and Nematomorpha
larvae (Taraschewski, 2005). Larval forms of Cestoda typically bear hooks,
present even in basal extant Cestoda like Gyrocotylidae (Xylander, 2005)
and Amphilinidea (typically 10), which can be retained in the adult forms

=
acanthodian L. gaujicus; (e) Schematic drawing of circlets of fossil hooks (Modified from
Upeniece (1999).) found in juveniles of placoderm fish A. ornata (No 1e11), in juveniles
and adults of acanthodian L. gaujicus (No 12e23), and in/on crustacean Mysidacea (No
24); (f) Fossil hooks found in juvenile acanthodian body near the scapula (see also
Figure 1(e), No. 17), LDM 270/4a; (g) fossil hooks found near a clam shrimp. All speci-
mens derive from the Middle Devonian, Liepa (Lode) pit. Dark grey circles, squares e
possible endoparasites; Light grey circles, squares e possible ectoparasites.
100 Kenneth De Baets et al.

such as in Amphilinidea (Rohde, 2005). Derived Cestoda have a specialized


attachment device (the scolex) that has a highly variable morphology and
may have hooks: Diphyllidea typically possesses a scolex bearing a dorsal
and ventral set of apical hooks (Caira and Reyda, 2005), some Cyclophylli-
dea have a dome-shaped structure at the end of the scolex, the rostellum,
which may be armed with hooks arranged in one or more circles (Bush
et al., 2001), while others like Trypanorhyncha can have a scolex with
four retractable tentacles bearing hooks (Caira and Reyda, 2005). Most au-
thors agree that the fossil circlets of hooks probably belong to platyzoan hel-
minths (Upeniece, 2001, 2011; Poinar, 2003), although we cannot entirely
exclude the possibility that they belong to a now-extinct lineage of parasites.
A reinvestigation of these attachment structures with particular focus on
taphonomy, their composition (element analysis) and the three-dimensional
structure using computer tomography can be particularly useful for disen-
tangling phylogenetic affinity as it did for the elements of the now-extinct
conodonts (Purnell and Donoghue, 1997; 2005; Goudemand et al., 2011;
Murdock et al., 2013). Whatever the exact taxonomic affinity of the parasite
hook circlets, they remain the oldest direct evidence for the presence of
helminthegnathostome and helminthevertebrate association in the fossil
record (Boucot and Poinar, 2010).
Age: The finds of the Lode Formation were described initially as Early
Frasnian, Upper Devonian (Upeniece, 2001), although most authors now
assign this to the Upper Givetian, Middle Devonian (Mark-Kurik et al.,
1999; Jurina and Raskatova, 2012; Luksevics et al., 2012; Mark-Kurik and
P~oldvere, 2012; Luksevics et al., 2014). This corresponds with at least
381.9 Ma, the minimum age assigned to the GivetianeFrasnian boundary
(382.7 Ma  0.8 Myr: Becker et al., 2012). It is common practice in geolog-
ical and paleontological studies to use Ma for ‘Million years ago’, while XX
Myr is often used to refer to a duration of XX million years.
Luksevics et al. (2009) attributed various skeletal pathologies from Mid-
dle (Givetian) to Upper Devonian (Frasnian, Famennian) gnathostomes to
cestode and trematode infestations. However, the characteristics of these
(Luksevics et al., 2009) and other pathologies like skin lesions (Petit,
2010; Petit and Khalloufi, 2012) are insufficient to attribute them to partic-
ular group of parasites confidently, or even rule out potential other causes.
Interestingly, they also overlap temporally with the presence of blister pearls
in Devonian ammonoids (Rakoci nski, 2012), which might also have been
caused by parasitic flatworms, although no conclusive evidence for a parasitic
flatworm infestation was found (De Baets et al., 2011, 2013, 2015).
Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence 101

2.2 Silurian blister pearls and calcareous concretions in


bivalve shells
As (blister) pearls and volcano- to igloo-shaped concretions can be induced
by intermediate stages of parasitic flatworms (G€ otting, 1974, 1979; Lauckner,
1983; Campbell, 1985; Ituarte et al., 2001, 2005), their first occurrence in
the Silurian (Kríz, 1979; Liljedahl, 1985, 1994; De Baets et al., 2011) might
already indicate the presence of derived parasitic flatworms in the Silurian.
Pearls and blisters can, however, be caused by a variety of irritants, including
other parasites, shell burrowing organisms and inorganic particles (G€ otting,
1974; Lauckner, 1983). The earliest known fossil blister pearls from the Silu-
rian (Kríz, 1979; Liljedahl, 1985, 1994) and earliest known free pearls from
Triassic (Kutassy, 1937; Conway Morris, 1981; Combes, 2001; Geyer et al.,
2005; Rouse, 2005; Boucot and Poinar, 2010) are therefore not character-
istic for parasitism unless parasitic remains can be found inside of them
(De Baets et al., 2011). This is not straightforward since it has been demon-
strated that the remains of soft-bodied helminths can be destroyed during the
pearl formation process (Lauckner, 1983). However, other pathologies are
believed to be more characteristic for particular lineages of parasitic flat-
worms such as Gymnophallidae including shell pits (Ruiz and Lindberg,
1989; Ruiz, 1991; Huntley, 2007; Todd and Harper, 2011, Figure 1(e);
Huntley and Scarponi, 2012; Huntley et al., 2014; Huntley and Scarponi,
2015; Huntley and De Baets, 2015) and volcano- to igloo-shaped calcareous
concretions (Campbell, 1985; Ituarte et al., 2001, 2005; Figure 2(aec);
Huntley and De Baets, 2015). Ituarte et al. (2001, 2005) demonstrated a
link between igloo-shaped concretions and gymnophallid digenean flat-
worms, which these authors traced back to 6400 years in the Holocene. Su-
perficially, similar igloo-shaped concretions have, however, also been
reported from the Upper Silurian (Liljedahl, 1985, 1994; Figure 2(d)), but
the Paleozoic occurrence of this structure is not consistent with extant
host associations of Gymnophallidae, which typically have shorebirds (Char-
adriiformes) as final hosts (Ching, 1995), although some forms also infest
humans as final hosts (Lee and Chai, 2001). The earliest fossils that can be
confidently assigned to extant lineages of charadriiform birds are stem-group
representative of Alcidae from the Upper Eocene of North America (Mayr,
2011), although older charadriiform-like fossils have been reported from the
Lower Eocene of Denmark (Bertelli et al., 2010, 2013). Molecular clock es-
timates usually place the origin of shorebirds in the Cretaceous (Paton et al.,
2003; Baker et al., 2007), although this might be based on the incorrect
102 Kenneth De Baets et al.

(a) (b)

(c)

(d) (e)

Figure 2 Shell structures (igloo-shaped concretions, shell pits) which have been linked
with gymnophallid trematodes (Digenea) in extant and fossil bivalves. (a) Metacercaria
lodged in live position into an igloo-shaped calcareous covering of Gaimardia trapesina
(MLP 5659) from Beagle Channel in Ushuaia; note the noncalcified area around the
anterior end of the larva (photo: Cristian Ituarte; refigured from Ituarte et al. (2005).);
(b) Scanning electron micrograph of a left valve of Cyamiomactra sp. from a Holocene
sample of Río Varela (Tierra del Fuego) showing a single igloo-shaped covering just
below the anterodorsal margin (Photo: Cristia n Ituarte; refigured from Ituarte et al.
(2005).); (c) Upper view of an igloo-shaped covering in G. trapesina (MLP 5659) from
Beagle Channel in Ushuaia showing the non-calcified area in front of the igloo opening
(Photo: Cristian Ituarte; refigured from Ituarte et al. (2005).); (d) Igloo-shaped concretion
found close to posterior adductor muscle scar in the Silurian bivalve Nuculodonta got-
landica (SGU Type 1030) from the Halla Formation of Gotland (Modified from Liljedahl
(1994).); (e) Interior of right valve of Venericor clarendonensis (NHMUK PI TB 14236)
from the Eocene (subdivision B2 of the London Clay) with irregular shell deformations
and shell pits interpreted to have been produced in response to digenean trematode
infestation. Photo courtesy of Jon Todd; compare Todd and Harper (2011).
Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence 103

placement of fossil taxa (Dyke and Van Tuinen, 2004; Thomas et al., 2004;
Mayr, 2011) and/or other methodological artefacts (cf. Ksepka et al., 2014).
The appearance of shorebirds in the Cretaceous or Early Paleogene suggests
that the Paleozoic structures were probably caused by a different group of
parasites or even epizoa (Liljedahl, 1985, 1994) with similar behaviour,
although we cannot rule out the possibility that gymnophallids, or closely
related (now potentially extinct) taxa or their ancestors, had different life cy-
cles and host associations in the past. Shell pits have so far been traced back
only to the Eocene (Ruiz and Lindberg, 1989; Todd and Harper, 2011;
Huntley and De Baets, 2015), which is more or less consistent with the pres-
ence of gymnophallideshorebird associations (Figure 2).
Age: The Silurian occurrence of an igloo-shaped concretion was found
in the silicified M€ollboss 1 fauna from the Halla Formation (previously Halla
Beds) of Gotland (Liljedahl, 1985, 1994). Jeppsson et al. (2006) correlated
M€ ollboss 1 with the parvus graptolite biozone and the Ozarkodina bohemica
longa conodont subzone 2 as defined by Calner and Jeppsson (2003). The
top of the Pristiograptus dubius parvus e Gothographus nassa graptolite biozone
has been dated to 428.18  0.4796 Myr, yielded an minimum age of
427.7 Ma (Melchin et al., 2012). This is consistent with UePb age of
428.45  0.35 Myr obtained by Cramer et al. (2012) for the Gr€ otlingbo
bentonite at the nearby locality H€ orsne 3, which has been correlated with
M€ ollboss 1 (Jeppsson et al., 2006) and probably accounts for some of the sil-
ification of the strata there (Mikael Calner, personal communication 2014).

2.3 Permo-Carboniferous egg remains in shark coprolites


The earliest confident record of parasitic flatworms with complex parasite
life cycles are eggs attributed to Cestoda from the Rio do Rasto Formation
(Dentzien-Dias et al., 2013), which has been assigned to the Middle to Late
Permian (Holz et al., 2010). The eggs were obtained from a coprolite
(Figure 3(a)), which was isolated from its host and forms part of a set of
more than 800 coprolites of different shapes and sizes found in a geograph-
ically restricted area (Dentzien-Dias et al., 2012, 2013). It was identified as a
shark coprolite by its spiral structure and fossil content (Dentzien-Dias et al.,
2012, 2013). The eggs occur in a cluster (Figure 3(b)) and are ovoid, smooth
shelled and with a small operculum (polar swelling) suggesting that they are
nonerupted eggs (Figure 3(c) and (d)). Most eggs are filled with pyrite and
one egg is suggestive of containing a developing larva (Figure 3(c) and
(d)). The eggs vary little in size within the cluster, ranging from 145 to
155 mm in length and 88e100 mm in width. The morphological features
104 Kenneth De Baets et al.

(a) (b)

(c) (d)

Figure 3 Fossil evidence for the presence of derived parasitic flatworms (Cestoda) in
the Middle Permian (Modified from Dentzien-Dias et al. (2013).): (a) Picture of the spiral
heteropolar coprolite from the Rio do Rasto Formation, which has yielded the cestode
eggs, before destructive thin section analysis; (b) Thin section of the coprolite part con-
taining parasite eggs clustered in; (c) Cestode egg with a developing embryophore.
(d) Partial reconstruction of egg in (c) with interpretations of the observed structures.
Abbreviations: C ¼ capsule or shell; E ¼ embryophore (ochosphere); H ¼ putative
developing hooklets; I ¼ inner envelope; M ¼ oncospheral membrane; O ¼ outer
envelope; P ¼ putative polar thickening; Op ¼ operculum; S ¼ somatic cells.

of these eggs (operculum, egg shape and size: Figure 3(c) and (d)) as well as
their deposition together in an elongate arrangement (Figure 3(b)), which is
typical of modern tapeworm eggs deposited in mature segments or proglot-
tids, corroborates their cestode affinity.
Age: The coprolite derives from the upper member of the Rio do Rasto
Formation, which has also yielded a variety of vertebrate faunas (Dentzien-
Dias et al., 2012). The locality is located near Posto Queimado, where verte-
brate faunas indicate a Guadalupian (Late WordianeCapitanian) age (Cisneros
et al., 2012; Dias-Da-Silva, 2012). The coprolite should therefore be older
than the Guadalupian (Capitanian)eLopingian (Wuchiapingian) boundary
dated to at least 259.4 Ma (259.8  0.4 Myr: Henderson et al., 2012).
Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence 105

Older reports of potential cestode eggs (Zangerl and Case, 1976; Combes,
2001) within a Carboniferous coprolite are still controversial (Boucot, 1990;
Poinar, 2003; Dentzien-Dias et al., 2013). Strictly speaking, this coprolite
should be called a cololite as the fossilized faecal remains were found lodged
within its producer (Hunt et al., 2012). Boucot (1990) considered the report
as fairly speculative as the urea-rich environment of the dead shark would
probably lead to the rapid decomposition of such eggs, but the latest discovery
of cestode eggs in a Permian shark coprolite (Dentzien-Dias et al., 2013) illus-
trate that their interpretation as helminth eggs cannot be excluded. However,
further analyses of the morphology and the arrangement of these spherical
bodies are necessary to confirm their assignment to cestodes (Zangerl and
Case, 1976; Combes, 2001) or other parasitic helminths.
Age: The Cobelodus aculeatus specimen with the putative cestode eggs
derives from the Stark Shale, the core black shale member of the Dennis
Formation of the Missouri Series, near Fort Calhoun, Nebraska. It was
assigned to the Westphalian D by Zangerl and Case (1976) without any in-
formation corroborating this assignment. The Missouri series form part of
the local Missourian stage, which largely corresponds with the Kasimovian
(Falcon-Lang et al., 2011), which also includes the Stark Shale (Rosscoe,
2008; Rosscoe and Barrick, 2013). An age older than the Kasimoviane
Gzhelian boundary (303.6 Ma according to the 2012 Geological Timescale:
Davydov et al., 2012) can therefore be used as minimum constraint.
Pending reinvestigation of this fossil, it could extend range of cestode
eggs in shark coprolites by an additional 40 Myr.

2.4 Cretaceous egg remains in terrestrial archosaur


coprolites
The oldest fossil evidence for Trematoda is an egg which was recovered from
an Early Cretaceous isolated terrestrial vertebrate coprolite found near Bernis-
sart in Belgium (Poinar and Boucot, 2006). The producers of these coprolites
(and therefore also hosts of the parasites) are still debated (Chin et al., 1998;
Baele et al., 2012). Both Bertrand (1903) and Poinar and Boucot (2006) pre-
sented arguments that they could have been produced by theropod dinosaurs
(as opposed to crocodiles). However, theropod coprolites are rare (Hone and
Rauhut, 2010), particularly when compared with coprolites of aquatic verte-
brates (Chin, 2002) such as crocodylians in contemporary deposits (Hunt
et al., 2012). Their seemingly precise assignment to ‘Megalosaurus’ dunkeri is
therefore questionable, as it is based on the co-occurence of a single metarsal
in the same deposits. This metatarsal was originally assigned to M. dunkeri
106 Kenneth De Baets et al.

(now Altispinax dunkeri), but its morphology is only sufficient to assign it to


theropods at best (Pascal Godefroid, personal communication 2014). Never-
theless, it remains the oldest evidence for trematodes in terrestrial predatory
archosaurs (Poinar and Boucot, 2006).
Age: The fossil-bearing strata are now more precisely dated to be of Late
Barremian to Early Aptian age (Yans et al., 2005; Schnyder et al., 2009; Yans
et al., 2012), corresponding with the upper part of magnetochron M1n, M0r
and the basal part of M0n. This yields an approximate minimum age for
these strata of 125.93 Ma, the age attributed to the top of magnetochron
M0r by Ogg (2012), or a more conservative age of 125.7 Ma, the age
assigned to the base of the Tethyan Deshayesites deshayesi ammonoid biozone
(Schnyder et al., 2009) by Ogg et al. (2012).

2.5 Eocene shell pits in intermediate bivalve hosts


The oldest evidence for the presence of Gymnophallidae might lie in the
Eocene in the form of characteristic shell pits found in their intermediate
bivalve hosts (Ruiz and Lindberg, 1989, Figure 2(e), Todd and Harper,
2011). These characteristic pits have been reported throughout the Cenozoic
from the Eocene to the Holocene (Johannessen, 1973; Ruiz and Lindberg,
1989; Ruiz, 1991; Huntley, 2007; Todd and Harper, 2011; Huntley and
Scarponi, 2012, 2015; Huntley et al., 2014; Huntley and De Baets, 2015).
These pits have been commonly linked with Gymnophallidae (Ruiz and
Lindberg, 1989; Todd and Harper, 2011), although superficially similar
structures might also be caused by other digenetic trematodes such as Lep-
ocreadiidae (Ituarte et al., 2001; see review by Huntley and De Baets, 2015).
Age: The oldest precisely dated shells (Venericor clarendonensis) with pits
derive from subdivision B2 of the London Clay, Eocene (Todd and Harper,
2011). Berggren and Aubry (1996) assigned this unit to upper calcareous
nannofossil zone NP11, which corresponds with a minimum age of 53.9 Ma
according to the 2012 Geological Timescale (Vandenberghe et al., 2012).
Further support could come from the distribution of volcano-shaped
(Campbell, 1985) to igloo-shaped calcareous concretions (Ituarte et al.,
2001, 2005), which have been traced back to at least 6240  70 years BP
in the Holocene (Ituarte et al., 2005). Despite a certain degree of variability
in these structures in extant bivalves, they are believed to be characteristic for
gymnophallid trematodes (Campbell, 1985; Ituarte et al., 2001, 2005).
Studies on pathology have focused on invertebrate intermediate hosts
(Ruiz and Lindberg, 1989; Ituarte et al., 2001, 2005; Huntley, 2007;
Huntley and Scarponi, 2012; Huntley et al., 2014; Huntley and De Baets,
Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence 107

2015), although some pathologies in vertebrate intermediate hosts have also


been linked with parasitic flatworms. The best examples are probably the
teratological limb malformations in North American amphibians, which
have been linked with the trematode Ribeiroia on several occasions (Johnson
et al., 2001, 2002; Stopper et al., 2002; Johnson and Sutherland, 2003; John-
son and Chase, 2004; Koprivnikar et al., 2012) and could potentially be found
in the fossil record (cf. Fr€
obisch et al., 2014). Nevertheless, limb malforma-
tions e including supernumerary limbs and bone bridges e can have various
other causes, meaning their interpretation is not always straightforward
(Blaustein and Johnson, 2003; Lunde and Johnson, 2012).

2.6 Eggs remains in a Pleistocene mammal coprolite


The oldest Quaternary flatworm evidence is derived from an isolated Mid-
dle Pleistocene mammal coprolite ( Jouy-Avantin et al., 1999), which these
authors attributed to Ursidae based on its morphology and associated fossil
finds. The morphology of the eggs (asymmetrical shell, the brown colour
and the presence of an operculum) is characteristic of dicrocoelid flatworms,
which makes this the oldest direct evidence for the presence of dicrocoelid
flatworms (Digenea: Dicrocoelidae). They could not be assigned to a partic-
ular genus, although their dimensions are reminiscent of Dicrocoelium and
Eurythrema based on egg measurements.
Age: The coprolite (H13 HEN5 1526) derives from an archeological
layer at the Caune de l’Arago cave (Tautavel, Pyrénées-Orientales, France)
and could be dated to a minimum age of 550,000 years BP (Jouy-Avantin
et al., 1999) during a cold and dry climatic period (Lumley et al., 1984).

2.7 Holocene evidence for parasitic flatworms from ancient


remains
Other Quaternary parasitic flatworm fossils and subfossils derive from the
Holocene, mostly from archeological sites (see Gonçalves et al., 2003 for a
review, Searcey et al., 2013; Ara ujo et al., 2014; Beltrame et al., 2014),
with possible ages up 6368 years BP for Trematoda and ages up to
10,000 years BP for Cestoda. They can provide upper constraints for the
earliest appearance of various taxa of Cestoda and Trematoda, including
genera and species. The age assignment used in archeological publications
can be a bit confusing. Before Present (BP) stands for a timescale, which
starts at the 1st of January 1950 reflecting the fact that radiocarbon dating
became practicable around that time and also antedates large-scale nuclear
weapons testing altering the global ratio of carbon isotopes (Taylor,
108 Kenneth De Baets et al.

1985). Archeological publications often use BC (Before Christ) and AD


(Anno Domini). Hundred years BP is 100 years before 1950 (i.e. the year
AD 1850). At ages older than about 0.5 Ma, the difference between BP
and AD becomes negligible. We herein use the dates mentioned in the orig-
inal publications to avoid confusion. Note that age assignment might change
or differ according to the dating methods used (Iles, 1980). We recommend
using the most conservative age estimates using reliable methods.
Remains of the Cestoda Diphyllobothrium pacificum can be traced back to
about 10,000e4000 BP according to Reinhard (1992), although the exact
evidence for such an age were not discussed in this paper. The record of ano-
plocephalid cestodes can be traced back to at least 8920  200 years BP
based on eggs founds in coprolites attributed to humans (Fugassa et al.,
2010). Anoplocephalid remains which could be more specifically deter-
mined as Monoecocestus can be found in rodent coprolites dated as old as
6700  70 years BP (Sardella et al., 2010). The earliest reports of Hymenole-
pis were dated approximately from 4000 to 2000 years BC (Gonçalves et al.,
2003) and Taenia eggs from an Egyptian mummy attributed to about
3200 years BC (Reyman et al., 1977). According to Gonçalves et al.
(2003), trematodes (Fasciola as well as Opisthorchioidea) can be traced
back to at least 5400  40 to 5230  40 years BP (Roever-Bonnet et al.,
1979), Dicrocoelium can be traced back to 3384e3370 BC (Dommelier
Espejo, 2001), Schistosoma can be traced back to 3200 years BC based on
the discovery of Schistosoma haematobium antigen in the shin tissue of an
Egyptian predynasty mummy (Deelder et al., 1990) and Schistosoma ova in
another contemporary mummy (Reyman et al., 1977), and as Clonorchis
sinensis could be traced back to a mummy from Chu Dynasty (475e
221 years BC) with an age of at least 2171 years BP (Wen-yuan et al.,
1984). Eggs of S. haematobium were one of the earliest to be discovered in
Egyptian mummies.
Recently, ancient DNA of echinostomatid trematodes was extracted
from coprolites of the extinct ratite bird Megalapteryx from New Zealand
(Wood et al., 2013), which might range from about 6368 years BP to the
694  30 years BP, coincident with the time of their extinction (Wood
et al., 2012).

2.8 Free-living flatworms


The body fossil record of free-living flatworms is also of little help as it is
poorer or even more patchy than the fossil record of parasitic flatworms
(Poinar, 2003). The oldest free-living flatworm body fossils derive from
Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence 109

Eocene Baltic amber (Poinar, 2003) and calcareous nodules of Miocene age
(Pierce, 1960; Poinar, 2003), and those of flatworm egg capsules from Qua-
ternary lake sediments (Frey, 1964; Harmsworth, 1968; Gray, 1988). These
fossils considerably post-dated divergence time estimates for free-living flat-
worms derived from molecular clock studies. Older molecular clock studies
place the origin of (free-living) Platyhelminthes deep in the Precambrian
(Hausdorf, 2000; Otsuka and Sugaya, 2003), but more recent relaxed molec-
ular clock studies place their origins between the latest Precambrian (Edia-
caran) and the early Cambrian (Douzery et al., 2004; Peterson et al., 2004,
2008; Erwin et al., 2011). Some Ediacaran fossils have occasionally been
related to free-living flatworms (Allison, 1975; Palij et al., 1979; Fedonkin,
1985), although they cannot be confidently assigned to the phylum (Conway
Morris, 1981; Labandeira, 2002; Erwin et al., 2011). Even Dickinsonia was
assigned to flatworms at one point (Palij et al., 1979; Conway Morris,
1981). The taxonomic position of Dickinsonia has been heavily debated
(Retallack, 2007; Brasier and Antcliffe, 2008) and this taxon is often inter-
preted as one of the earliest divergent metazoans (Xingliang and Reitner,
2006; Sperling and Vinther, 2010). Various Permian to Triassic trace fossils
have also been attributed to turbellarians including Polycladida and Tricladida
(Alessandrello et al., 1988; Knaust, 2010). The assignment of trace fossils to
this phylum is also problematic as various worm-like groups with similar ecol-
ogy and mode of locomotion could also have produced these traces (Sei-
lacher, 2007). Curvolithus has also been attributed to flatworms (Seilacher,
2007), but could also have been produced by other taxa with similar behav-
iour (Buatois et al., 1998). Further studies of traces produced by extant forms
as well as fossil traces associated with body fossils are therefore important to
confidently assign them to the phylum (Collins et al., 2000; Knaust, 2010).
The oldest parasitic flatworm fossils are therefore not only important for
putting constraints on free-living flatworms, but also on the presence of
Platyzoa in the fossil record, a group currently containing both parasites
(Platyhelminthes, Acanthocephala) and free-living taxa (Wey-Fabrizius
et al., 2013). The assignment of Cambrian fossils (cambroclaves) to the Acan-
thocephala as suggested by some authors (Qian and Yin, 1984), which has also
been followed in some recent classifications (Amin, 2013), is highly question-
able and widely rejected (Conway Morris et al., 1997; Elicki and Wotte,
2003; Kouchinsky et al., 2012). These problematic Cambrian organisms
can be classified as Lophotrochozoa at best (Kouchinsky et al., 2012);
Compare Conway Morris and Crompton (1982) and Near (2002) for further
speculations and hypotheses on the origin and evolution of parasitism towards
110 Kenneth De Baets et al.

the rise of the Acanthocephala. Furthermore, the oldest accepted record of


Rotifera, the free-living relatives of Acanthocephala, derives from Dominican
amber deposits (Waggoner and Poinar, 1993), which is now more confi-
dently dated to the Miocene (Iturralde-Vinent and MacPhee, 1996;
Iturralde-Vinent, 2001). The oldest confidently assigned Acanthocephala re-
mains have been reported from archeological sites (Gonçalves et al., 2003);
some dating back to 9500 years BC according to Fry and Hall (1969). Consid-
ering that multiple authors (Upeniece, 2001, 2011; Littlewood and Donovan,
2003) have suggested that the Middle Devonian hook circlets might belong to
a platyzoan helminth, a putative reinvestigation of these fossils could be used
to constrain the evolutionary history of this entire group. Many studies on
extant flatworms have focused on the hook elements of particular groups
(Vignon and Sasal, 2010; Vignon, 2011) or taxa (Shinn et al., 2003). Informa-
tion and illustrations of these helminth structures can also be found in
comprehensive systematic treatments: Yamaguti (1959), Schmidt (1986)
and Khalil et al. (1994) for Cestoda; Yamaguti (1963a) for Monogenea and
Yamaguti (1963b) and Golvan (1969) for Acanthocephala.

3. INTERPOLATING OR EXTRAPOLATING EXTANT


PARASITEeHOST RELATIONSHIPS AND THE
ASSUMPTION OF PARASITEeHOST COEVOLUTION
Analysis of the range of current parasiteehost associations has often
been used to infer the evolutionary origin of parasitic organisms (Littlewood
and Donovan, 2003). With the exception of highly derived taxa, parasitic
flatworms do not parasitize hagfishes or lampreys (Littlewood, 2006).
This may suggest that parasitic flatworms evolved in basal gnathostomes
(Littlewood, 2006), which would lie somewhere around the Cambriane
Ordovician based on the host fossil record (Friedman and Sallan, 2012;
Donoghue and Keating, 2014). This considerably predates the oldest gener-
ally accepted fossil evidence for parasitic flatworms, but the fossil record
indicates that other groups like pentastomids, which parasitize vertebrates
today and might have done in the past, were already around at this time
(Walossek and M€ uller, 1994; Walossek et al., 1994; Maas and Waloszek,
2001; Waloszek et al., 2005; Sanders and Lee, 2010; Castellani et al.,
2011). If we map the fossils of parasitic flatworms on their host phylogenies
(Figure 4), they are at least consistent with extant parasitic flatwormehost
associations, which is not the case for all parasites (Figure 5). Pentastomids
mainly parasitize terrestrial vertebrates today (Christoffersen and De Assis,
Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence 111

Figure 4 Fossil finds of putative flatworm fossils discussed in the text mapped on their
host phylogeny, which was modified from Donoghue and Smith (2003) and Rowe
(2004) taking into account new phylogenetic hypotheses summarized in Donoghue
and Keating (2014).

2013), but in the CambrianeOrdovician (Walossek and M€ uller, 1994;


Walossek et al., 1994; Waloszek et al., 2005; Castellani et al., 2011), they
are found in marine deposits and there were no terrestrial vertebrates to serve
as hosts at this time. Their morphology indicates a parasitic lifestyle, but the

Figure 5 Comparisons of the consistency between extant and fossil host ranges of
parasitic flatworms and pentastomids. Host phylogeny was modified from
Goudemand et al. (2011). Note that the host gap would be considerably greater if
the position of conodonts would be more basal as postulated by some authors (Blieck
et al., 2010; Turner et al., 2010). Recent discoveries of Silurian pentastomids associated
with ostracods even further extend the host gap between fossil and extant pentasto-
mids (Siveter et al., 2015).
112 Kenneth De Baets et al.

exact host of these marine forms is still unknown as they were not found
directly associated with their hosts. Some have suggested their hosts might
have been conodonts (Walossek and M€ uller, 1994), of which tooth-like
remains have been commonly found in these deposits. Interestingly, the
CambrianeOrdovician fossil pentastomids resemble larvae of modern forms
that can infest fish, making it conceivable that these small pentastomids
represent adults that spent their entire life cycle on small fish-like vertebrates
(Sanders and Lee, 2010). The range of the host gap between Cambrian and
extant pentastomids (Figure 5) might therefore depend on the systematic
position of conodonts, which is still debated. Most authors agree that con-
odonts are chordates, probably either stem- or crown-vertebrates (Blieck
et al., 2010; Turner et al., 2010; Goudemand et al., 2011; Murdock et al.,
2013; Donoghue and Keating, 2014). Interestingly, putative pentastomid
remains were recently also reported from ostracods within the Silurian
Herefordshire Lagerst€atte (Siveter et al., 2015), which further increases the
host gap between extant and fossil pentastomids. This might suggest that in-
vertebrates might have been the initial hosts in the marine realm, if ostracods
are the final hosts as suggested by these authors and if no host switching
occurred between the Cambrian and the Silurian. However, pentasto-
midehost associations from the Cambrian and Ordovician lagerst€atten
would be necessary to further test this hypothesis.
Thus, it is not always possible to precisely constrain parasiteehost asso-
ciations in the fossil record. This is not only the case for isolated remains
of parasites not directly attached to their hosts (Castellani et al., 2011), but
also for parasite remains found in isolated coprolites not confidently assign-
able to precise host taxa (Jouy-Avantin et al., 1999; Poinar and Boucot,
2006; Dentzien-Dias et al., 2013).
Fossils of potential hosts might be common or present in the same layers,
although without direct evidence for a parasitic relationship (attached or
found within well-preserved body fossils of their hosts), appointing a poten-
tial host remains within the realm of speculation. In the case of intermediate
hosts, where the fossil evidence is often pathologies or traces, it is hard to be
certain of the identity of the culprits since various organisms with similar
behaviour can produce similar traces. Furthermore, it might also be hard
to identify the final host without finding remains of the putative parasite
associated with them. Predatoreprey relationships might provide a clue
(Ruiz and Lindberg, 1989; De Baets et al., 2011), but direct evidence for
predation from one taxon on another is rare in the fossil record too (Brett
and Walker, 2002; Walker and Brett, 2002). Nevertheless, age in itself might
Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence 113

be sufficient to rule out certain hosts if they had not yet evolved, they must
have had different intermediate and/or final hosts at that time. Although the
hosts of CambrianeOrdovician pentastomids remain speculative, hosts
assignable to taxa they currently parasitize were not around yet, so they
must have had additional parasiteehost associations in the past which are
now extinct.

4. MOLECULAR CLOCK STUDIES


Molecular clock (timetree) methods for calibrating phylogenies
have the potential to be useful to discriminate evolutionary scenarios in
parasite evolution or hosteparasite associations (Hypsa, 2006). However,
molecular clocks still need to be calibrated to obtain absolute age estimates,
which is not that straightforward among parasite groups with a patchy fossil
record. Thus, a cophylogenetic approach has been used (Hafner et al.,
1994; Page et al., 1998; Light and Hafner, 2007), which may in turn pro-
vide a robust evolutionary timescale for apparent cospeciating symbiotic
species when the timescale of the host lineage is (comparably) well con-
strained (Moran et al., 1993, 1995). Due to the lack of well-preserved spec-
imens in parasitic flatworms, most molecular clock studies have relied on
the host fossil record to inform divergence estimates (Verneau et al.,
2002, 2009a,b; Olson et al., 2010; Badets et al., 2011; Héritier et al.,
2015). More rarely biogeography (focusing on vicariance events) has
been invoked to constrain molecular clock estimates of parasitic flatworms
(Zietara and Lumme, 2002; Waltari et al., 2007; Badets et al., 2011;
Martínez-Aquino et al., 2014). Only one study (Perkins, 2010) used the
parasitic flatworm fossil record as a calibration, although it relied on the
Upper Devonian and Carboniferous putative flatworm fossils, whose taxo-
nomic assignment to Monogenea and Cestoda, respectively, is still debated
(as discussed above). Other studies have relied on molecular substitution
rates derived from other studies (Despres et al., 1992; Zietara et al.,
2002; Huyse and Volckaert, 2005), which is even more problematic
(Papadopoulou et al., 2010; Hipsley and M€ uller, 2014).
The best practice for using fossils for molecular clock calibration has been
discussed and reviewed extensively (Donoghue and Benton, 2007; Benton
et al., 2009; Parham et al., 2012). Most authors agree that the fossil speci-
mens can only directly provide a well-justified minimum constraint for
the origin of some particular lineages. According to Parham et al. (2012),
114 Kenneth De Baets et al.

fossil calibrations are well justified if the following criteria are fulfilled:
(1) listing of museum numbers of specimen(s) that demonstrate all the rele-
vant characters and provenance data, (2) availability of apomorphy-based
diagnoses of the specimen(s) or an explicit, up-to-data, phylogenetic analysis
that includes the specimen(s), (3) explicit statements on the reconciliation of
morphological and molecular data sets, (4) specification of the locality and
stratigraphic level (to the best current knowledge) from which the calibrat-
ing fossils are derived, (5) reference to a published radioisotopic age and/or
numeric timescale with details on its selection. Divergence time estimation is
not possible with minimum constraints alone, as the substitution rate is var-
iable and unknown; therefore, at least one point calibration or maximum
constraint is required to calculate the substitution rate and absolute diver-
gence times (Warnock et al., 2012).
It would therefore be more appropriate to use the oldest estimate (95%
confidence maximum) for the origin of the total group from a robust
molecular clock analysis as the maximum, and the oldest fossil assignable
with confidence to the crown group (as the minimum), to constrain the
evolutionary history of the host (and the parasite). For example, if the origin
of parasitic flatworms occurred during the early evolution of gnathostomes
as suggested by Littlewood (2006), this would mean they originated bet-
ween the Cambrian (643 Ma: oldest confidence intervals of Erwin et al.,
2011 for this node) and the earliest well-dated fossils that can be confidently
assigned to crown-group gnathostomes deriving from Ordovician
(w421.8 Ma: Benton et al., 2009; Donoghue and Keating, 2014). Alterna-
tively, the entire 95% confidence posterior interval (from robust molecular
clock studies) for diverging host clades could be used as priors on the clade
ages in the parasites.
A more conservative and less circular approach would be to use the lat-
est robust relaxed molecular clock estimates for the origin of their free-
living ancestors (744 Ma: oldest confidence of Erwin et al., 2011 for this
node) and the earliest certain appearance of parasitic flatworms in the fossil
record, which would be only Permian (>259.4 Ma as discussed above).
This would yield quite large confidence intervals (cf. Warnock et al.,
2012 for Parasitiformes), but such estimates would be more honest and
accurate (closer to reality) than seemingly precise estimates which are argu-
ably inaccurate, since the origin of parasitism falls outside the calibration
interval a priori (Warnock et al., 2011). Furthermore, reinvestigation of
putative flatworm trace or body fossils from Upper Silurian (>427.7 Ma)
or Middle Devonian (>381.9 Ma) deposits might further narrow this
Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence 115

time interval in the future. The fossil record also provides constraints on the
origin of Cestoda in shark hosts (Dentzien-Dias et al., 2013) and Trema-
toda in archosaur hosts (Poinar and Boucot, 2006). Furthermore, the fossil
record provides upper constraints on the origin of Gymnophallidae in the
form of characteristic pathologies, dicrocoelid flatworms derived from eggs
in coprolites as well as several genera and even species from archeological
sites (e.g. Dicrocoelium, Diphyllobothrium, Fasciola, Monoecocestus, Schistosoma,
Taenia).
The oldest fossil evidence for schistosomes are antigens deriving from a
3200 BC Egyptian mummy, but the origin of this group is believed to be
considerably older based on the evolutionary history of their intermediate
or final hosts (Lawton et al., 2011). Davis (1993) suggested that the genus
Schistosoma arose before the breakup of the supercontinent Gondwana
over 150 Ma based on the distribution of their snail hosts and that ancestors
of Asian schistosomes were carried to Asia via India after it separated from
Africa. More recent studies (Snyder and Loker, 2000) have suggested a
younger, ancestral Asian origin somewhere in the Miocene, which might
indicate that schistosomes only colonized Africa around 15e20 Ma (Lawton
et al., 2011). Performing a robust molecular clock analysis using dates of fos-
sil Schistosoma and their hosts might be a more formal way to test these
hypotheses. In some cases, additional historical dates might become avail-
able to constrain certain nodes such as the possible slave transport of Schis-
tosoma mansoni to South America (Lockyer et al., 2003b), which is so far not
contradicted by finds of older remains of S. mansoni in archeological sites of
South America (Gonçalves et al., 2003). Direct dating of samples yielding
ancient DNA (Wood et al., 2013) might also provide additional constraints
in such studies. However, a recent study by Mello et al. (2014) has demon-
strated that the assignment of calibration information to deeper phyloge-
netic nodes is more effective in obtaining more precise and accurate
divergence time estimates compared to analyses involving calibration at the
shallowest node.
Most authors agree that multiple, well-justified calibrations are the best
approach to obtain the most robust and accurate molecular clock estimates
(Warnock et al., 2011; Parham et al., 2012). Note that careful a priori selec-
tion of suitable calibration points cannot be replaced by using as a posteriori
cross-validation procedures (Near et al., 2005; And ujar et al., 2014) as these
only verify consistency (Clarke et al., 2011). In some cases, multiple inaccu-
rate calibrations might be consistent, which can result in erroneous rejection
of more reasonable calibrations. Furthermore, consistent calibrations may be
116 Kenneth De Baets et al.

redundant by definition, since they fail to correct for changes in rate varia-
tion (Clarke et al., 2011; Warnock et al., 2015). Furthermore, calibration
should be implemented in the most conservative way, which might result
in less precise, but ultimately more accurate divergence estimates (Warnock
et al., 2012).
In the absence of a suitable fossil record, one could resort to the use of
biogeographic events or calibrations related only to the host fossil record.
Nevertheless, both methods also have their problems and add an additional
component of circularity to calibration procedures depending on the
hypotheses being tested (Hipsley and M€ uller, 2014). Biogeographic calibra-
tions as they are currently implemented are problematic (Goswami and
Upchurch, 2010; Kodandaramaiah, 2011; De Baets and Donoghue, 2012;
Hipsley and M€ uller, 2014), and they should be implemented more con-
servatively. It should be established when a certain barrier, causal to a given
speciation event, actually occurred (De Baets and Donoghue, 2012;
Warnock, 2014).
Most importantly, there remains an assumption that biogeographic distri-
butions have not changed significantly in geological time, making it harder to
establish whether biogeographic barriers were coincident with speciation
events, and introduce an aspects of circularity (Crisp et al., 2011). Having
taxon-area relationships consistent or inconsistent with biogeographic
events, does not necessarily mean that these clades diversified at the same
time as these events, because older events might have led to similar distribu-
tions (pseudo-congruence) or younger events might have altered their dis-
tributions (pseudo-incongruence; see Donoghue and Moore, 2003). Even
for some of the classical examples of groups with current distributions
congruent with vicariance, such as onychophorans and cichlids, studies
have demonstrated that divergence might predate (Murienne et al., 2014)
or postdate (Friedman et al., 2013) the continental break-up of superconti-
nents, respectively.
Using the fossil record of hosts also introduces an aspect of circularity in
addition to other considerations related with fossil calibrations (Donoghue
and Benton, 2007; Parham et al., 2012) as discussed above. It assumes that
the current parasiteehost associations did not markedly change through
geological time, which is not necessarily true, particularly in groups which
are estimated to range several hundred million years into the past (e.g. the
pentastomid example we discussed above). Using hosts also leads to circular
reasoning when employing them to investigate hypotheses of parasiteehost
coevolution. In highly host-specific lineages with simple life cycles like the
Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence 117

Polystomatidae (Figure 6), it might work well, but for groups with common
host switches and/or complex life cycles this approach might be less suitable.
The most conservative way to implement them would be to use the oldest
reliable estimate for the origin of this group as a maximum and the oldest
from well-attributable fossil to this lineage as a minimum. Polystomatid flat-
worms are one of the most host-specific groups of parasitic flatworms and
their direct life cycle that involves a short free-living aquatic larval stage
(which means they are probably only passively disseminated by their hosts),
have made them an ideal model to test the use of constraints from biogeog-
raphy and the host fossil record (Bentz et al., 2001, 2006; Verneau et al.,
2002, 2009a,b; Badets et al., 2011). Verneau et al. (2002) used 425 Ma to
calibrate the split between Actinopterygii and Sarcopterygii (Figure 6),
although this event must have happened at the latest by about 419 Ma
(Zhu et al., 2009). However, it would be more conservative to use the oldest
robust estimate from relaxed molecular clock studies for the separation of
actinopterygian from sarcopterygians and the earliest fossil confidently
assigned to either tetrapods or lungfishes to constrain this node (Badets
et al., 2011). The oldest stem-group lungfish is generally considered to be
Diabolepis (Friedman, 2007; Qiao and Zhu, 2009), while one of the oldest
ingroup lungfishes might be Westollrhynchus (Qiao and Zhu, 2009). Badets
et al. (2011) also suggested that some dates might be consistent with the
break-up of the supercontinent Gondwana, although this needs to be
further tested with additional sampling.
Taxon sampling can play a large role in tree reconstruction and interpre-
tation with respect to biogeography (Trewick and Gibb, 2010) or host
switching (Hafner and Page, 1995). In the case of lineages or parasitee
host associations, which have been around for many hundreds of millions
of years, host range changes and extinction might contribute significantly
to missing taxa, making it hard to infer past biogeographical distribution
or parasiteehost associations, from extant data alone. There is at least
some evidence that extinction might also have played a role in parasitic flat-
worms and other helminths over longer timescales as several parasiteehost
associations documented in the (sub)fossil record are now evidently extinct
(Upeniece, 2001, 2011; Poinar and Boucot, 2006; Wood et al., 2013).
Furthermore, molecular studies with greater taxonomic coverage have
particularly focused on biomedically or economically important taxa such
as Schistosomatidae (Lockyer et al., 2003b; Orélis-Ribeiro et al., 2014) or
particular lineages with a high host specificity such as Polystomatidae (Bentz
et al., 2001, 2006; Badets et al., 2011, 2013; Héritier et al., 2015). To better
118 Kenneth De Baets et al.

Figure 6 Ultrametric tree of neobatrachian polystomes inferred from MULTIDIVTIME


(Modified after Verneau et al. (2009b).). Calibration points (black rectangles, nodes
1e3) were deduced from historical biogeographical scenarios suggested by Bentz
et al. (2001, 2006) and Badets et al. (2011). The divergence of the lineage associating
Metapolystoma, Eurasian and African Polystoma from their closest South and North
American relatives (nodes 1 and 2) was constrained between 65 and 56 Myr, reflecting
vertebrate exchanges between the two Americas in the Paleocene (Gayet et al., 1992)
and possible dispersal to Eurasia via Beringia. The divergence between the European
Polystoma species (i.e. Polystoma gallieni) and the lineage grouping Metapolystoma
and African Polystoma was constrained between 25 and 5 Myr, reflecting the
Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence 119

understand the evolutionary history using molecular methods, it is essential


to sample as many distinct lineages of parasites as possible as well as their free-
living relatives, focusing particularly on evolutionary important taxa which
have putative fossil records (e.g. Gymnophallidae, basal Monogenea, Ces-
toda) or reliable geological constraints derived from biogeography or the
evolutionary history of their hosts.
When no appropriate constraints are available, relative rates of uncali-
brated molecular clocks can be used to test the support or reject the temporal
congruence of parallel distributions or parasite-host evolution (Loader et al.,
2007; Hibbett and Matheny, 2009; Loss-Oliveira et al., 2012). Nevertheless,
it should be kept in mind when interpreting the results that the rate of
molecular evolution might be significantly different between parasites and
hosts (Page et al., 1998) or within and between lineages of parasites and/
or hosts (Thomas et al., 2006, 2010; Bromham, 2009), which can bias the
results of such studies (Hipsley and M€ uller, 2014). Furthermore, novel prob-
abilistic approaches make it possible to incorporate in biogeographic infer-
ence, estimates of the divergence time of lineages as well as external
sources of evidence such as climate, geography, their fossil record or ecolog-
ical tolerance (Sanmartín, 2012).

5. CONCLUSIONS AND FUTURE PROSPECTS


The earliest fossil evidence for the presence of helminths falls in the
Middle Devonian in the form of hooks, some of which are most reminis-
cent of extant Monogenea, although some could also belong to Acantho-
cephala or more derived flatworms (Cestoda). The oldest secure record of
parasitic flatworms with complex parasite life cycles lies in the Permian
which can be confidently assigned to cestodes, although the presence of

=
hypothesized ages of dispersal routes between Eurasia and Africa (Rage, 1988; Bentz
et al., 2001). Finally, the root prior was set at 160 Ma (sd  5 Myr), corresponding to an
initial divergence separating Asian and Australian polystomes from all other neobatra-
chian polystomes (Badets et al., 2011), hypothetically corresponding to a separation of
the western and eastern components of Gondwanaland. Divergence time estimates
(see Verneau et al., 2009b) are reported for two nodes that are relevant for understand-
ing the origin of the new Malagasy genus, i.e. Madapolystoma (see Du Preez et al.,
2010). According to Verneau et al. (2009b), Madapolystoma would have diverged
from Eupolystoma about 116 Ma (node A) and the first crown divergence in Madapo-
lystoma (node B) would have occurred about 63 Ma.
120 Kenneth De Baets et al.

igloo-shaped concretions reminiscent of those caused by gymnophallid


trematodes in extant bivalves might already indicate the presence of
derived parasitic flatworms with complex parasite life cycles in the Late
Silurian (>428 Ma). These Silurian occurrences are, however, not consis-
tent with evolutionary history of current gymnophallid hosts (shorebirds),
which are believed to have appeared somewhere between the Cretaceous
and Eocene. Characteristic pits in bivalves shells indicative for the presence
of digenetic trematodes (Gymnophallidae) appear already in the Eocene
(Ruiz and Lindberg, 1989; Todd and Harper, 2011; Huntley and De Baets,
2015), which is more or less consistent with the presence of their final host
in the fossil record. The first evidence for terrestrial parasitic flatworms and
trematodes was found in the form of eggs within a Lower Cretaceous
coprolite (Poinar and Boucot, 2006), which can be confidently attributed
to archosaurs (potentially theropod dinosaurs or crocodylians). The earliest
evidence for dicroelid trematodes (Jouy-Avantin et al., 1999) falls at about
0.55 Ma in the Middle Pleistocene. Various extant genera and species have
been described from younger archeological sites (Gonçalves et al., 2003;
Araujo et al., 2014). Several putative flatworm fossils need additional study
to confidently assign them to a certain lineage of flatworms including pla-
tyzoan helminth hooks in Middle Devonian gnathostomes, putative
cestode eggs in a Carboniferous shark coprolite and eggs in a Cretaceous
archosaur coprolite. Remarkably, the fossil record of parasitic flatworms
in considerably better than that of free-living flatworms (Poinar, 2003)
and Platyzoa in general (Conway Morris and Crompton, 1982; Wey-
Fabrizius et al., 2013) and it could therefore be used to constrain the evolu-
tionary origin of flatworms and other Platyzoa. Only rarely have studies
been performed to assess the evolution of these structures over larger scales;
e.g. see Malmberg (1990) for Monogenea, which is a rather controversial
study for different reasons (Gusev, 1992). A comparative analysis of hook
elements of acanthocephalans and parasitic flatworms (Monogenea, Ces-
toda) in a new molecular phylogenetic framework would therefore be in
order to more confidently assign the fossil hook circlets to a certain clade
or phylum. Furthermore, the study of eggs as well as hook circlets, which
is now largely done with destructive methods and in two dimensions,
would benefit from CT-scanning technologies to characterize their 3D-
morphology and structure in a nondestructive way and potentially reveal
additional details or fossils which otherwise might be destroyed by the sam-
ple preparation process (e.g. thin-sectioning, chemical sample preparation,
resedimentation procedures).
Constraining the Deep Origin of Parasitic Flatworms and Host-Interactions with Fossil Evidence 121

Fossil evidence can only provide minimum time constraints and is not avail-
able for all lineages of parasitic flatworms. Interpolations based on parasiteehost
associations or biogeographic events can potentially be used to supplement fos-
sil constraints. However, circularity in testing hypotheses should be avoided
and caution should be taken when multiple host-switching events are sus-
pected. Before using such calibrations it should be at least verified if this hypoth-
esis is robust to a wider sampling of extant and extinct taxa as well as the
evolutionary history of their hosts, where the sampling and fossil record might
be comparatively better. We therefore advise implementing such calibrations in
the most conservative way. For calibrations based on the evolutionary history of
parasites or their hosts, this would correspond with using the oldest estimate
based on relaxed molecular clock estimates as maximum and the oldest well-
attributable fossils of the parasite or its host as a minimum; for calibrations based
on biogeographic events, this would correspond to the using the oldest age of
the oldest geological event that could have influenced the distribution of the
parasites and their hosts as a maximum and the youngest age of the geological
events that could have influenced their distribution as a minimum.
Several recent discoveries indicate that exceptionally preserved gnathos-
tomes or their coprolites might yield additional finds of parasitic flatworm
fossils, particularly their attachment organs or their eggs (Littlewood and
Donovan, 2003; Poinar and Boucot, 2006; Dentzien-Dias et al., 2013),
which can be characteristic for certain lineages. Novel methods like exper-
imental decay studies or computer tomography might provide additional
insights into the phylogeny, 3D-morphology and ecology of such fossils.
The future of constraining the evolutionary history of Platyzoa and parasitic
flatworms lies in molecular clock methodology by combining information
from the geological record (particularly body fossils or eggs) and molecular
sequences with the fewest assumptions. Characteristic pathologies might also
put constraints on the evolutionary history of parasitic flatworm, although
this still needs to be further studied in extant and fossil hosts to establish a
robust relationship with a particular lineage of parasites (Campbell, 1985;
Ituarte et al., 2001, 2005).

ACKNOWLEDGEMENTS
Michael Calner (Lund University), Ervıns Luksevics (University of Latvia, Riga), Steve Ross-
coe (Hardin-Simmons University), Pascal Godefroit (Royal Belgian Institute of Natural Sci-
ences, Brussels) and Jon Todd (Natural History Museum, London) are thanked for pointing
us to literature with the latest stratigraphic assignment of the Silurian, Upper Devonian,
Carboniferous, Cretaceous and Eocene flatworm fossils, respectively. Jon Todd (Natural
122 Kenneth De Baets et al.

History Museum, London) and Cristian Ituarte (Museo Argentino de Ciencias Naturales,
Buenos Aires) kindly put pictures of bivalve pathologies linked to trematode parasites at
our disposal. This research was partially funded by an SNF grant (2012e141438) to Kenneth
De Baets. Rodney Bray (Natural History Museum, London, retired), John Huntley (Univer-
sity of Missouri, Columbia), Tim Littlewood (Natural History Museum, London) and Rachel
Warnock (Smithsonian National Museum of Natural History, Washington) kindly read and
commented on previous versions of this manuscript.

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CHAPTER FOUR

From Fossil Parasitoids to Vectors:


Insects as Parasites and Hosts
Christina Nagler, Joachim T. Haug1
Department of Biology II, Functional Morphology Group, University of Munich (LMU),
Planegg-Martinsried, Germany
1
Corresponding author: E-mail: jhaug@bio.lmu.de

Contents
1. Introduction 139
1.1 Insects as parasites and hosts 139
1.2 Insects in the fossil record 140
2. Insect Parasitism sensu stricto (s. str.) e Paraneoptera 142
2.1 Phthiraptera 142
2.1.1 General aspects 142
2.1.2 Phylogenetic inference of appearance and molecular estimations of early 143
evolution
2.1.3 Fossil representatives 145
2.2 Hemiptera 146
2.2.1 General aspects 146
2.2.2 Phylogenetic inference of appearance and molecular estimations of early 146
evolution
2.2.3 Fossil representatives 146
3. Insect Parasitism s.str. e Antliophora 147
3.1 Siphonaptera 148
3.1.1 General aspects 148
3.1.2 Phylogenetic inference of appearance and molecular estimations of early 148
evolution
3.1.3 Fossil representatives 149
3.2 Diptera 152
3.2.1 General aspects 152
3.2.2 Phylogenetic inference of appearance and molecular estimations of early 153
evolution
3.2.3 Fossil representatives 154
4. Insect Parasitism s.str. e Neuropteroida 159
4.1 Neuroptera (Mantispidae) 159
4.1.1 General aspects 159
4.1.2 Phylogenetic inference of appearance and molecular estimations of early 160
evolution
4.1.3 Fossil representatives 160

Advances in Parasitology, Volume 90


© 2015 Elsevier Ltd.
j
ISSN 0065-308X
http://dx.doi.org/10.1016/bs.apar.2015.09.003 All rights reserved. 137
138 Christina Nagler and Joachim T. Haug

4.2 Coleopterida (Coleoptera, Meloidae) 161


4.2.1 General aspects 161
4.2.2 Phylogenetic inference of appearance and molecular estimations of early 162
evolution
4.2.3 Fossil representatives 162
5. Parasitoids 163
5.1 Hymenoptera 163
5.1.1 General aspects 163
5.1.2 Phylogenetic inference of appearance and molecular estimations of early 166
evolution
5.1.3 Fossil representatives 167
5.2 Strepsiptera 169
5.2.1 General aspects 169
5.2.2 Phylogenetic inference of appearance and molecular estimations of early 170
evolution
5.2.3 Fossil representatives 171
6. Plant Parasitism (versus Phytophagy) 172
6.1 General aspects 172
6.2 Phylogenetic inference of appearance and molecular estimations of early 173
evolution
6.3 Fossil representatives 173
7. Insects as Hosts 174
7.1 Nematoida 174
7.1.1 General aspects 174
7.1.2 Phylogenetic inference of appearance and molecular estimations of early 174
evolution
7.1.3 Fossil representatives 175
7.2 Mites 175
7.2.1 General aspects 175
7.2.2 Phylogenetic inference of appearance and molecular estimations of early 176
evolution
7.2.3 Fossil representatives 176
7.3 Pseudoscorpions 177
7.3.1 General aspects 177
7.3.2 Phylogenetic inference of appearance and molecular estimations of early 178
evolution
7.3.3 Fossil representatives 179
8. Insects as Vectors 179
8.1 General aspects 179
8.2 Phylogenetic inference of appearance and molecular estimations of early 181
evolution
8.3 Fossil representatives 182
9. Conclusion 182
Insects as Parasites and Hosts 139

10. Outlook 183


Acknowledgements 184
References 184

Abstract
Within Metazoa, it has been proposed that as many as two-thirds of all species are para-
sitic. This propensity towards parasitism is also reflected within insects, where several
lineages independently evolved a parasitic lifestyle. Parasitic behaviour ranges from
parasitic habits in the strict sense, but also includes parasitoid, phoretic or kleptopara-
sitic behaviour. Numerous insects are also the host for other parasitic insects or meta-
zoans. Insects can also serve as vectors for numerous metazoan, protistan, bacterial and
viral diseases. The fossil record can report this behaviour with direct (parasite associated
with its host) or indirect evidence (insect with parasitic larva, isolated parasitic insect,
pathological changes of host). The high abundance of parasitism in the fossil record
of insects can reveal important aspects of parasitic lifestyles in various evolutionary lin-
eages. For a comprehensive view on fossil parasitic insects, we discuss here different
aspects, including phylogenetic systematics, functional morphology and a direct com-
parison of fossil and extant species.

1. INTRODUCTION
1.1 Insects as parasites and hosts
Insecta is often considered to be the largest animal group comprising
over half of all metazoan species (Mayhew, 2007). Also, it has been estimated
that only about 20% of all existing insect species have been described so far
(Grimaldi and Engel, 2005). Considering that over 60% of all insect species
have been proposed to be parasites (Price 1980), we could estimate that
there should be at least 600,000 parasitic insect species in the modern fauna
(although one could ask how reliable these estimations are).
Ectoparasitism has been suggested to have evolved not less than 30 times
in different insect groups (Grimaldi and Engel, 2005). Ectoparasitism and
especially haematophagy occurs, for example, in fleas (Siphonaptera), lice
(Phthiraptera), midges (Diptera), some beetles (Coleoptera) and bugs (Hem-
iptera) (Pe~
nalver and Pérez-de la Fuente 2014, Lukashevich and Mostovki,
2003). Other insects, such as mantid lacewings (Mantispidae) and blister bee-
tles (Meloidae) are endoparasites or kleptoparasites.
While parasites (in the strict sense) do not kill their host, parasitoids do
(Kathirithamby, 2009). Parasitoidism is an important feeding strategy for
different wasps and relatives (Hymenoptera), at least in their larval stages,
140 Christina Nagler and Joachim T. Haug

but also for twisted-wing ‘parasites’ (Strepsiptera) and occasionally also for
other insects. In contrast to most parasites, the size relation of host and para-
sitoid is oddly skewed. While parasites are usually significantly smaller than
their hosts, parasitoids reach about the same size as their host. Often we
also see parasitoids that have parasitoids as host, a phenomenon known as
hyperparasitoidism (Kathirithamby, 2009). Besides parasitoidism, another
important parasitic mode (in the widest sense) is plant parasitism, which
occurs in several insect groups, e.g., hemipterans, coleopterans, dipterans
or hymenopterans.
Finally, insects do not only act as parasites themselves, but many serve as
hosts also for other insects, nematode and nematomorph worms and mites.
They also are hosts to a plethora of bacteria, viruses and protists. Many
notable pathogens, including Trypanosoma, Plasmodium and Dengue virus
use insects as vectors, to become widely distributed (e.g. Poinar, 2014a).

1.2 Insects in the fossil record


The indirect fossil record of insects dates back to the Silurian, 420 million
years ago (ma), based on possible insect coprolites (Labandeira, 2006 and
references therein). Molecular estimations argue for an even earlier origin
(e.g. Misof et al., 2014). Yet, no definitive insect body fossil has been found
that old. The oldest body fossil that was interpreted as an insect is a single
specimen of a supposed insect nymph from the Late Devonian, ca. 425 ma
(Garrouste et al., 2012). However, H€ ornschemeyer et al. (2013) rejected
this interpretation and interpreted it as ‘poorly preserved Devonian
arthropod’ based on a reinvestigation of the specimen. Other putative
Devonian insects tend to be rather fragmentary (e.g. Engel and Grimaldi,
2004; 400 ma).
Definitive and more complete insect body fossils have been described
from the Carboniferous (350 ma) and they already appear quite diversified
at that time (e.g. Shear and Kukalova-Peck, 1990). Many major modern in-
sect groups make their appearance later in the Triassic, 250 ma and many
minor modern extant insect groups (‘families’) find their origins in the
Cretaceous, 120 ma (Grimaldi and Engel, 2005).
The oldest fossil evidence for arthropod parasitism in general is
provided by pentastomids from the Cambrian (495 ma; Castellani et al.,
2011 and references therein). However, while pentastomids are arthropods
they are not insects. Parasitism in insects originated several times
(Labandeira, 2002) and existed definitely since the Triassic (250 ma; see
below).
Insects as Parasites and Hosts 141

Parasitized and parasitic insects are preserved as fossils in rocks and in


numerous occasions in amber. Amber, fossilized tree resin, preserves soft-
bodied specimens as well as organisms with a cuticle, to an exceptionally
detailed degree (Pohl et al., 2010; Lewis and Grimaldi, 1997) providing
unique snapshots of life as it was millions of years ago.
We can roughly distinguish four different types of fossil, which allow
parasitism to be inferred in the fossil record:
1. The most direct cases are parasites directly associated with their hosts.
Typical examples are mites on insects, or nematodes emerging from an
insect (see below). Inclusions in amber are perfect examples of this
kind of preservation (e.g. Poinar, 2014a).
2. Also quite direct is finding isolated parasites, i.e., parasites without their
hosts. In such cases, a morphological comparison to extant relatives can
give clues; a fossil flea will be as parasitic as a modern one. In cases where
we have no closely related extant form, a functional morphological com-
parison to modern parasitic forms can still be a strong indicator for a parasitic
lifestyle e presumably because their morphology is known to be modified
directly as a result of their parasitic lifestyle. More rarely, the analysis of the
contents of the digestive or circulatory system might also be informative.
3. More indirect evidence for parasitism, applicable to many insect groups,
is the finding of free-living developmental stages of a parasite. This type
of evidence relies heavily on comparison with modern forms.
4. Another type of indirect evidence is the influence on morphology,
growth and development of the host as a reaction to parasitism. This is
especially telling (but not only) in cases of plant parasitism indicated by
galls, leaf mines and asymmetric growth. However, it can be difficult
to identify the responsible organisms for these pathologies. Also here
inference relies heavily on comparisons with extant parasiteehost reac-
tions (e.g. McNaughton, 1983).
In the following, we provide examples of fossil insect parasitism in various
insect groups. Parasitism is meant here in its broadest sense, parasitism sensu
lato. This includes, for example, parasitism sensu stricto (traditional type of
parasite), parasitoidism (host about the same size and is killed) plant parasitism
(plant is ‘forced’ to help the insect) and kleptoparasitism (a parasite taking
prey or other useful material from the host; Rozen, 2003; Sivinski et al.,
1999). Furthermore, we consider cases where insects are hosts or vectors for
other organisms. Due to the enormous diversity of insects, we will not be
able to cover every possible fossil example insects involved in parasitic re-
lationships, but we tried our best to cover all major fossil examples.
142 Christina Nagler and Joachim T. Haug

2. INSECT PARASITISM SENSU STRICTO (S. STR.) e


PARANEOPTERA
Not all insect groups are known to have parasitic representatives. As
far as we could find, there seem to be no unequivocal parasitic representa-
tives of Entognatha, Archaeognatha, Zygentoma, Odonatoptera, Ephemer-
optera, Palaeodictyoptera or Polyneoptera. Hence active parasitism appears
to be restricted to eumetabolan insects (Paraneoptera þ Holometabola).
Paraneoptera includes the groups Phthiraptera (chewing lice and sucking
lice), Psocoptera (book lice, bark lice), Hemiptera and Thysanoptera.
Phthiraptera is most likely an in-group of Psocoptera (e.g. Beutel et al.,
2014), traditionally both have been placed together in the group Psocodea.
Psocodea or Psocoptera (if simply accepting that Phthiraptera are psocopter-
ans) is sister group to Hemiptera plus Thysanoptera, both being again sister
groups (Light et al., 2010; Johnson and Clayton, 2003). Active parasitism
occurs in Phthiraptera, which are obligate ectoparasites of birds and mam-
mals, and also in some Hemiptera.

2.1 Phthiraptera
2.1.1 General aspects
The group Phthiraptera, or true lice, currently comprises 4900 extant species.
They are traditionally split into two subgroups, ‘Mallophaga’, the chewing
lice, and Anoplura, the sucking lice (Grimaldi and Engel, 2005). The chewing
lice are named for their chewing mouthparts and include Amblycera, Ischno-
cera and Rhynchophthirina (Johnson and Clayton, 2003).
All phthirapterans are obligate ectoparasites of birds or mammals. They
are extremely modified for their parasitic lifestyle and behaviourally adapted
for particular microhabitats on the hosts (Johnson and Clayton, 2003). All
stages (including the adults) are wingless and dorsoventrally flattened.
They posses claws for clinging to hair or feathers and have modified
mouthparts for feeding (Light et al., 2010). The true lice are highly host-
and site-specific and spend their entire life on the host (as the only group
of ectoparasitic arthropods except mites). The females lay large eggs and atta-
ch them to the hair or feathers of their host with a special secretion (Martill
and Davis, 1998). Due to the dependence of their life cycle to the host and
their host specificity, Phthiraptera is a candidate for being the most special-
ized group of parasites among insects. They are a model system for phyloge-
netic studies including co-speciation and coevolution (Wappler et al., 2004;
Johnson and Clayton, 2003).
Insects as Parasites and Hosts 143

After hatching, phthirapterans develop through three nymphal stages to


the adult. The lice feed on keratin in hair or feathers, secretions or blood.
Their ancestors most likely had simple chewing mouthparts and were free
living in the nests or burrows of vertebrates. Later in their evolutionary his-
tory, they apparently became more dependent on their hosts and adapted
from associates to parasites. They fed directly from their hosts and developed
iteratively more modified mouthparts, dependent on where on the hosts
they lived and their chosen diets (Light et al., 2010).
Amblycera (traditionally classified as ‘Mallophaga’) is the sister group to
all remaining phthirapterans. They are obligate parasites mostly of birds, but
about 12% parasitize mammals such as rodents (Grimaldi and Engel, 2005;
Johnson and Clayton, 2003).
The group Ischnocera is the largest group of ‘Mallophaga’ with approx-
imately 3080 species. About 2700 feed on birds and 380 on mammals
(Yoshizawa and Lienhard, 2010).
Rhynchophthirina includes only three species; they parasitize elephants
and wild pigs. All of them possess an elongated ‘rostrum’ which bears the
mandibles in a 180 angle from the ‘normal’ position to break through
the skin and feed on blood. They are the sister group to Anoplura and it
is likely that Anoplura evolved from a Rhynchophthirina-like ancestor
(Light et al., 2010; Johnson and Clayton, 2003).
Anoplurans, the sucking lice, parasitize only mammals. The mouthparts
and the head of the 550 extant species are extremely modified and adapted
to the mammalian host.

2.1.2 Phylogenetic inference of appearance and molecular


estimations of early evolution
Liposcelidae, traditionally classified as ‘Psocoptera’ or book lice are the sister
group to Phthiraptera (Yoshizawa and Johnson 2010). Due to a discovery of
a representative of Liposcelidae in mid-Cretaceous amber of Myanmar
(about 100 ma), the minimal divergence time of true lice and Liposcelidae
is 100 ma. Cretoscelis burmitica (Figure 1(a)) from amber of Myanmar
(Grimaldi and Engel, 2006), although not parasitic itself, provides an impor-
tant calibration point for the appearance of true lice.
Recent findings of troctomorphs, another in-group of Psocoptera, show
a minimal age for the entire group Psocodea to be 135 ma (Early Creta-
ceous; Azar et al., 2015a). Grimaldi and Engel (2005) estimated the evolu-
tionary appearance of lice to be around 145 ma, where the host of lice could
be an early mammal, bird, another feathered theropod dinosaur or a haired
144 Christina Nagler and Joachim T. Haug

Figure 1 Fossil representatives of Psocodea (Paraneoptera). (a) Cretoscelis burmitica


(Liposcelidae, Psocodea) (modified from Grimaldi and Engel (2006, Figure 2) with kind
permission of the Royal Society). (b) Saurodectes vranskyi (modified from Grimaldi and
Engel (2005, Figure 38.12) with kind permission of Cambridge University Press and David
Grimaldi). (c) Megamenopon rasnitsyni (Phthiraptera, Psocodea) (modified from the fossil
pictured in Wappler et al. (2004), Figure 1(a) with kind permission of the Royal Society). (d)
Psittacobrosus bechsteini (Phthiraptera, Psocodea) (modified from Mey (2005), Figure 1
with kind permission of Eberhard Mey).

pterosaur. Based on molecular dating techniques, Smith et al. (2011) sup-


ported the notion that the early hosts of lice were feathered theropod dino-
saurs. The appearance of Amblycera (the earliest offshoot of Phthiraptera)
has been suggested to be around 120 ma, with the ancestral host again being
an early feathered dinosaur (Wappler et al., 2004).
Molecular data indicate a slightly older origin of lice, at least in the Early
Cretaceous (Yoshizawa and Johnson 2003), which would be more or less
Insects as Parasites and Hosts 145

congruent with the fossil record. Yet, also even earlier origins have been
suggested (e.g. Martill and Davis, 1998).
Molecular data support an evolutionary scenario from free-living detri-
tivorous generalistic psocodeans over liposcelid-like forms to highly special-
ized obligate ectoparasitic phthirapterans (Yoshizawa and Johnson, 2003).
Representatives of Liposcelidae have been found in nests of birds, mammals
or in the plumage of birds and fur of mammals, feeding on faeces, shed fur
and feathers (Grimaldi and Engel, 2006). This association may have given
the input to a permanent parasitism in lice (Yoshizawa and Lienhard, 2010).
Based on molecular data, Anoplura supposedly appeared in the Late
Cretaceous (77 ma) and soon after the CretaceousePalaeogene boundary
(before 65 ma), they radiated and adapted to different mammalian in-groups
(Smith et al., 2011; Light et al., 2010).

2.1.3 Fossil representatives


Due to the close connection between these ectoparasites and their hosts, fossils
of Phthiraptera are rare. To date, six possible cases have been discovered: Voigt
(1952) reported louse eggs on hair in Baltic amber, which has been recognized
by various authors. Grimaldi and Engel (2005) and Wappler et al. (2004)
considered this discovery has very little systematic value, but Mey (2005)
emphasized its importance and suggested a reinvestigation of the material.
Rasnitsyn and Zherikhin (1999) described Saurodectes vrsanskyi (Figure
1(b)) from the Zaza Formation of Baissa (130 ma), and interpreted it as an
ischnoceran louse. Yet, its systematic attribution was based on an elimination
process of other insect groups. Grimaldi and Engel (2005) stated that it is an
‘ectoparasite with phthirapteran affinities’ and later (Grimaldi and Engel,
2006) as a ‘putative louse or close relative, but also an exceedingly bizarre
insect’. Mey (2005) followed this statement. Dalgleish et al. (2006) proposed
that Saurodectes vrsanskyi is neither a phthirapteran nor could be assigned to
any other insect ‘order’.
Cuticular remains from the Triassic of Saptura Badin (215 ma) were
described as a louse by Kumar and Kumar (2001). Subsequent authors inter-
preted these remains as that of an oribatid mite (Dalgleish et al., 2006; Mey,
2005; Wappler et al., 2004).
The single specimen of Amblyceropsis indica from the Triassic Bagra For-
mation (Kumar, 2001) was also described as a putative louse. Yet, it is likely
also a mite, probably a representative of Prostigmata (Dalgleish et al., 2006;
Mey, 2005; Wappler et al., 2004).
Megamenopon rasnitsyni is 44 million years old from the Messel Lagerst€atte
in Germany and resembles modern menoponid lice (Figure 1(c)). The
146 Christina Nagler and Joachim T. Haug

specimen is likely an ectoparasite of aquatic birds, as in the gut of this para-


sitic louse remains of feathers have been found (Wappler et al., 2004). The
newest discovery was Psittacobrosus bechsteini by Mey (2005). It seems now
extinct, but is not really a fossil (Figure 1(d)); its host is a specimen of the
bird Ara tricolor found in the 1980s.
To conclude: only the last two specimens, of M. rasnitsyni and P. bech-
steini, can be assigned to Phthiraptera without any doubts. There is hence
only one direct phthirapteran fossil, namely, M. rasnitsyni with its last meal
in it. The phthirapteran eggs should be reinvestigated to clarify their system-
atic position.

2.2 Hemiptera
2.2.1 General aspects
Hemiptera includes Fulgoromorpha, Cicadomorpha (together forming
Auchenorrhyncha), Coleorrhyncha, Sternorrhyncha (all four groups
together formerly referred to as ‘Homoptera’) and Heteroptera (Beutel
et al., 2014). A prominent haematophagous group within Hemiptera is
Reduviidae; some species are commonly known as kissing bugs (Grimaldi
and Engel, 2005). Two other groups, Cimicidae and Polyctenidae, contain
also several haematophagous species (Yao et al., 2014). The exact relation-
ship of the hemipteran subgroups is still under discussion (Beutel et al., 2014;
Li et al., 2012).

2.2.2 Phylogenetic inference of appearance and molecular


estimations of early evolution
Their high diversity is often explained as having diverged with the radiation
of angiosperms coincident possibly with their phytophagous behaviour.
Phylogenetic analyses indicate that the origin of Hemiptera lies in the
Late Permian (Li et al., 2012). They have been considered to have evolved
by means of a phytophagous strategy giving way to arthropod predation and
finally becoming haematophagous, around 110e32 ma (Otalora-Luna et al.,
2015). The haematophagy should have evolved at least three times in these
bugs (Ribeiro et al., 2012). A recent finding extends the record of haema-
tophagous hemipterans to the Early Cretaceous (145 ma) (Yao et al., 2014).

2.2.3 Fossil representatives


There is one questionable compression fossil ascribed to Reduviidae from
the Early Cretaceous (140e120 ma) and some reduviids were discovered
in Burmese (Early Cretaceous), Canadian (Late Cretaceous) and Dominican
Insects as Parasites and Hosts 147

(Miocene) amber (Poinar and Poinar, 2005; Poinar, 1992). Remarkable


fossil representatives from the Early Cretaceous in China (145 ma) have
been described by Yao et al. (2014). They provided evidence for haema-
tophagy on mammals, birds or avian-rafted dinosaurs with the aid of
geochemical data.

3. INSECT PARASITISM S.STR. e ANTLIOPHORA


The exact relationships within Holometabola have been in flux. Yet,
the current (more or less stable) hypothesis suggests that wasps, ants and bees
(Hymenoptera) are the sister group to all remaining holometabolans. These
form two sister groups Neuropteroidea and Mecopteroidea (based on larval
morphological characters and on molecular data, Peters et al., 2014;
Labandeira, 2011). Active parasites (in the strict sense) are known in both
of the latter groups.
The monophyletic group Mecopteroidea (Panorpida of some authors)
consists of Mecoptera, Diptera (together Antliophora) and Trichoptera
and Lepidoptera (together Amphiesmenoptera; Beutel et al., 2014; Peters
et al., 2014). The ancestor of Mecopteroidea most likely existed in the
Permian already.
Within Antliophora, Diptera is the sister group to Mecoptera (Peters
et al., 2014; Beutel et al., 2011; Wiegmann et al., 2009). Siphonaptera (fleas),
traditionally considered to be the sister group of Mecoptera, has been repeat-
edly resolved as an in-group of Mecoptera (e.g. Whiting, 2002, and below).
Antliophorans are characterized by an elongation of the mouthparts.
This appears to be part of their ground pattern. This might be seen as a
possible preadaptation to a blood-sucking (haematophagous) type of ecto-
parasitism. As will be outlined in detail below, haematophagy is a ground
pattern feature for dipterans and fleas, but also some mecopterids appear
to have fed on blood. While most modern mecopterids feed on flowers,
this source of food was not yet readily available when the group diversified.
Hence, we might even speculate that the elongate mouthparts in the stem
species of Mecopteroidea were already used for blood sucking and ectopar-
asitism could represent an autapomorphy of Mecopteroidea. Mecopterans
feeding on flowers could then represent a novelty, similar to evolutionary
changes in Diptera (see below for details).
Most mecopterans are insects with extremely elongated mouthparts and
an elongate body. Larvae are generally scavengers and adults feed on nectar
148 Christina Nagler and Joachim T. Haug

(Poinar, 2012b). Certain scorpionflies from the Early Cretaceous (100 ma)
have long pointed mouthparts with fine serrations, this indicates that these
early mecopterans fed on blood (Boucot and Poinar, 2010).
Some fossils of the Late Jurassic (150e140 ma) indicate a Mesozoic age
for the sister group to the fleas (Grimaldi and Engel, 2005) and that this
type of fossil scorpionflies may have led to Siphonaptera (Huang et al.,
2012; Poinar, 2012b). It has also been suggested that Siphonaptera is either
an in-group (Friedrich and Beutel 2010) or the sister group (Whiting et al.,
2008) to the mecopteran in-group Boreidae. Despite the fact the exact
origin and relationships of fleas and other scorpionflies remains partly un-
clear, we can still state that with the radiation of mammals in the Palaeocene
and the obligate ectoparasitism of fleas, Siphonaptera radiated far more
recently than other mecopteran groups (Grimaldi and Engel, 2005).

3.1 Siphonaptera
3.1.1 General aspects
Siphonaptera, the true fleas, are laterally compressed, wingless obligate ecto-
parasites. They feed exclusively on the blood of mammals (94%) and birds
(6%) (Poinar, 2012b). About 2500 living species are known and they are
evolutionarily successful as they are a long-lived lineage that has radiated suc-
cessfully across multiple hosts (Poulin and Morand, 2000). Like many other
insect parasites, fleas have reduced eyes, reduced antennae, no wings, large
claws and modified mouthparts to pierce the skin of the host and suck blood
(Lukashevich and Mostovki, 2003; Rasnitsyn and Quicke, 2002). Interest-
ingly all insect ectoparasites have a dorsoventrally flattened body, except
fleas, where it is laterally compressed. In contrast to lice, fleas do not generally
spend their whole life on the host. Larvae often live in or near the nest of the
host and feed on host faeces, exfoliated skin; others are predators or even can-
nibals (Grimaldi and Engel, 2005; Rasnitsyn and Quicke, 2002).

3.1.2 Phylogenetic inference of appearance and molecular


estimations of early evolution
Based on molecular studies, Siphonaptera is considered to be monophyletic;
Tungidae, with its species retaining numerous plesiomorphic characters, likely
represents the sister group to all other fleas (Beutel et al., 2014; Whiting et al.,
1997, 2008). It is still controversial as to which fossils are indeed all part of the
early evolutionary history of fleas. The systematic and phylogenetic position
of some Mesozoic fossils is still not settled (Gao et al., 2013a; Perrichot et al.,
2012; Poinar, 2012b; Vransky et al., 2010; see below).
Insects as Parasites and Hosts 149

Flea-like ancestors have been considered to have shifted step by step


from pterosaurs to mammalian hosts (Gao et al., 2012; Huang et al.,
2012; Poinar, 2012b). Mesozoic flea-like fossils indicate a possible diversifi-
cation of Siphonaptera at least in the Late Jurassic (150 ma) (Gao et al.,
2013a; Huang et al., 2012).

3.1.3 Fossil representatives


Due to the close connection between siphonapterans and their hosts, fleas
are rare in the fossil record just like lice (Lukashevich and Mostovki, 2003).
• Extinct adult fossil specimens of Siphonaptera (Figure 2(b)) ascribed to
extant genera have been found in Eocene Baltic amber and in Miocene
Dominican amber (40e50 ma) (Perrichot et al., 2012; Poinar, 2012b;
Lukashevich and Mostovki, 2003; Lewis and Grimaldi, 1997). These
species found in amber indicate the evolution for modern species-groups
in the Middle Caenozoic (Perrichot et al., 2012).
While such clear in-group fossils are easy to recognize as such, there are also
some more challenging Mesozoic findings:
• Strashila incredibilis (Figure 2(f )) from the Jurassic of Transbaikalia in East
Siberia (Rasnitsyn, 1992). It has long, slender legs to grasp its host, but is
thought to have been unable to walk on the ground, which would indi-
cate a permanent life on the host (Grimaldi and Engel, 2005). Rasnitsyn
and Quicke (2002) supposed S. incredibilis as possible sister group to Tar-
winia and Saurophthirus (see next points). However, recent morphological
study indicates that Strashilidae are highly specialized dipterans (flies)
(Huang et al., 2013).
• Saurophthirus longipes (Figure 2(e)) from the Early Cretaceous Zaza For-
mation of Baissa, central Siberia (Ponomarenko, 1976). This large ecto-
parasitic insect with long, slender legs closely resembles certain Mesozoic
giant fleas (Huang et al., 2012; see below). Some extant ectoparasitic bat
flies show similar body proportions and legs (Grimaldi and Engel, 2005;
Lukashevich and Mostovski, 2003). Rasnitsyn and Quicke (2002) pro-
posed Saurophthirus as sister group to Tarwinia and true fleas. Gao et al.
(2013a) assigned S. longipes to the ‘family’ Saurophthiridae (representing
an empty, useless bracket) and supposed it to represent the closest relative
to modern fleas.
• A specimen of Tarwinia australis (Figure 2(c)) and three other (similar
appearing) specimens from the Early Cretaceous Koonwarra sediments
of Victoria (Jell and Duncan, 1986). These are thought (by Grimaldi
and Engel, 2005) to be ‘the early close relative of fleas from the
150 Christina Nagler and Joachim T. Haug

Figure 2 Fossil representatives of Mecopterida (Mecopteroidea). (a) Mosquito-like scor-


pionfly (Boreidae, Mecoptera) (modified from Grimaldi and Engel (2005, Figure 12.3) with
kind permission of Cambridge University Press and David Grimaldi). (b) Eospilopsyllus kob-
berti (Siphonaptera, Mecopterida) (modified from Perrichot et al. (2012, Figure 1) with
kind permission of Magnolia Press). (c) Tarwinia australis (Siphonaptera, Mecopterida)
(modified with permission from Elsevier from Huang et al. (2014, Figure 4)). (d) Pseudopu-
licidae sp. (Pseudopulicidae, Siphonaptera) (modified with permission from Macmillan
Publishers Ltd from Huang et al. (2012, Figure 2(a))). (e) Saurophthirus longipes (Sauroph-
thiridae, Siphonaptera) (modified from Rasnitsyn (1992, Figure 5) with kind permission of
Alexander Rasnitsyn). (f) Strashila incredibilis (Siphonaptera, Mecopterida) (modified from
Rasnitsyn (1992, Figure 2) with kind permission of Alexander Rasnitsyn).

Mesozoic’. After a current reinterpretation of the holotype, T. australis is


a definitive early representative of the lineage to Siphonaptera, and has
some particular features that are closely related to another Mesozoic giant
flea group, Pseudopulicidae (see below; Huang, 2015).
Insects as Parasites and Hosts 151

• Mesozoic giant fleas: two species (Figure 2(d)) from the Middle Jurassic
(165 ma) and one species from the Early Cretaceous (125 ma) in China.
These specimens share morphological characters with extant fleas, but
retain plesiomorphic features like nonjumping hind legs. Also they
have similar mouthparts in siphonate mecopterids. These giant fleas
might document an early diversification towards haematophagy (Huang
et al., 2012), assuming this is not a plesiomorphic feature. All three spe-
cies were ascribed subsequently to Pseudopulicidae (see below; Huang
et al., 2013)
• Pseudopulex jurassicus from the Middle Jurassic and Pseudopulex magnus from
the Early Cretaceous (Gao et al., 2012). These specimens share some
morphological characters with extant fleas, but could represent an extinct
lineage in early flea evolution (Gao et al., 2012). The morphological data
indicate that Pseudopulicidae (including these two) represent an early
offshoot of the siphonapteran lineage (Gao et al., 2012). Subsequently
Gao et al. (2013a) suggested Tarwinia þ Pseudopulicidae as sister group
to Saurophthirus þ the modern fleas based on morphological characters.
• Saurophthiridae. With Saurophthirus exquisitus from the Lower Creta-
ceous Yixian Formation in China et al. (Gao et al., 2013a). This species
has short and slender piercingesucking stylet mouthparts. Hence Sau-
rophthiridae (including another species S. longipes see above) resembles
the true fleas more than any other Mesozoic flea or flea-like fossil.
This indicates a divergence of Saurophthiridae and true fleas in the
Late Jurassic (Gao et al., 2013a). However, Grimaldi and Engel (2005)
saw no features that indicate special relationships to true fleas, but may
be because at the point of their review the only known Saurophthirus
was S. longipes, where the mouthparts were not preserved.
All flea-like Mesozoic fossils are definitely not true fleas in the strict sense
(Poinar, 2012b), but are more likely early offshoots of the evolutionary line-
age towards them (some may also represent other groups, see above). One
could simply consider modern fleas (including most amber fossils) as Siphon-
aptera sensu stricto, while using Siphonaptera sensu lato for the Mesozoic flea-
like fossils plus Siphonaptera s.str., instead of discussing at which point the
term ‘flea’ should be applied. Hence, we can state that early representatives
of Siphonaptera sensu lato (before the node of Siphonapetra sensu stricto) were
likely parasitizing feathered dinosaurs, pterosaurs or early mammals as ecto-
parasites grasping with their long legs (Gao et al., 2013a; Rasnitsyn, 1992;
Ponomarenko, 1976; Jell and Duncan, 1986). Their habitus indicates a strict
ectoparasitic lifestyle, adapted more for attachment than jumping (as in
152 Christina Nagler and Joachim T. Haug

modern forms). The early representatives of Siphonaptera sensu lato appear


not to have entangled themselves in hair or feathers. They could have either
pierced through scales or fed on the skin between the scales on nonfeathered
dinosaurs (Poinar, 2012b) or they could have parasitized the membrane of
the wings of pterosaurs (Gao et al., 2013a, 2012; Huang et al., 2012; Vransky
et al., 2010).

3.2 Diptera
3.2.1 General aspects
The superdiverse insect group Diptera is cosmopolitan and with 154,000
described species represents 10e12% of all described animal species
(Lambkin et al., 2013). Dipterans are easily recognizable as their hind wings
are reduced to halteres.
The ancestral feeding mode for Diptera is blood-sucking. Females of
groups which retain this mode have mandibles, which function as lancets
(Grimaldi and Engel, 2005). Haematophagy is obligate for females (of
blood-sucking species) to complete each gonadotrophic cycle and produce
fertile eggs (Greenwalt et al., 2013). Early divergent representatives of
Diptera, like midges and craneflies, resemble mecopterans in basic
morphology, with their long wings and long, dangling legs. Haematophagous
groups within the Diptera are numerous: Phlebotominae, Sycorinae, Culici-
dae, Corethrellidae, Ceratopogonidae, Simuliidae, Rhagionidae, Tabanidae,
Carnidae, Muscidae and Glossinidae (Grimaldi and Engel, 2005).
Extant adults of Chironomidae feed on nectar and honeydew, but early
representatives of Chironomidae from the Triassic and Jurassic were still
haematophagous. Such forms had biting mandibles, like Aenne triassica
from the Late Triassic of England (210 ma; Azar and Nel, 2012).
Extant representatives of Culicidae are blood suckers of almost all verte-
brates. Hence, likely fossil hosts could have been early mammals, lizards,
snakes, turtles, crocodilians, but also nonavian dinosaurs (Poinar et al., 2000).
Species of Corethrellidae are known as frog-biting midges. These tiny
midges are host-specific and parasitize frogs. 105 extant and 7 fossil species
are known (Borkent, 2014). Female frog-biting midges find their hosts
by listening to the mating calls of the host frogs (De Silva and Bernal, 2013).
Representatives of Ceratopogonidae or biting midges are small, but have
well-developed wings. Representatives of older lineages feed on vertebrates,
while more derived species feed on insects as ectoparasites (Borkent et al.,
2013; Pérez-de la Fuente et al., 2011). Ceratopogonidae is very species
rich, with 6180 extant species (Borkent, 2014; Greenwalt et al., 2013).
Insects as Parasites and Hosts 153

Simuliidae or blackflies are a group with 2100 extant species (Craig et al.,
2012). The claws of fossil forms indicate that early representatives of
Simuliidae fed on feathered nonavian dinosaurs or early birds (Currie and
Grimaldi, 2000).
Psychodidae with about 3000 extant species has received special scienti-
fic attention due to their medical significance. Within Psychodidae,
representatives of Sycorinae and Phlebotominae are parasitic blood feeders
(Grimaldi and Engel, 2005).
The parasitic groups Tabanidae and Rhagionidae are in-groups of
Tabanomorpha (Kerr, 2010). Species of Rhagionidae are known as water
snipe flies and are a relatively small group with about 500 extant species
(Zhang, 2012). About 50 extant species are parasitic on birds, mammals or
amphibians, mainly species of Symphoromyia (Zhang, 2012). In other groups,
plesiomorphic are parasitic while derived forms have abandoned this strat-
egy. An exception might be Rhagionidae, which is thought to have evolved
a predatory lifestyle, while parasitic forms evolved de novo from this strategy
(Grimaldi and Engel, 2005).
The elongate mouthparts of the 4500 species of Tabanidae (Zhang,
2012) are well suited for blood- and nectar-feeding at the same time (Karoyli
et al., 2014) and they have been considered to be the first pollinators of early
angiosperms (Labandeira, 2010).

3.2.2 Phylogenetic inference of appearance and molecular


estimations of early evolution
Dipterans are thought to have evolved in the latest Permian to the earliest
Triassic, 247 ma, when other insect lineages became extinct. After the
TriassiceJurassic mass extinction event (about 200 ma), early brachycerans
(e.g. Tabanidae) radiated and new dipteran larval types evolved. These
larvae lived in soil, likely due to the drying of aquatic and semiaquatic
habitats. Hence brachycerans became one of the most dominant insect
groups. In the Early Cretaceous (145 ma), the more derived brachyceran
in-groups, Cyclorrhapha and Schizophora, radiated (Lambkin et al.,
2013; Wiegmann et al., 2011; Reidenbach et al., 2009). In this period,
dipteran in-groups evolved all kind of new diets: phytophagy, coprophagy,
necrophagy, larval or adult predators, leaf mining and different types of
parasitism (Grimaldi and Engel, 2005; Rasnitsyn and Quicke, 2002).
Hence while blood sucking and haematophagy seem to be the ancient
diet of dipterans, this type of diet must have been lost (but also regained)
independently several times. Most often it was displaced by nectar feeding
154 Christina Nagler and Joachim T. Haug

multiple times during the radiation of angiosperms in the Lower


Cretaceous (Choufani et al., 2013; Greenwalt et al., 2013; Azar and Nel,
2012; Krenn and Asp€ ock, 2012; Zhang, 2012).
Modern dipterans do not use their mandibles to chew. It is supposed that
the first ‘non-mandibulate’ forms occurred after the Lower Cretaceous (Azar
and Nel, 2012). Yet, due to the less patchy geographic distribution of
culicids they have been considered to have existed before the separation
of Pangaea, 300e200 ma (Harbach and Greenwalt, 2012).
Ceratopogonidae þ Chironomidae is the sister group to Simuliidae þ
Thaumaleidae. Fossils ascribed to Simuliidae (176 ma) and Thaumaleidae
(146 ma) indicate that biting midges (Ceratopogonidae) should have evolved
at the latest in the Late Jurassic (Beutel et al., 2014; Borkent et al., 2013; Chou-
fani et al., 2013). The earliest direct fossil evidence comes from the Lebanese
amber (122 ma; Borkent et al., 2013; Pérez-de la Fuente et al., 2011).
Psychodidae has been thought to have evolved by the Triassic (248 ma)
before the breakup of Pangaea (Andrade Filho et al., 2009, 2007; Azar and
Nel, 2003). The protozoan Leishmania is supposed to have coevolved with psy-
chodidans (Andrade Filho and Brazil, 2003). It is likely that psychodidans
evolved from a blood-sucking form parasitic on nonavian dinosaurs or ptero-
saurs gradually to a nectar- and pollen-eating form, since only the old lineages
Sycoracinae and Phlebotominae are still parasitic (Azar and Nel, 2003).
Tabanomorph-like forms are thought to be the oldest representatives of
Brachycera and radiated probably 200 ma (Lambkin et al., 2013; Wiegmann
et al., 2011). Tabanidae (Figure 3(a)) are considered to have evolved quite
recently in the Early and Middle Cretaceous (Beutel et al., 2014).
Culicomorpha with Nymphomyiidae, Culicoidea and Chironomoidea
are thought to represent early radiations (Lambkin et al., 2013). This
interpretation is more or less congruent with a recent molecular study
(Wiegmann et al., 2011). Culicidae (mosquitoes) should have evolved
during the Middle Jurassic, 191 ma (Reidenbach et al., 2009), based on
molecular data. Still all these inferences are dependent on certain relation-
ship assumptions and the exact relationships within Diptera are still not satis-
fyingly clarified (Beutel et al., 2014).

3.2.3 Fossil representatives


Dipteran fossils are numerous especially in amber. A number of examples
include the following:
• The oldest representative of Diptera has been considered to be Grauvogelia
arzvilleriana from the Middle Triassic Voltzia-Buntsandstein (240 ma) (Gall
Insects as Parasites and Hosts 155

Figure 3 Fossil representatives of Diptera (Mecopteroidea) (a and b); Mantispidae


(Neuroptera, Neuropteroida) (c and e); Meloidae (Coleoptera, Coleopterida) (f). (a)
Laiyangitabanus formosus (Tabanidae, Diptera) (modified with permission from Elsevier
from Zhang (2012, Figure 2(a))). (b) Burmaculex antiquus (Culicidae, Diptera) (modified
from Grimaldi et al. (2002, Figure 36(b)) with kind permission of the American Museum
of Natural History). (c) Dicromantispa electromexicana (Mantispidae, Neuroptera)
(modified from Engel and Grimaldi (2007, Figure 5) with kind permission of the American
Museum of Natural History). Body length 10.4 mm. (d) Micromantispa cristata
(Mantispidae, Neuroptera) (modified with permission from Elsevier from Shih et al.
(2015, Figure 5(a))). (e) Mantispa styriaca (Mantispinae, Mantispidae) larva (modified
from Ohl (2011, Figure 2(b)) with kind permission from Springer Science and Business
Media). (f) Epispasta abbreviata (Meloidae, Coleoptera) larva (modified with permission
from Elsevier from Bologna et al. (2008, Figure 1(f))).
156 Christina Nagler and Joachim T. Haug

and Grauvogel, 1966). As haematophagy is thought to be ancestral for


Diptera, we might assume a similar mode of life for this species.
• Only slightly younger is the fossil of a nematoceran (mosquito-like form)
in 230 ma Triassic amber from Italy (Schmidt et al., 2012).
• Specimens of dipterans are the most common and most diverse forms in
amber inclusions; in Spanish amber dipterans are in 38% of all biological
inclusions (Delclos et al., 2007; Grimaldi et al., 2002). Due to their abun-
dance in lake sediments and their swarm behaviour, dipterans in general
are very frequent in the fossil record (Grimaldi and Engel, 2005).
• Fossil chironomids are abundant not only as inclusions in amber but also
as impressions from the Triassic to the Cretaceous (Lukashevich and
Przhiboro, 2015; Azar and Nel, 2010; Azar et al., 2008; Jarzembowski
et al., 2008; Veltz et al., 2007; Ansorge, 1996; Kalugina and Kovalev,
1985; Kalugina, 1974, 1976, 1980, 1993). Yet, only Triassic and Jurassic
forms appear to have been haematophagous, while the younger forms
were most likely already feeding on nectar and other flower products.
• Culicidae (mosquitoes) is represented in the fossil record by at least 25
species; 11 are known in amber, 14 are preserved as compression or
impression fossils (Hulden and Hulden, 2014; Greenwalt et al., 2013).
Due to their larvae, which have an obligate connection to water, most
fossil mosquitoes are preserved in lake or other lacustrine sediments
(Briggs, 2013). The fossils range from the Middle Cretaceous to the
Oligocene. Some Eocene fossils have been ascribed to modern mosquito
species (Harbach and Greenwalt, 2012; Poinar et al., 2000; Grimaldi
et al., 2002; Briggs, 2013). The oldest fossil mosquito Burmaculex antiquus
(Figure 3(b)) from Burmese amber (100 ma) has been proposed to repre-
sent the sister group to all remaining culicids. This is based on the reten-
tion of several plesiomorphic characters that show an intermediate
condition between modern mosquitoes and other midges (Harbach
and Greenwalt, 2012; Borkent and Grimaldi, 2004). Grimaldi et al.
(2002) stated that the gut of this specimen contains granular material,
possibly representing a blood meal. This statement has not been further
supported.
• One of the most spectacular findings is a modern-type mosquito, Culiseta
sp., from the Kishenehn shale in Montana (46 ma). With the aid of time-
of-flight secondary ion mass spectrometry, very high level of iron in the
abdomen of the midge could be detected (Greenwalt et al., 2013). This
was interpreted as a fossilized blood meal providing a direct evidence for
haematophagy in fossil representatives of Culicidae.
Insects as Parasites and Hosts 157

• The oldest representative of Corethrellidae is Corethrella cretacea, 122 ma


from Lower Cretaceous Lebanese amber (Szadziewski, 1995; Borkent,
2008).
• The fossil record of Ceratopogonidae is one of the best known among
insects with 274 fossil species (Borkent, 2014) and with countless spec-
imens in all 15 major amber deposits currently known. This abundance
is connected to (1) the close association of their habitats and resin sour-
ces, (2) their small size and (3) their swarming behaviour (Szadziewski
et al., 2015; Pérez-de la Fuente et al., 2011). Amber specimens have
been recorded from Lebanese amber (122 ma) to Dominican amber
(15 ma; Szadziewski et al., 2015; Choufani et al., 2014; Borkent,
2000; Sontag and Szadziewski, 2011). Compression fossils of biting
mites are rare. The oldest compression fossil is Archiaustroconops besti
of Southern England from the Purbeck Limestone group (146 ma), rep-
resenting a single wing (Borkent et al., 2013). The oldest specimen
ascribed to Leptoconops, and hence a presumed representative of Leba-
noculicoidinae (sister group to all other Ceratopogonidae), was found
in Lebanese amber (122 ma) (Borkent et al., 2013; Borkent, 2001,
2000). Leptoconops also has extant representatives. This was used as an
indication of morphological stability in Ceratopogonidae for million
of years, which has been related to a lack of change in diet of Cerato-
pogonidae during the radiation of the angiosperms (Borkent and Craig,
2004; Choufani et al., 2013).
• Archicnephia ornithoraptor from the Cretaceous amber (90 ma) of New Jer-
sey is the only amber inclusion of a representative of Simuliidae known
so far (Grimaldi and Engel, 2005). The oldest definitive representatives of
Simuliidae are Kovalevimyia lacrimosa from the Late Jurassic of Siberia (176
ma) and a Simulimima grandis pupa from the Middle Jurassic of Siberia
(Currie and Grimaldi, 2000).
• Representatives of Psychodidae are diverse and abundant in the fossil
record with 74 species (Azar and Nel, 2003). Psychodidans occur in
Lower Cretaceous Burmese, Lebanese, France and Spain amber (120e
135 ma) to Miocene Mexican and Dominican amber, but also in the
Early Jurassic of Germany (180 ma) and in the Late Triassic of Virginia
(210 ma; Azar et al., 2015b; Ibanez-Bernal et al., 2014; Petrulevicius
et al., 2011; Andrade Filho et al., 2009; Andrade Filho et al., 2008;
Andrade Filho et al., 2007; Blagoderov et al., 2007; Poinar, 2007;
Grimaldi and Engel, 2005; Andrade Filho and Brazil, 2003; Azar and
Nel, 2003; Brazil and Andrade Filho, 2002; Fraser et al., 1996; Ansorge,
158 Christina Nagler and Joachim T. Haug

1994). Sycoracinae, a more derived psychodid in-group, occurred first in


Cretaceous amber of France and New Jersey (Azar and Salame, 2015;
Petrulevicius et al., 2011; Azar, 2007). Two discoveries give direct evi-
dence for the haematophagy of Psychodidae. Penalver and Grimaldi
(2005) reported a swarm of specimens of Phlebotominae associated
with mammalian hair from the Miocene Dominican amber. The more
spectacular one is the observation of nucleated erythrocytes with parasi-
tophorous vacuoles in the gut of an amber-embedded sand fly (Poinar
and Poinar, 2004a).
• Due to the close connection between the water snipe flies (Tabanomor-
pha) and trees, they are a well-represented group in fossil deposits; 80
species have been described (Solorzano Kraemer and Nel, 2009). Gallia
alsatica, one of the oldest fossils among snipe flies, comes from the Jurassic
of France (200 ma; Krzeminski and Krzeminska, 2003). Snipe flies have
been considered to be abundant during the Jurassic and declined during
the Cretaceous (Mostovski, 2008). However, numerous Cretaceous fos-
sils have been found, which indicate that snipe flies were in fact still
abundant and widespread (Solorzano Kraemer and Nel, 2009). A recent
finding from China, Qiyia jurassica, an aquatic parasitic fly larva from the
Jurassic (150 ma) could be a representative of the early lineage of
Tabanomorpha and would support their supposedly Jurassic age (Chen
et al., 2014).
• Horse flies (an in-group of Tabanomorpha) have been reported from
Miocene Mexican amber (20 ma; Strelow et al., 2013) from Dominican
amber, Baltic amber (Trojan, 2002) and the Cretaceous New Jersey
amber (Grimaldi et al., 2011) with 28 species (Strelow et al., 2013).
The oldest representatives of Tabanidae are impression fossils from the
Lower Cretaceous of China (Zhang, 2012), Europe (Mostovski et al.,
2003) and America (Grimaldi et al., 2011).
Summing up, first representatives of Diptera are as old as the Triassic.
Their evolutionary history shows a gradual evolution from ancestral
blood-feeding, hence ectoparasitism, to a predatory or nectar-feeding life-
style, sometimes also with reversal to blood sucking. Several indications of
haematophagy (Greenwalt et al., 2013; Poinar, 2011b, 2007, 2005a,b,
2004a; Poinar and Telford, 2005; Poinar and Poinar, 2004a) and two asso-
ciations with the remains of their host (Vullo et al., 2010; Penalver and
Grimaldi, 2005) give also more evidence for their parasitic lifestyle and func-
tion as vectors in the past. Within the brachyceran lineages of Diptera several
groups evolved parasitoidism. Yet this behaviour is quite scattered
Insects as Parasites and Hosts 159

(phylogenetically) and not associated with functional morphological special-


izations. Hence identifying this behaviour in a fossil is more than challenging
and therefore not further followed here.

4. INSECT PARASITISM S.STR. e NEUROPTEROIDA


Comparably recent molecular- and morphologically based phyloge-
netic analyses indicate that Coleopterida and Neuropterida are sister groups,
the parent group named Neuropteroida (Beutel et al., 2011; Wiegmann
et al., 2009). Neuropterida consists of Neuroptera þ Megaloptera (Asp€ ock
and Asp€ ock, 2008) and its sister group Raphidioptera (Beutel et al., 2014;
Wiegmann et al., 2009).

4.1 Neuroptera (Mantispidae)


Within Neuroptera, there are approximately 6000 described species (Beutel
et al., 2014). Neuroptera has been considered to have originated in the
Permian (Grimaldi and Engel, 2005). The only known parasitic in-group
of Neuroptera is Mantispidae.

4.1.1 General aspects


Mantispidae (mantid lacewings) is a group within Neuroptera with 400
species known globally (Engel and Grimaldi, 2007). They are distinct by a
mantodean-like appearance e they have prominent raptorial forelegs, elon-
gated ‘necks’ and well-developed eyes (Grimaldi and Engel, 2005). There
are generally four in-groups recognized: Drepanicinae, Calomantispinae,
Mantispinae and Symphrasinae. All larvae are all highly specialized obligate
parasites of spiders or hymenopterans (Grimaldi and Engel, 2005); most
larvae of Mantispinae are parasitic on spider eggs.
The first instar larva is active and very mobile, whereas the next two
stages are immobile. Larvae of Mantispinae are obligate parasites of spiders’
egg sacs. Some larvae are ectoparasitic on spiders, before these produce an
egg sac. Hence they feed on haemolymph until they finally can parasitize
the egg sac and feed on the eggs (Ohl, 2011; Engel and Grimaldi, 2007).
It is necessary that the larvae are agile, to find and reach a spider’s egg sac.
If a mantispid larva attaches to a juvenile spider, the larva remains within
the chambers of the book lungs of the spider until the next year, when
the spider will become adult and produce an egg sac. Thus, the host spider
induces and terminates a diapause of the mantispid larvae (Ohl, 2011). The
160 Christina Nagler and Joachim T. Haug

larva of the fossil Dicromantispa moronei has been proposed as a parasitoid of


spiders, yet without further explanation (Engel and Grimaldi, 2007).

4.1.2 Phylogenetic inference of appearance and molecular


estimations of early evolution
Grimaldi and Engel (2005) suggested a radiation within Mantispinae during
the Palaeogene (60 ma) hence a rather young age. Haring and Asp€ ock
(2004) predicted an origin in the Late Triassic (202 ma) or the Early Jurassic
(200 ma) based on molecular data. Also adult forms provide evidence since
the Early Cretaceous (Shih et al., 2015; Poinar and Buckley, 2011). A fossil
larva in amber found by Ohl (2011) (see below) is the first direct fossil record
of a parasitic larva of Mantispinae and provides their minimum age (Eocene,
44 ma). Two fossil species ascribed to Drepanicinae demonstrate an appear-
ance of these at least in the Late Cretaceous (100e66 ma; Shi et al., 2015).
Hence also Mantispidae is at least that old.

4.1.3 Fossil representatives


• Ohl (2011) found one spider-boarding larva ascribed to Mantispinae in
Middle Eocene Baltic amber (44 ma) on a juvenile clubionid spider in
a typical position, anterior on the opisthosoma (Figure 3(e)). The larva
has a flattened, elongated body and bears strong thoracic legs, that imply
active movement of the larva. This morphology indicates that it is likely
the first instar larva of a species of Mantispinae. This represents the first
and so far only discovery of a fossil mantispid larva (Ohl, 2011).
• Adult mantispidans, which would indirectly indicate the presence of
parasitic larvae, are rare in the fossil record (Engel and Grimaldi, 2007;
Wedmann and Makarkin, 2007). Only 14 species have been ascribed
to Mantispidae. Five of them were found in amber: Micromantispa cristata
(Figure 3(d)) in Cretaceous amber of Myanmar (Shih et al., 2015),
Doratomantispa burmanica in Burmese amber (Poinar and Buckley,
2011), Dicromantispa electromexicana in Mexican amber (Engel and
Grimaldi, 2007), D. moronei in Dominican amber (Engel and Grimaldi,
2007), Feroseta prisca in Dominican amber (Poinar, 2006).
• The others were found in deposits dating from the Jurassic (Wedmann
and Makarkin, 2007; Ansorge and Schl€ uter, 1990; Panfilov, 1980), the
Cretaceous (Makakrin, 1996; Makarkin, 1990), the Eocene (Wedmann
and Makarkin, 2007; Cockerell, 1921) and the Oligocene (Nel, 1988).
Two additional fossils ascribed to Mantispidae are two species of Mantis-
pidiptera, described by Grimaldi (2000) and Whalfera venatrix, described by
Insects as Parasites and Hosts 161

Engel (2004). The assignment of these two fossils to Mantispidae is


doubtful at best (Wedmann and Makarkin, 2007).

4.2 Coleopterida (Coleoptera, Meloidae)


Coleoptera and Strepsiptera are now considered to represent sister groups
within the monophyletic group Coleopterida (Beutel et al., 2014). This
sister group relationship has been established rather recently based on molec-
ular- and morphologically-based phylogenetic analysis (Beutel et al., 2014,
2011; Niehus et al., 2012; Wiegmann et al., 2009).
Approximately 355,000 extant species and 600 fossil species of
Coleoptera have been described (Grimaldi and Engel, 2005). The lineage
of Coleoptera is extremely diverse and abundant on all continents (Beutel
et al., 2014). Archostemata is thought to be the (extant?) sister group of all
remaining coleopterans. They have been considered to have originated in
the Permian (Beutel et al., 2014). Yet, Bethoux (2009) interpreted the
Carboniferous fossil Adiphlebia lacoana as a possible early coleopteran
implying an older age of the coleopteran lineage. This interpretation has
been questioned by Kukalova-Peck and Beutel (2012). In the Late Triassic,
the large coleopteran in-groups Myxophaga and Adephaga radiated, also
first representatives of Polyphaga appeared (Beutel et al., 2014; Grimaldi
and Engel, 2005). Another radiation of Coleoptera took place in the
Jurassic. A dramatic increase in species richness occurred in the Late Creta-
ceous, possibly coupled to the radiation of the angiosperm plants (Beutel
et al., 2014).

4.2.1 General aspects


Blister beetles (Meloidae, Coleoptera) are a monophyletic in-group of Ten-
ebrionoidea with almost 3000 species (Bologna et al., 2008). Meloidae have
two exciting evolutionary modifications: the terpenoid cantharidin and
hypermetabolous development (Grimaldi and Engel, 2005). Due to the
damaging effect on the digestive tract of animals, the terpenoid cantharidin
is effective against predators. Thus it protects meloids and their eggs from
predators. It also acts as a sexual attractor and is linked to the sexual behav-
iour in the in-group Meloinae (Bologna et al., 2008; Capinera, 2003).
Cantharidin causes blisters on the skin of sensitive animals (some humans
or horses), which led to their common name ‘blister beetles’ (Capinera,
2003). Hypermetabolous development includes seven larval stages, where
the first so-called triungulin phase is the most important one, when we
look on parasitism (Grimaldi and Engel, 2005). The triungulin larva
162 Christina Nagler and Joachim T. Haug

(Figure 3(f)) is often highly specialized for ectoparasitic behaviour in the


form of phoresy (Chmielewski, 1977 named phoresy ‘transportation para-
sitism’) and is adapted to reach its host. One of their strategies is to wait
on flowers and attach to the host with their grasping claws on the thoraco-
pods. Thus, the host takes them in its nest and they parasitize the clutch
(Engel, 2005). They parasitize Hymenoptera (Apoidea) and sometimes
grasshoppers (Acridoidea; Bologna et al., 2008; Capinera, 2003). Once
locating the host’s egg pod, the larvae feed on eggs and moult briefly in
the second stage from larval instars IIeV (Capaneira, 2003). After two
more stages, the larva will be a pupa and is found in the soil.

4.2.2 Phylogenetic inference of appearance and molecular


estimations of early evolution
The triungulin larva evolved once in the stem-group Meloidae (Meloinae,
Tetraonycinae, Nemognathinae) around 112 million years old. It has been
suggested that phoresy appeared at least seven times independently within
Meloidae (Bologna et al., 2008), but appears unlikely when applying the
concept of Occam’s razor. Molecular clock studies indicate an even earlier
appearance of Meloidae, during the Early Cretaceous (125e135 ma).
They appear to have radiated fast with the acquisition of parasitism and
hypermetabolism (Bologna et al., 2008).

4.2.3 Fossil representatives


There are three fossils of meloid triungulins.
• Poinar (1992) described a larva of Meloidae sp. on the pronotal dorsal
surface of the extinct bee, Proplebeia dominicana, from Early Miocene
Dominican amber. A similar relationship between Meloidae and stingless
bees is not known nowadays, thus this fossil indicates a loss of this hoste
parasite relationship (Engel, 2005).
• Larsson (1978) described an isolated meloid triungulin from Middle
Eocene Baltic amber, yet this interpretation has been questioned (Engel,
2005).
• The oldest and definitive direct observation of a hosteparasite relation-
ship has been found in Middle Eocene Baltic amber (45 ma; Engel,
2005). Engel (2005) described meloid triungulins on the setae of the
bee Protolithurgus ditomeus (Megalichidae, Hymenoptera). If you consider
that bees are quite uncommon in amber, it was very lucky to find one
with meloid triungulins on it.
Insects as Parasites and Hosts 163

5. PARASITOIDS
5.1 Hymenoptera
5.1.1 General aspects
Hymenoptera is one of the most diverse groups among insects. Currently
there are 125,000 extant described species, traditionally divided in two
groups: ‘Symphyta’ (‘plant wasps’) and Apocrita (‘waisted wasps’) (Delcl os
et al., 2007). Parasitoidism, hyperparasitoidism and kleptoparasitism occur
in numerous in-groups: Orussidae (a group of ‘plant wasps’), Stephanoidea,
Ephialtioidea, Megalyroidea, Trigonalyoidea, Evanoidea, Proctotrupo-
morpha, Ichneumonoidea (all of these Apocrita, formerly also together
called Parasitica) and some groups of Aculeata (Grimaldi and Engel,
2005). Surprisingly the hosts of most extant species appear to be unknown
(Engel and Perrichot, 2014).
The only symphytan parasitoid group is Orussidae, which is the likely sis-
ter group to Apocrita (Grimaldi et al., 2002). Given this pattern of character
distribution, parasitoidism appears to have evolved in or slightly before the
stem species of Orussidae þ Apocrita (and was lost in apocritan in-groups).
Orussidans were diverse and abundant in the Jurassic and Cretaceous and
were associated with trees due to their ectoparasitoidism of wood-boring
beetles and wood wasps. The wasp waist is restricted to Apocrita. This
morphological character appears to provide them a better mobility of the
abdomen and hence the ovipositor. This appears to have been an essential
novelty for effective parasitoidism.
Like species of Orussidae, species of apocritan groups branching off early,
Stephanoidea and Megalyroidea, are ectoparasitoids of wood-boring beetles
and symphytan wasps (Grimaldi and Engel, 2005). Stephanoideans have a
very similar biology to species of Orussidae. The females use their elongated
ovipositor to pierce through wood into the host that is later eaten by the
parasitoid larvae (Engel et al., 2013a). This type of biology is also retained
the next group branching of the lineage towards the more derived apocri-
tans, Ephialtioidea (Figure 4(a)).
Representatives of Megalyroidea parasitize not only wood-boring bee-
tles (as the groups before) but also spheciform wasps. Their close relatives,
trigonalyoideans, are hyperparasitoids, hence are parasitoids on parasitoid
larvae (Perrichot, 2013).
Representatives of Evanoidea are diverse. The supposedly ancestral
appearing representatives of Aulacidae (Figure 4(b)) are parasitoids, but the
164 Christina Nagler and Joachim T. Haug

Figure 4 Fossil representatives of Hymenoptera. (a) Praeproapocritus flexus (Ephialtiti-


dae, Ephialtioidea) (modified with permission from John Wiley & Sons from Li et al.
(2013, Figure 3)). (b) Aulacus eocenicus (Aulacidae, Evanoidea) (modified after Nel and
€eg (2004, Figure 1)). (c) Tagsmiphron spiculum (Stigmaphronidae, Ceraphronidea)
Plo
(modified with permission from Elsevier from McKellar and Engel (2011, Figure 2A)). (d)
Necrobythus pulcher (Scolebythidae, Chrysidoidea) (modified with permission from
Elsevier from Engel et al. (2013b, Figure 4(b))). (e) Deinodryinus areolatus (Dryinidae,
Chrysidoidea) (modified after Gugliemino and Olmi (2011), Figure 2).

more derived forms such as evaniids and gasterupiids are larval predators of
cockroach oothecae (Grimaldi and Engel, 2005). Their inferred oldest rela-
tives are species of the extinct group Praeaulacidae; species of this group
were abundant in the Jurassic and Early Cretaceous of Australia and Asia
(Li et al., 2014).
Proctotrupomorpha is a group of usually very small and tiny parasitoids
(except the giant Pelicinidae). In-groups are Stigmaphronidae, Ceraphroni-
dea, Platygastroidea (Grimaldi and Engel, 2005). These wasps are
Insects as Parasites and Hosts 165

endoparasitoids of wood-boring or cone-boring beetles, flies, symphytans,


lepidopterans or green lacewings and some are hyperparasitoids on other
apocritan species (Shih et al., 2013). Species of Platygastridae and Scelionidae
(in-groups of Platygastroidea) are both endoparasitoids of insect and spider
eggs. Scelionidan species do not complete their development until the
host has reached adultness (Grimaldi et al., 2002). The known representa-
tives of Ceraphronidea (Figure 4(c)) are either endoparasitoids of caterpillars,
beetles, dipteran pupae, Hemiptera, other apocritans or Thysanoptera or
hyperparasitoids on apocritans or aphidid hemipterans (McKellar and Engel,
2011).
Among Ichneumonoidea (Braconidae and Ichneumonidae) the species
of less-derived in-groups are ectoparasitoids of wood-boring beetles, cater-
pillars and wood wasps. Within Ichneumonoidea different lineages switched
multiple times from ecto- to endoparasitoidism (Grimaldi and Engel, 2005).
All ichneumonid endoparasitoids possess a special poison that manipulates
the host to construct a specific protection for the ichneumonid larva. Ecto-
parasitoids in contrast suppress the immune system of the host with a poly-
DNA-virus (Longdon and Jiggins, 2012). Although ichneumonids are well
reported since the Early Cretaceous, such a virus could not be directly
detected or visualized (Longdon and Jiggins, 2012).
In Aculeata (including ants, bees, stinging wasps), only a few lineages
retain a plesiomorphic parasitoid lifestyle. This is known in Chrysidoidea,
Vespoidea and Apoidea. Chrysidoidea appears to be the less-derived group
and is rather species poor. Representatives are ectoparasitoids of butterfly
larvae (Lepidoptera), of beetle larvae (Coleoptera), of web spinners
(Embioptera), of walking sticks eggs (Phasmatodea) and sometimes klepto-
parasitic on bees and vespids (Azar, 2007). The larvae of species of Dryinidae,
an in-group of Chrysidoidea, parasitize adult and nymphal cicadas (Auche-
norrhyncha; Olmi et al., 2014a; Guglielmino and Olmi, 2011). The oldest
fossil dryinids have been ascribed to a cosmopolitan extant genus. This has
been seen as an indication that the morphology of these forms was preserved
since the Cretaceous (Olmi et al., 2014b).
Within Vespoidea only few ‘primitive’ lineages are parasitoids, namely
Tiphiidae, Pompilidae, Sapygidae, Mutillidae, Rhopalosomatidae and
Scoliidae. Tiphiidae comprises species that are ectoparasitoids of ground-
dwelling larval beetles, such as species of Scarabeidae. Species of Pompilidae
are also ectoparasitoids of spiders, they paralyze their hosts. Sapygidae in-
cludes forms that are ectoparasitoids of larval wasps or kleptoparasites of
bees. Species of Mutillidae are ectoparasitoids of different holometablous
166 Christina Nagler and Joachim T. Haug

groups, such as bees, wasps, flies, moths, beetles, but also cockroaches. Spe-
cies of Rhopalosomatidae are ectoparasitoids of crickets. Lastly species of
Scoliidae are ectoparasitoids of ground-burrowing beetles (Grimaldi and
Engel, 2005).
Also in the lineages that diverged from the ancestral type of parasitoidism
and switched to other strategies, parasitoidism (or parasitism?) has (re-)
evolved. For example, some ants are secondarily ectoparasitoids or klepto-
parasitic, but no fossil forms of these have been found so far (Grimaldi
and Engel, 2005). Within eusocial bees, different types of kleptoparasitism
are known (Litmann et al., 2014). Also species of spheciform wasps, Ampu-
licidae, Sphecidae and Crabronidae are parasitoids. Their larvae feed on the
living host for several larval stages, entering the host’s body and live as endo-
parasitoid. After the host is dead, the larvae spin a cocoon and pupate within
the host (Grimaldi and Engel, 2005). Spheciform wasps are evolutionarily
important as they are the sister group to bees (e.g. Johnson et al., 2013).

5.1.2 Phylogenetic inference of appearance and molecular


estimations of early evolution
It has been put forward that the key feature in hymenopteran evolution was
the development of parasitoidism, which triggered the largest radiation of
parasitic arthropods in the wide sense (including parasitoidism). Derivatives
of early branchings in Hymenoptera are phytophagous, xylophagous and
fungivorous, but with the origin of parasitoidism (estimated about
210 ma) hymenopterans diversified rapidly.
These forms should have evolved at least in the Early Triassic, as Hyme-
noptera is considered to be the sister group to the remaining holometabolans
(Wang et al., 2014a; Engel et al., 2013a; Klopfstein et al., 2013; Sharkey
et al., 2012; Heraty et al., 2011; McKenna and Farrell, 2010). Yet, it remains
unclear if these suggestions include the possibility that we might have holo-
metabolous forms already in the Carboniferous.
The fossil wood wasp Cratoenigma articulata from the Lower Cretaceous
of Brazil seems to be an ‘intermediate’ form between the endophytic (non-
parasitoid) forms of Xyledoidea and the parasitoid species of Orussidae
(Krogmann and Nel, 2012).
Based on phylogenetic and morphological studies, it is likely that the
radiation of Orussidae took place in the Middle Cretaceous (100 ma;
Vilhelmsen and Zimmermann, 2014). Fossils ascribed to Proctotrupomor-
pha from the Cretaceous support a possible Jurassic age of the group
(Grimaldi and Engel, 2005). Within the proctotrupomorph Platygastroidea
Insects as Parasites and Hosts 167

the in-group Chalcidoidea underwent a spectacular radiation during the


Eocene (55e35 ma; Heraty and Darling, 2009). Chalcidoidean species are
endoparasitoid or hyperparasitoid on a large range of hosts among insect par-
asitoids. The group has been estimated to comprise not less than 500,000
species (Heraty and Darling, 2009). For Ceraphronidea, a Cretaceous origin
has been proposed, based on their biogeographic distribution (Perrichot
et al., 2014).
In short, Hymenoptera evolved latest in the Middle Triassic (230 ma, but
probably even earlier), parasitoidism in this group originated near the
TriassiceJurassic boundary (210 ma). This lead to a rapid radiation of
Apocrita in the Jurassic (195 ma). Aculeatan species existed from the Jurassic
(155 ma) onward and radiated in the Early Cretaceous (140 ma). The
occurrence of ants and bees was coupled to the radiation of angiosperms
in the Middle Cretaceous (125e100 ma; Ward et al., 2014; McKellar and
Engel, 2012).

5.1.3 Fossil representatives


• A specimen of Xyleoidea (saw flies) represents the oldest hymenopteran
fossil. It comes from the Middle Triassic (220 ma) of Kyrgyzstan in Cen-
tral Asia (Rasnitsyn, 1969). Slightly younger finds are from the Upper
Triassic of Argentina (Lara et al., 2014) and from the Middle Jurassic
of China (Wang et al., 2014b). Among the saw flies is the largest
hymenopteran fossil with an estimated wing span of 92 mm (Gao
et al., 2013b).
• The fossil record of Orussidae is sparse with only two specimens from
Cretaceous amber of Siberia and New Jersey, and two specimens from
the Late Jurassic of Kazakhstan and from the Oligocene of Colorado
(Vilhelmsen and Zimmermann, 2014; Vilhelmsen et al., 2013; Delcl os
et al., 2007; Grimaldi and Engel, 2005; Vilhelmsen, 2003).
• There are only a few fossils of Stephanoidea known so far. They have
been found in the Late Cretaceous of New Jersey, the Middle Eocene
Baltic amber and the Middle Cretaceous Burmese amber. Additionally
there is a single compression fossil from the EoceneeOligocene bound-
ary of Florissant (Engel et al., 2013a; Grimaldi and Engel, 2005).
• The few fossils ascribed to Ephialtioidea stem from the Early Jurassic to
the Early Cretaceous (Li et al., 2013).
• Megalyroideans are known from Cretaceous Siberian amber, Burmese
amber and New Jersey amber and from Baltic amber (Delcl os et al.,
2007). An in-group, Stigmaphronidae, exclusively known from the
168 Christina Nagler and Joachim T. Haug

Cretaceous, includes an additional fossil that provides direct evidence for


their endoparasitoidism (Engel and Perrichot, 2014; Arillo, 2007): a fossil
stigmaphronid hymenopteran from Mesozoic Spanish amber shows ovi-
positing into a dipteran (Alonso et al., 2000).
• Trigonalyoideans are rare in amber, but abundant as compression fossils
(Early Cretaceous; 125 ma) (Engel and Perrichot, 2014; Delcl os et al.,
2007).
• Evanoid fossils have been described from Cretaceous Lebanese amber,
Myanmar amber and New Jersey amber, as well as based on compression
fossils from the Lower Cretaceous (Engel, 2013a; Jennings et al., 2013;
Delcl os et al., 2007; Grimaldi and Engel, 2005; Nel et al., 2004).
• Proctotrupomorphans have been reported from the Early Jurassic of Asia,
from the Cretaceous of China, from the Cretaceous of Spain, from the
Lower Cretaceous of Brazil and from the following amber deposits:
New Jersey Baltic, Burmese, Dominican, Canadian, Mexican, Late
Eocene, Eocene Rovno, Miocene amber from Peru (Perrichot et al.,
2014; Barling et al., 2013; Engel, 2013b; Krogmann, 2013; Shih et al.,
2013; Kolyada and Petrovsky, 2011; McKellar and Engel, 2011; Poinar
and Huber, 2011; Heraty and Darling, 2009; Delcl os et al, 2007;
Grimaldi and Engel, 2005).
• Representatives of platygastrid Serphitoidea as well as of Scelionidae and
Platygastridae are already known from the Cretaceous, but are not found
in younger deposits (Engel and Perrichot, 2014; Grimaldi and Engel,
2005; Grimaldi et al., 2002).
• The early record of modern in-groups of Ichneumonidea comes from
the Lower Cretaceous. Fossils are abundant as both, amber inclusions
and as compression fossils until the Palaeogene (McKellar et al., 2013;
Ortega-Blanco et al., 2012; Delcl os et al., 2007; Grimaldi and Engel,
2005). Notable specimens are fossils come from Baltic and Dominican
amber: (1) a braconid larva emerging from an ant (Poinar, 2002) (2) an
ichneumonid female ovipositing into a caterpillar (Poinar and Miller,
2002) (3) an ichneumonid larva attached to a spider (Poinar, 1992) and
(4) an ichneumonid larva that spins its cocoon over the eggs of a spider
(Poinar, 2004b).
• There are more fossil forms of Chrysidoidea, dating from the Early
Cretaceous to the Early Miocene, of (Figure 4(d)) than there are extant
species (Engel et al., 2013b; Grimaldi and Engel, 2005). Within Chrys-
idoidea, the group Dryinidae (Figure 4(e)) is the best recorded ectopar-
asitic group in amber (Arillo, 2007). Grimaldi and Engel (2005) reported
Insects as Parasites and Hosts 169

a fossilized leafhopper with an attached thylacium, a protective structure


formed by retained parts of the exuviae of the first instar larva of the
parasitoid.
• Most vespoid in-groups occur since the Early Cretaceous, but the oldest
known specimen is a pompilid spider wasp (hence likely a parasitoid)
from Middle Cretaceous amber of Myanmar (Grimaldi et al., 2002).
• There are several spheciform wasps from the Caenozoic preserved as
compression fossils and amber inclusions (Antropov, 2000; Antropov
and Pulawski, 1996). The Caenozoic fossils resemble the modern spheci-
form wasps (Grimaldi and Engel, 2005).
• The Cretaceous Pompilopterous (Rasnitsyn, 1975), as the name suggest,
was interpreted as a spider wasp, but has been redescribed as a spheciform
wasp (Rasnitsyn, 1998). In a comparable case, the Lower Cretaceous fos-
sil Cariridris bipetiolata (Brandao et al., 1990) has been originally described
as ant, but was redescribed as a spheciform wasp (Dlussky and Rasnitsyn,
2003).

5.2 Strepsiptera
5.2.1 General aspects
Strepsipterans are obligate endoparasitoids; Strepsiptera comprises ca. 600
extant species. These parasitize numerous different types of insects, mainly
representatives of Auchenorrhyncha (like Cicadellidae, Membracidae),
Hymenoptera, Hemiptera and Zygentoma (Rasnitsyn and Quicke, 2002).
Part of their success has been attributed to their pronounced sexual
dimorphism and life cycle. Strepsipteran males bare halteres and hind wings.
They are agile fliers, but live only a few hours, to find a female
(Kathithiramy, 2009; Grimaldi and Engel, 2005). Most females are wingless
and sack-like, lack functional eyes and antennae. In some groups which
retain some more ancestral features, females bear short antennae, reduced
(but still present) eyes and legs. They live their entire life within the host.
The hosts’ life span can last until all strepsipteran larvae emerge from the
host (Kathithiramby, 2009).
The larvae hatch immediately when the egg is laid (ovovivipary). The
first larva, is called a triungulin (cf. Meloidae). This larva actively searches
for a host. Most of them search for larvae or nymphs, some go for eggs
(Kathithiramby, 2009). After finding a potential host, the strepsipteran larva
attaches to the host; special enzymes allow the larva to enter the host.
To avoid the host’s immune defence, the larvae mimic the host at a mo-
lecular level. This mechanism is unique among insect parasitoids and
170 Christina Nagler and Joachim T. Haug

explains their success (Kathitiramby, 2009). The development of strepsipter-


ans is classified as hypermetamorphosis (again cf. Meloidae). After the triun-
gulin larva, there are four further larval stages. Finally the last larval stage
emerges from host to pupate externally in all males. In species in the less-
derived group Mengenillidae, the females also leave the host to pupate.
All other females remain endoparasitic in the host, only the anterior region
is visible from the outside (Kathithiramby, 2009).
One special case within Strepsiptera, Myrmecolacidae shows the so-
called heterotrophic heteronomy (see Kathirithamby et al., 2010). The hosts
for males are ants, those for females are grasshoppers, crickets and mantids.
Pohl and Kinzelbach (2001) suggested that the primary hosts of Myrmeco-
lacidae were ants. A related case is known in endoparasitoid Aphelinidae
(Kathithiramby, 2009). Representatives of the extinct strepsipteran in-group
Mengeidae were parasitoids of Zygentoma (silverfish; Grimaldi and Engel,
2005).

5.2.2 Phylogenetic inference of appearance and molecular


estimations of early evolution
The systematic and phylogenetic position of Strepsiptera has long been
controversial. They have been thought to be the most problematic group
of insects in terms of its systematic placement (Pohl et al., 2010). Grimaldi
and Engel (2005) proposed that it would not be surprising, if Strepsiptera
is a highly modified lineage, derived from holometabolans, such as stem-
group neuropterids or mecopteroids. Probably during the Eocene (45
ma), the transition between less-derived and modern strepsipterans took
place (Kathithitramby, 2009).
Recent molecular- and morphologically-based phylogenetic studies
provide support that Strepsiptera is the sister group to Coleoptera (Boussau
et al., 2014; Pohl and Beutel, 2013; Niehuis et al., 2012). The extinct forms
Protoxenos, Cretostylops and Mengea are considered to be the derivatives of the
evolutionary lineage towards modern Strepsiptera. This is based on morpho-
logical data, especially CT analysis of Mengea tertiaria in Baltic amber (Beutel
et al., 2014; Pohl et al., 2010). The newly discovered Bahiaxenidae
(Figure 5(a)) from Brazil has been considered to be the sister group of the
remaining modern Strepsiptera. They have been interpreted as a relic group
having changed only little since the Permian (Bravo et al., 2009). Within the
remaining modern strepsipterans, excluding Bahiaxenidae, Eoxenos has been
resolved as the sister group to all remaining forms (McMahon et al., 2011;
Bravo et al., 2009).
Insects as Parasites and Hosts 171

Figure 5 Fossil parasitoid strepsipterans (Figure 5a and b); plant parasitic gall wasp
(Figure 5(c)). (a) Bahiaxenos relictus (Bahiaxenidae, Strepsiptera) (modified with permis-
sion from John Wiley & Sons from Bravo et al. (2009, Figure 2)). (b) Bohartilla kinzelbachi
(Bohartillidae, Strepsiptera) (modified from Grimaldi and Engel (2005, Figure 10.88) with
kind permission of Cambridge University Press and David Grimaldi). (c) Gall-forming cyn-
ipidan (Cynipidae, Hymenoptera) (modified from Grimaldi and Engel (2005, Figure 11.17)
with kind permission of Cambridge University Press and David Grimaldi).

5.2.3 Fossil representatives


• The majority of strepsipteran fossils have been found in various types of
amber: Burmese (100 ma), Canadian (75 ma), Eocene Baltic (42e45 ma)
and Miocene Dominican (25 ma; Cook, 2014; Pohl et al., 2012, 2010,
2005; Kogan and Poinar, 2010; Kathirithamby and Hendricks, 2008;
Poinar, 2002; Pohl and Kinzelbach, 2001, 1995; Kulika, 2001;
Kinzelbach and Pohl, 1994; Kathirithamby and Grimaldi, 1993; Lutz,
1990; Kinzelbach and Lutz, 1985; Kinzelbach, 1983, 1979; Kulika,
1979; Ulrich, 1927; Meng, 1866). Mainly forms ascribed to Mengeidae,
Mengenillidae and Myrmecolacidae have been found. A great diversity
of less-derived Strepsiptera has been found in Cretaceous Burmese
172 Christina Nagler and Joachim T. Haug

amber. In Baltic and Dominican amber, more modern (Figure 5(b)) and
less-derived strepsipterans occur together.
• Some fossils provide quite direct evidence for the extraordinary life cycle
of strepsipterans and direct evidence for their parasitoid lifestyle: (1) two
puparia on an ant specimen in Middle Eocene oil slate of Messel (Lutz,
1990), (2) an ant with an emerging parasite preserved in amber (Pohl and
Kinzelbach, 2001), (3) an empty male puparium associated with a hyme-
nopteran preserved in amber, (4) two parasitized planthoppers, from one
of these planthoppers emerge larvae (Poinar, 2004b) and preserved in
amber, (5) a female specimen ascribed to Myrmecolacidae parasitizing
an ant in Baltic amber (Pohl and Kinzelbach, 2001).

6. PLANT PARASITISM (VERSUS PHYTOPHAGY)


6.1 General aspects
Numerous insects consume plants. Yet some insects also make use of
plants in other ways. Some insects oviposit eggs into plants and induce the
growth of galls; this is a form of plant parasitism. In leaf miners, the larvae
feed on the plants until they emerge as pupa or adult, thus it is comparable
to larval parasitoids feeding within insects. However, here the line to phy-
tophagy is not easy to draw.
Galls are remarkable structures occurring on all organs of a plant. With
galls an insect is forcing the plant to provide nutrition and/or a habitat,
thus this should represent a case of true parasitism. Galls can be also induced
by bacteria, fungi, mites, viruses and nematodes (Knor et al., 2013). Gall-
inducing insects are representatives of Cynipidae (gall wasps), Cecidomyii-
dae (gall midges), Psyllidae (jumping plant lice), Thysanoptera (thrips),
Anisoptera (dragonflies), phytophagous hymenopterans (sawflies), Coleop-
tera (beetles), Aphididae (plant lice), Tingidae (lace bugs), Cicadellidae (leaf-
hoppers) and some heterocerans (moths) (Knorr et al., 2013; Grimaldi and
Engel, 2005). Moth larvae are important leaf miners, the egg is oviposited
into the leaf and the larvae feed on the mesophyll until they pupate and
fall on the ground (Labandeira et al., 1994).
Exceptionally preserved fossils from the US provided an uncompressed
planteinsect system from the Palaeocene (Donovan et al., 2014; Wappler
et al., 2009). In such systems, it is possible to identify the parasite that caused
fossil mines and galls (Carvalho et al., 2014; Donovan et al., 2014; Grimaldi
and Engel, 2005), based on their unique characteristics; e.g. position on the
plant, shape, host specificity, path of the mine and size.
Insects as Parasites and Hosts 173

6.2 Phylogenetic inference of appearance and molecular


estimations of early evolution
Inducing galls has evolved multiple times independently among the insects.
This ability is considered to have originated first about 300 ma in the
Carboniferous in a not further known holometabolous larva (Labandeira,
2011). But this attribution has been considered doubtful, as also mites
may produce comparable galls (Grimaldi and Engel, 2005; Rasnitsyn and
Quicke, 2002).
A significant radiation of gall-inducing and also leaf-mining insects
occurred in the Late Cretaceous, most likely coupled to the radiation of
the angiosperms (Knorr et al., 2013; Rasnitsyn and Quicke, 2002;
Labandeira et al., 1994). Several fossils indicate an origin of Cynipodea in
the Jurassic. The origin of gall making in Hymenoptera occurred first in
the Middle Cretaceous when first forms of Fagacea (beeches and oaks)
appeared in the fossil record (Grimaldi and Engel, 2005).
The gall midges (Cecidomyiidae) are known since the Late Jurassice
Early Cretaceous (Grimaldi and Engel, 2005). The main radiation of Ceci-
domyiidae took place during the Palaeogene coupled to the evolution of
flowers (Wappler et al., 2010). These dipterans have been considered to
have originated in the Late Jurassic, at first parasitizing gymnosperms and
switching later to angiosperms (Labandeira et al., 1994). Most fossil galls
resemble their modern counterparts, which emphasizes the long-term
evolutionary coexistence and coevolution of host plant and parasitic gall-
making insect (Knorr et al., 2013; Krassilov, 2007). For a more comprehen-
sive review, see Labandeira (2013) and Labandeira and Currano (2013).

6.3 Fossil representatives


There are numerous plant fossils with galls (Palaeogallidae) and mines
(Palaeominidae) on plants as well as adult free-living plant parasitic insects.
Hence we only list here some examples:
• The oldest representative of Cynipidae (Figure 5(c)) is from Baltic amber
and could induce galls on rosaceans, like modern relatives (Grimaldi and
Engel, 2005).
• There is one extraordinary fossil: galls on the seed of a redwood from the
Miocene of Germany containing larval and pupal gall midges (M€ ohn,
1960).
• Pott et al. (2008) reported eggs which were found inside the interior of a
fossil leaf from the Carnian of Austria (150 ma). They suggested
174 Christina Nagler and Joachim T. Haug

the possible parent could have been a dragonfly, due to the elongated
ovipositor, that is needed to pierce through the robust leaves of bennet-
titalean plants. Yet also other insect groups possess long ovipositors.
• There are some leaf-mining fossils that appear extremely similar to their
modern counterparts: moths on oaks (for 20 million years), moths on
poplars (for 20 million years), moths on mahogany (for 40 million years)
and beetles on Heliconia (for 70 million years) (Grimaldi and Engel,
2005).

7. INSECTS AS HOSTS
7.1 Nematoida
7.1.1 General aspects
The monophyletic group Nematoidea consists of the two sister groups
Nematomorpha (hairworms) and Nematoda (roundworms) (Bleidorn
et al., 2002; Schmidt-Rhaesa, 2013).
Within the hairworms, 350 extant species are known which fall into two
groups: Gordiida with freshwater and terrestrial forms and Nectoma with
marine forms (Schmidt-Rhaesa, 2013). Gordiids have a free-living aquatic
phase and an obligate parasitic phase on terrestrial invertebrates. The parasite
goes through two hosts; the final host (insect) has to eat the intermediate
host (freshwater snail, small aquatic insects; Poinar, 2011a; Labandeira,
2002; Schmidt-Rhaesa and Ehrmann, 2001). Extant species parasitize
carabid beetles, grasshoppers, cockroaches and praying mantids (Schmidt-
Rhaesa and Ehrmann, 2001).
Nematoda includes about 10,500 species that are endoparasites of arthro-
pods and vertebrates (Poinar and Thomas, 2014; Poulin, 2006). Although
there are about 20,000 described extant nematode species, several million
species have been estimated (Schierenberg and Sommer, 2011; Poinar,
2012a). Fossil nematode parasites are treated in detail elsewhere in this
volume (Poinar, 2015).

7.1.2 Phylogenetic inference of appearance and molecular


estimations of early evolution
Nematoidea has been considered to have originated in the Precambrian
(Poinar, 2011a, 2013a, 2015b; Rota-Stabelli et al., 2013). Cambrian fossils
of cycloneuralians are diverse and hence indicate an older divergence of
the subgroups (e.g. Maas, 2013 and references therein).
Insects as Parasites and Hosts 175

7.1.3 Fossil representatives


It has been considered that less-derived forms parasitize less-derived insect
groups (Blattaria and Mantoptera) and more derived nematomorph groups
parasitize more derived insects, like coleopterans (Schmidt-Rhaesa and
Ehrmann, 2001), due to coevolutionary processes. Hence although the
direct fossils are rare, we could assume a similar age to these insect groups.
The oldest nematomorph fossils were found in Cretaceous deposits (Poinar
and Buckley, 2006).
There are some fossils that need to be discussed in reference to Gordiida
recorded so far.
• Cretachordodes burmitis comes from the Early Cretaceous Burmese amber
(100e110 ma), yet it is an isolated specimen, without a host (Poinar and
Buckley, 2006).
• Other nematomorph fossils include two females in association with
their cockroach host from Dominican amber (15e45 ma) (Poinar,
1999). A fungus and its ecology indicate, that their habitat was
moist to wet, which is attractive to roaches and carabids and that
small forest streams seem to be their aquatic habitat (Schmidt-Rhaesa,
2013).
• Other fossil worms of Palaeoscolecida may resemble Nematomorpha
(Xianguang and Bergstr€ om, 1994), but have been interpreted to
be early offshoots of the lineage towards Priapulida (Harvey et al.,
2010).
• Shergoldana australiensis from the Middle Cambrian of Queensland,
Australia, resembles a nematomorph larva in many aspects (Maas et al.,
2007). Yet, this form may have lived in the meiofauna, similar to kino-
rhynch cycloneuralians.

7.2 Mites
7.2.1 General aspects
Acari comprises about 55,000 described extant species, known as mites.
They can be free-living herbivorous and scavenging, as well as predatory,
or parasites of insects and vertebrates (Dunlop and Penney, 2012; Pereira
et al., 2012). They are also important vectors of several viruses and bacteria,
for example Borrelia burgdorferi that causes Lyme disease and might have
already been so in the past (Poinar 2014a,b, 2015). Mites use insects, partic-
ularly termites, ants and other arthropods for transport in a phoretic way also
(Dunlop and Penney, 2012).
176 Christina Nagler and Joachim T. Haug

7.2.2 Phylogenetic inference of appearance and molecular


estimations of early evolution
The origin of mites was estimated to be in the Late Silurian (Mans et al.,
2011). For the parasitic in-group Astigmata an origin in the Middle
Permian, 270 ma, has been proposed based on molecular data (Garwood
and Dunlop, 2014; Dabert et al., 2010). Phoretic behaviour in mites has
been proposed to have evolved at least in the Eocene (44e49 ma; Dunlop
et al., 2012).

7.2.3 Fossil representatives


Acari are comparably abundant in the fossil record with 309 fossil records
(Dunlop and Penney, 2012).
• A representative from the supposedly more ancestral Anactinotrichida is
known from Rhynie chert of Scotland (395 ma) and other Devonian
sites (Norton et al., 1988).
• Some parasitic mites in amber are associated with their host. Parasitic
mites (Figure 6(c)) of the species-rich group Leptus have been preserved
in Baltic amber. They occur together with their host, a wide range of
dipterans, like fungus gnat (Limoniidae), window gnats (Empididae)
and Dolichopodidae, but also with different types of hymenopterans
(Dunlop et al., 2014; Arillo, 2007).
• In Baltic amber, water mites have been found too. They parasitize rep-
resentatives of Chironomidae (nonbiting midges) or Trichoptera (caddis
flies; Arillo, 2007). Mites parasitizing representatives of Drosophilidae,
Chironomidae, Sciaridae and moths have been reported from Domin-
ican amber (Arillo, 2007).
• Cretaceous fossils (in amber, but also compression fossils) of mites
(Figure 6(d)) preserve them still attached to their insect hosts (Judson
and Maakol, 2009; Arillo, 2007; Dunlop, 2007; Klompen and Grimaldi,
2001; Poinar et al., 1997).
• Mites from Spanish amber and Lebanese amber, both from the Lower
Cretaceous, have been reported to parasitize several forms of Diptera
(Arillo, 2007; Labandeira, 2002).
• There are also mites parasitizing hemipterans from several different
amber deposits (Poinar et al., 2012; Azar, 2007; Koteja and Poinar,
2005).
• Phoretic behaviour has been reported from Cretaceous amber sites and
Eocene Baltic amber (Dunlop et al., 2012; Azar, 2007).
Insects as Parasites and Hosts 177

Figure 6 Vectors and hosts. (a) Pheidole dentata (Myrmicinae, Formicidae) parasitized by
nematodes (modified after Poinar (2012a, Figure 6(c))). (b) Lutzomyia adiketis
(Phlebotominae, Diptera) (modified after Poinar (2008b, Figure 1)). (c) Myrmozercon sp.
(Mesostigmata, Acari) attached to Ctenobethylus goepperti (Dolichoderinae, Formicidae)
(modified from Dunlop et al. (2014, Figure 1(b)) with kind permission of the Royal Society).
(d) Erythraeid mite (Erythraeidae, Acari) on a chironomid midge (Chironomidae, Diptera)
(modified from Poinar and Krantz 1997, Figure 2 with kind permission from Springer Science
and Business Media). (e) Cheliferidae indet (Cheliferoidea, Pseudoscorpionida) (modified
from Judson (2009, Figure 5(b)) with kind permission of Geodiversitas and Mark Judson).

7.3 Pseudoscorpions
7.3.1 General aspects
There are currently 3533 described extant species and 41 fossil species of
pseudoscorpions (Harvey, 2013). Pseudoscorpions distantly resemble
scorpions, yet their posterior segments are not differentiated as a tail. Also
pseudoscorpions possess a characteristic cheliceral spinning apparatus
178 Christina Nagler and Joachim T. Haug

(Dunlop, 2010). The minute pseudoscorpions live in cryptic environments


and are predators of other nonvertebrates (Del-Claro and Tizo-Pedrosos,
2009; Grimaldi and Engel, 2005). Representatives of a few pseudoscorpion
groups show highly complex behaviour and are subsocial in the form of
brood care (Del-Claro and Tizo-Pedroso, 2009). All pseudoscorpions
have chelate pedipalps (a major reason why they distantly resemble scor-
pions) and many groups have a venom gland inside the pedipalp.
With their chelate pedipalps some pseudoscorpions temporarily attach
themselves to larger nonvertebrates. This is done in a way that does not
affect the locomotion capacities of the host, and allows dispersal via phoresy
(Poinar, 2013b; Boucot and Poinar, 2010; Judson, 2009; Szymkowiak et al.,
2007). Some pseudoscorpions are host-specific and some are also site-
specific on the host (Poinar, 2013b; Boucot and Poinar, 2010). Species of
Tridenchthoniidae, Lechytiidae, Syarinidae, Geogarypidae, Larcidae,
Sternophoridae, Cheiridiidae, Chernetidae and Cheliferidae are known to
be phoretic (Szymkowiak et al., 2007). Host species are known from
Coleoptera, Lepidoptera, Homoptera, Diptera (Aguiar and B€ uhrnheim,
1998) and other arthropods (Grimaldi and Engel, 2005).

7.3.2 Phylogenetic inference of appearance and molecular


estimations of early evolution
The origin of arachnids has been considered to be in the Silurian. The fossil
record of pseudoscorpions reaches back to the Devonian (Dunlop, 2010).
Due to some complex morphological characters, traditionally pseudoscor-
pions are interpreted as the sister group to camel spiders (Solifugae; Dunlop,
2010). Recent morphological and molecular studies resolved a sister group
relationship between pseudoscorpions and scorpions (Garwood and
Dunlop, 2014; Pepato et al., 2010), yet this would mean that the long
time stable group Lipoctena would represent an artefact.
Cheliferoidea (which has representatives showing phoretic behaviour)
has been considered to be the most derived group of pseudoscorpions due
to their morphology and behaviour. The origin has been suggested to be
older than the Cretaceous, because representatives were diverse and wide-
spread in the Cretaceous already (Judson, 2009).
It has been proposed that phoresy originated at least five times within
pseudoscorpions (Judson, 2004). The phoretic relationship between pseudo-
scorpions and invertebrates provides evidence for a long-standing and stable
coevolution (Boucot and Poinar, 2010; Judson, 2004).
Insects as Parasites and Hosts 179

7.3.3 Fossil representatives


• The only non-amber and oldest pseudoscorpion fossil is Dracochela depre-
hendor from the Middle Devonian (374e92 ma), based on isolated cuticle
fragments (Schawaller et al., 1991). It remains unclear whether this spe-
cies was phoretic.
• The next younger fossil is known from approximately 250 million years
later in Cretaceous amber. It is a nymphal specimen attributed to Che-
liferoidea from Upper Cretaceous Canadian amber (Schawaller, 1991).
About the same age are three pseudoscorpions (two specimens of Heur-
taultia rossiorum and one undescribed specimen) (Figure 6(e)) from the
Lower Cretaceous Albian amber from France (Judson, 2009). Also there
are two specimens from Burmese amber (Judson, 2000; Cockerell,
1920), several specimens from Dominican amber (Judson, 1998) and
also from Baltic amber (Hendrickx et al., 2006). Another species has
been described from Miocene Chiapas amber (Riquelme et al., 2014).
Undescribed pseudoscorpions have been reported in Upper Cretaceous
New Jersey amber (Grimaldi et al., 2002), Lower Cretaceous Lebanese
amber (Grimaldi, 1996) and Lower Cretaceous Albian amber (Delcl os
et al., 2007).
• Five subfossil specimens of unclear exact age have been reported from:
(1) Zanzibar copal, Chelifer eucarpus, (2) two pseudoscorpions from
Madagascan copal and (3) two specimens from Colombian copal
(Judson, 2010).
• There are several fossils with direct very evidence for phoresy: pseudo-
scorpions on beetles (Poinar, 2013b, 1992; Grimaldi, 1996), on flies
(Judson, 2004; Poinar et al., 1998), on a snipe fly (Ross, 1998), on a nem-
atoceran fly (Kosmowska-Ceranowicz, 2001), on a braconid wasp
(Weitschart and Wichard 1998), on a moth (Boucot and Poinar,
2010), all preserved in various types of amber.

8. INSECTS AS VECTORS
8.1 General aspects
Extant insects are important vectors for numerous viruses, bacteria and
protist, but it is difficult to give fossil evidence for it (Poinar, 2014b). The
most important arthropods that serve as vectors are haematophagous insects
and arachnids (ticks).
180 Christina Nagler and Joachim T. Haug

Extant lice transmit significant human diseases. Examples are trench


fever, typhus, relapsing fever, but also wildlife diseases, like swine pox,
anaplasmosis, dermatomycosis, Lebombo virus or heartworms (Mitchell,
2015; Light et al., 2010).
Fleas via their mouthparts can transmit one of the most devastating
diseases in human history: the plague that is caused by the bacteria Yersinia
pestis. Also they are vectors for several worm parasites and protists (Grimaldi
and Engel 2006).
Additionally cockroaches, coprophagic beetles and synanthropic flies,
whiteflies, leafhoppers and treehoppers are important vectors of protozoan
parasites and viral elements, called geminiviruses (Graczyk et al., 2005;
Czosnek et al., 2001).
One of the most important groups in transmitting pathogens is Diptera,
especially in-groups such as sand flies, mosquitoes, blackflies and tsetse flies
(Poinar, 2014b). Almost 10% of all described extant sand flies transmit bac-
teria, viruses and protozoans, with trypanosomatids as the most widely
distributed pathogen. All forms of Trypanosomatida are parasitic (Lopes
et al., 2010). The intracellular protozoan Leishmania, an in-group of Trypa-
nosomatida is spread through bites by sand flies.
Phlebotomines transmit several animal trypanosomes, malaria parasites,
bacteria and rhabdovirus (Azar and Nel, 2003). It has been proposed that
free-living trypanosomatids associated with food sources for dipteran larvae
were eaten by these, and then were still present in the adult stage of a
dipteran, and then transmitted to vertebrates (Poinar, 2008b, 2007).
Ceratopogonids and mosquitoes are vectors for more than 300 viruses
that cause, for example, breakbone fever, river blindness or elephantiasis
(Grimaldi and Engel, 2005). The most ‘famous’ disease transmitted by culi-
comorphans is malaria that is also caused by a protozoan parasite.
An important endosymbiotic bacterium is Wolbachia that has been
reported to be transmitted by almost all terrestrial arthropods as well as nem-
atodes (Koutsovoulos et al., 2014).
Aphids and some beetle species mechanically transport fungus spores
and infect plants, due to their phytophagy, with phytopathogen fungi
(Kluth et al., 2002). Aphids, leafhoppers, spittlebugs, flea beetles, cucumber
beetles, psyllids and fruit flies serve as vectors for several bacterial phyto-
pathogens that damage plants (Nadarasah and Stavrinides, 2011). Endosym-
biotic bacteria, viruses and protozoans can influence the biology of
their insect vectors. They can be mutualistic, parasitic and commensalic
(Longdon and Jiggins, 2012). Also some viruses, cytoplasmic polyhedrosis
Insects as Parasites and Hosts 181

virus (CPV) and nuclear polyhedrosis virus (NPV), infect only insects and
are distributed among their populations, whereas some attack mammals
and birds also. These viruses are always fatal to the population of the
infected insects.

8.2 Phylogenetic inference of appearance and molecular


estimations of early evolution
Throughout their evolution sand flies and parasitic organisms likely have
coevolved. Due to their haematophagy parasitic diseases are likely as old
as the sand flies themselves (Azar and Nel, 2003). Thus the protozoan
parasites should have originated at least in the Early Cretaceous, 140 ma,
together with species of Ceratopogonidae as their ancient vectors (Pérez-
de la Fuente et al., 2011; Poinar, 2008a).
The association of hemipterans and trypanosomas originated at a similar
time, in the Middle Caenozoic, supposedly with bats as primary hosts
(Otalora-Luna et al., 2015; Poinar, 2005c). Similar parasites that were
vectored by sand flies have been proposed to have contributed to the extinc-
tion of the dinosaurs (Azar and Nel, 2003). The similarity of fossil and extant
and fossil trypanosomes has been seen as a strong indication for haematoph-
agy in the past (Poinar, 2004a; Greenwalt et al., 2013).
The interaction between wolbachians and insects is stable at least since
100 million years according to some molecular studies (Cerveau et al.,
2011).
The recent discovery of Arsenophonus, a c-proteobacterium, probably
played an important role in the evolution of bat flies and louse flies for
the development of their true ectoparasitism, at least 20 ma (Duron et al.,
2014).
Current research on phytopathogens transmitted via insects sheds new
light on their evolution. The traditional role of insects might have evolved
over a transitional stage, where the insect served as vector and host, to the
final form with the insect as host. Thus phytopathogenic bacteria evolved
to become insectopathogenic bacteria (Nadarasah and Stavrinides, 2011).
Different insect-borne viruses, which are viruses transmitted by insects,
have been considered to exist for at least 100 million years. These may
have coevolved with certain species of Diptera (Psychodidae and Culico-
morpha) since the Early Cretaceous, thus providing an evolutionary path
for vertebrate infections (Poinar and Poinar, 2005). The long relationship
of parasites and insects indicates a coevolutionary mechanism (Czosnek
et al., 2001).
182 Christina Nagler and Joachim T. Haug

8.3 Fossil representatives


Despite the small size of many of the organisms, there have indeed been
some fossil finds in amber that were interpreted as including:
• numerous flagellates (similar to Trypanosoma) on a faecal pellet of a hae-
matophagic hemipteran from Dominican amber (Poinar, 2005c)
• two trypanosome parasites (Paleoleishmania proterus and Paleoleishmania
neotropicum) from the gut and proboscis of a specimen of Phlebotominae
(Figure 6(b)) from Dominican amber and Burmese amber (Poinar,
2008a; Poinar and Poinar, 2004b)
• a supposed CPV and Trypanosoma infection in a midge from Burmese
amber (Poinar and Poinar, 2005); the provided images cannot easily be
used to judge this ascription.
• a supposed NPV in a sand fly from Burmese amber (Poinar and Poinar,
2005). Also here the images provided in the description hardly allow a
confident judgement or interpretation.
• three fungal pathogens from insects in Dominican amber (Poinar and
Poinar, 2005).
• different plasmodia on dipteran specimens from Cretaceous amber
(Poinar, 2011b; Poinar and Telford, 2005)

9. CONCLUSION
Given the shear vastness of examples of parasitism in and by insects, it
is hard to draw any major conclusions. However, a few overriding patterns
can be mentioned.
Two of the four hyperdiverse lineages appear to have their early radia-
tions coupled to parasitism sensu lato, namely Hymenoptera and Diptera.
So we can indeed ask what made these two lineages so successful. In both
cases, the parasitic act is directly linked to the provision of nutrition to
offspring, in early hymenopterans by injecting the egg into a host, and in
dipterans by haematophagy of the female to have enough nutrients to be
stored in the eggs. Compared to other lineages the parasitic act is therefore
less of an ‘everyday business’, which mainly means that in both lineages the
mobility of the adult is retained. This is quite different, for example, in fleas
or lice, where developing successful dispersal mechanisms are likely one of
the important factors in the early diversification of these two lineages.
Another similarity is that in both Hymenoptera and Diptera, there were in-
dependent switches to feeding on flower products, which likely triggered a
Insects as Parasites and Hosts 183

Figure 7 Timescale of the discussed groups. Dashed lines indicate the ghost range of
the respective groups. Solid lines are based on actual findings of the respective
groups.

second diversification. Also we find lineages within Hymenoptera and


Diptera that switched back again to parasitic lifestyles. This parallel type of
pattern in Hymenoptera and Diptera might be superficial, yet it would be
an interesting candidate pair for a closer comparison, including fossil data.
This must remain a task for future approaches. An overview of the origin
of the discussed species is given in Figure 7.

10. OUTLOOK
With the given examples, we provide direct and indirect evidence for
palaeoparasitology concerning insects. Regrettably most fossil examples for
palaeoparasitism only provide indirect evidence for parasitism (pathological
changes of the host, functional morphology of the isolated parasite, phylo-
genetic inference) and these are more difficult to compare to their extant
counterparts. Nevertheless, these fossils have the potential to reveal impor-
tant aspects of the origins and diversification of parasitic lifestyles in various
evolutionary lineages. But even with all these fossil examples, for which
there is a much better record than in many other metazoan groups, we
184 Christina Nagler and Joachim T. Haug

only get a phenomenological insight. To understand the evolution, biology,


ecology and morphology of these fossil parasitic insects, we have to combine
several methods, e.g. phylogenetics, biogeographics, taphonomy, geochem-
ical studies, molecular studies, fossil record and extant species.
Fossils provide a snapshot of the historical biogeography, evolutionary
history and morphological diversification. They also provide their minimum
age. While molecular data are generally thought to help to develop an
evolutionary scenario only fossils allow a true look into former times. Yet,
this is not a one-way road, also knowledge on extant forms is necessary to
better understand fossil specimens. Only holistic approaches with a mature
concept of reciprocal illumination between fossil and extant knowledge
will provide a more detailed understanding of the evolutionary processes
leading to the modern forms.
To tell their ‘true’ story (or at least to come closer to it) more and
more fossils are needed, especially in groups that are considered to have
a sparse fossil record. Often parasitic insects would not be recognized
due to their size or lifestyle, but it is important to find these fossils.
Much of the direct evidence for parasitism is found in amber, because
this resin preserves specimens with microscopic details. Thus, the smallest
mite can be visible on an insect. But also fine-grained sedimentary rocks
preserve fossil specimens very well. Unfortunately ectoparasites may well
be removed during the preparation process, often because they were not
recognized as parasites.
With the aid of additional fossils, we can hope to identify more interme-
diate forms between fossils and extant species or between different lifestyles,
we are able to answer questions of the functional morphology, their ecol-
ogy, their environmental impact, their evolution with their minimum
age, radiations and extinctions and the changing of their lifestyle from free
living to parasites to vectors.

ACKNOWLEDGEMENTS
Foremost we thank the editors for the invitation to contribute to this volume. CN is funded
by the Studienstiftung des deutschen Volkes with a PhD fellowship. JTH is kindly funded by
the German Research Foundation (DFG) under Ha 6300/3-1. Both authors thank J. M.
Starck, Munich, for his support. We thank all people involved in providing free and low-
cost software, such as OpenOffice, CombineZM, CombineZP, Image Analyzer.

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(Insecta: Psocodea)?: A comparison of phylogenetic signal in multiple genes. Molecular
Phylogenetics and Evolution 55, 939e951.
Yoshizawa, K., Lienhard, C., 2010. In search of the sister group of true lice: a systematic
review of booklice and their relatives, with an updated checklist of Liposcelididae
(Insecta: Psocodea). Athropod Syst. Phylog. 68, 181e195.
Zhang, J., 2012. New horseflies and water snipe-flies (Diptera: Tabanidae and Athericidae)
from the lower Cretaceous in China. Cretac. Res. 36, 1e5.
CHAPTER FIVE

Trace Fossil Evidence of


TrematodeeBivalve
ParasiteeHost Interactions
in Deep Time
John Warren Huntley*, 1, Kenneth De Baetsx
*Department of Geological Sciences, University of Missouri, Columbia, MO, USA
x
Fachgruppe Pal€aoUmwelt, GeoZentrum Nordbayern, Friedrich-Alexander-Universit€at
Erlangen-N€urnberg, Erlangen, Germany
1
Corresponding author: E-mail: huntleyj@missouri.edu

Contents
1. Introduction 202
2. Trematode-Induced Shell Malformations in Living Bivalve Molluscs 206
3. Occurrences of Trematode-Induced Pits in Fossil and Subfossil Bivalves 211
3.1 Taxonomic, temporal and ecological occurrences 211
3.2 Taphonomy and the origin of the trematodeebivalve parasiteehost 217
interaction
3.3 Trematode-induced malformations as palaeoenvironmental indicators 220
4. Detrimental Effects of Trematodes on Living Bivalves and Their Potential 222
Evolutionary Implications
5. Concluding Remarks 225
Acknowledgements 226
References 226

Abstract
Parasitism is one of the most pervasive phenomena amongst modern eukaryotic life
and yet, relative to other biotic interactions, almost nothing is known about its history
in deep time. Digenean trematodes (Platyhelminthes) are complex life cycle parasites,
which have practically no body fossil record, but induce the growth of characteristic
malformations in the shells of their bivalve hosts. These malformations are readily pre-
served in the fossil record, but, until recently, have largely been overlooked by students
of the fossil record. In this review, we present the various malformations induced by
trematodes in bivalves, evaluate their distribution through deep time in the phyloge-
netic and ecological contexts of their bivalve hosts and explore how various tapho-
nomic processes have likely biased our understanding of trematodes in deep time.
Trematodes are known to negatively affect their bivalve hosts in a number of ways
including castration, modifying growth rates, causing immobilization and, in some
Advances in Parasitology, Volume 90
© 2015 Elsevier Ltd.
j
ISSN 0065-308X
http://dx.doi.org/10.1016/bs.apar.2015.05.004 All rights reserved. 201
202 John Warren Huntley and Kenneth De Baets

cases, altering host behaviour making the host more susceptible to their own
predators. Digeneans are expected to be significant agents of natural selection. To
that end, we discuss how bivalves may have adapted to their parasites via heterochrony
and suggest a practical methodology for testing such hypotheses in deep time.

1. INTRODUCTION
Interpreting the history and evolutionary implications of antagonistic bi-
otic interactions in the marine invertebrate fossil record has been a primary
theme in palaeobiology during the last few decades. The primary focus of
this pursuit has been the examination of predatoreprey interactions, which
has highlighted the likely role of antagonistic interactions in shaping macro-
evolutionary trends (Vermeij, 1977; Signor and Brett, 1984; Kowalewski
et al., 1998; Kelley and Hansen, 2003; Madin et al., 2006; Huntley and
Kowalewski, 2007). Competitive interactions have received some attention
in the literature (Hermoyian et al., 2002; Huntley et al., 2008; Tyler and
Leighton, 2011), but may not be an important agent of natural selection in
benthic marine environments (Stanley, 2008). Parasitism, however, is one
of the most pervasive phenomena amongst modern eukaryotic life (Poulin
and Morand, 2000) and, relative to predation, almost nothing is known about
it in deep time (Littlewood and Donovan, 2003). Parasites and the traces they
leave behind have been preserved as fossils (Moodie, 1923; Cameron, 1967;
Fry and Moore, 1969; Conway Morris, 1981; Ruiz and Lindberg, 1989;
Boucot, 1990; Savazzi, 1995; Feldmann, 1998; Feldman and Brett, 1998;
Littlewood and Donovan, 2003; Boucot and Poinar, 2010), but the docu-
mentation of the intensity of specific parasiteehost interactions through
deep time is rare indeed (for some notable exceptions see Brett, 1978;
Baumiller and Gahn, 2002; Gahn and Baumiller, 2003; Klompmaker et al.,
2014; Wilson et al., 2014; De Baets et al., 2011, 2015a). Based upon their
relative positions within trophic webs, parasites are likely to be more abun-
dant and diverse than predators in modern ecosystems. There is an increasing
appreciation for the roles of parasites in shaping communities (Hudson et al.,
2006) and promoting evolvability (Zaman et al., 2014), but what role have
they played in shaping ecological and macroevolutionary trends of their hosts
in deep time? In order to discern the importance of parasitism in deep time,
one must first explore its origin in a phylogenetically informed context, sys-
tematically analyze the occurrence and intensity of parasiteehost interactions
through geologic time, consider the potential biases introduced by the process
of fossilization and try to disentangle these biases from the biotic record so that
Trace Fossil Evidence of TrematodeeBivalve ParasiteeHost Interactions in Deep Time 203

we can understand how the biases might distort our view of the history of
parasiteehost interactions.
Bivalve molluscs serve as hosts to a diverse group of parasites and disease-
causing agents including viruses, prokaryotes (e.g. Chlamydia and Rickettsia),
fungi, protistans, parazoans (e.g. boring sponges like Cliona) and metazoans
(e.g. platyhelminths, annelids, molluscs, bryozoans and arthropods); see
Lauckner (1983) for an excellent account of the myriad parasites and diseases
of bivalves. Given that many parasites are typically small-bodied and often
lack biomineralized skeletons, we should not expect an extensive record
of body fossils (although, of course there are exceptions: Fry and Moore,
1969; Baumiller and Gahn, 2002; Gahn and Baumiller, 2003; Poinar,
2003; amongst others); therefore, we must seek evidence for parasitism in
the form of traces and malformations on the mineralized hosts. Unfortu-
nately, not all interactions result in the production of a trace or shell
malformation.
A variety of taxa can produce or induce the formation of a trace or shell
malformation when interacting with the bivalve. Indeed, one of the primary
challenges when interpreting these traces is determining if the interaction
was ante-mortem or postmortem, relative to the bivalve. From this perspec-
tive, we can categorize such interactions and their resulting traces into two
groups: (1) interactions that are the result of active boring or shell destruction
by the putative parasite, and, thereby, we cannot distinguish between a
liveedead and a liveelive interaction, and (2) interactions that induce a
growth reaction by the bivalve, and, thereby, we know that the trace or mal-
formation was the result of a liveelive interaction.
Many taxa produce this first type of trace in bivalves and they may not
be, in some cases, strictly parasitic in origin. For instance, spionid polychaete
worms will frequently bore into calcium carbonate substrates (including
bivalves) and produce characteristic U-shaped (and sometimes more com-
plex shaped) borings with paired openings adjacent to one another on the
valve surface (Blake and Evans, 1973; Thayer, 1974; Zottoli and Carriker,
1974; Huntley, 2007; Rodrigues, 2007; Huntley and Scarponi, 2015). Spio-
nids are generally capable of suspension- and deposit-feeding (Dix et al.,
2005). Their boring activity likely weakens their host’s shell and valve and
site preference of spionids suggests they kleptoparasitize the feeding currents
of their hosts (Huntley, 2007; Rodrigues, 2007). The work of Rodrigues
et al. (2008) revealed that spionid borings in live brachiopods of coastal Brazil
were nearly always occupied by live spionids, whereas live spionids were not
identified in borings found in dead brachiopods from the same location.
204 John Warren Huntley and Kenneth De Baets

Despite evidence for liveelive interactions in modern settings, we cannot


always say with certainty that such traces were produced on live bivalves
in the past. There are many other taxa that bore into bivalves and other
carbonate substrates, which may or may not be parasitic, including sponges
(e.g. Cliona), foraminifera, bryozoans, barnacles, bivalves and predatory gas-
tropods (Boucot, 1990; Boucot and Poinar, 2010). Given that these traces
can be made following the death of the putative host they will not be
considered further here.
In order to maximize the likelihood of studying liveelive interactions in
the fossil record, it is imperative to investigate interactions where the actions
of the parasite induced a growth reaction by the host. Such traces are also
made by the aforementioned, potentially kleptoparasitic and shell weak-
ening, spionid polychaetes in the form of mudblisters. Mudblisters form
when the spionid begins boring at the growing margin of the bivalve, result-
ing in a raised blister within the valve, which is filled with mud and worm
faeces (Blake and Evans, 1973; Huntley, 2007; Huntley and Scarponi, 2015).
Similar blister and tube-like traces of unknown origin have been docu-
mented in the fossil record (Boucot, 1990; Boucot and Poinar, 2010).
Ozanne and Harries (2002) document the occurrence of ‘bubbly nacre’
and ‘Hohlkehle’ (a rib-like malformation on the valve interior) in Cretaceous
inoceramids of the Western Interior Seaway. Though the taxonomic iden-
tities of the culprits are uncertain, Ozanne and Harries (2002) suggested that
the traces were the result of pathogens or parasites between the mantle and
shell wall and parasitic polychaetes, respectively. Savazzi (1995) reported
shell malformation of diverse morphologies, including cavities, pits, ridges
and crests, near the ligament in Pliocene Isognomon (Hippochaeta) maxillatus
from Northwestern Italy. Savazzi (1995) hypothesized that these traces
were the result of bivalve growth (rather than bioerosion) responding to
what was likely a polychaete endoparasite. In both examples, we are left
hypothesizing the taxonomic nature of the putative parasite.
There is a parasiteehost interaction that has been comparatively well-
studied in modern ecosystems, which results in the induction of characteristic
host shell malformations, and is, therefore, amenable to study in deep time via
the fossil record of bivalve hosts. Digenean trematodes (Platyhelminthes) are
endoparasitic flatworms with complex life cycles that can include free-
swimming stages, one or more intermediate stages within an invertebrate
host (bivalves, gastropods, arthropods, annelids), occasionally and subsequently
a vertebrate intermediate and/or a final stage within a vertebrate definitive
host (Cribb et al., 2001, 2003; Littlewood, 2006). Trematodes can cause all
Trace Fossil Evidence of TrematodeeBivalve ParasiteeHost Interactions in Deep Time 205

manner of trouble in their bivalve hosts including castration, stunted growth,


gigantism, immobilization and induced risky behaviour (Swennen, 1969; Lim
and Green, 1991; Ballabeni, 1995; Taskinen, 1998; Hechinger et al., 2009).
The soft-bodied trematodes themselves have very low body fossilization
potential (Poinar, 2003; Littlewood and Donovan, 2003; De Baets et al.,
2015b); however, gymnophallid trematodes are known to induce the growth
of an array of shell malformations on the interior of the bivalve, when it is
serving as a second intermediate host, within the pallial line (the best known
being oval pits with raised rims), which have a greater, more continuous
fossilization potential.
Ruiz and colleagues (Ruiz and Lindberg, 1989; Ruiz, 1991) docu-
mented a 5-million-year history of parasitism amongst bivalves of North
America and identified the oldest known occurrences of gymnophallid
trematode-induced pits in three genera from the Eocene (Lutetian) strata
of the Paris Basin (a record that was recently extended to an even earlier
Age of the Eocene (Ypresian) by Todd and Harper (2011) from the London
Clay of southern England). For nearly two decades this initial study stood
alone in its attempt to document trematodeebivalve interactions in deep
time. Recently, the fossil record of trematode-induced malformations has
garnered more attention due to the increasing recognition of its potential
for revealing the ecological and evolutionary implications of parasiteehost
interactions in deep time and amongst modern death assemblages (Ituarte
et al., 2001, 2005; Huntley, 2007; Todd and Harper, 2011; Huntley and
Scarponi, 2012, 2015; De Baets et al., 2015b). Indeed, high temporal reso-
lution records of Holocene trematode malformations provide unique in-
sights into the influence of climate change on parasitic interactions
through geologic time and enable us to make predictions for how such in-
teractions will potentially respond to anthropogenic climate change in the
future (Huntley et al., 2014). Ruiz and Lindberg (1989) hypothesized that
the gymnophallid-bivalve parasiteehost interaction originated in Europe
during the Eocene, expanded to the North American Atlantic coast by
the Miocene, and again to the North American Pacific coast by the Plio-
cene. These results are, of course, highly preliminary and warrant further
study to determine the timing of the origin and dispersal of this interaction.
The purpose of this paper is to review our current state of knowledge of
the fossil record of trematodeebivalve interactions and to outline prospects
for future inquiry. This includes discussions of the morphologies of gymno-
phallid trematode-induced malformations in bivalves, examples of living par-
asites in close proximity to malformations in the shells of their hosts, the
206 John Warren Huntley and Kenneth De Baets

temporal distribution of reliable trematode traces within the phylogenetic


context of their bivalve intermediate hosts, the life and feeding modes of
infested bivalve taxa through geologic time, problems of taphonomy and
how they influence our understanding of the origin and history of trema-
todeebivalve interactions, the utility of trematode traces as palaeoenviron-
mental indicators and the negative effects of trematodes on bivalves and
their likely evolutionary implications. Despite all that we have learnt about
this interaction in deep time, many more questions about the origin and
history of this interaction present themselves. Indeed, there is room for addi-
tional palaeontologists and neontologists to address these important (palaeo-)
ecological questions.

2. TREMATODE-INDUCED SHELL MALFORMATIONS IN


LIVING BIVALVE MOLLUSCS
Live digenean (mostly gymnophallid) trematodes have been found
living in close spatial proximity to shell malformations on the interior of
their bivalve hosts. These malformations have taken a variety of forms,
and these forms span a range of utility for being characteristic traces of trem-
atodes (Figure 1). Ranging from the most to the least reliable, indicators of
trematode parasitism are pits, igloos, blister pearls, free pearls, irregular
calcareous deposits (ICD) and valve discolouration (Table 1).
The best known characteristic shell malformations induced by trematode
parasites are oval-shaped pits with raised rims (Figure 1(a) and (b)). Ruiz and
Lindberg (1989) suggested that these pits are not features of shell erosion,
rather, the pits are the result of shell growth intended to encapsulate the
parasite. This interpretation is evidenced by growth lines wrapping around
the pit structure when viewed in thin section rather than the pit cutting
across growth lines (as would be expected with shell erosion). Most trema-
tode taxa found living in association with pits are members of the Gymno-
phallidae and were parasitizing taxa from the bivalve families Veneridae,
Semelidae, Cardiidae and Psammobiidae (Table 1; Johannessen, 1973;
Campbell, 1985; Ruiz and Lindberg, 1989; Ituarte et al., 2001, 2008).
Though gymnophallids are typically considered to be the digeneans respon-
sible for inducing pit growth in their hosts, an unknown species from the
digenean family Lepocreadiidae has been found living in association with
a pit on the interior of a cyamiid bivalve, Gaimardia trapesina from southern
Argentina (Table 1; Ituarte et al., 2001). Pits are the traces most frequently
cited as fossil indicators of trematode parasitism (Ruiz and Lindberg, 1989;
Trace Fossil Evidence of TrematodeeBivalve ParasiteeHost Interactions in Deep Time 207

Figure 1 Images of trematode-induced shell malformations. Photomicrographs of


trematode-induced pits in (a) Holocene Potamocorbula amurensis from the Pearl River
Delta, China (Core PRD-10, sample 157) and (b) Holocene Chamalea gallina from the Po
Plain, Italy (Core 240S8, 13.10 m). (c) Flatbed scanner image of blister pearls in Eocene
(Lutetian) Sunetta semisulcata from the Paris Basin (Grignon, Faluni ere), France
(Gg2003/517, Museum National d’Histoire Naturelle). (d) Scanning electron micrograph
of igloo-shaped malformation in Recent Neolepton bennetti from the Falkland Islands
(Adapted from Ituarte et al. (2005).). (e) Photomicrograph of discolouration that may
be related to trematode infestation in Holocene Cyrenodonax formosana from the Pearl
River Delta, China (Core PRD-10, sample 120). (f) Photomicrograph of irregular calcar-
eous deposits that may be related to trematode infestation in Holocene C. formosana
from the Pearl River Delta, China (Core PRD-10, sample 124).

Ruiz, 1991; Huntley, 2007; Todd and Harper, 2011; Huntley and Scarponi,
2012, 2015; Huntley et al., 2014; De Baets et al., 2015b), and there is no
other biotic interaction (known so far) that induces the growth of an
oval-shaped pit with a raised rim.
Ituarte and colleagues (Ituarte et al., 2001, 2005; Presta et al., 2014) have
described unusual igloo-shaped morphologies of trematode-induced traces
from high-latitude shallow marine deposits in Argentina (Figure 1(d)).
Ituarte et al. (2001) interpret the igloo structures to represent a response
of the host meant to isolate the parasite. In this case, however, the parasite
is able to maintain an opening between the interior of the would-be blister
pearl (see below) and the space between the mantle and shell, thus
Table 1 Instances of living trematodes identified in contact with shell malformations in living bivalve hosts

208
Trematode parasite Bivalve host
Feeding
Family Species Trace type Family Genus species Life mode mode Reference
Gymnophallidae Gymnophallus sp. Pits, discolouration Veneridae Venerupis pullastra Infaunal Suspension Johannessen (1973)
Parvatrema rebecqui Pits Semelidae Abra tenuis Deposit Campbell (1985)
P. rebecqui Cardiidae Cerastoderma glaucum Suspension
Gymnophallus somateriae Pearls Mytilidae Mytilus sp. Epifaunal Jameson (1903)
e ‘Unknown distome’ Pearls Mytilidae Mytilus edulis Epifaunal Suspension Stunkard and Uzmann
Brachycoelium luteum ICD Donacidae Donax trunculus Infaunal (1958)
B. luteum Tellinidae Tellina fabula Deposit
Tellina tenuis
Tellina solidula
Distomum margaritarum Pearls Mytilidae M. edulis Epifaunal Suspension
D. margaritarum Mytilus galloprovincialis
‘Unknown trematode’ Margaritiferidae Margaritifera margaritifera
Proctoeces milfordensis Mytilidae M. edulis

John Warren Huntley and Kenneth De Baets


Gymnophallidae Bartolius pierrei ICD Mactridae Darina solenoides Infaunal Suspension Cremonte and Ituarte
(2003)
Unknown species Pits, pearls, discolouration Psammobiidae Tagelus plebius Ituarte et al. (2008)
ICD, discolouration Lomovasky et al. (2005)
ICD, discolouration, pearls Vazquez et al. (2006)
Bartolius sp. Igloo Neoleptonidae Neolepton cobbi e e Presta et al. (2014)
Unknown species Cyamiidae Gaimardia trapesina Epifaunal Suspension Ituarte et al. (2001)
Lepocreadiidae Unknown species Pits Cyamiidae G. trapesina Epifaunal Suspension Ituarte et al. (2001)
Gymnophallidae Parvatrema borealis Pits Veneridae Gemma gemma e e Ruiz and Lindberg
Transennella confusa Infaunal Suspension (1989)
Transennella tantilla

ICD ¼ irregular calcareous deposits.


Blank cells indicate the same content as the above cell and the dashed lines indicate that the value is unknown.
Trace Fossil Evidence of TrematodeeBivalve ParasiteeHost Interactions in Deep Time 209

producing an igloo-morphology. Bartolius sp. and two other gymnophallid


species whose genus- and species-level taxonomy were not resolved have
been identified living in igloo-shaped traces on the interior of cyamiid
and neoleptonid bivalves (Ituarte et al., 2001; Presta et al., 2014). Ituarte
et al. (2005) extended identified igloo-shaped traces into the subfossil record
in Holocene cyamiid, neoleptonid, and nuculanid Holocene bivalves from
Falkland Islands and Tierra del Fuego. Interestingly, Liljedahl (1985, 1994)
noted similar traces on the interior of praenuculid bivalves from Silurian
strata in Sweden, although these are not consistent with known extant
host-relationships between shore birds and gymnophallid trematodes
(compare De Baets et al., 2015b). Fossils give a minimum constraint to
the origin of modern shore birds or charadriiform-like forms to the Eocene
(Mayr, 2014), although various molecular clocks place the origin of Chara-
driiformes into the Cretaceous, although no unequivocal fossils have been
found from this interval (Smith, 2015).
Blister pearls are small, discrete, round to elongate, convex features on
the interior surface of bivalves which are sometimes associated with trem-
atode parasites (Figure 1(c)). When co-occurring with pits, blister pearls are
commonly of comparable size to the oval-shaped pits. The earliest known
blister pearls date from the late Silurian to early Devonian (Kríz, 1979;
Liljedahl, 1985, 1994; De Baets et al., 2011) and are often thought to repre-
sent overgrowths of dead parasites as in recent bivalves (Lauckner, 1983).
Campbell (1985) described shell malformations in the bivalve Abra tenuis
reacting against the trematode Gymnophallus rebecqui (termed ‘blisters’ by
the author) that are intermediate in morphology between oval pits and blis-
ter pearls. In no instance was the parasite completely isolated by the shell
malformation, but this morphology serves as further support for the
inducing of pearl growth by trematodes. Gymnophallid trematodes have
been found in association with pearl-bearing bivalve individuals from the
Mytilidae, Margaritiferidae and the Psammobiidae families in Europe,
North America and South America (Jameson, 1903; Stunkard and
Uzmann, 1958; Vazquez et al., 2006; Ituarte et al., 2008). Free pearls are
similar to blister pearls in that they are the result of a bivalve’s defensive
overgrowth of foreign bodies, however, they are not attached to the shell
wall. Free pearls date as far back as the Triassic (Kutassy, 1937; Conway
Morris, 1981; Littlewood and Donovan, 2003). Although various parasitic
flatworms have been associated with pearl formation (both blister and free),
it is important to note that other pathogens and inorganic particles can also
210 John Warren Huntley and Kenneth De Baets

result in pearl formation (Newton, 1908; G€ otting, 1974, 1979; Lauckner,


1983). Therefore one should use caution when attempting to positively
identify trematode parasitism via pearls.
ICD are low-relief malformations occurring in the interior of the shell.
ICDs are similar in morphology to spionid mudblisters except that there is
no void space in the valve underlying them. ICDs have been identified in
association with Brachycoelium luteum in donacid and tellinid bivalves from
France (Stunkard and Uzmann, 1958), and digenean trematodes (Bartolius
pierrei and two unidentified species) in mactrid and psammobiid bivalves
from Argentina (Cremonte and Ituarte, 2003; Lomovasky et al., 2005;
Vazquez et al., 2006; Table 1). Additionally, valve discolouration has
been identified in association with digenean trematodes in venerid and
psammobiid bivalves in Norway and South America (Johannessen, 1973;
Cremonte and Ituarte, 2003; Lomovasky et al., 2005; Vazquez et al.,
2006; Table 1). Features similar to ICDs and shell discolouration have
been identified in Cyrenodonax formosana from core-sampled Holocene de-
posits of the Pearl River Delta, China (Huntley et al., 2014). No association
with trematodes could be confirmed, of course, as these are subfossil
deposits. The probability of preserving discolouration likely decreases
dramatically with geologic age.
Blisters, ICD, and shell discolouration are the poorest diagnostic traces
of trematode parasites. Pits and igloos are highly diagnostic, in that they are
morphologically complex and no other known organisms induce the
growth of such structures today. Blister pearls and ICDs, by comparison,
are of a more simple morphology and could potentially be induced by
a diverse group of irritants (G€ otting, 1974, 1979; Lauckner, 1983).
Caceres-Martínez and Vasquez-Yeomans (1999) documented the presence
of pearls in Mytilus galloprovincialis and Mytilus californianus with copepods
and platyhelminths that also lacked trematodes (though other individuals
in the samples possessed various combinations of the three types of parasites
and pearls). Shell discolouration and ICDs can be linked to a number of
parasites including chromalvelolates (Haplosporidium nelsoni) and fungi
(Ostracoblabe implexa; Elston, 1990). One should only use blisters, ICDs
or shell discolouration as a direct evidence for trematode infestation in
the instance that the interaction is well documented amongst living repre-
sentatives or, at worst, with closely related taxa. Pits and igloos are the most
reliable proxies for gymnophallid trematode infestation in the fossil and
subfossil record.
Trace Fossil Evidence of TrematodeeBivalve ParasiteeHost Interactions in Deep Time 211

3. OCCURRENCES OF TREMATODE-INDUCED PITS IN


FOSSIL AND SUBFOSSIL BIVALVES
3.1 Taxonomic, temporal and ecological occurrences
It is instructive to explore the distribution of gymnophallid trematode
infestation across the phylogeny of their bivalve intermediate hosts in deep
time. Such a distribution can aid in the development of hypotheses regarding
the origin of this interaction and the potential nonbiological (taphonomic)
biases upon this record. In the interest of taking the most conservative
approach, only pits, igloos and igloo-like structures from fossil and subfossil
(Holocene samples from sub-surface deposits and surficial death assemblages)
records will be considered in this analysis. Data are compiled from occurrence
data from the North Sea coast of the Netherlands (Huntley, unpublished
data), museum survey of Eocene (Lutetian) bivalves in the collections of
the Museum National d’Histoire Naturelle (MNdHN; Paris; Huntley, un-
published data), and from the peer-reviewed literature. Bulk samples of death
assemblages from the swash zone were collected by the senior author at 10
locations in the Netherlands (Callantsoog, Egmond Aan Zee, Katwijk Aan
Zee, Hoek van Holland, Zandvoort, IJmuiden, Harlingen, Makkum,
Workum and Wierum) consisting of 7423 valves from 16 taxa. The senior
author conducted a cursory survey of the extensive Eocene (Lutetian) bi-
valves from the Paris Basin in the collections of the MNdHN on lots with
multiple specimens (1505 valves from 147 species occurrences) from
Grignon, Faluniere. The occurrence of trematode-induced traces was
plotted on the evolutionary time tree of the Bivalvia modified from Bieler
et al. (2014) (Figure 2, Table 2).
Trematode-induced traces have been identified in four of the six major
bivalve lineages (Bieler et al., 2014): Protobranchia, Pteriomorphia, Archihe-
terodonta and Imparidentia, including 46 genera from 19 families (Figure 2,
Table 2). This record is most complete in Eocene and younger sediments and
is characterized by significant temporal gaps. The two lineages in which trem-
atode traces have not yet been identified are Palaeoheterodonta and Anom-
alodesmata, but this might represent a sampling artefact given the dearth of
attention this interaction has historically received from palaeontologists.
The largest temporal gap in evidence for trematode infestation currently
exists in the Protobranchia lineage of bivalves. Liljedahl (1985) reported an
igloo-like trace in the praenuculid Nuculodonta gotlandica from the Silurian
of Sweden (compare Liljedahl, 1994). This trace is remarkably similar to
212 John Warren Huntley and Kenneth De Baets

Figure 2 Distribution of trematode-induced pits (P), trematode-induced igloos (I) and


igloo-like (IL) traces on bivalves found in fossil and subfossil death assemblages map-
ped onto the evolutionary time tree of Bivalvia (Adapted from Bieler et al. (2014).). Note
that geologic time is not to scale; the Cenozoic is exaggerated to show more details.
The Holocene time bin includes both sub-surface Holocene deposits and modern/Ho-
locene death assemblages. *The family Arcidae is not monophyletic in the analysis of
Bieler et al. (2014), but all members of this family are included within Pteriomorphia.
Temporal units from the oldest to the youngest are Cambrian, Ordovician, Silurian,
Devonian, Carboniferous, Permian, Triassic, Jurassic, Cretaceous, Paleogene (Paleocene,
Eocene, Oligocene), Neogene (Miocene, Pliocene), Quaternary (Pleistocene, Holocene).

the igloo structures described by Ituarte et al. (2005) in the nuculanid Yoldia
woodwardi from modern death assemblages in Argentina (Ituarte et al., 2005).
If Liljedahl’s igloo-like structures are indeed the result of trematode infesta-
tion, then these would be, by far, the oldest fossil evidence for trematodes and
parasitic flatworms in the fossil record (De Baets et al., 2015b). Currently,
more comparative work is required to determine the relatedness of the Silu-
rian igloo-like traces and trematode parasites. It cannot therefore be ruled
out, that they are related with other organisms with similar behaviour (De
Baets et al., 2015b). Significant temporal gaps in the trematode record also
Table 2 Occurrences of trematode-induced traces on fossil and subfossil bivalve death assemblages
Bivalve host

Trace Fossil Evidence of TrematodeeBivalve ParasiteeHost Interactions in Deep Time


Trace type Family Species Life mode Feeding mode Environment Country Age Reference
Pits Cardiidae Cerastoderma edule Infaunal Suspension Marine Netherlands Modern Huntley NL survey
Brackish
Cerastoderma glaucum Marine
Brackish
Donacidae Donax vittatus Marine
Mactridae Spisula sp.
Mactra stultorum
Myidae Mya arenaria Brackish
Pharidae Ensis sp. Marine
Tellinidae Macoma balthica Deposit/suspension Marine
M. balthica Brackish
Angulus tenuis Suspension Marine
Cardiidae C. glaucum Italy Huntley and Scarponi
Donacidae Donax semistriatus (2015)
Lucinidae Loripes lucinalis Chemosymbiotic
Mactridae Spisula subtruncata Suspension
Mytilidae Mytilus galloprovincialis Epifaunal
Veneridae Chamalea gallina Infaunal
Igloo Neoleptonidae Neolepton bennetti e e Marine Argentina Modern Ituarte et al. (2005)
Neolepton concentricum
Nuculanidae Yoldia woodwardi
Pits Corbulidae Potamocorbula amurensis Semi-infaunal Suspension Brackish China Holocene Huntley et al. (2014)
Donacidae D. semistriatus Infaunal Suspension Marine Italy Huntley and Scarponi
(2012)
Donax sp. USA Ruiz and Lindberg
Mactridae Mulinia sp. (1989)
Tresus sp.
Myidae Mya sp.

213
(Continued)
Table 2 Occurrences of trematode-induced traces on fossil and subfossil bivalve death assemblagesdcont'd

214
Bivalve host
Trace type Family Species Life mode Feeding mode Environment Country Age Reference
Semelidae Abra sp. Deposit/suspension England
Tellinidae Macoma sp. Canada
Sweden
Veneridae Ch. gallina Suspension Italy Huntley and Scarponi
(2012)
Gemma sp. USA Ruiz and Lindberg (1989)
Canada
Gouldia sp. USA
Psephidia sp.
Transennella sp.
Venerupis sp. Sweden
Igloo Cyamiidae Cyamiomactra sp. e e Marine Argentina Holocene Ituarte et al. (2005)
Pits Mactridae Mactra sp. Infaunal Suspension Marine Sweden Pleistocene Ruiz and Lindberg

John Warren Huntley and Kenneth De Baets


Mulinia sp. USA (1989)
Rangia sp. Brackish
Psammobiidae Sanguinolaria sp. e Marine Yemen
Tellinidae Tellina sp. Deposit USA
Veneridae Anomalocardia sp. Suspension
Gemma sp.
Parastarte sp.
Protothaca sp.
Tivela sp.
Transennella sp.
Venus sp.
Donacidae Donax sp. Sweden Pliocene
Tellinidae Tellina sp. Deposit USA
Veneridae Cyclinella sp. Suspension
Gemma sp.
Parastarte sp.

Trace Fossil Evidence of TrematodeeBivalve ParasiteeHost Interactions in Deep Time


Transennella sp.
Venericardia sp.
Tellinidae Arcopagia sp. Deposit/suspension France Miocene
Macoma sp. USA
Veneridae Chione sp. Suspension
Gemma sp.
Arcidae Arca (Barbatia) filigrana Epifaunal France Eocene Huntley MNdHN
Carditidae Cardita (Venericardia) planicosta Infaunal survey
Venericor clarendonensis England Todd and Harper (2011)
Glycymeridae Pectunculus (Glycymeris) pulvinatus France Huntley MNdHN survey
Lucinidae Corbis lamellosa Chemosymbiotic
Lucina caillati
Phacoides (Pseudomiltha) caillati
Phacoides (Pseudomiltha) giganteus
Phacoides concentricus
Mactridae Mactra semisulcata Suspension
Tellinidae Tellina patellaris Deposit
Tellina sp. Ruiz and Lindberg
(1989)
Veneridae Sunetta semisulcata Suspension Huntley MNdHN survey
Venus sp. Ruiz and Lindberg (1989)
Blisters Carditidae C. (Venericardia) planicosta Infaunal Suspension Marine France Eocene Huntley MNdHN survey
Tellinidae Tellina sinuata Deposit
Veneridae Cytheraea (Callista) laevigata Suspension
Meretrix (Callista) laevigata
Igloo-like Praenuculidae Nuculodonta gotlandica Infaunal Deposit Marine Sweden Silurian Liljedahl (1994)

Blank cells indicate the same content as the above cell and the dashed lines indicate that the value is unknown.

215
216 John Warren Huntley and Kenneth De Baets

occur in the oldest of bivalve lineages, Pteriomorphia. Trematode-induced


pits have been identified amongst three pteriomorphan families Arcidae
(Eocene), Glycymeridae (Eocene), and Mytilidae (Holocene). Fifty million
years separate these occurrences, and the seeming lack of trematode traces
from the Cambrian to Paleogene Periods might therefore also be partially
the result of insufficient sampling to date.
The oldest noncontroversial evidence for trematode infestation of bi-
valves is found in the Archiheterodonta lineage. Todd and Harper (2011)
presented clear evidence of trematode-induced pits in the carditid Venericor
clarendonensis from the Eocene (Ypresian) London Clay in the UK (compare
De Baets et al., 2015b). This is the only known instance of trematode infes-
tation amongst the archiheterodontids.
The majority of the instances of trematode traces have been identified
amongst 13 families in the Imparidentia. Pits have been identified amongst
12 of these families and igloos have been documented in the Cyamiidae and
Neoleptonidae families. The earliest occurrences of trematode traces in the
Imparidentia are pits in lucinid, mactrid, tellinid and venerid bivalves from
the Eocene-aged deposits (Lutetian) of the Paris Basin (Table 2). Amongst
these families, the Tellinidae and Veneridae display the most temporally
complete fossil record of trematode traces. Despite the large number of fam-
ilies displaying trematode-induced traces in the Imparidentia, the majority of
parasite occurrences are from the Pleistocene and Holocene.
The ecological distribution (i.e. life mode and feeding mode of hosts) of
trematode-induced malformations in bivalve intermediate hosts is roughly
comparable amongst living assemblages and death/fossil assemblages. As sug-
gested by Tables 1 and 2, appreciably more data are available from death and
fossil assemblages than from living assemblages. Trematode traces are most
commonly found amongst infaunal bivalve hosts, though this pattern is
more strongly expressed in death/fossil assemblages than in living ones
(Figure 3). Semi-infaunal and epifaunal taxa are less well-represented as
trematode trace-bearing hosts. Suspension feeding is the dominant feeding
mode of trace-bearing bivalve hosts (both live and dead/fossil) followed
by deposit-feeding and chemosymbiotic taxa (the latter only occurring in
the dead/fossil assemblages). These results, along with much of the other
data reported here, should be interpreted with the understanding that
much investigation remains to be done. To date, only a few research groups
have published one or more papers primarily on trematode malformations in
modern and fossil bivalves and a few more groups mention the interaction in
passing as a secondary topic.
Trace Fossil Evidence of TrematodeeBivalve ParasiteeHost Interactions in Deep Time 217

Figure 3 Life modes (a) and feeding modes (b) of bivalve hosts of trematodes (live in-
teractions and from traces in fossil and subfossil hosts).

3.2 Taphonomy and the origin of the trematodeebivalve


parasiteehost interaction
Patzkowsky and Holland (2012) argued that the primary problem in palae-
ontology is determining to what extent the fossil record can be literally inter-
preted as the history of life. Taphonomy is the study of all the processes
influencing the production of the fossil record, from the death of an organ-
ism until it is collected by a palaeontologist. Indeed, numerous taphonomic
filters introduce bias as organisms pass from the biosphere into the geosphere,
strongly influencing the record of biodiversity through deep time (Sepkoski
et al., 1981; Miller, 2000; Peters, 2005; Alroy et al., 2008; amongst many
218 John Warren Huntley and Kenneth De Baets

others); and this is no less true for the fossil record of trematodes. Trematodes
are amongst the least likely organisms to be preserved as fossils; indeed, they
have little to no body fossil record (Ruiz and Lindberg, 1989; Littlewood and
Donovan, 2003; Boucot and Poinar, 2010; De Baets et al., 2015b). Trema-
todes are small-bodied metazoans (typically submillimetre in length) that
produce neither biominerals nor recalcitrant organic material for skeletons.
The only means we have to study their occurrence in deep time are their
trace fossils (e.g. Littlewood and Donovan, 2003; Littlewood, 2006), the
characteristic pits and igloos whose growth they induce in their bivalve hosts.
Fortunately, the biomineralized skeletons of bivalves are much more robust
to the taphonomic vagaries of the fossil record than trematodes, and their
body fossil record extends to the Cambrian. Moreover, the morphology
of bivalves and the stratigraphic context of the sediments in which they
are preserved yield much information about the environment of deposition
and how the bivalves functioned in their environment (Stanley, 1970).
Despite the robust nature of the fossil record of bivalves (compared with
other taxa), it is still subject to significant taphonomic biases.
Bivalve skeletons are a composite material comprised of calcium carbon-
ate crystals (calcite and/or aragonite) and an organic matrix (Rhoads and
Lutz, 1980 and the chapters therein). The calcite polymorph is more stable
under temperature and pressure conditions at Earth’s surface than aragonite.
Indeed, aragonite often recrystallizes to calcite or preferentially dissolves dur-
ing the processes of sediment lithification and diagenesis. Anatomical detail is
typically lost during recrystallization as the primary aragonitic microstructure
recrystallizes into much larger crystals of blocky calcite. Specimens whose
aragonite dissolves can sometimes be preserved as steinkerns, or complete in-
ternal moulds formed by lithified infilling sediment. The preferential loss or
lowered resolution of aragonitic taxa has been cited as a significant factor
biasing our understanding of Phanerozoic diversity trends (Bush and
Bambach, 2004), and this factor could likely play a role in diminishing the
fossil record of trematode traces. Trematode traces are likely to be obliter-
ated by the coarse process of recrystallization, and internal moulds are not
as likely to display pits as the original shell material. Trematode pits have
been found preserved in positive relief on a Holocene steinkern (Huntley
et al., 2014) and blister pearls can potentially also be traced further back in
time (cf. De Baets et al., 2011); however, in many cases steinkerns are
comprised of sediment whose grain size is similar to or larger than the
millimetre-scale trematode pits, thereby reducing the likelihood of pre-
servation of parasite-induced malformations. Therefore, aragonitic or mixed
Trace Fossil Evidence of TrematodeeBivalve ParasiteeHost Interactions in Deep Time 219

aragonite/calcite taxa likely have a lower preservation potential in deep


time, thereby reducing the preservation potential of the parasitic traces
they harboured in life.
The nature of the sediment in which bivalve taxa are preserved can poten-
tially bias our ability to properly interpret the fossil record as well (Hendy,
2009). Geologically younger sedimentary layers are often unlithified which
allows for the easy extraction of whole bivalve valves. In rocks older than the
Cretaceous, it is rare to find unlithified sediments. Unless one uses time-
intensive physical and, in some cases chemical (e.g. dissolution of carbonate
rock with acid to extract silicified bivalves), extraction techniques, then ob-
servations are restricted to specimens exposed on the surface of rock slabs.
Since trematode-induced malformations are restricted to the interior of
the valve, one could only collect data from specimens with exposed interiors
that are free from encrusting epibionts and lithified sediments.
The temporally disparate distribution of both aragonite preservation and
lithified sediment are likely to be contributing explanations for our current
understanding of the temporal distribution of trematode traces. The earliest
reliable indicator of trematode infestation of bivalves is in the Ypresian stage
of the Eocene (V. clarendonensis; Todd and Harper, 2011; De Baets et al.,
2015b), but it is not unreasonable to hypothesize that the interaction between
these two groups originated much earlier in time. Bivalve molluscs first
appear in the early Cambrian (Jell, 1980) and putative parasitic flatworm re-
mains are known from the late Paleozoic (Zangerl and Case, 1976; Upeniece,
1999, 2001, 2011; Dentzien-Dias et al., 2013; De Baets et al., 2015b).
Furthermore, molecular clocks place the origin of bivalves as early as the Pre-
cambrian and current parasiteehost extrapolations place the origin of parasitic
flatworms (Neodermata) in the CambrianeOrdovician (Littlewood, 2006;
De Baets et al., 2015b). The roots in deep time for both host and parasite
coupled with the diverse array of host taxa already parasitized in the Eocene
seem to suggest an earlier origin for the interaction. Perhaps the search for the
origination of trematodeebivalve parasiteehost interaction should proceed
from the perspective of the definitive host rather than the intermediate
host. Indeed, phylogenetic analyses suggest that the adoption of bivalves, gas-
tropods and polychaetes as either first or second intermediate hosts is a derived
state that has evolved multiple times. The ancestral digenean life cycle has
fewer stages and is strongly linked with marine teleost fishes as vertebrate
definitive hosts (Cribb et al., 2003). In nearly all documented cases of trem-
atodes found in association with traces in living bivalves, the traces were
induced by the Gymnophallidae (Table 1), and marine shore birds are the
220 John Warren Huntley and Kenneth De Baets

definitive hosts for gymnophallid trematodes (Ching, 1995; Galaktionov,


2006). This association would suggest that the origin of the modern
trematodeebivalve interactions might be linked to the origin and radiation
of marine shore birds somewhere between the Cretaceous and the middle
Eocene (Ruiz and Lindberg, 1989; Mayr, 2014; Smith, 2015), though this
does not preclude the possibility that trematodes infested closely related
and/or ecologically similar predecessors of modern shore birds (compare
De Baets et al., 2015b for a review).

3.3 Trematode-induced malformations as


palaeoenvironmental indicators
Ruiz and Lindberg (1989) suggested that traces of trematodeebivalve inter-
action should serve as precise palaeoenvironmental indicators of intertidal en-
vironments. Given that marine shore birds are the typical definitive host of
gymnophallid trematodes, the infested bivalve second intermediate hosts
should occur in depths shallow enough for the birds to prey upon the bi-
valves. The depth distribution of trematode malformations has not, to our
knowledge, been addressed amongst living molluscan communities, but has
received more attention in the fossil record. Huntley and Scarponi (2012)
were able to approach the question of trematode depth distribution quantita-
tively using PleistoceneeHolocene molluscan assemblages from the Po Plain
of Northern Italy. Scarponi and Kowalewski (2004) provided the environ-
mental context for these 89 samples from three cores comprised of 98 genera
and over 23,000 molluscan specimens by conducting a detrended correspon-
dence analysis (DCA), identifying a primary environmental gradient related to
depth, and calibrating this gradient using the modern depth preferences of 24
of the most common extant genera in the samples. DCA was particularly use-
ful in this case because it provides ordination scores for taxa and samples. Since
the ordination scores for taxa were strongly correlated with preferred depth, a
regression analysis allowed for the calculation of depth values for the samples.
This, in turn, allowed for a refined and independent interpretation of the sea-
level curve from these samples to complement the one derived from sedimen-
tary and stratigraphic analysis. Huntley and Scarponi (2012) examined the
same samples for trematode-induced malformations and were able to quantify
the distribution of parasitism along the depth gradient (Figure 4). Water depth
for the examined samples ranged from 0 to 14 m depth. Trematode-infested
species occurrences were restricted to between 7 and 9 m depth, contrary to
the prediction of Ruiz and Lindberg (1989) that pits would be a reliable in-
dicator of intertidal environments.
Trace Fossil Evidence of TrematodeeBivalve ParasiteeHost Interactions in Deep Time 221

Figure 4 Frequency of Holocene bivalve species occurrences along a water depth


gradient from the Po Plain of Italy. Grey columns are noninfested species occurrences
and black columns are trematode-infested species occurrences. Adapted from Huntley
and Scarponi (2012).

One of the more intriguing results from Huntley and Scarponi’s (2012)
study was that trematode prevalence was significantly higher in lower shore-
face environments during times of sea-level rise (transgression) than in com-
parable environments during sea-level fall (regression). Huntley and
Scarponi (2012) suggested that differences in sedimentation rate and salinity
stability in the lower shoreface during sea-level rise and fall could have influ-
enced trematode prevalence, but, of course, it is very difficult to disentangle
the numerous abiotic and biotic variables that change with sea-level cycles.
In a follow-up study, Huntley and Scarponi (2015) examined modern death
assemblages from 11 locations in 2 sectors separated by the Po River Delta
along the Northern Adriatic coast of Italy. North of the Po River Delta,
conditions are very much like that during Holocene transgression with bar-
rier island/lagoon/estuary complexes. Conversely, the prograding Po River
Delta and adjacent strand plains to the south are quite similar to the environ-
mental conditions during relative regression in the Holocene. The counter-
clockwise flow of surface currents in the Northern Adriatic Sea diverts the
influence of the Po Delta to the south. This influence wanes with distance
to the south and is virtually absent to the north of the delta. As predicted,
trematode prevalence values amongst modern death assemblages were
high at north of the delta, nearly absent in the vicinity of the delta and
returned to higher values much further south of the delta, beyond its
222 John Warren Huntley and Kenneth De Baets

influence (Huntley and Scarponi, 2015). Additionally, Huntley et al. (2014)


documented extensive evidence for trematode parasitism of the estuarine
bivalve Potamocorbula amurensis in the Pearl River estuarine/deltaic deposits
in China over the last 9600 years. Specifically, Huntley et al. (2014) demon-
strated that trematode prevalence was significantly higher during the first
300 years of sea-level rise than during any other phase of sea-level rise and
delta progradation (relative sea-level fall) during the Holocene in the Pearl
River Delta. They were able to rule out changing salinity and host availabil-
ity as driving factors of trematode prevalence, but were not yet able to
address other environmental factors like temperature and nutrient availabil-
ity (see Cheng and Combes, 1990 for a review on environmental factors
influencing the invasion of molluscs by parasites). In these three case studies,
ranging across environment (estuary vs marine), time (Pleistocene, Holo-
cene and Recent) and geography (northern Italy and southern China),
one finds hints of a previously unobserved modern macroecological pattern
that was predicted from palaeontological data. As sea level rises and falls on
the time scales of millennia, many biotic and abiotic factors change as well
(Patzkowsky and Holland, 2012). Responses of these environmental vari-
ables may be linear or nonlinear and their influence on the biota (e.g. the first
intermediate hosts and the definitive hosts) can seem to be unpredictable.
This especially seems to be the case when dealing with ecological time scales,
which are miniscule in comparison to geologic time, however, as illustrated
in these case studies, interpretable patterns can emerge. There is a difference,
of course, in documenting a predictable biotic response to sea-level change
and in understanding the underlying driving factors. Trematode-induced
malformations may not always indicate intertidal environments, but their
prevalence values do seem to be systematically elevated during times of
sea-level rise, a pattern which may have dire consequences for future gener-
ations in the context of anthropogenic climate change and sea-level rise
(Huntley et al., 2014). For this reason, it is important that we are able to un-
derstand the mechanics driving the increase in prevalence.

4. DETRIMENTAL EFFECTS OF TREMATODES ON


LIVING BIVALVES AND THEIR POTENTIAL
EVOLUTIONARY IMPLICATIONS
Trematodes are known to negatively affect their (mollusc) hosts in a
number of ways including castration, modified growth rates, immobilization
and, in some cases, altered behaviour making the host more susceptible to
Trace Fossil Evidence of TrematodeeBivalve ParasiteeHost Interactions in Deep Time 223

predation (Swennen, 1969; Lim and Green, 1991; Ballabeni, 1995;


Taskinen, 1998; Hechinger et al., 2009); and are, therefore, expected to
be significant agents of natural selection. These negative impacts on individ-
uals scale up to influence population dynamics. Lauckner’s work with larval
digeneans on North Sea tidal flats (1984, 1987) demonstrated how parasitic
castration of first intermediate gastropod hosts was nearly always fatal (not so
in second intermediate hosts), targeted larger post-spawning individuals and
resulted in a seasonal reduction in mean body size giving the appearance of
negative growth. Trematode infestation also contributed to host mortality
by making individuals more susceptible to environmental stressors
(Lauckner, 1984, 1987). Trematodes affect the growth rates of their
molluscan intermediate hosts in various ways (Sousa, 1983; Sorensen and
Minchella, 2001 and references therein). Most studies have addressed the
effects of trematodes on the growth rates of gastropods as first intermediate
hosts; the stage during which trematodes are parasitic castrators. Gigantism
(Sorensen and Minchella, 1998) and stunted growth (Lafferty, 1993a,b)
have both been documented in numerous gastropod taxa, particularly
short-living freshwater species. The exact mechanism causing these changes
in growth rate is not always clear, but gigantism is likely either (1) a
nonadaptive response to parasitism wherein energy is diverted into growth
that would otherwise be spent on reproduction, (2) an adaptation of the host
to outlive the parasite or (3) an adaptation of the parasite to increase the
fitness of the host thereby increasing its own fitness (Taskinen, 1998).
Much less attention has been given to the influence of trematode parasites
on bivalve host life history. Bivalves typically serve as the second intermedi-
ate host for trematodes (the stage during which trematodes induce pits) and
occasionally as the first intermediate host (the castrating stage), so perhaps we
should not expect the same effects on bivalves as experienced by gastropods.
In a field-based experiment with freshwater Anodonta piscinalis bivalves from
Finland, Taskinen (1998) reported a density-dependent negative correlation
between parasite prevalence and bivalve growth rates. Similarly, Thieltges
(2006) demonstrated stunted growth rates in parasitized North Sea Mytilus
edulis relative to their nonparasitized counterparts. Thieltges (2006) attrib-
uted these differences to tissue disruptions, hampered ability of the bivalve
to ingest food particles and the growth of metacercarial cysts within the host.
It is clear that trematodes influence the growth rates of their hosts in
modern settings, but do these physiological responses scale up to evolu-
tionary changes in life history within lineages or are they merely expressed
at the scale of the individual? One would predict from life history theory that
224 John Warren Huntley and Kenneth De Baets

bivalves that reach first reproduction sooner (either via an increase in growth
rate or reproducing earlier at a smaller body size) would have an advantage
when dealing with trematode parasites. Ruiz and Lindberg (1989) and Ruiz
(1991) noted a statistically significant decrease in body size of the bivalve host
Transenella through the Pleistocene of California. They recognized that
trematode prevalence was positively correlated with host body size (also
recognized by Huntley (2007) and Huntley and Scarponi (2012)) and may
select for earlier first reproduction amongst bivalve hosts. Ruiz and Lindberg
(1989) interpreted the trend of decreasing body size through time as the
result of decreasing length of time to first reproduction in the ontogeny
of Transenella. However, this interpretation was based upon sizeeage rela-
tionships that need to be confirmed as consistent through geologic time.
An internal chronology can be established by investigating the presence of
seasonal variation and annual cycles in d18O (the ratio of 18O to 16O in a
sample relative to the same ratio in a standard, reported in per mil; often
an inverse proxy for temperature) values of bivalve carbonate along the
axis of maximum growth. Such seasonal variation could serve as an ‘ontoge-
netic clock’ for an individual that would enable one to calculate bivalve
longevity and growth rates through ontogeny (Jones et al., 1986; Romanek
and Grossman, 1989; Kirby et al., 1998; Goodwin et al., 2001; amongst
others). When these temperature proxy data are plotted relative to distance
from the umbo (the portion of the shell formed in the earliest stages of
ontogeny) growth rates can be quantified. Moreover, a significant decrease
in growth rate often indicates the onset of sexual maturity of marine inver-
tebrates (Romanek and Grossman, 1989). As an example, Figure 5 shows
the d18O values of shell carbonate samples (n ¼ 27) collected along the
growth axis from the umbo to the posteroventral margin of a Chamalea
gallina valve from the Northern Adriatic coast of Italy. The cycles are inter-
preted as three annual cycles and the sharp troughs likely represent growth
cessation in the winter. This specimen was live-collected and sacrificed in
February 2010; therefore, it is possible to determine the calendar years
that correspond to these annual cycles. Moreover, if we can estimate the
d18O value of the sea water in which this clam grew, it is possible to estimate
the actual temperature of the sea water (Grossman and Ku, 1986). In addi-
tion to providing an internal chronology for this individual clam, these data
suggest reduced growth in year two and an overall trend of increasing tem-
perature during the three years. Following this methodology, growth rates
and age at onset of sexual maturity of parasitized and nonparasitized individ-
uals could theoretically be approximated in order to test the influence of
Trace Fossil Evidence of TrematodeeBivalve ParasiteeHost Interactions in Deep Time 225

Figure 5 Oxygen isotope (d18O V-PDB) profile for an individual specimen of Chamalea
gallina from the Northern Adriatic Sea (Primi Piatti sample). The cyclical nature of the
profile suggests 3 years of growth, and the sharp ‘bottoms’ of the winter portion sug-
gest a hiatus of growth during the coldest months.

trematode parasitism on the life history of hosts through geologic time and
should be a fruitful avenue for future research.

5. CONCLUDING REMARKS
There is an increasing interest in elucidating parasiteebivalve interac-
tions through deep time. Trematodes, though lacking a continuous body
fossil record, induce the growth of a number of characteristic malformations
on the interior shell walls of their bivalve hosts, which can be traced back
in the fossil record. Gymnophallid trematodes living in close association
with malformations on the interior of living bivalves have been well-docu-
mented. Trematode pits and igloos have been identified in four of the six
major lineages within the bivalve evolutionary tree spanning back as far as
the Eocene (when they appear rather suddenly, in terms of geologic time
that is, in seven families from three lineages). Igloo-like structures have
been found in Silurian Protobranchia, but further work is required to
confirm their trematode origin and to explain the subsequent 420-
million-year gap in the igloo fossil record (compare De Baets et al.,
2015b). Large gaps in the fossil record of such structures might potentially
226 John Warren Huntley and Kenneth De Baets

indicate that a different culprit (e.g. parasite) is involved in older occurrences


(cf. Boucot and Poinar, 2010, p. 28). The sudden appearance of trematode
traces in the Eocene probably does not reflect the origin of the interaction;
rather a combination of taphonomic biases and too few people looking for
these traces likely mask a much older origin. A pattern of significantly
increased prevalence values in transgressive settings (sea-level rise) seems
to be emerging from marine and estuarine settings spaced widely in space
and time; a relationship which suggests that trematode prevalence will in-
crease in estuarine settings in the coming decades and centuries in the
context of anthropogenic climate change and sea-level rise. Trematodes
are known to influence the growth rates of their intermediate hosts in
various ways, but the long-term evolutionary implications of this negative
effect can only be tested in the fossil record through the establishment of ‘in-
ternal chronologies’ within individuals from lineages through deep time.
Though the efforts of many palaeobiologists and neontologists have greatly
expanded our understanding of parasiteehost interactions amongst trema-
todes and bivalves, many questions remain unanswered and some have
not even yet been asked.

ACKNOWLEDGEMENTS
John Huntley is grateful to Kenneth De Baets and Tim Littlewood for the invitation to
contribute to this volume. We thank reviewers Michelle Casey (University of Kansas) and
David Thieltges (NIOZ, Royal Netherlands Institute for Sea Research) for their thoughtful
and constructive suggestions that improved this manuscript. Gabriel Carlier and Marie-
Madeleine Blanc-Valleron extended kind hospitality and assistance during Huntley’s visit
to the Museum National d’Histoire Naturelle in Paris. Daniele Scarponi (Universita di
Bologna) and Paola De Muro kindly prepared the Primi Piatti bivalve sample. Stable isotope
samples were collected and analyzed by Ken MacLeod’s Methods in Paleoclimatology class at the
University of Missouri (Claire Beaudoin, Jesse Broce, Shannon Haynes, Page Quinton and
Tara Selly). Funding to conduct these analyses was generously provided by the Keller
Opportunities for Excellence Fund of the Department of Geological Sciences, University
of Missouri. Franz T. F€ ursich kindly encouraged and enabled the exploratory fieldwork of
the senior author that led to this line of inquiry. Fieldwork was made possible by a generous
Ford Ka grant from the Corey and Heather Long Foundation (JWH). Funding for this proj-
ect was generously provided by the Alexander von Humboldt Stiftung (Renewed Research
Stay Grant; JWH) and the University of Missouri Research Council (SRF-14-019; JWH).

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CHAPTER SIX

Fossil Crustaceans as Parasites


and Hosts
Adiël A. Klompmaker*, 1, Geoff A. Boxshallx
*Florida Museum of Natural History, University of Florida, Gainesville, FL, USA
x
Department of Life Sciences, Natural History Museum, London, UK
1
Corresponding author: E-mail: adielklompmaker@gmail.com

Contents
1. Introduction 234
2. Crustaceans as Hosts of Parasites 236
2.1 Fossil evidence 236
2.1.1 Isopod parasites in decapod crustaceans 236
2.1.2 Rhizocephalan barnacles in decapod crustaceans 244
2.1.3 Platyhelminthes in crustaceans 246
2.2 Equivocal fossil evidence 246
2.2.1 Ciliates on ostracods 246
2.3 Modern evidence only 246
2.3.1 Non-crustacean parasites 246
2.3.2 Crustacean parasites 247
3. Crustaceans as Parasites of Non-crustacean Hosts 249
3.1 Fossil evidence 249
3.1.1 Ascothoracidan barnacles in invertebrates 249
3.1.2 Copepods in echinoderms 252
3.1.3 Copepods in fish 253
3.1.4 Gall crabs (Cryptochiridae) in corals 259
3.1.5 Pentastomida 261
3.2 Equivocal fossil evidence 265
3.2.1 Barnacle borings attributed to Acrothoracica in marine invertebrates 265
3.2.2 Barnacles (Pyrgomatidae) in corals 266
3.2.3 Isopods (Cymothooidea) in fishes and squids 267
3.2.4 Crabs (Trapeziidae) and corals 269
3.3 Modern evidence only 269
3.3.1 Copepods 269
3.3.2 Tantulocarida 270
3.3.3 Branchiura 270
3.3.4 Ostracoda 271
3.3.5 Facetotecta 271
3.3.6 Thoracica 272
3.3.7 Malacostraca 272

Advances in Parasitology, Volume 90


© 2015 Elsevier Ltd.
j
ISSN 0065-308X
http://dx.doi.org/10.1016/bs.apar.2015.06.001 All rights reserved. 233
234 Adiël A. Klompmaker and Geoff A. Boxshall

4. Overview Fossil Evidence and Future Research 273


Acknowledgements 276
References 277

Abstract
Numerous crustacean lineages have independently moved into parasitism as a mode of
life. In modern marine ecosystems, parasitic crustaceans use representatives from many
metazoan phyla as hosts. Crustaceans also serve as hosts to a rich diversity of parasites,
including other crustaceans. Here, we show that the fossil record of such parasitic inter-
actions is sparse, with only 11 examples, one dating back to the Cambrian. This may be
due to the limited preservation potential and small size of parasites, as well as to pro-
blems with ascribing traces to parasitism with certainty, and to a lack of targeted
research. Although the confirmed stratigraphic ranges are limited for nearly every
example, evidence of parasitism related to crustaceans has become increasingly more
complete for isopod-induced swellings in decapods so that quantitative analyses can
be carried out. Little attention has yet been paid to the origin of parasitism in deep
time, but insight can be generated by integrating data on fossils with molecular studies
on modern parasites. In addition, there are other traces left by parasites that could
fossilize, but have not yet been recognized in the fossil record.

1. INTRODUCTION
Crustaceans can enter into a wide variety of interspecific associations
including mutualism, commensalism, phoresis, inquilinism and parasitism.
Discerning the precise nature of a close symbiotic association between two
species can be problematic, even when studying living organisms. It is espe-
cially difficult when dealing with fossils. Indeed, when considering fossil
symbiotic associations, Darrell and Taylor (1993) concluded that the terms
parasitism, mutualism and especially commensalism should be used with
caution or avoided altogether (compare Zapalski, 2011). In this chapter,
we define parasitism as a symbiotic relationship in which one organism
(the parasite) is nutritionally dependent upon another (the host) for at least
part of its life cycle and has a negative impact on the fitness of the host (cf.
Tapanila, 2008a, see also Kinne, 1980; Conway Morris, 1990; Rohde,
2005, for similar definitions). The parasitic nature of an association between
two fossil species can be inferred from (1) evidence of detrimental effects of
the inferred parasite on the host, such as reduced growth, by analogy with
related living taxa or (2) by the presence of cysts or swellings that were
inhabited by parasites. Parasitism can be further confirmed when the parasites
themselves are preserved. Surface scars caused by the attachment of sessile
Fossil Crustaceans as Parasites and Hosts 235

barnacles to the plastron and skull of turtles are known from the fossil record
(Hayashi et al., 2013), but modern turtle barnacles are not treated as parasites.
Such an association is a phoresis in which the barnacle is transported by the
host, but it is not nutritionally dependent on the host as it still uses its modi-
fied thoracic limbs for suspension feeding. Similarly, fossils of whale barnacles
such as Coronula are known (e.g. Hayashi et al., 2013), but again, these are
non-parasitic epibionts and are not the focus of this chapter.
The classification of the Crustacea is in a state of flux, although it is now
widely accepted that the Hexapoda emerged from within the Crustacea
and, therefore, that the traditional Crustacea is a paraphyletic taxon (see
Edgecombe, 2010; Giribet and Edgecombe, 2013). We follow a recent sys-
tematic review of the arthropods (Regier et al., 2010) that recognized four
main lineages, Oligostraca, Vericrustacea, Xenocarida and Hexapoda, within
a monophyletic Pancrustacea. The first three of these constitute the traditional
Crustacea and provide the focus for this chapter: only the first two are known
to contain parasites today. The Oligostraca contains two main parasitic linea-
ges, the Branchiura (e.g. Boxshall, 2005a) and Pentastomida (e.g. B€ ockeler,
2005; Christoffersen and De Assis, 2013). The Vericrustacea contains a far
greater diversity of parasitic forms within the sublineage Multicrustacea
including the wholly parasitic Tantulocarida (e.g. Boxshall, 2005b) as well
as numerous parasitic lineages within the subclasses Thecostraca (e.g. Asco-
thoracida, Rhizocephala, Thoracica) (e.g. Pérez-Losada et al., 2004; Glenner
and Hebsgaard, 2006; Rees et al., 2014), Copepoda (Boxshall, 2005c) and
Malacostraca. Within the Malacostraca, the majority of parasitic forms are pe-
racarids belonging to the Amphipoda (L€ utzen, 2005) or Isopoda (e.g. Lester,
2005; Williams and Boyko, 2012). The hosts used by parasitic crustaceans
include representatives of many aquatic metazoan phyla, from sponges and
cnidarians to chordates, including tunicates, fishes, reptiles and mammals.
Crustaceans also serve as intermediate or definitive hosts to an enormous
range of parasites, including protists (e.g. Levine, 1988), acanthocephalans
(e.g. Taraschewski, 2000), nematodes (e.g. McClelland, 2002), cestodes
(e.g. Dollfus, 1976), monogeneans (e.g. Okawachi et al., 2012) and dige-
nean trematodes (e.g. Cribb, 2005), and even other crustaceans. In the great
majority of platyhelminthecrustacean associations, the crustacean serves as
an intermediate host as, for example, in parasites of humans such as Guinea
worm (Dracunculus) and fish tapeworm (Diphyllobothrium latum), both of
which use freshwater copepods as intermediate hosts.
Crustaceans have an extensive fossil record stretching throughout the
Phanerozoic, but evidence of crustaceans serving as hosts for parasites, or
236 Adiël A. Klompmaker and Geoff A. Boxshall

exhibiting a parasitic mode of life is relatively rare. Body fossils of the para-
sites themselves are particularly rare, but evidence of palaeoparasitism may be
found more commonly in traces such as structures formed as a result of the
interaction between parasite and host. In this chapter, we aim to discuss the
fossil evidence of crustaceans as parasites and hosts, provide a brief overview
of exclusively modern examples and discuss the potential of finding their
traces in the fossil record. We also explore what molecular clock studies
reveal concerning the stratigraphic range over which such parasitic interac-
tions involving crustaceans may have occurred.
Institutional abbreviations: Geomuseum Faxe, Faxe, Denmark (OESM),
Naturhistorisches Museum Wien, Vienna, Austria (NHMW); Florida
Museum of Natural History, University of Florida, Gainesville, Florida,
USA (UF); Oertijdmuseum De Groene Poort, Boxtel, The Netherlands
(MAB k); Natural History Museum of Denmark, Geological Museum, Uni-
versity of Copenhagen, Denmark (MGUH).

2. CRUSTACEANS AS HOSTS OF PARASITES


2.1 Fossil evidence
2.1.1 Isopod parasites in decapod crustaceans
2.1.1.1 Modern evidence
Many modern decapod species exhibit a swelling in the branchial region
caused by a parasitic bopyroid isopod. Markham (1986, Table 3) found
that a total of 3.6% of species in various decapod clades were infested, but
Boyko and Williams (2009) raised this value to 4.9%, based on more com-
plete data (w12,200 instead of 7863 species). The Caridea and Anomura
both have relatively high infestation rates (12.7% and 12.0%, respectively)
compared to Brachyura (only 1.3%) (Boyko and Williams, 2009). Preva-
lence rates for bopyroids on decapod hosts are typically <30% (e.g. Rayner,
1935; O’Brien and Van Wyk, 1985; McDermott, 1991; Roccatagliata and
Lovrich, 1999; Gonzalez and Acu~ na, 2004; Dumbauld et al., 2011; Cericola
and Williams, 2015, Table 1), but rates may increase to 94% of specimens of
a population in the case of invasive bopyroids on naïve hosts (Smith et al.,
2008; Dumbauld et al., 2011).

2.1.1.2 Life cycle and parasitism


Decapod crustaceans are not the only hosts for bopyroids as life cycles typi-
cally involve two hosts. Adult females release epicaridium larvae that locate
Fossil Crustaceans as Parasites and Hosts 237

the intermediate host, typically a planktonic calanoid copepod (Baer, 1951;


Boyko and Williams, 2009, Figure 3), and moult into a microniscus larva.
After an extended period on the copepod host, the microniscus larva trans-
forms into a cryptoniscus larva that seeks out the definitive decapod host
(Dale and Anderson, 1982). This larva attaches to the gills in the branchial
chamber or to the abdomen of the decapod, develops into an adult female,
and subsequently mates with the smaller adult male. Bopyroid females feed
on haemolymph or ovarian fluids of the host (Williams and Boyko, 2012)
using their mandibles to pierce the inner cuticle (Bursey, 1978). Haemo-
lymph is also the source of nutrition for larvae on the copepod host (Boyko
and Williams, 2009). In addition to nutrients, these soft-bodied parasites also
benefit from the shelter that the decapod cuticle provides, in the case of
infestation in the branchial chamber. Negative impacts on the decapod
host include a reduced growth rate, lower fecundity leading to parasitic
castration in extreme cases, modification of secondary sex characters and
distortion of the epipodites (e.g. Tucker, 1930; Beck, 1980; Van Wyk,
1982; O’Brien and Van Wyk, 1985; McDermott, 1991; Gonzalez and
Acu~ na, 2004; Hernaez et al., 2010; Petric et al., 2010; Williams and Boyko,
2012). The effects of larval parasitism on the copepod hosts are not well
known, but may include reduced growth rate and a decrease in swimming
efficiency.

2.1.1.3 Fossil record


The fossil record of bopyroids is non-existent: no body fossils are known.
However, pronounced swellings of the branchial chamber of fossil decapods
are well known and widely accepted to represent swellings induced by para-
sitic isopods. These traces are, by far, the best known example of parasitism
in or by crustaceans from the fossil record, dating back to the Jurassic (e.g.
Hessler, 1969; Wienberg Rasmussen et al., 2008; Klompmaker et al.,
2014). Given the close morphological similarity to swellings induced by
bopyrids in modern decapods, Wienberg Rasmussen et al. (2008) referred
to them as bopyriform swellings. Boyko and Williams (2009) even specu-
lated that members of the Ioninae may have caused swellings in fossil crabs.
Klompmaker et al. (2014), however, expressed some doubt that these are all
caused by bopyrids, given the ancient age of such swellings, the lack of body
fossil evidence and the fact that other isopods may also cause swellings in the
branchial region. These authors referred to them as isopod-induced swel-
lings and formalized the name of this embedment structure by erecting
the ichnotaxon Kanthyloma crusta. They listed 88 host species, to which three
238 Adiël A. Klompmaker and Geoff A. Boxshall

further species are added here (see Figure 1) plus K. crusta in the crab Speo-
carcinus berglundi from the late Miocene (Tortonian) of California (Tucker
et al., 1994) and the crab Cristafrons praescientis from the Late Cretaceous
(SantonianeMaastrichtian) of Antarctica (Feldmann et al., 1993) based on
evidence from figures. Recently, Beschin et al. (2015) mentioned a swelling
in the branchial region of the Eocene (Ypresian) squat lobster Acanthogalathea
squamosa from Italy, but this record is difficult to confirm in the absence of a
figure. New fossil specimens exhibiting K. crusta have been reported recently

Figure 1 New examples of swellings (ichnotaxon Kanthyloma crusta) attributed to iso-


pods in the branchial region of fossil decapod crustaceans including squat lobsters (a,
d, e) and crabs (rest). (a) Galathea strigifera from the lower Palaeocene (Danian) Faxe For-
mation of the Faxe quarry, Denmark (e.g. Jakobsen and Collins, 1997; Lauridsen et al.,
2012; Lauridsen and Bjerager, 2014), OESM-10059-21721. (b) Goniodromites ?dentatus
from the Upper Jurassic (Tithonian) Ernstbrunn Limestone of the Ernstbrunn quarries,
Austria (e.g. Schweitzer and Feldmann, 2008; Robins et al., 2012, 2013; Schneider et al.,
2013), NHMW 2014/0194/0965. (c, g) Frontal and dorsal views of Cycloprosopon sp.
from the Upper Jurassic (Tithonian)eLower Cretaceous (Berriassian) part of the
Stramberk Formation of the Kotouc quarry, Czech Republic (e.g. Housa and Vasícek,
2004; Fraaije et al., 2013a), UF 252037. (d) Munida primaeva from the lower Palaeocene
(Danian) Faxe Formation of the Faxe quarry, Denmark, MGUH 31265. Specimen about
same size as (e). (e) Eomunidopsis navarrensis from the mid-Cretaceous (upper Albian)
Eguino Formation of the Koskobilo quarry, Spain (e.g. Fraaije et al., 2012, 2013b;
Klompmaker et al., 2011, 2012, 2013b; Klompmaker, 2013), MAB k2603. (f) Juvenile
Eodromites grandis from the Late Jurassic (Tithonian) Ernstbrunn Limestone of the
Ernstbrunn quarries, Austria, NHMW 1990/0041/4646. Kanthyloma crusta was previously
unknown from G. strigifera, M. primaeva and Goniodromites ?dentatus. Scale bars 5.0 mm.
Fossil Crustaceans as Parasites and Hosts 239

in taxa from which such swellings were already known (Fraaije, 2014, for
Gastrosacus wetzleri; Hyzný et al., 2014, for Galathea weinfurteri; Kornecki,
2014, for Cretocoranina testacea), highlighting the relatively common occur-
rence of such swellings. These swellings have been found mostly in fossil
true crabs (Brachyura) and squat lobsters (Galatheoidea); evidence of infes-
tation of lobsters and shrimps is relatively scarce (Wienberg Rasmussen
et al., 2008; Klompmaker et al., 2014). Only one swelling is known from
a shrimp (Franţescu, 2014), despite the common occurrence of isopods in
modern shrimps (Boyko and Williams, 2009). This can be explained by
the lower fossilization potential of shrimps due to their relatively soft
exoskeleton. Of note is the recent discovery of a swelling in the fixed finger
of a propodus of the Holo-Pleistocene ghost shrimp Glypturus panamacana-
lensis, but this swelling was probably not caused by a parasitic isopod
(Klompmaker et al., 2015).
Modification of secondary sex characters by epicaridean isopods, such as
feminization of the male chelae in shrimps (e.g. Tucker, 1930; Beck, 1980)
and widening of the abdomen in male crabs (Reinhard, 1956), has been
recorded in modern decapods, but this would be difficult to detect in fossils
unless specimens are exquisitely preserved.

2.1.1.4 Quantitative data per fauna


Quantitative data on infestation by isopods are sparse, although a few data
exist on prevalence rates by locality and/or by host taxon (Bachmayer,
1955; Housa, 1963; Radwa nski, 1972; Boucot, 1990; Wienberg Rasmussen
et al., 2008; Klompmaker et al., 2014). The latter authors collected data for
all species at a locality by systematically collecting all specimens they
encountered. They showed that more common species tend to have a
higher prevalence rate, potentially suggesting host specificity.

2.1.1.5 Infestation patterns through time


Inspired by the initial data set gathered by Wienberg Rasmussen et al.
(2008), Klompmaker et al. (2014) expanded this data set and figured infes-
tation patterns through geologic time (Figure 2). Both the number of species
exhibiting evidence of K. crusta and the percentage of species infested show a
peak during the Late Jurassic, after which values dropped to stabilize in the
Late Cretaceous and Cenozoic. Interestingly, the Late Cretaceous infesta-
tion of all species is <5%, which is comparable to today’s value (see Boyko
and Williams, 2009). This may suggest that infestation rates comparable to
today were already reached in the Late Cretaceous.
240 Adiël A. Klompmaker and Geoff A. Boxshall

Figure 2 The prevalence of parasitic, isopod-induced swellings in fossil decapod


crustaceans (ichnotaxon Kanthyloma crusta) throughout geologic time. Larger graph:
number of infested marine decapod, brachyuran, galatheoid anomuran and lobster
species standardized per 20 Myr per epoch. Inset shows the percentage of marine
decapod, brachyuran, galatheoid anomuran and lobster species infested per Jurassic
and Cretaceous epoch to circumvent the potential effect that the high species
diversity in the Late Jurassic (see Klompmaker et al., 2013a) may have on the pattern.
The peak infestation remains visible. (Modified from Klompmaker et al. (2014, Figures 5
and 6))

Klompmaker et al. (2014) suggested that the pattern through time is


likely to show one or more biological signals rather than being dominated
by collecting and reporting biases. Adaptations increasing resistance to infes-
tation, falls in diversity of infestation-prone groups (e.g. galatheoids),
copepod-related changes and/or changes in decapod size through time
may have contributed to the observed pattern. Most infested species from
the Late Jurassic originate from reef-associated settings, which is not surpri-
sing given that Klompmaker et al. (2013a, Figure 3) showed that most deca-
pods were found in reef-associated environments at that time. Given a
subsequent decline in the contribution of reef-associated decapods to overall
diversity, could the infestation peak in the Late Jurassic be solely explained
by reef abundance? This seems unlikely because coral-associated deposits
from the Late Cretaceous (Maastrichtian) of the Netherlands did not yield
a single specimen exhibiting K. crusta, and swellings in decapods in a reef
from the Palaeocene (Danian) of Denmark are rare (Klompmaker et al.,
2014; pers. obs. AAK).
Fossil Crustaceans as Parasites and Hosts 241

2.1.1.6 Age
This type of parasitism in decapods dates back to the Jurassic, possibly the
Early Jurassic (Toarcian) based on a lobster, although this is only inferred
from a drawing (Wienberg Rasmussen et al., 2008; Klompmaker et al.,
2014). Thus far, Middle Jurassic deposits have not yielded an example of
K. crusta, and this discontinuity adds to the uncertainty surrounding the Early
Jurassic record. Given the estimated occurrence of calanoid copepods as far
back as the Silurian, based on a phylogeny using morphological and mole-
cular evidence (Selden et al., 2010), and the presence of decapods since the
Devonian (e.g. Feldmann and Schweitzer, 2010; Gueriau et al., 2014; Jones
et al., 2014), Early Jurassic and older occurrences are theoretically possible as
the two host groups would have been available. Unfortunately, no rigorous
phylogenetic analyses of epicarideans including estimated divergence times
are known to us. The only study is based on limited evidence. Using three
species, Lins et al. (2012) showed that the last common ancestor of the
Bopyridae, Dajidae and Sphaeromatidae (non-parasitic) would root in the
Permian.
Some insight may come from related isopods such as the Cymothooidea
(e.g. Dreyer and W€agele, 2001; Boyko et al., 2013). Dreyer and W€agele
(2001, Figure 12) speculated that cirolanid-like cymothoids feeding on
fish evolved to become parasitic on/in fish (Cymothoidae), and also gave
rise to the Bopyridae infesting crustacean hosts, resulting in the radiation
of bopyrids. This radiation may be best expressed in the Late Jurassic
(Figure 2). The Cymothoidae have, however, no fossil record (Smit et al.,
2014), which may indicate a low preservation potential. The non-parasitic
Cirolanidae have an undisputed fossil record into the Middle Jurassic,
whereas the Cymothoida are known from the Early Triassic (Etter, 2014).
Thus, if Dreyer and W€agele’s (2001) hypothesis is correct and the fossil re-
cord is a reasonable representation of the occurrence of the Cymothoida,
then no isopod-induced swellings in decapod crustaceans are to be expected
from the Palaeozoic.

2.1.1.7 Biogeography
It is noteworthy that the oldest report of K. crusta originates from Indonesia
(although it is disputed), whereas all Late Jurassic and Early Cretaceous
occurrences are from Europe (Klompmaker et al., 2014, Table 3). A global
distribution of this type of parasitism does not occur until the Late Creta-
ceous with occurrences in Europe, North America, New Zealand and
Antarctica. Whether this European peak in the Late Jurassic and Early
242 Adiël A. Klompmaker and Geoff A. Boxshall

Cretaceous represents a sampling bias remains to be investigated. However,


given the abundant reefs in Europe during the Late Jurassic (Kiessling et al.,
1999, Figure 10) and the radiation of Brachyura and certain Anomura
(Klompmaker et al., 2013a), this peak may not be surprising.

2.1.1.8 On the erection of an ichnotaxon


In a note, Donovan (2015) cast doubt on the establishment of the ichno-
taxon K. crusta by Klompmaker et al. (2014) for the branchial swellings
exemplified in Figure 1. In his opinion, these represent pathological struc-
tures, and, as such, the ichnotaxon should not have been erected, following
Bertling et al. (2006, Table 1) who suggested that pathologies are in a ‘grey
zone’ and are ‘non-traces’. It was not addressed why these swelling do not
represent embedment structures. We welcome this opportunity to discuss
this issue further here.
Klompmaker et al. (2014, p. 12) did not specifically call these swellings
(classified as bioclaustrations) trace fossils in view of the ongoing discussion
as to whether such embedment structures should be treated as trace fossils.
Bertling et al. (2006) were of the opinion that bioclaustrations do not repre-
sent trace fossils, but many others disagree. Bioclaustrations were called trace
fossils by Palmer and Wilson (1988) and, more recently, by Tapanila and
Ekdale (2007), Bromley et al. (2008), Tapanila (2008b), McKinney (2009),
Knaust (2012), Santos et al. (2012) and C onsole-Gonella and Marquillas
(2014). The swellings in decapods were classified ichnotaxonomically
because as Bertling et al. (2006, p. 268) noted with regard to hybrid structures
resulting from borings and growth, ‘for convenience and in order to maintain
stability of names with a high ecological meaning, we advocate nomenclatu-
rally (not taxonomically) treating them as if they were ichnotaxa’. An ichno-
taxon name is convenient here and such swellings convey ecological insights
into the origin of parasitism in deep time. Boring and growth are both of note
in this case because the mandibles of isopods bore into the inner cuticle for
food extraction from the host resulting in the growth of the parasite today
(Bursey, 1978). Hybrid structures caused by parasites have been described
ichnotaxonomically (Vinn et al., 2014; Wilson et al., 2014a). Furthermore,
Wilson et al. (2014b, p. 1214) referred preserved embedment pits without
evidence of boring to an ichnotaxon (Oichnus). Similarly, Radwa nska and
Radwa nski (2005) and Boucot and Poinar (2010) called copepod-induced
swellings trace fossils.
Klompmaker et al. (2014) treated K. crusta as an embedment structure or
bioclaustration following Bertling et al. (2006, p. 267): ‘embedment
Fossil Crustaceans as Parasites and Hosts 243

structures in calcareous skeletons that are produced by an actively growing


organism around disturbing or irritating objects or living organisms’ because
the cuticle of the host continues to grow around the isopod. Such a swelling
represents a gradually formed indentation of the isopod embedding in the
substrate (¼ the cuticle of its decapod host), but in reverse so that the bulge
is formed from the inside of the branchial wall. The result is, however, the
same: the body is encased by or embedded within the host. K. crusta refers to
the (infilled) cavity that was created by the inhabitation of the isopod, not to
the cuticle surrounding it. Indeed, all the types represent internal moulds
without cuticle. Furthermore, Klompmaker et al. (2014, p. 13) referred to
the cuticle as the substrate (not the embedment structure), and they also
referred to swellings in the branchial region.
Donovan (2015) argued against erecting an ichnotaxon for a swelling
because, in his opinion, these swellings represent pathologies, and he gave
examples including the results of a mosquito bite and a gall-maker puncture,
citing Bertling et al. (2006). The latter authors noted that (2006, p. 268)
‘swollen tissue and plant reaction tissues may at best be considered ‘traces
of traces’ having an original tracemaker, whose trace (the puncture) is obli-
terated by the induced plant growth’, but also ‘if they do contain a recogni-
zable trace fossil, e.g. a boring, faecal pellets, a pupal chamber, or an exit hole
etc., they may be named as such’ in referring to an ichnotaxon. The swel-
lings described by Bertling et al. (2006) consist (nearly) entirely of animal
or plant tissue or carbonate created by the affected organism, which is the
direct result of the disease or irritation. This is very different in K. crusta.
The direct morphological result of infestation is a slower growth rate (as
recorded for modern isopod-infested decapods), a potentially thickened
cuticle and/or feminization of the claws (see above), but not the swelling it-
self, which represents the cavity of the isopod body, or the domicile of the
isopod. Unlike for the swellings described in Bertling et al. (2006) and
referred to in Donovan (2015), the isopod parasite creates space in the bran-
chial chamber in order to grow. This is not a direct expression or result of the
disease, but is the endpoint of a coevolutionary history of the embedment of
one organism within another. Therefore, the swellings in decapods do not fit
pathological structures as defined in Bertling et al. (2006) and cannot be
considered a ‘trace of a trace’: they constitute a recognizable trace of the
body of the isopod. Radwa nska and Radwa nski (2005, p. 114) made a similar
distinction between pathological and parasitic deformities in echinoid tests.
In conclusion, the swellings in the branchial region cannot be considered
pathological structures sensu Bertling et al. (2006). Rather, they represent
244 Adiël A. Klompmaker and Geoff A. Boxshall

bioclaustrations or embedment structures, and, as such, K. crusta is consi-


dered a valid ichnotaxon. Moreover, many other researchers also consider
bioclaustrations to be trace fossils.

2.1.2 Rhizocephalan barnacles in decapod crustaceans


Most modern rhizocephalan barnacles are parasitic on brachyurans and
anomurans, but some infest caridean and axiidean shrimps, stomatopods,
isopods, cumaceans and thoracican barnacles (e.g. Høeg, 1995; Høeg
et al., 2005). Infestation by rhizocephalans can cause castration of the
decapod host, feminization of males and a reduced host growth rate, to
the extent that moulting ceases and maximum size is reduced (e.g. O’Brien
and Van Wyk, 1985; Takahashi and Matsuura, 1994; Feldmann, 1998).
Infested females do not adopt male features, but males display female se-
condary sexual characters after infestation, best expressed in the form of the
claws and abdomen (Feldmann, 1998). The abdomen of a rhizocephalan-
parasitized male decapod may become broader, resembling that of a female
(O’Brien and Van Wyk, 1985) and the major claw of a male may not grow
as large, resembling a female claw (Feldmann, 1998). The parasite extracts
nutrients from the host via an embedded rootlet system that penetrates the
host’s internal tissues (see Feldmann, 1998, for additional details).
This type of parasitism is well known in modern decapods, but much less
is known from the fossil record. This is partly due to the incomplete preser-
vation of the majority of decapod specimens (i.e. disarticulation, complete
ventral sides are rare), to a lack of large samples of particular species and
perhaps to a lack of study of collections in which feminization might be
observed. Some evidence exists, however. Bishop (1974) was the first to
recognize a sexually aberrant fossil decapod, an intersex specimen of the
crab Dakoticancer overanus from the Late Cretaceous (Maastrichtian) of South
Dakota (USA). This specimen bears female gonopores, the abdomen appears
wider than in males (but narrower than in females), and the granular orna-
mentation on the sternum is the same as in males. The discovery of a second
conspecific specimen from the same locality (Bishop, 1983) confirmed that
the ornamentation on the sternum is the same as in males, the abdomen is of
intermediate width and the gonopores are most reminiscent of females (see
Bishop, 1983, Table 1). Feldmann (1998) considered that the latter would
qualify more likely as a parasitized specimen. Jones (2013) studied the Bishop
collection from the same area and found 11 intersex specimens of the same
fossil crab, and concluded that parasitism was the most likely explanation for
the occurrence of the intersex specimens. Feldmann (1998) described the
Fossil Crustaceans as Parasites and Hosts 245

best preserved examples of this type of parasitism, from specimens of the crab
Tumidocarcinus giganteus from the Miocene of New Zealand (Figure 3). A
feminized male showed a broader than usual abdomen and its major claw
was more like those of females in terms of size. He specifically attributed
this to parasitism by rhizocephalan barnacles, unlike previous accounts. It
should, however, be noted that parasitism by epicarideans (including non-
bopyroids such as entoniscids) can also result in the feminization of males,
including a widening of the abdomen and reduction in claws (Reinhard,
1956; Rasmussen, 1973), so that these infestations can ‘duplicate closely
the effects by Rhizocephala’ (Reinhard, 1956, p. 91). Careful examination
of the carapace may show slight deformations in entoniscid-infested crabs
(e.g. Miyashita, 1941; Shields and Kuris, 1985), but its expression may not

Figure 3 Normal female and male specimens of the Miocene crab (Tumidocarcinus
giganteus) from New Zealand, and a possible rhizocephalan barnacle infested conspe-
cific specimen showing feminization of the abdomen and claws. (a) Abdomen of a
mature female. (b) Ventral side of a mature male. (c) Ventral side of a juvenile female.
(d) Ventral side of a feminized male. Scale bars 10 mm. (From Feldmann (1998),
Figure 3)
246 Adiël A. Klompmaker and Geoff A. Boxshall

be obvious (e.g. Shields and Ward, 1998; Brockerhoff, 2004). Therefore,


ascribing feminization in fossil crabs to infestation by rhizocephalans is not
without uncertainty.

2.1.3 Platyhelminthes in crustaceans


Platyhelminth worms have been reported to infest Late Devonian (Frasnian)
fishes from Latvia based on the presence of hooks in 16 specimens of the pla-
coderm Asterolepis ornata and in 27 specimens of the acanthodian Lodeacan-
thus gaujicus (Upeniece, 1999, 2001, 2011; De Baets et al., 2015). Two
hooks were also found in a crustacean specimen ascribed to the Mysidacea,
but Upeniece (2001, 2011) considered the hooks too large relative to the
size of this crustacean for it to have been a host. Another hook was found
close to a Conchostraca (clam shrimp) specimen, but the inference that it
constitutes evidence of parasitism is not convincing. Modern crustaceans
can act as hosts of platyhelminthes (e.g. Fredensborg and Poulin, 2005;
Boyko and Williams, 2011), but the fact that only a single specimen out
of thousands of mysidaceans was reported to contain hooks (Upeniece,
2001) may indicate accidental parasitism of these crustaceans at best. For
comparison, over 300 A. ornata and more than 50 specimens of L. gaujicus
were found, of which 16 and 27 specimens yielded hooks.

2.2 Equivocal fossil evidence


2.2.1 Ciliates on ostracods
Weitschat and Guhl (1994) reported on stalked peritrichid ciliates (Cilio-
phora) attached on the inner part of the shell and on the epipodal appendages
of ostracods found within an Early Triassic ammonite from Spitsbergen.
Wilkinson et al. (2007) and Siveter et al. (2015) referred this association to
ectoparasitism. Given the definition of parasitism used here, we do not
consider these ciliates parasitic on the ostracods because they were inter-
preted to be filter feeding and not nutritionally dependent on their host
(see Weitschat and Guhl, 1994, Figures 9 and 10).

2.3 Modern evidence only


2.3.1 Non-crustacean parasites
Crustaceans serve as intermediate or definitive hosts to an enormous
range of unicellular and metazoan parasites and such infestations can be of
economic significance in large-scale commercial aquaculture. The produc-
tion of farmed marine penaeid crustaceans, for example, can be adversely
impacted by infections with various protists, including microsporidians,
Fossil Crustaceans as Parasites and Hosts 247

haplosporidians and gregarines (Lightner, 1993). The Acanthocephala were


once treated as a distinct phylum, but are now considered close relatives of
the rotifers within a single phylum, the Syndermata (Herlyn et al., 2003;
Wey-Fabrizius et al., 2013). Acanthocephalans typically use vertebrates as
final hosts, but many use crustaceans as intermediate hosts (e.g. Near,
2002; Weber et al., 2013). In marine species, amphipods are the commonest
intermediate host taxon, but others such as brachyuran crabs and mysida-
ceans are also used (Taraschewski, 2000). Nematodes are highly diverse
and numerous parasitic nematodes have heteroxenic life cycles that include
crustaceans as hosts (McClelland, 2002). The newly hatched larva of the
sealworm Pseudoterranova decipiens, for example, is ingested by benthic cope-
pods, amphipods or mysidaceans that in turn may be eaten by larger crusta-
ceans or small fish before being consumed by the mammalian final host.
Similarly, larval Anisakis are found in pelagic crustaceans such as copepods
and euphausiaceans that are fed on by larger nekton (fish and squid) that
form the diet of the final host. Cestodes typically use vertebrates as the final
host, but they have complex life cycles often involving a succession of two
or more intermediate hosts. Crustacean groups known to serve as either first
or second intermediate hosts include copepods, amphipods, mysidaceans,
branchiopods, barnacles, stomatopods and decapods (Dollfus, 1976). The
fish tapeworm of humans, D. latum, uses freshwater copepods as an interme-
diate host. Digenetic trematodes are also typically endoparasitic and have
similarly complex life cycles involving free-living stages as well as a succes-
sion of hosts (Cribb, 2005). While the first intermediate host is usually a
mollusk, the second can often be a crustacean that either consumes the
infective cercarial larva or is penetrated by it. In contrast, most monogeneans
are ectoparasites of aquatic vertebrates and have direct life cycles, but
Udonella is hyperparasitic on caligid copepods (Okawachi et al., 2012).
Most of these protist and platyhelminth parasites are microscopic and inhabit
the internal organs of their crustacean hosts; their impact on the host is un-
likely to leave a readily recognizable trace should the host be fossilized (see
Littlewood and Donovan, 2003; Littlewood, 2006).

2.3.2 Crustacean parasites


Crustaceans are used as hosts by parasitic crustaceans including all members
of the Tantulocarida as well as some copepods, isopods and cirripedes.
Various crustaceans serve as hosts to copepods of the family Nicothoidae
and it has been suggested that these tiny parasites are egg mimics since
they are commonly found in the marsupium of peracarids, in the brood
248 Adiël A. Klompmaker and Geoff A. Boxshall

pouch of myodocopan ostracods, or on the egg mass of decapods (Boxshall


and Halsey, 2004). This mimicry is presumed to reduce the risk of removal
by the host’s grooming behaviour. These egg mimics have little detectable
impact on the host, although a few other nicothoids that inhabit the bran-
chial chambers of their hosts are known to cause swellings or cysts (Boxshall
and Lincoln, 1983a, Figure 1(a)). Such cysts have the potential to be visible
on fossils of the hosts; however, no examples of fossil crustaceans infested by
nicothoids have yet been reported.
Marine crustaceans including copepods, ostracods and peracarid mala-
costracans are hosts to tantulocaridans. The Tantulocarida, established in
1983 (Boxshall and Lincoln, 1983b), are minute ectoparasites. The life
cycle includes an asexual and a sexual cycle that share a free living, infective
stage, the tantulus larva that is typically about 100 mm in length. In the
asexual cycle, the tantulus attaches to its crustacean host, sheds its post-
cephalic trunk and develops into a sac-like asexual female within which
develops the next generation of tantulus larvae (Boxshall and Lincoln,
1987). In the sexual cycle, after attaching to the host, the post-cephalic
trunk of the tantulus swells to form a sac within which a single adult
male or female develops. These free-swimming adults are the mating
stages, but are non-feeding (Huys et al., 1993). These tiny parasites attach
externally to their crustacean hosts using an oral disc only a few microns in
diameter, and use an oral stylet to make a single puncture in the host’s
cuticle. They are unlikely to be fossilized and cause only a minimal lesion
that would be on such a minute scale as to be unrecognizable as of tantu-
locaridan origin.
Ostracods, amphipods, euphausiaceans, copepods, barnacles, mysids and
other isopods are all known to serve as hosts to parasitic isopods of the su-
perfamily Cryptoniscoidea (e.g. Vannier and Abe, 1993, for ostracods).
The larval stages of cryptoniscoids are often ectoparasitic, while adults
may be ecto- or endoparasitic. In many cases, parasites have little discernable
impact on the host and no examples of fossil taxa from these groups have
been reported as harbouring isopod parasites. Some evidence in the fossil
record may be expected for barnacles because Hosie (2008, Figure 12(a))
showed a cryptoniscoid-induced swelling in the stalk of the modern barna-
cle Smilium zancleanum. Infection of modern decapods by members of the
Entoniscidae has been reported to cause asymmetrical carapaces (Miyashita,
1941; Shields and Kuris, 1985). Examples of this could also be expected from
the fossil record (Klompmaker et al., 2014), but may be difficult to differen-
tiate from swellings caused by bopyroids.
Fossil Crustaceans as Parasites and Hosts 249

3. CRUSTACEANS AS PARASITES OF
NON-CRUSTACEAN HOSTS
3.1 Fossil evidence
3.1.1 Ascothoracidan barnacles in invertebrates
These small barnacles (up to 8 mm in size) parasitize a variety of modern
marine hosts, particularly echinoderms (but not regular echinoids and sea cu-
cumbers) and cnidarians (gorgonians, zoanthids, scleractinians and antipatha-
rians) (e.g. Moyse, 1983; Grygier, 1996; Grygier and Høeg, 2005). Many are
endoparasitic in the main body cavity of asteroids and echinoids, but ectopa-
rasitic on anthozoans, crinoids and ophiuroids (references in Krawczy nski and
Wilson, 2011, but see Grygier and Høeg, 2005). Several ascothoracidans
(Ascothorax, Ulophysema and Dendrogaster) cause castration of their echinoderm
hosts (Grygier and Høeg, 2005). Grygier and Høeg (2005) noted that little is
known about their feeding behaviour, but basal forms have piercing and
sucking mouthparts while the more transformed genera such as Ulophysema
and Dendrogaster employ absorptive feeding, similar to rhizocephalans.
Body fossils of these barnacles are unknown, but structures attributed
to ascothoracidans have been reported from the fossil record (Figure 4;
Table 1). Voigt (1959) first recognized galls or cysts named Endosacculus
moltkiae in the Late Cretaceous octocoral Moltkia minuta that were attri-
buted to ascothoracidans because of morphological similarity to cysts of
modern representatives. Moyse (1983), for example, showed morphologi-
cally similar galls on modern octocorals. Subsequently, Voigt (1967) found
further Late Cretaceous evidence for infestation of octocorals, presumably
by an ascothoracidan, and a cyst in the early Palaeocene (Danian) hydroco-
ral Astya crassus was suggested to have been produced by parasitic crusta-
ceans (either copepods or ascothoracidans) by Bernecker and Weidlich
(2005), although their photograph (Figure 7(c-1)) does not allow identifi-
cation of the parasitic structure. Voigt (1959) was of the opinion that his
examples did not represent parasitism because the host was not particularly
damaged and continued to grow after infestation. He considered it did not
represent a true endoparasite deriving its food from the host; rather, he sug-
gested that commensalism or ‘syn€ okie’ (inhabitation of host and taking part
in meals of the host sensu K€ orner, 1979) was more appropriate. However,
research on modern ascothoracidans suggests that they are parasitic (see
Grygier and Høeg, 2005).
Fossils attributed to ascothoracidans have also been found in an echinoid
and possibly in a brachiopod. Madsen and Wolff (1965) described the
250 Adiël A. Klompmaker and Geoff A. Boxshall

Figure 4 Growth anomalies in octocorals and a brachiopod attributed to infestation by


ascothoracidan barnacles. (aed) Galls or cysts (ichnotaxon Endosacculus moltkiae) in
the octocoral Moltkia minuta from the Late Cretaceous (Maastrichtian) of the
Netherlands (a, b, d) and the Late Cretaceous (Campanian) of Sweden (c). ((b) ¼ holo-
type of E. moltkiae). (e) Possible ascothoracidan infestation (marked) in the brachiopod
Moorellina negevensis from the Middle Jurassic (late Callovian) of Israel. Scale bar (e)
0.2 mm; scale bar for others not available. ((aed) from Voigt (1959), pl. 25.7e25.9 and
26.2; (e) from Krawczyn ski and Wilson (2011), Figure 2(a))

presence of holes in a Late CretaceousePalaeocene echinoid and attributed


them to two specimens of Ulophysema based on similar holes in echinoids
produced by modern Ulophysema. There may be further evidence from echi-
noids: Bromley (2004) suspected that the two round holes in an Early Creta-
ceous echinoid attributed to boring gastropods by Kier (1981) may be the
work of ascothoracidans. Restudy of the specimen is called for. Krawczy
nski
and Wilson (2011) described a gall, possibly of ascothoracidan origin, in a
Fossil Crustaceans as Parasites and Hosts
Table 1 Structures attributed to ascothoracidan barnacles from the fossil record
Host taxon Name cyst/parasite Age Locality and country Stratigraphic unit References

Moltkia minuta Endosacculus Late Cretaceous The Netherlands ‘Maastrichter Voigt (1959)
(Octocorallia) moltkiae (late Tuffkreide’
Maastrichtian)
M. minuta E. moltkiae Late Cretaceous If€
o (Schonen), ‘Tr€
ummerkreide’, Voigt (1959)
(Octocorallia) (Campanian) Sweden rocks with
Actinocamax
mamillatus
Isis sp. Endosacculus (?) Late Cretaceous South Emba, Rocks with Voigt (1967)
(Octocorallia) najdini (late Kazakhstan Belemnella
Maastrichtian) arkhangelskii
Echinocorys Ulophysema Late Cretaceous Limfjord in North e Madsen and Wolff
(Echinoidea) ePalaeocene Jutland, Denmark (1965)
(?Maastrichtian
eDanian)*
Moorellina negevensis e Middle Jurassic Matmor Hills in Matmor Fm, Krawczy
nski and
(Brachiopoda) (late Callovian) Hamakhtesh lamberti Zone Wilson (2011)
Hagadol, Israel
* pers. comm. Sten Jakobsen to AAK.

251
252 Adiël A. Klompmaker and Geoff A. Boxshall

brachiopod from the Middle Jurassic of Israel. No ascothoracidan-infested


brachiopods are known today.
The fossil record of these traces has not yet been investigated exhaus-
tively given the limited stratigraphic range (Table 1). Also, Grygier and
Høeg (2005) suggested that galls formed by members of the Petrarcidae
(e.g. Grygier, 1990) could be recognized in fossil scleractinian corals.

3.1.2 Copepods in echinoderms


Thirteen families of copepods parasitize exclusively echinoderms, and some
representatives of several other families also use echinoderms as hosts. While
most of these copepods are ectoparasites, members of the Chordeumiidae
live within cysts of host origin or within the genital bursae of their ophiuroid
hosts and can cause swellings that are visible externally. Two families living
on echinoid hosts are known to induce their hosts to form galls. The three
species of Calverocheridae form galls in their host’s spines (Stock, 1968),
while the two species of Pionodesmotidae form galls within the test of
the host (Bonnier, 1898; Anton et al., 2013). The hosts of both families
are deep-sea echinothuriid echinoids that are atypical sea urchins in having
a soft and flexible body. Calverocherids induce the host to create galls in
spines on the adoral surface; these galls are typically asymmetrical and located
near the middle of the spine. The gall has one pore located at its distal end.
Stock (1968) described the swelling as consisting of loose calcareous material
around an ampulla inside which a single copepod is found. Pionodesmotids
are rarely reported: more than a century passed between the establishment of
the type species and the discovery of a second. Pionodesmotes domhainfharrai-
geanus lives within endocysts located in the ambulacral region on the adoral
side of the host echinoid’s test (Anton et al., 2013). These cysts have a single
opening and are not visible externally. Exocysts caused by the asterocherid
copepod Cystomyzon dimerum containing multiple openings are formed on
modern hydrocorals (Zibrowius, 1981). Fossil endocysts have not been
found yet, but exocysts on the surface of echinoid tests, referred to as the
ichnotaxon Castexia douvillei, and the so-called ‘Halloween pumpkin-
mask’ cysts resembling the exocysts in modern hydrocorals (Zibrowius,
1981) (Figure 5), have both been suggested to be treatable as trace fossils
by Radwa nska and Radwa nski (2005). Halloween pumpkin-mask cysts
are also known from fossil crinoids (Radwa nska and Radwa nski, 2005).
Other, older interpretations of the trace maker of the latter cysts exist
including trematodes, myzostomid annelids and ascothoracid barnacles
(e.g. Mehl et al., 1991; Richter, 1991; Neumann and Hostettler, 2004).
Fossil Crustaceans as Parasites and Hosts 253

Figure 5 Examples of Halloween pumpkin-mask cysts (aee) and cysts ascribed to the
ichnotaxon Castexia douvillei (fei), all inferred to be caused by copepod parasites. (a, b)
The modern hydrocoral Stylaster papuensis from Tagula Island, Louisiade Archipelago,
southwest Pacific, showing cysts induced by the copepod Cystomyzon dimerum. (c,
d) Copepod cyst in the gonopore of an echinoid test of Acrosalenia spinosa from the
Middle Jurassic (Bathonian) of Bicqueley, Lorraine, France. (e) Three cysts in a crinoid
stem of Isocrinus tuberculatus from the Early Jurassic (Sinemurian) of Germany. (fei)
Two cysts in an echinoid test of Collyrites dorsalis from the Middle Jurassic (Callovian)
of Mortagne-au-Perche, Orne, France. Smallest cyst (h) located in an ambulacral co-
lumn, whereas the larger one (i) is positioned in an interambulacral column. Scale
bars unavailable in source articles. ((a, b) from Zibrowius (1981), pl. 1.8 and 2.4; (c, d)
from Radwan ska and Poirot (2010), Figure 4; (e) from sole figure in Weinfurtner (1989);
(fei) from Radwanska and Radwan ski (2005), Figure 11.1)

A list of echinoderms inferred to be infested by copepods resulting in cysts or


swellings is presented in Table 2. Thus far, only Jurassic occurrences, chiefly
from Europe, are known.

3.1.3 Copepods in fish


A single species of parasitic copepod from a fish host is known from body
fossils: Kabatarina patersoni was recovered from two skulls of an
Table 2 Echinoderms inferred to be infested by copepods resulting in cysts or swellings
Locality and Stratigraphic

254
Host taxon Name cyst Age country unit (if known) References

Acrosalenia spinosa Halloween Middle Jurassic Bicqueley, Lorraine, Caillasse a Anabacia, Radwa
nska and
(Echinoidea) pumpkin-mask (early France convergens Poirot (2010)
e test Bathonian) Subzone
A. spinosa Halloween Middle Jurassic Luc-sur-Mer, Basse- Caillasses de Basse- Radwa
nska and
(Echinoidea) pumpkin-mask (late Bathonian) Normandie, Ecarde Poirot (2010)
e test France
Acrosalenia Halloween Middle Jurassic Calvados, France Richter (1991)
hemicidaroides pumpkin-mask (Bathonian)
(Echinoidea)
e test
Cidaroida Halloween Late Jurassic Germany Goldfuss (1829)
(Echinoidea) pumpkin-mask
e test
Plegiocidaris Halloween Late Jurassic (early Ludwag Quarry, Mehl et al. (1991)

Adiël A. Klompmaker and Geoff A. Boxshall


coronata pumpkin-mask Kimmeridgian) Oberfranken,
(Echinoidea) Germany
e test
P. coronata Halloween Late Jurassic Teuchatz Quarry, Mehl et al. (1991)
(Echinoidea) pumpkin-mask (middle Oberfranken,
e test Kimmeridgian) Germany
P. coronata Halloween Late Jurassic Obermain-Alb, Hildner (2014)
(Echinoidea) pumpkin-mask (Kimmeridgian) Germany
e test
Paracidaris Halloween Late Jurassic Aargau, Switzerland Birmenstorfer Mehl et al. (1991)
laeviuscula pumpkin-mask (middle Schichten
(Echinoidea) Oxfordian) (Argovium)
e test
?P. laeviuscula Halloween Late Jurassic Aargau, Switzerland transversarium Zone Zbinden (1991)

Fossil Crustaceans as Parasites and Hosts


(Echinoidea) pumpkin-mask (middle
e test Oxfordian)
Hemicidaris Halloween Late Jurassic Bernese Jura, bimammatum Zone Zbinden (1991)
intermedia pumpkin-mask? (middle Switzerland
(Echinoidea) Oxfordian)
e test
Stomechinus Halloween Late Jurassic Reuchenette, Neumann and
perlatus pumpkin-mask? (Oxfordian) Switzerland Hostettler (2004)
(Echinoidea)
e test
Plegiocidaris Halloween Late Jurassic (late Bielawy Quarry, Radwa
nska and
monilifera pumpkin-mask Oxfordian) Couiavia region, Radwa nski
(Echinoidea) Poland (2005)
e test
Plegiocidaris Halloween Late Jurassic Poitou, France Nicolleau and
crucifera pumpkin-mask (Oxfordian) Vadet (1995)
(Echinoidea)
e test
H. intermedia Halloween Late Jurassic Chasseral-Kette, Mehl et al. (1991)
(Echinoidea) pumpkin-mask (middle Switzerland
e test Oxfordian)
?H. intermedia Halloween Late Jurassic (early Ma1ogoszcz, Holy Upper Oolite Radwa
nska and
(Echinoidea) pumpkin-mask Kimmeridgian) Cross Mountains, Member Radwa nski
e ?test Poland (2005)
P. crucifera e Late Jurassic Near Cze˛ stochowa, Radwa
nska and
(Echinoidea) (middle Poland Radwa nski
e spine Oxfordian) (2005)

255
(Continued)
Table 2 Echinoderms inferred to be infested by copepods resulting in cysts or swellingsdcont'd
Locality and Stratigraphic

256
Host taxon Name cyst Age country unit (if known) References
Echinoidea e Halloween Middle Jurassic Israel Matmor Borszcz et al. (2014)
spine pumpkin-mask (Callovian) Formation
Isocrinus Halloween Early Jurassic Autobahn A9, near Weinfurtner (1989)
tuberculatus pumpkin-mask (Sinemurian)* G€oggelsbuch near
(Crinoidea) e Allersberg,
stem Germany
Millericrinus Halloween Late Jurassic France De Loriol (1886)
horridus pumpkin-mask (Oxfordian)
(Crinoidea) e
stem
Collyrites dorsalis Castexia douvillei Middle Jurassic Marolles, Sarthe, Lambert (1927)
(Echinoidea) (late Callovian) France
e test
C. dorsalis C. douvillei Middle Jurassic Courgeou, Orne, Mercier (1936)

Adiël A. Klompmaker and Geoff A. Boxshall


(Echinoidea) (late Callovian) France
e test
C. dorsalis C. douvillei Middle Jurassic Mortagne-au- Radwanska and
(Echinoidea) (late Callovian) Perche, Orne, Radwa nski
e test France (2005)
Collyrites acuta C. douvillei Middle Jurassic Caucasus, Solovyev (1961) and
(Echinoidea) (¼Canceripustula (Callovian) Daghestan and Solovyev and
e test nocens) Turkmenistan Markov (2013)
Collyrites ellipticus C. douvillei Middle Jurassic Wrwsowa Knobby layer Radwanska and
(Echinoidea) (Callovian) (Cze˛ stochowa), Radwa nski
e test Polish Jura, (2005)
Poland
Fossil Crustaceans as Parasites and Hosts
C. ellipticus C. douvillei Middle Jurassic Picrzchno near Knobby layer Radwa nska and
(Echinoidea) (Callovian) Klobuck, Polish Radwa nski
e test Jura, Poland (2005)
C. ellipticus C. douvillei Middle Jurassic Zawiercie, Polish Knobby layer Radwa nska and
(Echinoidea) (Callovian) Jura, Poland Radwa nski
e test (2005)
Cladocyclus None e body fossil Early to Late Serra do Araripe, Santana Formation Cressey and
gardneri (fish) copepod Cretaceous Ceara, Brazil (nodules mostly Patterson (1973)
e gill Kabatarina (Aptian from Romualdo and Cressey and
chambers pattersoni eCenomanian)x Member) Boxshall (1989)
Ventalepis e Late Devonian Pavari site on Ketleri Formation Luksevics et al.
ketleriensis (Famennian) Ciecere River, (2009)
(fish) e scale Latvia
Holoptychius sp. e Late Devonian Pavari site on Ketleri Formation Luksevics et al.
(fish) e scale (Famennian) Ciecere River, (2009)
Latvia
Psammolepis e Middle Devonian J~
oksi (Kalmetum€agi) Gauja Formation Luksevics et al.
venyukovi (fish) (Givetian) locality on Piusa (2009)
e scale River, Estonia
* Infested crinoid species and its age determined using Simms (1989).
x
Stages derived using Martill (2007).

257
258 Adiël A. Klompmaker and Geoff A. Boxshall

actinopterygian fish, Cladocyclus gardneri, which were preserved in calcareous


nodules (Table 2; Figure 6). These originate primarily from the Romualdo
Member of the Santana Formation (Cretaceous: AptianeCenomanian) (see
Martill, 2007) of the Serra do Araripe, Ceara in northern Brazil (Cressey and
Paterson, 1973; Cressey and Boxshall, 1989). It is likely that their environ-
ment was marine. Kabatarina is classified in the family Dichelesthiidae, a fa-
mily that also contains two extant genera of fish parasites, both monotypic
(Boxshall and Halsey, 2004). Kabatarina is the sole fossil representative of
the order Siphonostomatoida.
Fish are by far the most commonly reported hosts for modern parasitic
copepods, with over 2000 species known, and they can have a marked
impact on the host. The feeding activity and attachment mechanisms of
ectoparasitic copepods can cause erosion of the host’s epidermis and stimu-
late tissue proliferation and fibrotic responses in affected host tissues
(Boxshall, 1977, 2005c). Lesions apparent on Devonian fish have been
tentatively attributed to infestation by various parasites, including copepods
(Table 2). Luksevics et al. (2009, p. 342), based on the similar size and di-
mensions of the round fossulae in scales and skeletal elements of Devonian
sarcopterygian and placoderm fishes, suggested an ‘interpretation of these
structures as being produced by parasites similar to copepod crustaceans’.
In particular, Luksevics et al. (2009) inferred that perforations of scales

Figure 6 The copepod Kabatarina pattersoni found in the fish Cladocyclus gardneri from
the Early Cretaceous of Brazil. (a) Lateral view of cephalothorax showing mouthparts
and anterior swimming legs. (b) Reconstruction of adult female ((a) from Cressey and
Boxshall (1989), pl. 1.2; (b) from Cressey and Patterson (1973), Figure 1, Science 180,
1283e1285, reprinted with permission from AAAS). Scale bars 100 mm.
Fossil Crustaceans as Parasites and Hosts 259

may result from the feeding activity of ectoparasitic crustaceans, such as co-
pepods. However, other causative agents are possible so the involvement of
copepods cannot be confirmed. Lesions in fishes can have diverse causes,
making it difficult to identify in fossil fishes without preserved pathogen
remains (Petit, 2010; Petit and Khalloufi, 2012).

3.1.4 Gall crabs (Cryptochiridae) in corals


Members of the Cryptochiridae inhabit corals, living in either pits or in true
galls created by modifying the coral (e.g. Abelson et al., 1991; Carricart-
Ganivet et al., 2004; Figure 7). Verrill (1867) was the first to call a crypto-
chirid species parasitic after studying specimens of Hapalocarcinus marsupialis
modifying its coral host to form galls. In contrast, Hiro (1937) referred to
Hapalocarcinus and Cryptochirus as commensal to their coral hosts. Subse-
quently, Kropp (1986) convincingly demonstrated that three cryptochirid
species (H. marsupialis, Utinomiella dimorpha and Cryptochirus coralliodytes
(¼ Favicola rugosa)) feed on coral mucus, debris and/or coral pieces instead
of filter feeding on particles from the water. Kropp (1986) had reservations
about calling them parasites, as he considered that mucus feeding by crypto-
chirids would not represent a metabolic drain on the corals. Johnsson et al.
(2006) concurred and suggested they should not be called parasites. The key
question is to what extent mucus feeding constitutes a sufficient negative

Figure 7 Modern crescentic cryptochirid crab dwelling of Troglocarcinus corallicola in


the coral host Colpophyllia natans from Curaçao (Modified from Van der Meij (2014),
Figure 1(b)). Fossil evidence of similar-shaped dwellings has been found recently.
260 Adiël A. Klompmaker and Geoff A. Boxshall

impact on the resources of the coral to justify calling these crabs parasitic,
which is typically not specified in definitions of parasitism. Simon-Blecher
and Achituv (1997) suggested that C. coralliodytes is a parasite of faviid corals
because specimens settle on a coral polyp resulting in the death of that polyp,
they inhibit coral growth rate (as shown quantitatively) and create depres-
sions in the coral skeleton around the pits. Simon-Blecher et al. (1999)
found that the same species encouraged algal and fungal growth in and
around the pit, and that the crabs feed on coral mucus, possibly leading to
an energy loss for the coral. They also speculated that mucus removed by
crabs could decrease the efficiency of feeding by the polyps. Based on qua-
litative observations, Mohammed and Yassien (2013) considered that the
gall-forming species H. marsupialis and Opecarcinus aurantius would have no
effect on coral growth. Carricart-Ganivet et al. (2004) analysed the gut con-
tents of Troglocarcinus corallicola and found green pigments, filamentous algae,
foraminifera and some suspended material, suggesting that this species ob-
tained its food at least partially from material deposited in the depression
around its cavity. Recently, Nogueira et al. (2014) showed a positive, signi-
ficant correlation between cryptochirid (Kroppcarcinus siderastreicola) cavity
size and size of the depression around the coral Siderastrea stellata, high-
lighting the negative effect of that cryptochirid on coral growth. Recent
articles refer to cryptochirids by the all-inclusive term obligate symbionts
(e.g. Badar o et al., 2012; Van der Meij, 2014, 2015; Van der Meij and
Schubart, 2014; Canario et al., 2015), but Wei et al. (2013) mentioned
both obligate symbionts and parasites. Obvious benefits for the coral are
unknown. In conclusion, there is continuing debate as to whether crypto-
chirids are commensal or parasitic on their host corals, but the argument for
parasitism is strongest for C. coralliodytes. The fact that multiple species feed
on coral mucus and can impact coral growth indicate that at least some
cryptochirids can be considered as coral parasites.
Their fossil record was unknown until very recently, when Portell and
Klompmaker (2014) reported on characteristic crescentic domiciles attri-
buted to cryptochirids in Pleistocene corals from Florida. Subsequently,
De Angeli and Ceccon (2015) claimed the first cryptochirid body fossil,
Montemagrechirus tethysianus, from the Eocene (Ypresian) of Italy. The small
size (w5 mm) and the environment (coral reef) match the attributes of mo-
dern cryptochirids. The overall shape (longer than wide) of the carapace also
fits the Cryptochiridae, but several major differences are evident in the fron-
tal part (the posterior part exhibits few characters). First, the rostrum contains
two pronounced spines in Montemagrechirus that are not present in any of the
Fossil Crustaceans as Parasites and Hosts 261

52 currently known modern species. Moreover, the orbits of the fossil spe-
cies are directed anterolaterally, which is highly unusual for modern crypto-
chirids (only Pseudocryptochirus viridis and two deep water species of
Cecidocarcinus show a somewhat similar orbital position, 5.7%). Of further
note is the well-calcified shell, which is why Montemagrechirus was preserved.
The shell of modern cryptochirids is usually soft and can even be transparent
(Utinomi, 1944; Guinot et al., 2013, for H. marsupialis) or the posterior part
of the carapace is soft (Potts, 1915, for Cryptochirus), although Utinomi
(1944) mentioned that the carapace of Cryptochirus is rather hard. The some-
what transparent nature of cryptochirid carapaces may be observed also in
Badar o et al. (2012) and Van der Meij and Schubart (2014). Portell and
Klompmaker (2014) did not report any remains of cryptochirid shell associ-
ated with the domiciles and no other fossil cryptochirid body fossils have
been found to date, consistent with the relatively soft nature of the carapace.
The anterolateral position of the orbits in combination with the narrowing
of the carapace posteriorly in Montemagrechirus suggests that eyes would have
protruded anterolaterally from the carapace, which may not be most suitable
condition to inhabit a pit or tunnel (indeed, eyes and orbits are typically
directed forward in cryptochirids). This morphology would argue against
parasitism in corals together with the well-calcified shell that would not
be needed for a truly parasitic form living in a pit or gall. Therefore, we
do not consider this taxon further. Whether Montemagrechirus represents an
early cryptochirid (perhaps prior to becoming parasitic) or should be classi-
fied in a different family should be addressed anew.

3.1.5 Pentastomida
Molecular evidence consistently places the Pentastomida as sister group to
the Branchiura, and these two taxa together are referred to as the Ichthyos-
traca which, together with the Mystacocarida and Ostracoda, forms the Oli-
gostracan branch of the Pancrustacea (e.g. Regier et al., 2010; Oakley et al.,
2013; Giribet and Edgecombe, 2013). However, controversy still surrounds
the classification of the Pentastomida, since fossil and some morphological
data have been interpreted as evidence that they represent stem-lineage de-
rivatives of the Euarthropoda and, therefore, cannot be considered crusta-
ceans. Waloszek et al. (2006) concluded that the phylogenetic position of
the Pentastomida remained unresolved, but Castellani et al. (2011) consi-
dered their derivation from the Euarthropodan stem-lineage to be the
most plausible hypothesis. As molecular phylogenetics has moved away
from target-gene approaches towards phylogenomics and transcriptomics
262 Adiël A. Klompmaker and Geoff A. Boxshall

(see Giribet and Edgecombe, 2013), analyses of the flood of new sequence
data have continued to support a sister relationship between the Pentasto-
mida and the Branchiura within the Oligostraca (e.g. Regier et al., 2010;
Sanders and Lee, 2010; Oakley et al., 2013). There is not yet, however,
any stable estimate of divergence times between them: Sanders and Lee
(2010), using data from five genes, estimated a divergence time of 519 Ma
(but with confidence limits of 292e616 Ma), whereas Oakley et al.
(2013) arrived at a maximum estimate of 424 Ma for this split using new
transcriptome data sets plus existing nuclear genome, mitochondrial
genome, EST and ribosomal DNA data. The Oakley et al. (2013) estimate
of divergence time for the Pentastomida and Branchiura conflicts with the
suggested presence of pentastomids in the Cambrian.
Regardless of their correct taxonomic placement, we address parasitism of
this group here. Modern pentastomids, or tongue worms, are obligate para-
sites at all stages of their life cycle (B€
ockeler, 2005). Their definitive hosts are
frequently snakes, but also amphibians, turtles, crocodilians, lizards, birds and
mammals including humans; many of these same taxa, as well as freshwater
and marine fishes and insects, also serve as intermediate hosts (B€ ockeler,
2005; Poore, 2012; Christoffersen and De Assis, 2013). Modern pentastomids
are bloodsuckers (sea birds, reptiles) or feed on mucus and sloughed cells
(mammals) (B€ ockeler, 2005). Currently, 144 species and subspecies are
known (Christoffersen and De Assis, 2013); Poore (2012) listed 124 species.
From the fossil record, only 10 named species are known (Table 3;
Figure 8), all of them from the early Palaeozoic and most are based on phos-
phatized specimens. Andres (1989) was the first to suggest the resemblance of
fossil specimens to pentastomids based on Early Ordovician specimens from

Oland (Sweden), but Walossek and M€ uller (1994), Walossek et al. (1994),
Waloszek et al. (2006) and Castellani et al. (2011) described all known
CambrianeOrdovician species thus far, all presumably representing larvae.
Most fossil species are stratigraphically confined to Upper CambrianeLower
Ordovician strata (Table 3). Recently, putative adult pentastomids from the
Silurian Herefordshire Lagerst€atte were reported to be attached to ostra-
cods: such ectoparasitism is unknown in modern pentastomids (Siveter
et al., 2015). A targeted search for specimens in Palaeozoic or Mesozoic
fine-grained limestone deposits of deep-water origin should, eventually,
yield additional species. Such Konservat-Lagerst€atten, in which phosphati-
zation can take place, have yielded most of the species known thus far
(Walossek and M€ uller, 1994; Walossek et al., 1994; see Maas et al., 2006,
for discussion on preservation). Specimens may have been overlooked
Table 3 The species of Pentastomida known from the fossil record
Species Age Locality and country Stratigraphic unit References

Fossil Crustaceans as Parasites and Hosts


Aengapentastomum Late CambrianeEarly Stora Backor quarry, Ceratopyge Waloszek et al. (2006)
andresi Ordovician V€asterg€
otland, Sweden Limestone
(late Tremadocian) (reworked)
Boeckelericambria Late Cambrian Roadcut between Zone 5C Walossek and
pelturae (late Furongian) Haggården and M€uller (1994)
Marieberg, Kinnekulle,
V€asterg€
otland, Sweden
Haffnericambria Late Cambrian Trolmen at the Kinnekulle, Zone 5C Walossek and
trolmeniensis (late Furongian) V€asterg€
otland, Sweden M€uller (1994)
Heymonsicambria Late Cambrian Kinnekulle area, Zone 5 Castellani et al. (2011)
ahlgreni (late Furongian) V€asterg€
otland, Sweden
Heymonsicambria Late Cambrian Trolmen at the Kinnekulle, Zone 5C Walossek and
gossmannae (late Furongian) V€asterg€
otland, Sweden M€uller (1994)
Heymonsicambria Late Cambrian Trolmen at the Kinnekulle, Zone 5 Walossek and
kinnekullensis (late Furongian) V€asterg€
otland, Sweden M€uller (1994)
Heymonsicambria Late CambrianeEarly Stora Backor quarry, Ceratopyge Walossek and
repetskii Ordovician (late V€asterg€
otland, Sweden Limestone M€uller (1994)
Tremadocian) (?reworked)
Heymonsicambria Late Cambrian Trolmen at the Kinnekulle, Zone 5C Walossek and
scandica (late Furongian) V€asterg€
otland, Sweden M€uller (1994)
Heymonsicambria CambrianeOrdovician Green Point, Martin Point Member, Walossek et al. (1994)
taylori boundary Newfoundland, Canada Green Point
Formation
Invavita piratica* mid-Silurian (Wenlock, Herefordshire, England Volcanoclastic deposit, Siveter et al. (2015)
late Sheinwoodian to Wenlock Series
early Homerian)

263
* Putative pentastomid.
264 Adiël A. Klompmaker and Geoff A. Boxshall

Figure 8 Larvae from fossil pentastomids. (a) Lateral view of Heymonsicambria scandica
from the Late Cambrian (late Furongian) of V€astergo €tland, Sweden. (b) Ventral view of
Heymonsicambria taylori from the Late CambrianeEarly Ordovocian of Canada. (c)
Ventrolateral view of Boeckelericambria pelturae from the Late Cambrian (late Furon-
gian) of V€astergo €tland, Sweden. Scale bars 50 mm. ((a) from Walossek and M€ uller
(1994), Figure 4(a), reproduced by permission of The Royal Society of Edinburgh and Dieter
Waloszek from Transactions of the Royal Society of Edinburgh: Earth Sciences 85, 1e37; (b)
from Walossek et al. (1994), pl. 1.3).

because of their small size: the largest described CambrianeOrdovician


specimen has a length of 780 mm (the Canadian species), making them diffi-
cult to recognize with the naked eye, although the suggested Silurian spe-
cimens range from 1 to almost 4 mm in length, mainly due to a long trunk
(Siveter et al., 2015). Moreover, their generally soft bodies except for the
cuticle do not fossilize easily.
Surprisingly, all known fossil species are found in marine deposits,
whereas modern species are mostly known from terrestrial animals. Given
their very similar morphology to today’s representatives (evolutionary stasis),
Walossek and M€ uller (1994) suggested that modern representatives must
have derived from marine ancestors instead of from terrestrial arthropods.
early Palaeozoic specimens were most likely parasitic and Walossek and
M€ uller (1994) and Walossek et al. (1994) inferred that the Cambriane
Ordovician ones may have lived internally in cavities such as their host’s
gill chambers, as deduced from the limb morphology. If correct, the larvae
were already highly adapted to their hosts in the earliest Palaeozoic
Fossil Crustaceans as Parasites and Hosts 265

(Waloszek et al., 2006). Walossek and M€ uller (1994) noted that all
CambrianeOrdovician pentastomids were associated with conodonts.
Thus, it could be speculated that these early vertebrates were hosts to penta-
stomids (compare Sanders and Lee, 2010; De Baets et al., 2015). Considering
the small size of early Palaeozoic pentastomids, which are interpreted as adults
by Sanders and Lee (2010; but compare Castellani et al., 2011 for a different
view) and resemblance to larvae of extant pentastomids that infect interme-
diate hosts such as fish, it has been suggested by these authors that the small
Palaeozoic forms confined their entire life cycle to small fish-like vertebrates
present around that time (Sanders and Lee, 2010). They may have transi-
tioned to a more continental habitat along with their hosts in the Late Devo-
nian, when the amphibians arose from lobe-finned fish (e.g. Daeschler et al.,
2006), giving rise to reptiles later in the Palaeozoic. The discovery of Silurian
pentastomids on marine ostracods suggests that early pentastomids used
invertebrate taxa (arthropods) as hosts (Siveter et al., 2015). This does, how-
ever, not preclude a mid-to-late Palaeozoic terrestrialization of pentastomids
during the vertebrate radiation on land, as Siveter et al. (2015) also pointed
out. Alternatively, an invertebrate route onto land cannot be entirely
excluded either. Further pentastomid fossil evidence, preferably still associ-
ated with their host, is needed to test these speculative hypotheses.

3.2 Equivocal fossil evidence


3.2.1 Barnacle borings attributed to Acrothoracica in marine
invertebrates
In their overview of the fossil record of parasitism in marine invertebrates,
Baumiller and Gahn (2002, Table 1) listed several instances of acrothoracican
barnacle borings in Jurassic and Cretaceous belemnites (Seilacher, 1968),
Devonian platyceratid gastropods (Baird et al., 1990) and Devonian brachio-
pods (Rodriguez and Gutschick, 1977). Boucot and Poinar (2010)
mentioned many more examples of acrothoracican borings in Palaeo-
zoiceCenozoic marine invertebrates. Taylor and Wilson (2003) even
mentioned the presence of such borings in gastropods from the Ordovician,
but did not refer to them as parasites. Baumiller and Gahn’s (2002) claim of
parasitism appears ambiguous. For example, Tomlinson (1969, p. 11) stated
that ‘the (acrothoracican) cirriped can, at most, be considered a modest shell-
weakening pest, and in general does little if any harm to the host. All species
of the order collect food without taking from or giving anything of value to
the host’. Furthermore, Baird et al. (1990, p. 233) inferred ‘that the relation-
ship between the barnacles and the host gastropods was one of obligate
266 Adiël A. Klompmaker and Geoff A. Boxshall

commensalism, perhaps bordering on parasitism’. Seilacher (1969) and


Ba1uk and Radwa nski (1991) further discussed the commensal nature of
acrothoracican barnacle borings in various fossil invertebrates. Although
difficulties exist to identify commensalism in the fossil record (see Zapalski,
2011), commensalism appears the best descriptor of this symbiotic relation-
ship, in accord with Patton (1967). Therefore, it is not considered further
here.

3.2.2 Barnacles (Pyrgomatidae) in corals


Santos et al. (2012) recently described evidence for parasitism in the middle
Miocene coral Tarbellastrea reussiana by the barnacle Ceratoconcha aff. C. cos-
tata (Figure 9). The coral provided a habitat and protection from predators,
and a filter feeding location. Negative effects on the host included inhibition
of skeletal growth, modification of coral wall geometry and the secretion of
additional material in response to stress. Santos et al. (2012) indicated that
these barnacles do not feed on coral tissue, but instead use their thoracic cirri
for filter feeding purposes. Probably for this reason, Malay and Michonneau
(2014, Table 1) classified extant species of Ceratoconcha as planktotrophic
rather than parasitic. The barnacle does undoubtedly hijack part of the
food of the coral, especially for the polyps surrounding the barnacles, but
it is not nutritionally dependent on the corals themselves. Therefore, we

Figure 9 Several cross-sections of specimens of the pyrgomatid barnacle Ceratoconcha


aff. C. costata next to an example of the trace fossil Imbutichnus costatum (arrow) resul-
ting from the overgrowth of the coral Tarbellastrea reussiana of this barnacle from the
middle Miocene (LanghianeSerravalian) of Portugal. Scale bar 5 mm. (Modified from
Santos et al. (2012), Figure 3(d))
Fossil Crustaceans as Parasites and Hosts 267

consider that this relationship is better described as commensalism. Members


of this genus are known from the Oligocene to the present (Ross and
Newman, 2002), although the Oligocene occurrence was based on a per-
sonal communication only. Santos et al. (2012) indicated that pyrgomatids
were associated with corals at least since the Miocene, while they may
have appeared in the early Cenozoic, based on molecular analyses (Tsang
et al., 2014). Savignium, Pyrgoma, Cantellius and Nobia may represent an in-
termediate step from filter feeding to full parasitism. After analysing carbon
isotopic composition of these barnacles and their coral hosts, Achituv et al.
(1997) suggested that these taxa may depend on the host as a source of food
to a great extent, which was supported by the presence of coral tissue in the
stomach contents of one species. However, their cirral nets are probably still
used for filter feeding and they may have fed on expelled zooxanthellae as
well (Achituv et al., 1997). Although Ceratoconcha and the other taxa are
not widely accepted to be parasitic, there is a group within the Pyrgomatidae
that is accepted as such. Ross and Newmann (1995) erected the Hoekiini
tribe for species feeding exclusively on tissue of the coral Hydnophora with
their biting trophi (mouthparts), while the aberrant cirri do not serve to cap-
ture food. Ross and Newman (1969) suggested that the retention of vestigial
appendages in Hoekia monticulariae could mean that its coral-eating habit has
evolved recently, or that the juveniles still use them. They speculated that
the parasitic relationship developed within the last 10 Ma. A late Cenozoic
origin is corroborated by Malay and Michonneau (2014), who suggested
that hoekiines evolved quite recently given that this tribe represented a rela-
tively short branch in their phylogeny. Their fossil record is non-existent
thus far. Their relatively thin and fragile wall will not be easily preserved,
but the calcareous portion of the basis with an amoeboid outline has a better
preservation potential (Ross and Newman, 2002). Moreover, it may be
more readily recognized given the shape.

3.2.3 Isopods (Cymothooidea) in fishes and squids


Boucot and Poinar (2010) cited Bowman (1971) describing a case of possible
parasitism. Bowman (1971, p. 540) documented the isopod Palaega lamnae
from the Upper Cretaceous (Coniacian) Lower Austin Chalk of Texas
(USA) and tentatively noted that ‘the isopod could have been associated
with the Lamna [shark] either as a parasite or as a scavenger on the corpse,
but there is no evidence to support either role except for their occurrence
together’. Wieder and Feldmann (1992) questionably included this isopod
in Palaega until more complete material is discovered and concurred with
268 Adiël A. Klompmaker and Geoff A. Boxshall

the note of Bowman (1971). If placement within the Cirolanidae proves


correct, then it could be inferred that P. lamnae is a scavenger since modern
cirolanids are free-living scavengers and predators (Smit et al., 2014). The
fossil record of Cirolanidae is relatively well known (e.g. Wieder and
Feldmann, 1992; Hyzný et al., 2013) and provides some evidence of
scavenging. For example, fossil cirolanids were found within the carcass
of an actinopterygian fish from the mid-Cretaceous (Albian) of Australia
(Wilson et al., 2011), suggesting a scavenging life mode. Another inte-
resting observation is the occurrence of Palaega pisana in association with
a Pliocene ‘whale fall community’, which would have provided ample
feeding opportunities for predators and scavengers such as Palaega (Pasini
and Garassino, 2012a). A similar claim was made by Pasini and Garassino
(2012b) for Palaega sp. and P. steatopigia from the Pliocene. Claims of para-
sitic cirolanid species from the fossil record lack evidence (Palaega williamso-
nensis: Rathbun, 1935; Cirolana enigma: Wieder and Feldmann, 1992) with
the possible exception of Polz et al. (2006), who suggested that the Late
Jurassic (late Kimmeridgian) Palaega nusplingensis may have been parasitic
on account of its attachment to the ventral side of teuthoid squid
(Figure 10). However, they could not exclude the possibility that the
specimen was feeding on the squid carcass. The same applies to at least
20 cymothooids attached to a water bug from the Late Jurassic (Tithonian)
of Solnhofen, Germany, where scavenging was deemed more likely (Polz,
2004). In summary, there is no convincing evidence of parasitism by fossil
Cirolanidae including Bowman’s P. lamnae.

Figure 10 Holotype of Palaega nusplingensis from the Late Jurassic (late Kimmeridgian)
of Germany. This specimen is mentioned to be attached to the ventral side of a teu-
thoid squid. Scale bar 1 mm (Modified from Polz et al. (2006), pl. 3.2).
Fossil Crustaceans as Parasites and Hosts 269

Other modern members of the superfamily Cymothooidea are parasitic


such as Cymothoidae, but their fossil record is non-existent (Smit et al.,
2014). Etter (2014, p. 939) considered that there is no definite fossil record
of predatory or parasitic Aegidae, Tridentellidae, Corallanidae and
Cymothoidae. The first three families are mentioned to be commensal to
and/or micropredators of modern fish (Smit et al., 2014). Unless members
of these families and the Cirolanidae changed their lifestyle throughout
evolutionary history from parasitic to non-parasitic, their presence in the
fossil record does not suggest parasitism. To our knowledge, members of
the modern Cymothoidae do not leave distinct traces that would help to
identify them as parasites in the fossil record.

3.2.4 Crabs (Trapeziidae) and corals


Boucot and Poinar (2010, p. 36) listed these crabs as being potentially para-
sitic to corals, feeding on coral mucus. They were classified as obligate ecto-
parasites by Knudsen (1967). Trapeziid crabs are known to extend back to
the Eocene (Schweitzer, 2005; Beschin et al., 2007; De Angeli and Ceccon,
2013). However, their relationship is better described as mutualism (e.g.
Stimson, 1990; Schweitzer, 2005; McKeon and Moore, 2014) because
corals derive benefit as these crabs remove material from and defend the
corals from starfish predators (e.g. Glynn, 1983a,b). Therefore, this relation-
ship is not addressed further here.

3.3 Modern evidence only


3.3.1 Copepods
Nearly half of all known marine copepod species live in close symbiotic as-
sociation with other organisms. Although in many cases the precise nature of
the association between the copepod and its host has not been elucidated,
copepods are known to be parasitic on hosts representing virtually every
phylum of aquatic metazoans. Boxshall and Halsey (2004) noted records
of associated copepods from Porifera, Cnidaria, Platyhelminthes, Nemertea,
Sipunculida, Echiura, Annelida, Mollusca, Arthropoda, Bryozoa, Phoro-
nida, Brachiopoda, Echinodermata, Hemichordata and Chordata (including
urochordates as well as vertebrates). The largest copepods (body length of up
to 80 mm) are parasites of cetaceans and large fishes, but most are small (body
length 1.0e2.0 mm) and, given their lack of a calcified cuticle, have limited
fossilization potential. Parasitic copepods are known to cause visible lesions,
such as swellings, cysts or galls on certain hosts, but such macrolesions are
relatively rare. In the majority of species, the impact on the host is more
270 Adiël A. Klompmaker and Geoff A. Boxshall

subtle and highly unlikely to be detected in a fossil. Cysts and galls attributed
to infestation by parasitic copepods are known for some modern hard-
bodied host taxa such as scleractinian corals (Zibrowius, 1981; Dojiri,
1988; Buhl-Mortensen and Mortensen, 2004; Kim and Yamashiro, 2007),
echinoids (Stock, 1968, 1981, see also Section 3.1.2) and crustaceans
(Boxshall and Lincoln, 1983a), but not from others, such as the Mollusca.
No trace fossil attributed to a parasitic copepod has yet been reported
from soft-bodied hosts, such as polychaete worms or tunicates because of
the host’s low preservation potential.

3.3.2 Tantulocarida
About 35 species of tantulocaridans are currently known, either from para-
sitic stages attached to marine crustaceans, or from their free-living infective
larvae collected from the meiofauna in marine sediments from shallow
coastal waters to the deep-sea (Mohrbeck et al., 2010). Larvae are typically
about 100 mm in length. Whereas asexual adult females can attain a
maximum size of about 1.4 mm, sexual adults of both sexes are less than
1 mm in length (Boxshall and Lincoln, 1987; Huys et al., 1993). Their small
size and lack of a calcified cuticle indicate a poor fossilization potential.

3.3.3 Branchiura
Branchiuran fish lice are all external parasites of fishes (for example Figure 11),
with the exception of Dolops ranarum that uses freshwater amphibians as hosts.
Three genera, Chonopeltis, Dolops and Dipteropeltis, are exclusively freshwater
in distribution, while the largest genus, Argulus, occurs on both marine and
freshwater fishes. With the exception of Dolops that attaches by means of

Figure 11 Two adult females of Argulus japonicus parasitic on a goldfish showing a


typical lesion with a surface swelling and haemorrhaging.
Fossil Crustaceans as Parasites and Hosts 271

paired clawed limbs, branchiurans typically attach to their host using paired
suckers derived from the maxillules (Gresty et al., 1993). They feed while
on the host, but adult females detach in order to lay eggs on submerged
hard substrates. In Argulus, the eggs hatch directly into an infective larva
equipped with cephalic swimming appendages that atrophy in subsequent
parasitic stages. Once erroneously treated as a subgroup of the Copepoda,
the Branchiura is now recognized as a distinct subclass of Oligostraca. No fos-
sils are known, but the estimated suggested sister-group relationship of Bran-
chiura with the Pentastomida (Sanders and Lee, 2010; Regier et al., 2010;
Oakley et al., 2013) suggests a Cambrian origin (see Section 3.1.5). The
feeding activity of branchiurans on the epidermis of their hosts can cause le-
sions including epidermal erosion, localized swelling and haemorrhaging
(Figure 11), but such traces, even if fossilized, are very general and would
be hard to attribute to a specific parasite taxon.

3.3.4 Ostracoda
Ostracods are a diverse modern group with a rich and extensive fossil record,
but the existence of parasitic forms is equivocal. A few ostracods live in close
symbiotic associations. Members of the podocopan family Endocytheridae,
for example, inhabit the burrows of freshwater decapods, but are probably
commensals according to Hobbs and Peters (1977), and will not be treated
further. It has also been argued that the myodocopan cypridinids Vargula
parasitica and Sheina orri are parasitic on the gills and in the nasal cavities of
various elasmobranch and actinopterygian fishes (e.g. Harding, 1966), but
Cohen (1983) considered that no myodocopids were truly parasitic and
she suggested that these ostracods were scavengers on injured or unhealthy
fish. Bennett et al. (1997) examined S. orri on the gills of a shark and docu-
mented local distortion of gill lamellae accompanied by tissue damage at all
sites of ostracod attachment, but they were unable to confirm that the ostra-
cods had ingested shark tissue. The ostracods were typically found in small
pockets between adjacent gill filaments. Bennett et al. (1997) concluded
that S. orri was parasitic, but such soft tissue features would have a low fossi-
lization potential.

3.3.5 Facetotecta
The adults of the Facetotecta are as yet unknown, but the free-swimming
larval stages are widely distributed in coastal marine waters. Facetotectan
larvae, the so-called Y-larvae, have their body enclosed within a bivalved
carapace (Glenner et al., 2008), but it is not calcified and no fossils are known
as a result. The hosts of the presumed parasitic adults are unknown.
272 Adiël A. Klompmaker and Geoff A. Boxshall

3.3.6 Thoracica
A scattered assortment of pedunculate thoracican barnacles has switched
from their ancestral suspension feeding to a parasitic mode of life. Anelasma
squalicola is the sole representative of the family Anelasmatidae and is typi-
cally found embedded in the skin of deep-sea sharks behind the dorsal fin
(Rees et al., 2014; Leung, 2014). A recent molecular clock study (Rees
et al., 2014) places the split of Anelasma from Capitulum at 126.5 Ma. Rhizo-
lepas species are parasitic on marine polychaete hosts (Day, 1939). Both
Rhizolepas and Anelasma have an atrophied suspension-feeding apparatus
and depend, at least in part, on nutrients absorbed from their host via an
embedded rootlet system. Heteralepadomorph barnacles typically live in as-
sociation with hosts, many inhabiting the gills of decapods, and they typi-
cally have reduced or absent valves, so their fossilization potential is
presumably lower than for typical barnacles. Most heteralepadomorph bar-
nacles are likely commensal, but Koleolepas species participate in a tripartite
symbiosis, living on gastropod shells inhabited by hermit crabs and carrying
sea anemones. They are typically attached beneath the pedal disc of the
anemone and feed by cropping its tentacles (Yusa and Yamato, 1999).
The shell plates are reduced or even absent in these thoracicans and their
fossilization potential is presumably lower than typical sessile or stalked
barnacles.

3.3.7 Malacostraca
The whale lice (Cyamidae) are dorsoventrally flattened amphipods found on
various cetacean hosts. Cyamids were traditionally treated as a wholly para-
sitic infraorder of the amphipod suborder Caprellidea (cf. Martin and Davis,
2001), but are now treated only as a family of parasites contained within a
much large clade (infraorder Corophiida) of free-living amphipods that
are predominantly detritivores (Myers and Lowry, 2003; Lowry and Myers,
2013). Whale lice cannot swim and lack any planktonic dispersal phase in
their life cycle; it is therefore presumed that infestation spreads only during
intraspecific bodily contact between host individuals.
Gnathiid isopods have free-living, non-feeding adults that inhabit ca-
vities in muddy sediments, in dead barnacles or in sponges, but the juveniles,
praniza larvae, feed on the blood of elasmobranch and actinopterygian fishes.
Engorged praniza larvae drop off their hosts between blood meals, rather as a
terrestrial tick. They have a very distinctive appearance, but their thin non-
calcified cuticle, which allows for their gorging feeding behaviour, is likely
to limit their fossilization potential.
Fossil Crustaceans as Parasites and Hosts 273

4. OVERVIEW FOSSIL EVIDENCE AND FUTURE


RESEARCH
Fossil evidence of parasitism in crustaceans is confined primarily to
decapod crustaceans (Figure 12). Swellings in decapod crustaceans caused
by infestation by isopods are by far the best represented evidence of para-
sitism in or by crustaceans. Ninety-three infested species and hundreds of
infested specimens have been found (e.g. Wienberg Rasmussen et al.,
2008; Klompmaker et al., 2014; herein). Nearly every other example of
parasitism is represented by only few specimens and/or is known from a
limited confirmed stratigraphic range (black in Figure 12). The stratigraphic
range of many other examples can be greatly extended because of their
modern existence, assuming that parasitism occurred in the time in between
the fossil and modern occurrences. This applies especially for examples of
parasitism based on body fossils. Platyhelminth hooks in crustaceans and
the inferred Devonian occurrence of copepods on fish are not without
doubt, however (see above). Excellent preservation certainly has helped
in the case of Palaeozoic pentastomids and the Cretaceous fish parasite,
the copepod Kabatarina. These examples have in common that the evidence
for parasitism is small in size compared to the other examples in Figure 12.
The length of the only copepod body fossil in a fish is w1.0 mm, the length
of larval pentastomids is 0.78 mm and platyhelminth hooks are only
0.4 mm long (Cressey and Boxshall, 1989; Walossek et al., 1994; Upe-
niece, 2001). This small size explains the spotty occurrence of this type of
parasitism in combination with rare circumstances allowing preservation
of such fossils. The lack of targeted research may also be a factor.
Many opportunities for additional research exist. Even though swellings
in decapod crustaceans are the most common evidence of parasitism
involving crustaceans, examples of K. crusta are as yet not documented for
many stratigraphic stages and even some epochs. Moreover, very limited
quantitative data exist per locality, highlighting the need for additional
research by systematically collecting all available specimens. Whether abun-
dant species are more heavily infested than rare species, as was suggested by
Klompmaker et al. (2014) for the Koskobilo (Spain) locality, should be
investigated further by focusing on a locality where specimens exhibiting
K. crusta are common. The discovery of additional infested taxa will help
to refine and re-evaluate the trends shown in Figure 2. Less quantitative,
but equally useful, additional evidence can be gained from the reporting
of new examples of parasitism discussed here given the spotty distribution
274 Adiël A. Klompmaker and Geoff A. Boxshall
Figure 12 Stratigraphic ranges of examples of parasitism in or by crustaceans as recognized herein. Equivocal fossil evidence (3.2) is not

Fossil Crustaceans as Parasites and Hosts


included. Grey bars represent probable occurrences based on modern or bracketing fossil occurrences in that host. The resolution used
for determining first and last occurrences is the stage level if known (see text and tables for details). Horizontal stippled lines mark boun-
daries between the Phanerozoic eras. A question mark refers to uncertain evidence of parasitism of an example that has confirmed occur-
rences. Categories in bold, italic font are based on body fossil evidence of parasites, whereas the rest is based on structures (swellings, cysts,
galls, domiciles and intersex evidence) induced by the inferred parasite. The Devonian occurrences of copepods in fish are based on round
traces on scales instead of copepod body fossils as in the Cretaceous. Timescale (left part) produced with TSCreator 6.3 (http://www.
tscreator.org).

275
276 Adiël A. Klompmaker and Geoff A. Boxshall

of confirmed occurrences shown in Figure 12. Systematic surveying of exist-


ing collections and the collection of additional material in the field are likely
to yield results. It is conceivable that the stratigraphic ranges of many exam-
ples could be expanded considerably. This would help to pinpoint the
earliest occurrence of parasitism for each group and may also serve as calibra-
tion points for molecular studies of particular parasite clades. Furthermore,
not much is known about the prevalence of parasitism in nearly every
example mentioned in Figure 12 except for isopod infestations in decapods.
Such data may help to evaluate the commonness of parasitism and its
possible effect on the evolution of the infested group.
A strategy to increase the number of fossil examples of parasitism
involving crustaceans is to identify modern traces of parasitism that do not
yet have a fossil record. Many modern parasites stimulate localized tissue res-
ponses in their hosts and some of the examples identified herein involve in-
ternal skeletal elements or hard external body coverings that have potential
for fossilization and could be the focus of targeted research. We recognize
that size is an issue so special emphasis should be placed on submillimetre
and millimetre scale features. Other traces of parasitism are rather generic,
local small pits, and will remain difficult to attribute to a particular parasite
taxon. It is apparent from Figure 12 that there is a long history of parasitism
involving crustaceans. Divergence times indicating the putative origin of
parasitism are available for some crustaceans, for example, the thoracican
barnacles (Rees et al., 2014; Tsang et al., 2014), but similar studies are
lacking for other large taxa such as the copepods. There is a continuing
need for such molecular studies to complement palaeontological research
focused on fossil parasites and their traces.

ACKNOWLEDGEMENTS
We are very grateful to Kenneth De Baets and Tim Littlewood for the invitation to
contribute to this volume, for their useful comments, and the former also for useful literature
suggestions. We also thank John Jagt and Andrei Solovjev for providing useful literature;
G€unter Schweigert for useful literature and Figure 5(e), Barry van Bakel for discussion about
the specific placement of the Goniodromites specimen; Dieter Waloszek for Figure 8(a) and (c);
Sten Jakobsen for information on Echinocorys from Denmark; Rodney Feldmann for the sug-
gestion to work on this paper; Andreas Kroh for museum numbers for the Ernstbrunn spe-
cimens; Jesper Milan for the loan of a specimen from the Geomuseum Faxe; Roger Portell,
Sean Roberts and Alex Kittle for assistance with UF collections; René Fraaije for a museum
number of Oertijdmuseum De Groene Poort; Sancia van der Meij for Figure 6; Cristina
Robins for reading and commenting on part of the text. Mark Wilson and Joachim Haug
also kindly commented on earlier draft of this manuscript; their comments are much appre-
ciated. Our gratitude goes to all these persons. Furthermore, the following publishers,
Fossil Crustaceans as Parasites and Hosts 277

organisations, journals and persons are acknowledged for permission to reproduce various
images: PLOS ONE, The Paleontological Society, Springer, AAAS, Acta Geologica Polo-
nica, Contributions to Zoology, Micro Press, Rosenstiel School of Marine and Atmospheric
Science of the University of Miami, Dieter Waloszek, NRC Research Press, The Royal
Society of Edinburgh, The Palaeontological Association and Staatliches Museum f€
ur Natur-
kunde. This work was in part supported by the Jon L. and Beverly A. Thompson Endow-
ment Fund, an Arthur James Boucot Research Grant (Paleontological Society) and a
COCARDE Workshop Grant (ESF) to A.A.K. This is University of Florida Contribution
to Paleobiology 687.

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CHAPTER SEVEN

A Prejudiced Review of Ancient


Parasites and Their Host
Echinoderms: CSI Fossil Record
or Just an Excuse for
Speculation?
Stephen K. Donovan
Department of Geology, Naturalis Biodiversity Center, Leiden, The Netherlands
E-mail: Steve.Donovan@naturalis.nl

Contents
1. Introduction 292
2. Interpretations and Confidence 294
2.1 Problems of interpretation 295
2.2 Limits of confidence 297
3. Some Examples 298
3.1 A coralecrinoid association from the Mississippian 299
3.2 A growth deformity in a Mississippian crinoid 302
3.3 Epizoobionts infesting a Mississippian crinoid 304
3.4 Platyceratid gastropods infesting Upper Palaeozoic crinoids 306
3.5 Site selectivity of pits in echinoid tests, Upper Cretaceous 313
4. Discussion 319
5. Conclusions 323
Acknowledgements 323
References 323

Abstract
Recognizing the presence of a parasite and identifying it is a relatively straightforward
task for the twenty-first century parasitologist. Not so the pursuit of ancient parasites in
fossil organisms, a much more difficult proposition. Herein, Boucot’s seven-tiered
scheme of reliability classes is applied as a measure of confidence of the recognition
of putative parasitism in two echinoderm classes, Upper Palaeozoic crinoids and a
Cretaceous echinoid (high confidence is 1, low confidence 7). Of the five examples,
the parasitic(?) organism is preserved in only two of them. A zaphrentoid coral on
the camerate crinoid Amphoracrinus may have robbed food from the arms (Category
1 or 2B). A pit in what appears to be a carefully selected site on the disparid crinoid
Synbathocrinus is associated with a growth deformity of the cup (Category 4). Multiple
Advances in Parasitology, Volume 90
© 2015 Elsevier Ltd.
j
ISSN 0065-308X
http://dx.doi.org/10.1016/bs.apar.2015.05.003 All rights reserved. 291
292 Stephen K. Donovan

pits in an Amphoracrinus theca are also associated with a deformed cup, but it is more
difficult to interpret (Category 4 or 7). Some specimens of the camerate crinoid
Neoplatycrinites have circular grooves or depressions posteriorly, presumably produced
by coprophagic/parasitic platyceratid gastropods (Category 1). Site selectivity of pits in
the echinoid Hemipneustes places them preferentially adjacent to respiratory tube feet
(Category 4). From these examples it is deduced that sparse infestations of borings or
epizoozoic organisms permit a more confident interpretation of organism/organism in-
teractions; dense accumulations, possibly following multiple spatfalls, mask such
patterns.

1. INTRODUCTION
Consider the task of the parasitologist. There may or may not be an
actual physical manifestation of the attentions of a parasite in a human being,
sheep, favourite pet dog or fish bought from a fishmonger, but its presence is
easily confirmed (or otherwise) using the wide range of biomedical, biochem-
ical and gene sequencing tools currently available. A stool is collected, blood
sampled or the fish cut open, and the hunt is on. Not only can the parasite be
identified, but its life cycle elucidated and its genes sequenced. In the twenty-
first century, all this can be done before lunch.
The hunter of fossil parasites, in my own case, in ancient echinoderms,
has none of these advantages. We may confidently speculate that many or
most parasites in ancient echinoderms left no evidence of their presence and
we will never know that they were ever there. Such navel contemplation is
the easy part. Commonly, where there is evidence of some interaction
between an organism, parasite or not, and the host, this is preserved as
some invasive structure (boring) into the echinoderm’s endoskeleton.
This may or may not be associated with a growth deformation of the
host. Borings without growth deformities must be regarded as not proven
parasitism, as such traces of interaction can occur after the death of the echi-
noderm, either soon after (Donovan, 2014; Donovan et al., 2014a) or mil-
lions of years later (Donovan and Lewis, 2011; Donovan, 2013). Associated
growth deformities show that the boring was engendered while the echino-
derm was alive and able to react to the invasion. What commonly does not
get preserved is the producer of the boring, which almost invariably lacks a
mineralized (and thus easily preserved) skeleton, so our interpretation of its
purpose (parasitism, or failed or successful predation, or something else)
must be made in ignorance of the simple fact, whodunit? The parasitologist
looks for parasites; the palaeoparasitologist works by necessity without
A Prejudiced Review of Ancient Parasites and Their Host Echinoderms 293

parasites, except for rare examples such as parasites with preservable skele-
tons such as parasitic snails (see below) or rare mineralized producers of pits
such as Phosphannulus M€ uller et al., 1974 (Welch, 1976; Werle et al., 1984;
Boucot, 1990, pp. 32e34).
So, what can we hope to achieve? As already intimated, many palaeon-
tological investigations of echinoderms and putative parasites begin with the
recognition of pits and boreholes in the echinoderm endoskeleton. Pits, bor-
ings and related structures in ancient substrates, such as tracks, trails, burrows
and coprolites, are trace fossils, representing evidence of ancient organic ac-
tivity. The study of trace fossils is ichnology. Only rarely is the producing
organism preserved adjacent to a trace except in certain settings, such as
the shells of boring bivalves which may be preserved in their borehole in
limestone (for example, Donovan and Jagt, 2013a). It is a mantra of ichnol-
ogy, the study of trace fossils, that a given organism may have produced a
range of trace fossils, representing different activities, and that a particular
morphology of trace fossil may have been produced by more than one group
of organisms, involved in similar activities. Trace fossils are given Latinized
binomens, but these do not refer to an organism per se, but to the sedimen-
tary structure that is the trace fossil. That is, their classification as sedimentary
structures is analogous to, but not part of, Linnean classification. It is a com-
mon ‘game’ in ichnology to speculate on the identity of producing organ-
isms, but it is incorrect to be too dogmatic about such assertions (Donovan,
2010). Pits in live echinoderms commonly produce growth reactions in the
endoskeleton, either inhibiting growth or causing swellings of various mor-
phologies, but these are pathologies of the echinoderm and are not part of
the trace fossil (Donovan, 2015). Further, trace fossils are named on
morphology and not substrate (Pickerill, 1994); for example, it was
suggested that borings in the echinoderm test that cause a range of growth
deformations should be referred to Tremichnus Brett, 1985, but all morpho-
logically similar small round holes are more correctly referred to Sedilichnus
M€ uller, 1977, a senior synonym of the widely used Oichnus Bromley, 1981
(Zonneveld and Gingras, 2014; see also Pickerill and Donovan, 1998;
Donovan and Pickerill, 2002).
If this sounds daunting, then add to this the confusion introduced by the
taphonomy, the study of the preservation of our infested echinoderm. There
are some organisms which have simple skeletons that are commonly pre-
served whole, such as gastropods, shelled cephalopods, tube-dwelling
worms, foraminiferans and stony corals, or disarticulated into just a few
pieces, including bivalve molluscs, brachiopods and ostracods. Most other
294 Stephen K. Donovan

groups of organisms have complicated, multielement skeletons that fall apart


soon after death; one individual can be preserved as tens or hundreds of
individual pieces. The latter include the vertebrates, arthropods, plants and
echinoderms. Commonly, evidence of a possible parasitic interaction is
found in a fragment of echinoderm that cannot be classified with any con-
fidence any closer than class or order. And, of course, it may be that the para-
sitic infestation weakened the skeleton so that it is more prone to
disarticulation postmortem than otherwise.
So, palaeoparasitology of echinoderms most commonly involves recog-
nizing pathological growth deformities produced in response to structures
generated by parasitic(?) organisms. The producing organisms are not them-
selves commonly preserved or otherwise identifiable (although two specific
examples where the parasite is preserved are discussed below) and the echi-
noderm may be preserved as only a fragment of endoskeleton that can only
be classified to class level, such as a fragment of crinoid column. If we accept
this as the starting point for this paper, then we can, at least, describe some
good examples that lead to reasonable interpretations.
The morphological terminology of the crinoid endoskeleton is explained
in Ubaghs (1978) and Moore et al. (1978); for that of the echinoid test, see
Smith and Kroh (2011). Specimens discussed below are deposited in the
following institutions: Department of Earth Sciences, the Natural History
Museum, London, England (BMNH); Naturalis Biodiversity Center,
Leiden, the Netherlands (RGM); and Natuurhistorisch Museum Maastricht,
Maastricht, the Netherlands (NHMM).

2. INTERPRETATIONS AND CONFIDENCE


A great diversity of disease-carrying and parasitic organisms infest
extant echinoderms (Jangoux, 1987a,b,c,d), although they are rarely para-
sitic themselves (Rouse in Rhode, 2005, pp. 248e250). It is only in exam-
ples where infestations of ancient echinoderms caused some recognizable
deformity in skeletal growth, or the exceedingly rare cases in which the
infesting organism itself is fossilized, that an indication of disease or parasitism
can be identified in the fossil record (Conway Morris, 1981; Boucot, 1990;
Littlewood and Donovan, 2003). For example, parasites may produce
distinctive galls or cysts in echinoid radioles (Warén and Moolenbeek,
1989), asteroid arms, crinoid pinnules and cirri, and ophiuroids discs
(Grygier, 1988). Examples of non-cyst-like structures produced by
A Prejudiced Review of Ancient Parasites and Their Host Echinoderms 295

purported parasites which are considered below infest Upper Palaeozoic


crinoid thecae and Cretaceous echinoid tests.

2.1 Problems of interpretation


Interpretations of exotic interactions between ancient (or even extant) or-
ganisms are commonly problematic and rarely leads to hard conclusions,
apart from examples such as simple encrustations or boring invasions with
numerous modern analogues. For an example of the problem of interpreting
ancient interactions with echinoderms which is not parasitism, but certainly
exotic, consider the lectotype specimen of the primitive mollusc Phthipodo-
chiton thraivensis (Reed, 1911) (see Sutton and Sigwart, 2012; Figure 1

Figure 1 Phthipodochiton thraivensis (Reed, 1911), BMNH G47258, lectotype, from the
Upper Ordovician of south-west Scotland. (After Donovan et al. (2010), Figures 2 and 3(c),
respectively.) (a) The specimen showing the valves of the chiton, preserved as natural
moulds and curving up from the lower centre to the right, past the label and towards
the top left. Scale bar represents 10 mm. (b) High-resolution X-ray microtomography
image of the complete gut contents (valves removed). Scale bar represents 1 mm.
296 Stephen K. Donovan

herein) from the Upper Ordovician Lady Burn Starfish Beds of south-west
Scotland. Mark Sutton and Julia Sigwart imaged the concealed structure of
this specimen using high-resolution X-ray microtomography (for full
details, see Donovan et al., 2010, pp. 935e936). This revealed a string of
shelly material preserved in a position that would correspond to the gut in
an extant chiton. The most prominent component of this string is a group
of nine crinoid columnals of more or less similar morphology that are inter-
preted as being derived from an individual of the camerate Macrostylocrinus
cirrifer Ramsbottom, 1961 (Donovan et al., 2011b), a common taxon at
Lady Burn.
Multiple lines of evidence indicate that this association is not a hydrody-
namic accumulation (Donovan et al., 2010). The columnals represent
ingested hard parts that were passing through the spiral gut of the chiton
at the time of death. Chitons are commonly thought of as simple grazers,
feeding on encrusting algae on rock surfaces, but many living chitons live
on animal matter (Fulton, 1975; Latyshev et al., 2004) and examination of
gut contents in living species shows a variety of food preferences, in some
species highly specialized (Sirenko, 2000).
Almost nothing is known regarding the predators and scavengers of
Ordovician crinoids (Meyer and Ausich, 1983; Baumiller and Gahn,
2003). Determination of predation and scavenging of Ordovician crinoids
has been mainly inferential, although there is suggestive evidence for pred-
atory decapitation in some disparids (Donovan and Schmidt, 2001), perhaps
a Category 3 association sensu Boucot (1990; see below). Category 1 asso-
ciations of crinoids as prey are rare throughout the fossil record, and the
example discussed herein is the oldest and the most unexpected.
Crinoid columnals may have been consumed by this chiton due to pre-
dation, scavenging or ingestion of sediment rich in crinoid bioclasts. The last
seems unlikely; unless the chiton was particularly unselective, it would more
likely have harvested organic matter from finer grained sedimentary parti-
cles. Predation or scavenging is thus more probable, but equally plausible.
The speculation of predatory versus scavenging behaviour may appear trivial
in this example, but it is analogous to the sometimes heated discussions of the
habits of Tyrannosaurus rex Osborn, 1905 e predator or scavenger e which
have engendered a diverse correspondence (for a recent discussion, see
Erickson, 2014). Whichever, such crinoidivory in this ancient Scottish
mollusc is unexpected, being unknown from extant chitons; like T. rex,
we lack a modern analogue to provide an answer.
A Prejudiced Review of Ancient Parasites and Their Host Echinoderms 297

To give a further echinodermal example of an organismeorganism


interaction that defies entirely confident interpretation, consider the
well documented record of otherwise well-preserved Palaeozoic crinoids
that retain evidence of regeneration of one or more arms (see Baumiller
and Gahn, 2003, 2004). These are commonly interpreted as evidence of
successful predation on the arms of crinoids, but as of yet there is no
entirely satisfactory explanation of why anything should have been eating
such a poorly nutritious part of the animal. Extant crinoids carry their go-
nads mainly in their arms and pinnules (Breimer, 1978, pp. T18eT19),
making these nutritious organs the principal targets for predators. If eaten,
an arm can be regenerated; the comatulid Antedon bifida (Pennant, 1777) is
gravid throughout the year, presumably to tempt predators and divert
them from the visceral mass, although the reproductive season is only a
month (Nichols, 1994). Palaeozoic crinoids lacked this adaptation and it
is assumed that the gonads were included within the cup, although some
taxa may have adapted their large anal sacs to bear the gonads (Lane,
1984). Both I and other authorities (V.J. Syverson, October 2013, personal
communication) are of the opinion that predation on the arms of Palaeo-
zoic crinoids may be evidence of predation, not on the innutritious arms of
crinoids, but on some nutritious organism(s) or group(s) of organism(s) that
lived on the arms. This is entirely speculative as I am not aware of reports of
likely prey organisms being preserved on the arms; they may have been
unmineralized and thus unlikely to be fossilized. The evidence is good
for the predation of the arms of Palaeozoic crinoids, but not good for
the reason why.

2.2 Limits of confidence


The two examples given above e one particular, one general e demonstrate
something of the difficulties of making a precise interpretation of the inter-
actions between echinoderms and other organisms even when the data is
good. What is needed at this juncture is some qualitative measure that re-
searchers can apply to their deliberations to give their readers a ‘feel’ of
the level of confidence with which they are made. I suggest one way
forward, admittedly preliminary, is an adaptation of Boucot’s (1990,
pp. 9e10) original reliability classes which he applied to myriad examples
that he examined for evidence of behaviour and coevolution in the fossil re-
cord. The reader is referred to the original publication for more explanation
and many more examples, as this tabulation is merely a brief abstract of a
298 Stephen K. Donovan

much greater body of argument and evidence. Briefly, Boucot’s categories


are summarized thus:

Category 1 The rare examples where the evidence is incontrovertible.


Category 2A Organisms preserved in close association, but not actually in
position.
Category 2B Arguments based on functional analogy with closely related taxa.
Category 3 Fairly certain, based on known behaviour of living analogues.
Category 4 Less certain due to the producer of evidence being unknown.
Category 5A High degree of uncertainty about the maker.
Category 5B Examples where modern biogeographic evidence is crucial.
Category 6 Fairly speculative, such as functional determinations of wholly
extinct taxa.
Category 7 Highly speculative, little reliability.

Of the two examples given above, I would place the Ordovician crinoi-
divorous chiton in Boucot’s Category 2A and would change it to Category 1
if a modern analogue was discovered. Predation on the arms of Palaeozoic
crinoids is best assigned to Category 4 or, perhaps, 5A.

3. SOME EXAMPLES
The structure of this paper was determined by personal preference. It
could have written as the echinodermal parts of Conway Morris (1981)
brought up-to-date, a revision of the parasitism parts of various reviews of
echinoderm taphonomy (such as Meyer and Ausich, 1983; Donovan,
1991b) or a parasitism paper modelled on the review of predation on cri-
noids by Baumiller and Gahn (2003). Rather, I have something a little
different in approach from all of these, preferring to focus on a few selected
examples from my own experience rather than a review that attempted to be
too broad and, in consequence, lacked detail.
Actual examples of putative parasitic infestations of fossil echinoderms
are desirable at this stage to demonstrate something of the range of evidence
available and how it has been interpreted. Most of the examples lean heavily
on my own research, which explains why they preponderantly concern my
beloved crinoids. I consider it preferable to discuss the familiar in this review
than try to spread the text too thinly across the many extinct and extant clas-
ses of echinoderms. My intention here is to demonstrate broad principles
that can be extrapolated to a reader’s own investigations.
A Prejudiced Review of Ancient Parasites and Their Host Echinoderms 299

3.1 A coralecrinoid association from the Mississippian


(Figure 2)
Material, locality and horizon: BMNH EE5797 (Figure 2) is from Salt-
hill Quarry, Clitheroe, Lancashire [SD 7550 4265], England, one of the
most important localities for Mississippian (Lower Carboniferous) echino-
derms in north-west England (Donovan et al., 2003; Kabrna, 2011). The
crinoid theca was found in the Cover Mudstone, present at the top of the
lower Viséan (¼ upper Chadian) Salthill Cap Beds of the Bellman Lime-
stone Member.
Description: (Based on Donovan et al., 2005, pp. 43e44.) BMNH
EE5797 is an undeformed calyx (Figure 2(a) and (b)) of the monobathrid
camerate crinoid Amphoracrinus gilbertsoni (Miller in Phillips, 1836). Preserva-
tion of camerate crinoids as their golf ball-like thecae, lacking most if any of
the contiguous arms and stem, is common at this locality. The most notice-
able variance is that Wright (1955, p. 195) noted ‘. posterior interbrachial
area [¼ CD interray] much wider than the others .’ BMNH EE5797 has
an AB interray that is almost as wide as the CD interray at the level of the
base of the free arms; the other three interrays are narrower and all of about
the same width.
The solitary rugose coral may be a zaphrentoid (Mitchell, 2003). It is
small in comparison to the crinoid calyx. It is preserved in transverse
section (Figure 2(c)) and is apparently less than 2.0 mm high, although it
has obviously been depressed into the crinoid calyx as indicated by a series
of more or less concentric fractures. More precise systematic identification
has not been possible on the basis of this single section. The coral is situated
in the AB interray, in close contact with the anterior branch of the B
ray arm.
Discussion: There are a number of lines of evidence to indicate that the
solitary coral was attached to the crinoid calyx in life (Donovan et al., 2005),
although an actual attachment area per se is not clearly apparent and,
assuming it to be present, could only be exposed by destructive techniques.
The corallite is small (Figure 2(c)). Although solitary rugose corals were typi-
cally unattached in adulthood, as larvae (and, plainly, in subsequent early
growth stages) they were capable of cementation to a variety of hard sub-
strates (see, for example, Hubbard, 1970, p. 203).
The coral corallite is preserved more or less perpendicular to the surface of
the crinoid calyx and has been pushed into it, being surrounded by concentric
cracks which have broken across plates, probably due to post-depositional
300 Stephen K. Donovan

Figure 2 (aec) BMNH EE5797, Amphoracrinus gilbertsoni (Miller, 1821, in Phillips,


1836), encrusted by a solitary rugose coral. (After Donovan et al. (2005), Figure 1.) Scale
bars represent 10 mm. (a) Theca of crinoid. A ray (¼ anterior) central; note the coral in
the AB interray (left) at the same level as the base of the free arms. The anal pyramid is
subapical and situated about mid-way between the apex of the tegmen and the arms
on the opposite side of the specimen to the A ray (¼ CD interray). Note that the AB
interray is broader than the EA interray (right of A ray arm). (b) Apical view. A ray (¼
anterior) towards top of page, AB interray upper right, CD interray (posterior) towards
bottom of page. Note regular pentagonal outline of undeformed specimen. (c) The
corallite of the coral. Note how the curved breakage of the crinoid around the coral
follows the outline of the coral theca and has not resulted in disarticulation of plates.
(def) BMNH E71430, Synbathocrinus conicus Phillips, 1836, dorsal cup and proximal
column, with single borehole of Sedilichnus paraboloides (Bromley, 1981). Scale bar
represents 5 mm. (d) Lateral view with E ray central. Note boring and oral surface
sloping anteriorly (that is, to left). (e) EA interray central, showing the prominent boring
in the R:R:B plate triple junction (compare with Figure 3(a)). (f) D ray, showing slope of
oral surface towards EA interray (compare with Figure 3(b)).
A Prejudiced Review of Ancient Parasites and Their Host Echinoderms 301

compactional strain. Although the position of the coral on the crinoid could
be merely coincidence, the unusual width, which we interpret as growth
rather than postmortem deformation (Figure 2(b)), of the AB interray is
reminiscent of the sorts of deformities that are known to be induced in
echinoderms by interactions with encrusting organisms (Meyer and Ausich,
1983).
All these lines of evidence support the supposition of an original
biotic relationship between the host crinoid and its attached coral in
life; that is, the living coral was an epizoozoan (sensu Taylor and Wilson,
2002) on the living crinoid. In the Mississippian of the British Isles, it is
more common to find crinoids, particularly their columns, encrusted by
colonial tabulate corals than by either solitary or colonial rugose corals
(see, for example, Donovan and Lewis, 1999). The close association of
A. gilbertsoni with a solitary rugose coral would thus be worthy of comment
under any circumstances, but it is the position with respect to the crinoid
calyx and the presumed life orientation of the latter that excites particular
comment. In attaching to the calyx of a crinoid, the solitary coral has
gained an advantage from its elevated position would have been above
the turbid bottom layers of the water column, so water currents would
have been essentially sediment free. The importance of feeding is further
emphasized by the corallite being hard against the B ray arm in the AB
interray. The A ray is anterior and, if A. gilbertsoni formed a parabolic filtra-
tion fanlike modern rheophilic crinoids (Macurda and Meyer, 1974), the
coral would have been directed into the clean water currents, being posi-
tioned up-current from the anal pyramid. The situation in close contact
with the B ray arm is at least suggestive that the coral may have actively
harvested food with its tentacles from the adoral groove of the crinoid’s
arm. Although obviously speculative, this supposition is supported by the
unusual width of the AB interray, a growth deformity which probably
resulted from a reaction to the coral and prevented it from interfering
with the feeding activity of the A ray arm, too. The available evidence is
at least highly suggestive that this coral was both a filter feeder and a parasite
on the crinoid.
Reliability: Category 1 or 2B. Boucot (1990, p. 9) stated (Category 2B)
that ‘With organisms belonging to extinct higher taxa [such as rugose corals
and camerate crinoids] functional analysis of behavior from morphology is
clearly less reliable’. But other groups of crinoids and stony corals are extant
and well known, so Category 1 is at least plausible.
302 Stephen K. Donovan

3.2 A growth deformity in a Mississippian crinoid


(Figures 2(def) and 3)
Material, locality and horizon: BMNH E71430 (Figures 2(d) and 3) is
from Salthill Quarry, Clitheroe, Lancashire [SD 7550 4265], England
(Donovan et al., 2003; Kabrna, 2011; Section 3.1 herein). The crinoid theca
was found in the lower Viséan (¼ upper Chadian) Salthill Cap Beds of the
Bellman Limestone Member.
Description: (Based on Donovan, 1991a, p. 2.) The specimen is a dorsal
cup, with the two most proximal columnals of the column, of the disparid
crinoid Synbathocrinus conicus Phillips, 1836 (Wright, 1952, pp. 134e136, pl.
36, Figures 10, 21 and 22). The cup has been bored once, in the EA interray,
at the triple suture between the E and A radials, and the basal in the EA
interray (Figures 2(d) and 3(a, b)). The boring is circular with a rounded
margin; the cavity is a conical, flat-bottomed pit which does not break
through into the body cavity and is assigned to Sedilichnus paraboloides
(Bromley, 1981). The cup is not swollen around the excavation, unlike
the common reaction to borings seen on some crinoid columns from the
same site, but the cup is less developed on the bored side, the oral surface
sloping towards the EA interray (Figures 2(f) and 3(b)).

Figure 3 BMNH E71430, Synbathocrinus conicus Phillips, 1836. (a, b) Camera lucida
drawings of the dorsal cup and proximal column. (After Donovan (1991a), Figure 2.)
Scale bar represents 5 mm. (a) EA interray central (compare with Figure 2(e)), showing
the position of the boring. (b) DE interray central, showing how the oral surface slopes
down towards the region of infestation, presumably a growth reaction to the distur-
bance. Key: RR ¼ radial circlet; BB ¼ basal circlet; COL ¼ most proximal part of column.
(c) Schematic oral view based on BMNH E71430. (After Donovan (1991a), Figure 3.)
Carpenter rays (AeE) indicated, corresponding to the positions of the arms; X is the po-
sition of the anal series (¼ posterior). Small arrows mark positions of cryptic B:B:R plate
triple sutures; large arrows mark positions of prominent R:R:B plate triple sutures. Key:
1 ¼ in the same position of the anal series; 2 ¼ adjacent to the anal series; 3 ¼ distant
from the anal series; * ¼ position of boring. Current flow would have been from the top
of the page.
A Prejudiced Review of Ancient Parasites and Their Host Echinoderms 303

Discussion: Borings in the cup of Synbathocrinus are rare. Brett (1978)


suggested that pit-forming organisms on Palaeozoic crinoids were host spe-
cific; I have looked at hundreds of specimens of this genus, from the Missis-
sippian of North America and Europe, and the Permian of Timor, for almost
25 years and have failed to find a second bored specimen.
The excavating organism selected its site with some precision. That
the boring was made in a live crinoid is undoubted, with growth pro-
ceeding with greater vigour on the side opposite to the pit (Figures 2(f)
and 3(b)). In life, all sides of the cup would have been equally available
for infestation by borers and encrusters with the crown elevated above
the substrate. The boring was made precisely at the triple suture between
two radial (R) and a basal plates (B) (Figures 2(d) and 3(a)). The three
B:B:R triple junctions, in the A, C and E rays are cryptic and can only
tentatively be distinguished; in contrast, the five R:R:B sutures are readily
apparent (Figures 2(def) and 3(c)). Sutures between plates, bonded
together by collagenous ligament fibres, would have been easier to bore
into, either mechanically or chemically, than the solid calcite of the plates;
therefore, the position of S. paraboloides is interpreted as a choice made for
ease of infestation by the boring organism, the identity of which remains
unknown.
Why bore into the EA interray, rather than at one of the four other triple
plate sutures? The sutures labelled 3 in Figure 3(c), in the EA and AB inter-
rays, are the most up-current (¼ anterior) plate triple junctions and, thus,
they are also the potential borehole sites most removed from the anal series
(X). This suggests that the pit-forming organism was not a coprophage. The
most probable life strategy of the pit-former was as a hard substrate dweller
that fed by filtration (compare with Brett, 1978, 1985). It would be attached
to the highest ‘fixed’ point of the crinoid, just below the oral surface and the
arms, and always orientated into the prevalent current by the crinoid. It is
presumed to have removed part of the suspended particulate food that
would otherwise have been ingested by the crinoid. Whether this contrib-
uted to the deformation of the cup or it was mainly a reaction to the forma-
tion of the pit must remain uncertain.
Reliability: Category 4. ‘For some types of behavioral evidence there is
an even larger degree of uncertainty about the maker of this evidence. This is
particularly true for many trace fossils’ (Boucot, 1990, p. 9). No determina-
tion of the borer can be made apart from that it was small, unmineralized and
probably a filter feeding invertebrate.
304 Stephen K. Donovan

3.3 Epizoobionts infesting a Mississippian crinoid (Figure 4)


Material, locality and horizon: BMNH EE8728 (Figure 4) is from Salthill
Quarry, Clitheroe, Lancashire [SD 7550 4265], England (Donovan et al.,
2003; Kabrna, 2011; Section 3.1 herein). The crinoid theca was found in
the Cover Mudstone, present only at the top of the lower Viséan (¼ upper
Chadian) Salthill Cap Beds of the Bellman Limestone Member.

Figure 4 Multiple Sedilichnus paraboloides (Bromley, 1981) infesting the dorsal cup of
the Lower Carboniferous crinoid Amphoracrinus gilbertsoni (Miller in Phillips, 1836),
BMNH EE8728. (After Donovan et al. (2006), Figure 1.) (a) Base of dorsal cup, D-ray to-
wards top of page. (b) Enlargement of (a), showing how pits are concentrated on plates,
not crossing sutures. (c) Enlarged lateral view of (mainly) dorsal cup, E-ray central,
showing sub-horizontal arrangement of closely spaced pits. (d) Theca in lateral view,
same orientation as (c). Note absence of pits above the line of the arm facets. Specimen
whitened by ammonium chloride. Scale bars represent 10 mm (a, d) or 5 mm (b, c).
A Prejudiced Review of Ancient Parasites and Their Host Echinoderms 305

Description: (Based on Donovan et al., 2006, pp. 43e44.) The reader


has already been introduced to A. gilbertsoni and S. paraboloides (see above).
This description will concentrate on the pattern of infestation of pits on the
crinoid theca (Figure 4).
The theca preserves the dorsal cup, fixed arms and tegmen. Sedilichnus
paraboloides is found on all plates of the dorsal cup (basal and radial circlets),
not including the articular facet for the column (Figure 4(a) and (b)); on
fixed brachial plates (Figure 4(c)); and on interbrachial plates up to just above
the mid-height of the facet for the free arms (Figure 4(c), upper left). There
are no pits on the tegmen above this level (Figure 4(d)). The hemispherical
pits may be close packed together on individual plates, but are rarely in con-
tact; they do not occur on the depressed sutures between thecal plates, that
is, those of the dorsal cup and proximal fixed brachials (Figure 4(c)). Pits
(n > 50, all c.1 mm diameter) are common throughout the defined area
and ‘bald’ areas seen on some parts of the specimen are covered with pits
elsewhere in analogous positions in relation to the arms. The base of the
cup is angled to the long axis of the theca and slopes up towards the CD
interray.
Discussion: This infestation occurred while the crinoid was alive. Most
obviously, pits are distributed on the theca, below the level of arms,
through 360 , but are not found on articular facet of the column. Thus,
the embedding organisms had access to the entire lower half of the theca,
but the column facet would have been covered by the column in a living
crinoid. The absence of pits on the tegmen above the level of the arms is
most easily explained by the crinoid itself keeping this region free of any
infestation by the action of the tube feet. These are situated on the adoral
surface of the free arms, enabling them to ‘clean’ the tegmen, but not the
region below arm level. Presumably, the proximal column and aboral sur-
faces of the free arms, which are not preserved, could also have been
infested. Further, there is evidence for a growth deformity, that is, the
sloping base of the theca, which is analogous to the specimen of S. conicus
described above (Section 3.2).
The palaeoecology of the pit-forming organism is, in part, decipherable,
even if its identity remains obscure. There is the obvious segregation of
S. paraboloides on the substrate (see above), indicating that they were unable
to survive the attentions of the tube feet. The pits are concentrated on the
more elevated parts of the lower half of the theca, that is, they occur on the
more concave, central areas of plates (Figure 4(b) and (c)). The plate sutures,
which would presumably be easier regions for embedment (Section 3.2), are
306 Stephen K. Donovan

avoided; these sutures are sunken between the plates, so it is probable that
the small difference in height between sutures and plate centres was impor-
tant to the producers. This strongly supports a suggestion that they were fil-
ter feeding. Interestingly, S. paraboloides is distributed on the lower part of
the theca through 360 , and is apparently not selective with respect to the
life orientation of the crinoid, there being no obvious preference for anterior
(A-ray) or posterior (CD-interray) (but see Section 4, ‘Discussion’, below).
Pits are close packed, but in only very few instances overlap, suggesting that
this represents a gregarious accumulation of an organism that thrived on
elevated calcareous substrates, rather than successive pits formed by one or
a few individuals (compare with Donovan and Lewis, 2010).
Reliability: Category 4 (compare with Section 3.2) or 7, ‘. so highly
speculative as to have little reliability at all .’ (Boucot, 1990, p. 9). The
sloping base of the theca is analogous to the example of S. conicus, above,
in which a single pit is interpreted as engendering the aberration. In the pre-
sent example, with the theca heavily covered by borings below arm level,
there seems little connection between a growth deformity and an infestation
through 360 . The pits would have gained advantages attached to an elevated
cup, but any evidence that the association may have been parasitic is masked
by the dense accumulation of pits. The pit producer may have been conspe-
cific with that in Section 3.2; the specimens are from the same locality.

3.4 Platyceratid gastropods infesting Upper Palaeozoic


crinoids (Figures 5 and 6)
Material, locality and horizon: All specimens are members of the mono-
bathrid camerate genus Neoplatycrinus Wanner, 1916, from the Permian of
West Timor. RGM B9, Neoplatycrinus major Wanner (Figure 5(a) and (b)),
from Basleo (Charlton et al., 2002, Figure 2), Noil Tonini, West Timor (pre-
sumably about sites 6e8 of Webster, 1998). RGM ST.32842[1], Neoplatycri-
nus dilatatus Wanner, 1916 (Figure 5(cef)), comes from Toenino. RGM
T.4439[1], Neoplatycrinus sp. cf. N. dilatatus Wanner (Figure 5(g)), no associ-
ated locality data. RGM T.3851[1], N. dilatatus Wanner (Figure 6(aec)), no
associated locality data.
Description: (After Donovan and Webster, 2013, pp. 990e991.) The
gross morphologies of the Neoplatycrinus crinoid species from West Timor
were described in Wanner (1916); herein, only the modifications to the ge-
ometry of the form of the CD (posterior) interray in a few specimens are
described. Two broad morphologies are identified, one centred below
(Figure 5(a)) and the other centred on the periproct. RGM B9 has a theca
A Prejudiced Review of Ancient Parasites and Their Host Echinoderms 307

Figure 5 Homing scars of platyceratid gastropods (Lacrimichnus? isp.) on Permian


platycrinitid crinoids from West Timor. (After Donovan and Webster (2013), Figure 1.)
(a, b) RGM B9, Neoplatycrinus dilatatus Wanner, 1916, posterior (CD interray central)
and anterior (A ray central) views of theca, respectively. Note deeply sunken homing
scar. (ce