Prospects & Overviews
Review essays
Cephalopod origin and evolution:
A congruent picture emerging from
fossils, development and molecules
Extant cephalopods are younger than previously realised and were under major
selection to become agile, shell-less predators
Björn Kröger1), Jakob Vinther2) and Dirk Fuchs3)
Cephalopods are extraordinary molluscs equipped with
vertebrate-like intelligence and a unique buoyancy system
for locomotion. A growing body of evidence from the
fossil record, embryology and Bayesian molecular diver-
gence estimations provides a comprehensive picture of
their origins and evolution. Cephalopods evolved during
the Cambrian (530 Ma) from a monoplacophoran-like
mollusc in which the conical, external shell was modified
into a chambered buoyancy apparatus. During the mid-
Palaeozoic (416 Ma) cephalopods diverged into nauti-
loids and the presently dominant coleoids. Coleoids (i.e.
squids, cuttlefish and octopods) internalised their shells
and, in the late Palaeozoic (276 Ma), diverged into
Vampyropoda and the Decabrachia. This shell internalis-
ation appears to be a unique evolutionary event. In con-
trast, the loss of a mineralised shell has occurred several
times in distinct coleoid lineages. The general tendency
of shell reduction reflects a trend towards active modes
of life and much more complex behaviour.
.
Keywords:
Cambrian explosion; coleoidea; divergence estimate;
fossil record; Nautiloidea; Nectocaris
DOI 10.1002/bies.201100001
1)
Museum für Naturkunde Berlin, Berlin, Germany
2)
Department of Geology and Geophysics, Yale University, New Haven,
CT, USA
3)
Freie Universität Berlin, Institute of Geological Sciences, Berlin, Germany
602 www.bioessays-journal.com
Introduction
Cephalopods are the smartest and most complex invertebrates.
With their big brains [1], advanced visual perception and
muscular arms they have evolved complex behaviour [2, 3]
and exhibit curiosity and even distinct personalities.
Octopods can, for example, manipulate objects [4, 5] and
unscrew the lids of glass jars [6]. Chromatophores in some
cephalopod integuments allow them to instantly camouflage
themselves against predators [7], and perform complex com-
municative, mating and scare signals [8]. Their unique jet
propulsion system allows them to channel water out through
a funnel (or hyponome) via the large mantle cavity as a strong
current, which they use to escape from predators and travel
great distances. Another cephalopod novelty is the ink sac, an
organ that allows them to deter predators while making their
escape [9]. Cephalopods inhabit and forage in every marine
micro-environment from the deep sea to intertidal rocky shores,
and they are ecologically important in both tropical reefs and
arctic habitats [10].
Cephalopods have a rich fossil history. Their chambered
shells (phragmocone) are commonly preserved in the rock
record, and are collected for their beauty as stand pieces or
as ornamental inclusions in rocks carved into tiles, table tops
and even bath tubs (Fig. 1A,D). Their diversity and worldwide
distribution has made them the standard for stratigraphic
correlation in many geological time intervals [11]. Most fossil
*Corresponding author:
Jakob Vinther
E-mail: Jakob.vinther@yale.edu
Supporting information online
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.... Prospects & Overviews
Figure 1. Fossil and living cephalopods. A: A fossil shop in
Erfoud, Anti-Atlas Mountains, Morocco with restored ammonite
fossils and carved trays in Devonian orthocerid bearing rocks.
B: The exceptionally preserved octopod, Keuppia preserved with
soft parts, Hakel, Lebanon [16]. C: Vampyrotheuthis infernalis
(Photo by Kim Reichenbichler). D: A belemnite rostrum and
phragmocone in a polished tile of Jurassic Bavarian limestone,
Germany. E: Nautilus sp. from an aquarium in San Fransisco
(Photo by Ingrid Taylar). F: The octopus, Amphioctopus marginatus
(Photo by Mark Norman). G: A squid, Sepioteuthis australis
(Photo by M. Norman). H: The cuttlefish, Sepia apama (Photo by
M. Norman). I: The spirulid, Spirula spirula, the internal phragmocone
and the entire animal (Photo by M. Norman). J: Sepioloidea lineolata
(Photo: M. Norman).
cephalopods preserve the remains of the mineralised skeleton,
but exceptional fossil Lagerstätten have given insights into the
evolution and morphology of mainly soft-bodied cephalopods
(Fig. 1B) [12–17].
Extant cephalopods are organised into two major groups;
nautiloids (Fig. 1E, Fig. 2A) and coleoids [18] (Fig. 1F-J, Fig. 2B).
Nautiloids have an external shell while the coleoids have
internalised or completely lost the shell. Coleoids are the most
diverse cephalopod group today and are divided into two
groups – the ten-armed, Decabrachia (Fig. 1G-J) and the
eight-armed Vampyropoda (Fig. 1F). The latter group com-
prises the familiar octopods as well as the Vampire squids
(Fig. 1C), which actually have ten arms, but two arms are
reduced sensory filaments. More than 180 cephalopod
genera are known to inhabit modern oceans, although the
fossil record exposes a great wealth of forms well in excess of
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B. Kröger et al.
Review essays
4000 genera1. Several diverse cephalopod groups (Fig. 1A,B)
that dominated the Paleozoic and Mesozoic marine habitats
for tens to hundreds of millions of years are now entirely
extinct, such as the uniquely coiled and highly sculptured
ammonoids and the gigantic straight-shelled endocerids.
Here, we re-evaluate the pre-existing fossil record with
recent and novel molecular studies, and demonstrate that
previous hypotheses of cephalopod evolution converge with
evidence from molecular biological inference. We demonstrate
that hypotheses surrounding cephalopod evolution are well
illustrated in the fossil record, but call for some re-interpret-
ations. The remarkable fossil from the Burgess Shale,
Nectocaris pteryx has recently been hypothesised to be an
early stem group cephalopod [19] with affinities to the
coleoids. This study questions the validity of considering
Nectocaris as a cephalopod or mollusc.
Embryology recapitulates cephalopod
evolutionary history
A series of detailed morphological studies on embryos of
coleoids and Nautilus during the last few decades has
1
A conservative estimate yields c. 1700 Mesozoic ammonoid
species alone (Peg Yacobucci, pers. comm.), together with about
800 Paleozoic ammonoids based on the AMMON database
(www.wahre-staerke.com/ammon/) of D. Korn and A. Ilg (2007), and
c. 1800 Paleozoic genera of cephalopods that are for the most part
classically subsumed under the Nautiloidea by paleontologists (own
unpublished data).
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Figure 2. In extant cephalopods the body axes of the adult stages
are tilted perpendicularly versus embryonic stages. As a con-
sequence, the morphological anterior-posterior body axis between
mouth and anus and the dorso-ventral axis, which is marked by a
dorsal shell field, is tilted 908 in the vertical direction in the adult
cephalopod. Median section of A: Nautilus, B: Sepia showing the
relative position of major organs (Drawings by Brian Roach). C:
shared embryonic features in embryos of Nautilus (Nautiloidea) and
Idiosepius (Coleoidea) (simplified from Shigeno et al. 2008 [23] Fig.
8). Orientation of the morphological body axes is marked with a
compass icon (a, anterior; d, dorsal; p, posterior; v, ventral; dgl,
digestive gland; gon, gonad; ngl, nidamental gland).
shed new light on the cephalopod body plan [20–23],
and provides the basis for a much better understanding of
the evolutionary transitions that led to the origin of cephalo-
pods. With these morphological studies it is possible to
fill in the large gap that exists between the complex and
highly derived body plan of extant cephalopods and other
molluscs [24].
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Central to the discussion about this morphological transition
is the original body-axes: the relationships between the
anterior-posterior and dorso-ventral axis as demonstrated in
cephalopod arms, funnel and hood. Recent work has con-
firmed earlier assumptions that early embryonic bodies of
Nautilus and coleoids both have the same overall pattern as
typical gastropods (Fig. 2C) [22, 23]. The embryonic organs are
concentrically arranged around the dorso-ventral body axis. A
central dorsal external shell field exists, even in coleoids with
greatly reduced adult shells, such as the bobtail squid,
Idiosepius [23]. This observation shows that coleoids evolved
from ancestors with external shells.
The position of the funnel, which was debated for decades,
appears to be resolved; it can be located as a marginal mantle
fold in the posterior region of the embryo (Fig. 2C) [23].
A consequence of this embryological and developmental
evolution is that in adult Nautilus, as well as in coleoids,
the functional body axis (i.e. anterior-posterior in relation
to feeding and living orientation) is tilted perpendicular to
the morphological body axis (Fig. 2). Nautilus exhibit a
formula of five arm pairs in embryos, similar to that of coleoids
[20, 23], which means that the multiple tentacles (60 in total)
of adult Nautilus seems to be a derived character and not, as
previously assumed, the primitive state of cephalopods.
The embryological development of cephalopods elegantly
demonstrates how the body became re-oriented from an
originally dorso-ventrally flattened mollusc towards the
highly derived adult with an anterior-posteriorly elongated
body. Furthermore, cephalopod embryology demonstrates
how the shells of coleoid cephalopods became secondarily
internalised. These trajectories of modern cephalopod devel-
opment agree surprisingly well with evidence from the fossil
record, suggesting an evolutionary scenario of monoplaco-
phoran-like molluscs giving rise to cephalopods [23].
The first steps in cephalopod evolution:
A high conical chambered shell
Paleontological data allow for the reconstruction of the first
steps in cephalopod evolution. However, the research effort
and progress in paleontological studies on the origin of ceph-
alopods since the 1970s [25, 26] is moderate compared with
those from molecular biology. Molecular and fossil evidence
both demonstrate that the divergences of the major classes of
molluscs took place in the early Cambrian. The oldest known
undoubted cephalopod fossil is the middle Late Cambrian
Plectronoceras cambria (Walcott, 1905) (Fig. 3C,D). Slightly
younger cephalopod fossils are widespread and diverse,
suggesting that within a time interval of a couple of millions
of years [27], cephalopods began to flourish in the latest
Cambrian. The shell morphology of these most primitive forms
provides direct evidence for the presence of a Nautilus-type
buoyancy regulation already in Plectronoceras [28, 29].
A general outline of the soft body of Plectronoceras can be
reconstructed on the basis of the shape of its body chamber
(Fig. 3D). In Plectronoceras and other primitive cephalopods
the orientation of the body was different from later cephalo-
pods [28]. The body was oriented downwards and the shell
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Figure 3. The earliest known cephalopods resemble benthic mono-
placophoran-like molluscs with a high conical shell. A: Lateral view
of the Early Cambrian septate helcionellid Tannuella from Australia,
(SAMP 340151, South Australian Museum). B: Adapical view of
another specimen (SAMP 340152) showing details of a septum
(Photo courtesy of John Paterson). C: Two specimens of the Late
Cambrian Plectronoceras (USNM 57819), the oldest known bona
fide fossil cephalopod. D: Tentative reconstruction of Plectronoceras
(Drawing by Brian Roach). Scale bars: 3 mm.
situated on top, as in other molluscs. Also, the funnel was
posteriorly positioned, resulting in backwards exhalation and
forward direction of locomotion [28, 29] (Figs. 3C,D). Multiple
paired muscle attachment scars have been described in a
number of primitive cephalopods [28, 30] that are similar to
those of monoplacophoran-like molluscs.
Different paleontological hypotheses have been proposed
for the origin of cephalopods among fossil Cambrian mono-
placophoran-like molluscs and other forms [25, 26, 31–35]
(Table 1). The now classical, but debated, hypothesis of ceph-
alopod ancestry is that Plectronoceras derived from the tall,
conical, bottom-living (benthic) mollusc Knightoconus [25, 34, 35],
which has walls in the shell (septa) that separate multiple
Table 1. Compilation of phylogenetic hypotheses of important
cephalopod groups based on the fossil record. The time-tree of
Fig. 5 is based on the hypotheses considered most likely by the
current evidence.
Group Hypothesis
Plectronoceras Descendent of Monoplacophora [25, 28, 35]
Descendent of Helcionellida [31, 32]
Descendent of Hyolitha [33, 34]
Orthocerida Descendants of Ellesmerocerida [84]
Descendants of Plectronocerida [29]
Oncocerida Descendants of Ellesmerocerida [51]
Nautilus Descendent of Oncocerida [50, 56]
Descendent of Orthocerida, herein and [57]
Descendent of Barrandeocerida [55, 57]
Bactritida Early Devonian descendent of Orthocerida
[54]
Ammonoidea Early Devonian descendants of Bactritida
[85, 86]
Coleoidea Early Carboniferous descendants of
Bactritida [53, 72]
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B. Kröger et al.
chambers. More recently, the slender, chambered mollusc
Tannuella was described with nicely preserved specimens
from the Early Cambrian of South Australia [31] (Fig. 3A,B),
Review essays
and it has been hypothesised to also be a likely cephalopod
ancestor. These fossils suggest that cephalopod ancestors
were present in the Early Cambrian (appearing 530 Ma [36]).
Based on the morphological similarity of the earliest
undoubted cephalopods with Cambrian chambered molluscan
shells and on their soft body reconstructions, it can be
assumed that the cephalopod ancestral state resembled a
benthic monoplacophoran-like mollusc with a high conical
shell, which together with the embryological evidence con-
forms to a scenario of cephalopod evolution.
Nectocaris: A lost child of the Cambrian
Nectocaris pteryx was initially described from a single speci-
men from the famous Burgess Shale [37]. However, several
well-preserved specimens have recently been described [19].
This Early-Middle Cambrian animal has been reinterpreted
with an anatomy resembling extant coleoid cephalopods. In
particular, the presence of an anterior funnel-like structure
has been interpreted as a cephalopod funnel [19]. The
body appears to be dorso-ventrally flattened and flanked
by extensive lateral fins. The authors concluded that cepha-
lopods must have evolved from a much more complex ances-
tor, in which Nectocaris belongs to the stem group. This stem
group developed a near-bottom swimming (epibenthic nec-
tonic) mode of life and lacked a shell for buoyancy regulation
and it was suggested that shells re-evolved later in cephalo-
pods for that purpose [19].
Several problems arise with this interpretation, most nota-
bly the sequence of character acquisition which is almost
opposite to the sequence of events described herein and evi-
denced by morphology and embryology (see also [38]). The
fossil record of cephalopods has led to the hypothesis that the
chambered shell gradually gave rise to the swimming mode of
life of cephalopods, as echoed by their embryology. By sub-
sequent modification and internalisation of the shell, coleoids
developed a more active lifestyle and lateral fins (see below). If
a shell-less stem group exists with coleoid homologies, the
fossil record of cephalopods would be severely skewed [19].
When considering the structures in Nectocaris, alternative
interpretations can be surmised for some of the structures that
look similar to those of cephalopods. The supposed axial
cavity in Nectocaris is a narrow internal tube. As demonstrated
above in cephalopods, the mantle evolves during develop-
ment to form the axial mantle cavity through dorsal
elongation, which makes the visceral mass U-shaped, and
the only opening to the visceral tract and mantle cavity is
along the circumference of the head. It is unclear how a
cephalopod mantle cavity and its distinct embryological for-
mation could give rise to such a narrow tube as observed in
Nectocaris (Fig. 4), with an opening through a funnel and
tentatively also through two paired openings on either side
[19]. Furthermore, the supposed gut, which in all known
specimens is poorly differentiated from the axial cavity,
appears to be straight rather than U-shaped as would be
expected from axial mantle development in cephalopods.
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Figure 4. Convergent evolution towards cephalopod-like
morphologies: A nectocarid from Chengjiang, Early Cambrian, China
(referred to as Vetustovermis [40]). From the Yunnan Key Laboratory
for Palaeontology, courtesy of Hou Xian-Guang, along with an inter-
pretative line drawing, showing the funnel-shaped pharynx and
digestive tract, which Smith and Caron [19] have interpreted as a
cephalopod mantle cavity and funnel. Nectocarids do not exhibit
traits that confidently can be homologised to cephalopods or other
molluscs and seems to be an independent branch in the bilaterian
Tree of Life (see text).
The preservation of a gut (even folded) is quite typical in soft-
bodied fossils from Burgess Shale-type deposits [39], and with
>90 specimens of Nectocaris showing distinct internal
anatomy, it is peculiar that so few specimens show a gut trace
preserved alongside the suggested mantle cavity.
The funnel-shaped structure is also problematic. If the
interpretation of this structure as a funnel in a stem group
cephalopod with a straight gut is correct, then the funnel
should be in a posterior position as is observed from embryo-
logical studies. Furthermore, the funnel-like structure in
Nectocaris is closed, whereas the funnel in Nautilus is made
of two overlapping lappets derived from lateral folds, as
observed in the embryo. From a functional perspective, the
supposed axial cavity and the funnel could not function as
either a respiratory or jet propulsion system [38]. In cephalo-
pods, the funnel is a much smaller structure relative to the
axial cavity that tapers to form a canalised exhalant current,
whereas in Nectocaris it is expanding.
We have had a chance to study nectocarid specimens from
the early Cambrian, Chengjiang Lagerstätte in China, referred
to as Vetustovermis [40]. A previously undescribed specimen,
shown here (Fig. 4), preserves the supposed funnel as a
sediment-filled structure, directly connected to a narrow
axial tube. A more likely interpretation is that this tubular
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Prospects & Overviews ....
structure and the funnel are part of the digestive tract
and an eversible pharynx rather than a respiratory cavity.
Many other features are also difficult to homologise with
equivalents in cephalopods [19], such as the lateral fins and
camera-like eyes. Both structures evolved in the coleoids,
which according to both the fossil record and molecular clock
analyses evolved after the Silurian (see below). The lateral
fins could not have evolved prior to the Carboniferous, as the
shell is required to have internalised in order to liberate the
mantle and evolved in conjunction with a gradual reduction
of the shell.
Nectocaris is contrary to our understanding of cephalopod
evolution and character acquisition, and as such unlikely
to represent a primitive or even derived cephalopod.
While Nectocaris resembles a cuttlefish in overall appearance
and presumed nektonic, free-swimming mode of life, this
is demonstrably convergent. Nectocaris is most likely not a
mollusc, as it lacks any unequivocal molluscan apomorphies.
A more likely hypothesis is that Nectocaris represents
an independent lineage within the Lophotrochozoa, which
developed a mode of life remarkably similar to cephalopods.
Molecular divergence estimates show
that major diversification of cephalopods
took place in the middle and upper
Palaeozoic
Molecular studies of phylogenetic relationships among extant
cephalopods have employed a wide range of phylogenetic
techniques, as well as sequence alignments [18, 41]. These
analyses reveal monophyly of several higher groups, but the
resulting relationships are conflicting in some cases [41]. A
growing consensus shows that coleoids are organised in two
major groups: the Vampyropoda and the Decabrachia, while
nautilids are sister groups to the coleoids.
Also, in the last half-decade, the divergence times of ceph-
alopod groups have been estimated using different methods
[41–43] with different results (Table 2). In order to independ-
ently test the timing of divergence with a molecular clock, we
estimated the divergences of the major cephalopod groups
using a Bayesian relaxed molecular clock analysis with a set of
seven genes [44]. This set of genes is different from those
previously used to date cephalopod origins. We used multiple
external calibrations on a number of different outgroups using
parameters previously found to be optimal for this data [45].
Analyses were made using the phylogenetic package
Phylobayes [46] (Material and Methods are available in the
supplement). In our study (Fig. 5), the coleoids were estimated
to have diverged in the early to middle Permian
(276  75 Ma), while Nautilus diversified from coleoids at
the Silurian/Devonian boundary (416  60 Ma). Some of
these divergence dates are younger than previous estimations
[41, 47], but are similar to the study by Bergmann et al. [42] and
Warnke et al. [43], which used different genes, models and
software than employed here. This is evidence of a consistent
signal from the molecular record. The divergence estimates in
these analyses are congruent at several points with the fossil
record, but also call for some alternative hypotheses.
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Table 2. Compilation of divergence dates of previous molecular clock analyses. The results from using haemocyanin gene sequences
[42,43] are in good accordance with the Bayesian relaxed molecular clock analysis presented herein that yields a 416 W 60 Ma
cephalopod divergence and a 276 W 75 Ma coleoid divergence (see Fig. 4).

Review essays
Authors Group Method Hypothesis
Strugnell et al., 2006 Decabrachia Internal calibrations on a dataset of six mitochondrial Decabrachians evolved in the Early-
and nuclear genes and multiple coleoid taxa middle Palaeozoic (c. 360 Ma)
Strugnell et al., 2006 Vampyropoda Vampyropods diverged by or before
the Permian (c. 250 Ma)
Bergmann et al., 2006 Cephalopoda Haemocyanin gene sequence, single calibration of Divergence between Nautilus and
the cephalopod root with gastropods (520 Ma) Coleoidea at 415 ( 24 Ma)
Bergmann et al., 2006 Coleoidea Coleoid divergence at 242 Ma
Warnke et al., 2011 Cephalopoda Haemocyanin gene sequence, single calibration of Divergence between Nautilus and
the cephalopod root with gastropods (550 Ma) Coleoidea at 453  60 Ma
Warnke et al., 2011 Decabrachia Divergence between Spirula and
decabrachia at 150 (30) Ma

The ancestor of extant cephalopods – a
late-comer according to molecular data
The early Paleozoic evolutionary history of cephalopods is one
of a dramatic diversification in shell shapes (conchs). The
ancestral slender and slightly bent conch of Plectronoceras
led to perfectly straight conical forms, to strongly backward
and forward coiled forms, and to exotic dome-shaped conchs.
Similar conch morphologies evolved repeatedly and inde-
pendently in a number of lineages. A repeating theme in these
early groups is the evolution of coiled conchs [48]. Nautilus
(and the single other genus Allonautilus [49]) is the only extant
cephalopod among hundreds of extinct, coiled cephalopod
genera that evolved, often independently, since the Cambrian.
The reconstruction of the phylogeny of Nautilus is complicated
by a relatively high number of very similar, but independently
evolved, potential ancestors and by its rarity in pre-Carboni-
ferous sediments.
Traditionally the hypothesized ancestors of Nautilus were
positioned in a group of strongly curved Paleozoic cephalo-
pods, the Oncocerida (Fig. 5), which appeared in the earliest
Ordovician (480 Ma) and went extinct during the Paleozoic
[50, 51]. In contrast, the coleoids are hypothesised descend-
ents of a specialised group of cephalopods with simple straight
shells (the Orthocerida) [52, 53]. The fossil record indicates a
divergence between these hypothesised ancestors of Nautilus
and the straight ancestors of coleoids by the early Palaeozoic
(480 Ma) [50, 51, 54].
The molecular divergence estimates in this paper imply
a mid Paleozoic (416 Ma, latest Silurian) ancestor of
Nautilus and coleoids. In fact, the Paleozoic evolution
of the Nautilus lineage and their origin is highly disputed
[55–58]. Because of the extremely poor fossil record of poten-
tial pre-Carboniferous Nautilus ancestors, the reconstruction
of phylogenetic relationships of the few coiled forms known is
based largely on speculation. A mid-Paleozoic origin of the
ancestor of extant nautiloids in the lineage of coleoid straight-
shelled ancestors fits conveniently in the picture emerging
from paleontological data (Fig. 6A), but specific transitional
forms have yet to be discovered.
These new data have profound consequences for the
reconstruction of nautiloid origins and higher classification
of fossil cephalopods. The data suggest that Early Paleozoic
cephalopods should be conceived as stem group cephalopods,
outside the classification of extant cephalopods (Fig. 5). This
also has profound consequences for the reconstruction of the
‘ancestral cephalopod’ [59], because now all crown group
cephalopods together represent a relatively derived clade.
Thus, morphological characters, such as the presence of
five-arm compartments in Nautilus and coleoids and other
characters listed as cephalopod synapomorphies [60] do not
necessarily inform us about the appearance of Early
Palaeozoic stem group forms. Similarly, the otherwise puz-
zling observation that beaks seen in extant cephalopods are
not found in cephalopods older than from the Devonian period
would be explained if this organ is restricted to the cephalopod
crown group diverging at this time.
Shell internalisation led to a marked
increase in cephalopod complexity
Extant cephalopod diversity is dominated by coleoids with
internalised and often highly reduced rudimentary shells. This
transition from external to internal shells led to a much more
active mode of life as is evident when comparing Nautilus with
its coleoid sister-group of squids, cuttlefish and octopods. The
shell lost its protective function and became solely an efficient
buoyancy compensation device. The mantle was thereby liber-
ated to become a muscular pumping organ that led to a much
more powerful jet propulsion system and the mantle also
developed lateral fins for swimming.
To search for the origin of the coleoid habit and ancestry
one needs to look for the internalisation of the chambered part
of the shell, the phragmocone. It can be identified by the
presence of additional shell layers added to the outer
surface of the primary shell wall by encasing soft tissues.
This secondary deposit is secreted by the muscular mantle
and is commonly called a rostrum (Fig. 1D). The oldest unam-
biguous coleoid with a rostrum is Early Carboniferous in age
(Upper Mississippian) [53, 61]. Recently, the number of coleoid
relatives from younger Carboniferous strata has increased
significantly, but the details of their phylogenetic relationships
remain to be revealed [50, 61, 62]. Currently, a consensus among

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Coleoidea Nautiloidea
Review essays

Decabrachia Vampyropoda

Sepiolida Octopoda

Nautilida (Nautilus)
Spirulida (Spirula)

Vampyromorpha

other Mollusca
Enteroctopus

Cirroctopoda
Oegopsida
Euprymna
Idiosepius

Myopsida

Octopus
Sepiida

stem group
Coleoidea
ma
0

Ammonoidea
CENOZOIC

Belemitida
Diplobelida
CRETACEOUS

Orthocerida
100
Phragmoteuthida

?
Aulacocerida
JURASSIC

stem group
200 Cephalopoda
Bactritida
TRIASSIC

Donovanoconida
PERMIAN

septate monoplacophoran-like molluscs (e.g.Tannuella)

Hematitida

Oncocerida

300
CARBONIF.

Discosorida
DEVONIAN

monoplacophoran-like molluscs
Ellesmerocerida

400
ORDOVICI. SILUR.

Plectronocerida

loss of gladius

loss of phragmocone (no mineralised shell)

500
CAMBRIAN

internalised phragmocone

phragmocone

septa
EDIACARAN

mineralised shell molecular divergence datum

600

Figure 5. A molecularly calibrated time-tree of cephalopod evolution. Nodes marked in blue are molecular divergence estimates (see methods
in Supplemental Material). The divergence of Spirula from other decabrachiates are from Warnke et al. [43], the remaining divergences are
from analyses presented in this paper. Bold lineages indicate the fossil record of extant lineages, stippled lines are tentative relationships
between modern coleoids, partly based on previous studies [41, 76, 82] and fossil relationships are based on current consensus and hypoth-
eses presented herein. Shells of stem group cephalopods and Spirula in lateral view with functional anterior left. Shells of coleoids in ventral
view with anterior down. The Mesozoic divergence of coleoids is relatively poorly resolved compared to the rapid evolution of Cambro-
Ordovician stem group cephalopods. Many stem group cephalopod orders not discussed in the text are excluded from the diagram.

608 Bioessays 33: 602–613,ß 2011 WILEY Periodicals, Inc.

.... Prospects & Overviews
Figure 6. The tilting of the body axes of extant cephalopods. This
was a result of a polyphyletic and repeated trend towards enhanced
manoeuverability. The morphological body axes (anterior-posterior,
dorso-ventral) are tilted perpendicularly against functional axes in
A: the transition towards extant cephalopods, and B: in several stem
group cephalopods, such as in the Silurian Ascocerids (Drawings by
Brian Roach) modified from Furnish and Glenister, 1964, Fig. 190
[83] (Photo: Ascoceras bronni, Czechoslovakia, Bohemia, Early Late
Silurian, YPM 189333, scale bar: 1 cm).
paleontologists has emerged, whereby Coleoidea originated
within the bactritids, a group of extinct cephalopods with
straight, external shells [53] (Fig. 5).
The exact divergence time of crown group coleoids is
difficult to determine based on the fossil record. The fossil
record clearly indicates that coleoids had diversified at least by
the Triassic (see Box), which is in good agreement with our
molecularly estimated late-early Permian divergence. The
Box:
The fossil record of the coleoid radiation
The reconstruction of the phylogeny of fossil coleoids is
complicated by the rarity of fossils and often times
incomplete preservation. The existence of Paleozoic
representatives of the ten armed squids (Decabrachia)
is currently under discussion [62, 64, 87, 88]. The first
undoubted spirulids are known from Late Jurassic
deposits [87, 88]. This is in excellent accordance with
recent molecular clocks [43] (see Table 2). The first
occurrences of undoubted sepiids are from the Late
Cretaceous [89]. Similarly, the origin of the eight-armed
vampyropods is still debated. The first unequivocal evi-
dence of cirroctopods and octopods come from Late
Cretaceous deposits [16, 90]. Soft part morphologies
suggest vampyropod affinities of Mesozoic gladius-
bearing coleoids [81, 91–94]. Clear evidence of fossil
teuthids is still lacking [95].
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B. Kröger et al.
Review essays
molecular clocks suggest that the Carboniferous putative
crown group coleoids (Pohlsepia, Shimanskya) [63, 64] should
be interpreted as stem group coleoids, but this also requires
further morphologic and systematic scrutiny.
The combined data from molecular clock analyses and
fossils suggest that after the initial internalisation of the ceph-
alopod shell, which was a singular event, morphological
diversity of cephalopods with internal shells rapidly increased
during the later Paleozoic. The earliest representatives of the
coleoid crown group existed by the earliest Mesozoic. Most
likely, the transition from external to internal shells that led to
a much more active mode of life, more powerful jet propulsion
and effective manoeuverability initiated a late Paleozoic adap-
tive radiation of coleoids. The further reduction of the shell and
increased ability to engage in active life-modes remained a major
theme in the subsequent coleoid radiation until the present.
Convergent evolution and arms races led
to repeated events of shell reduction
Coleoid cephalopods exhibit several degrees of shell
reduction, including the complete loss of supporting hard
parts. However, this character state is far from diagnostic, as
several lineages within coleoids, in addition to other Palaeozoic
cephalopod groups, convergently developed varying degrees of
shell reduction. The major advantage of such drastic modifi-
cations is presumably linked to an increased ability to engage in
active modes of life, facilitated by efficient jet propulsion
systems. Cephalopods fully enclosed within a shell, such as
Nautilus, rely on so-called shell pumping [65] to generate
water propulsion. This is relatively sluggish compared to
the system employed by extant coleoids in which pumping
is achieved through flexing a muscularised mantle, allowing
for enhanced water flow and a more powerful exhalation.
Presumably, increased competition with other pelagic preda-
tors, such as fish, for targeted prey led to the selective pressure
towards reduced shells and increased mobility [66]. Listed below
are some of the identified pathways for shell reduction, most
of which happened convergently throughout cephalopods.
609
 B. Kröger et al.
Truncation of the shell
Several Paleozoic lineages started reducing the size of the
phragmocone relative to the soft body. This would have
Review essays
increased the overall manoeuverability and compactness of
the conch, without having to evolve an internal shell. Some
of the earliest forms to evolve a truncated shell are the
Ascocerida (460–416 Ma). Furthermore, they developed a
phragmocone obliquely and dorsally positioned inside the last
chamber in which the animal lives (body chamber); similar in
many respects to the sepiid cuttlebone [67, 68] (Fig. 6B).
Truncation also occurs in the Middle Silurian Sphooceras
[69], a unique cephalopod that sealed its apical chambers
with massive aragonitic deposits, and in the enigmatic
Carboniferous Brachycycloceras [70]. Another convergent
trend in the reduction of the phragmocone span is through
shell coiling [66].
The earliest undoubted cephalopod with an internal shell
is the Early Carboniferous Hematites [53, 71, 72] that evolved
from the bactritoids. The phragmocone is usually truncated
and the broken apex is subsequently overgrown to form the
rostrum. A diverse number of cephalopod fossils with straight
rostrate shells occur from the Late Carboniferous onwards.
These forms have been interpreted as stem group coleoids
(previous section).
Opening of the body chamber
Similar to the unrelated ascocerids, the Triassic phragmo-
teuthids (Fig. 5) reduced the ventral side of the body
chamber, which likely gave the anterior mantle more space
to allow for powerful muscular contractions and jet
propulsion.
Glossary
Convergent evolution: Describes the acquisition of the
same biological trait in unrelated lineages. An example is
the wings of bats and birds, which both evolved from the
tetrapod front limb and acquired a similar form and func-
tion independently. Such traits are called analogous traits.
Homologous traits, by contrast, were present in the last
common ancestor of both lineages.
Crown group: The smallest monophyletic group, or
clade, to contain the last common ancestor of all extant
members, and all of that ancestor’s descendants.
Lagerstätten: A German word for natural mineral
deposits (literally ‘‘storage place’’) used by paleontolo-
gists for a fossil locality that preserves fossils in extra-
ordinary quantity or quality.
Monophyletic: When a group of organisms are each
other’s closest relatives. Thus, a monophyletic group con-
tains all the descendants of the latest common ancestor.
Relaxed molecular clock: A statistical approach to
estimating divergence times between lineages using
Monte Carlo Markov Chain calculation. The method can
610
Prospects & Overviews ....
Development of a proostracum
In contrast to the Triassic phragmoteuthidids, several
Jurassic/Cretaceous coleoids lost the body chamber entirely
and an anteriorly projected proostracum evolved [73]. The
proostracum is an anterior prolongation of the phragmocone,
which provides an attachment site for the strong muscular
mantle. As a result, the phragmocone occupies only a com-
paratively moderate space in the posterior mantle.
Demineralisation
Varying degrees of demineralisation can be observed in shell
parts of various distantly related coleoids. A reduced thickness
of the rostrum can be seen for instance in the Jurassic/
Cretaceous Diplobelida [74, 75]. Descendents of the
Phragmoteuthida completely lost the ability to mineralise
their shells, resulting in the development of a purely organic
shell remnant, the gladius [61]. Although the origin of the
Decabrachia is still poorly understood, phylogenetic relation-
ships suggest that demineralisation must have independently
occurred at least three times within the Decabrachia [76, 77].
In coleoids, the loss of mineralisation is coupled with
the total loss of Nautilus-style buoyancy regulation. Neutral
buoyancy must be achieved through permanent swimming
or secreting low-density aqueous solutions in body tissues
(sulfate in octopods and vampyrotheutids; ammonia in
decabrachiates).
Reduction of the organic components of the shell
Within the Teudopseina, a Mesozoic group of eight-armed,
gladius-bearing vampyropods, there is a trend towards a
be different to a strict molecular clock model, which
assumes a constant rate of genetic substitutions across
organisms. This is rarely ever observed in natural systems.
Heterogeneous rates of molecular evolution can be esti-
mated by calibrating rates with external age information,
usually based on several appearances of taxa in the fossil
record. A Bayesian framework is particularly useful in this
endeavor, as temporal uncertainty in the fossil age can be
approximated by parametric distributions that act as pri-
ors on individual node ages.
Septa: The mineralised walls that separate chambers
in cephalopod shells.
Stem group: All the fossil forms that are closely
related to a crown group, but have not descended from
its last common ancestor. An example of this could be
Archaeopteryx, which is a stem group bird. Similarly,
Diplodocus and Stegosaurus are stem group birds.
Although very different to birds, all dinosaurs form part
of the lineage to birds and are thus stem groups.
Stratigraphy: Geological term for the study of the
correlation of rock units. Biostratigraphy utilises the fossil
record to correlate rocks by similar fossil content.
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.... Prospects & Overviews
reduced gladius [78–81]. The fin supports of the Cirroctopoda,
and the stylet-like shell vestiges of the Octopoda, are considered
to represent the remains of a teudopseid gladius. Reduction of
the gladius is most probably accompanied by a shift in the
locomotory mode. As exemplified by living cirroctopods, loco-
motion is heavily reliant on fin-powered swimming.
Total loss of the ability to secrete a shell
Some octopods completely lost the ability to secrete organic
shells (even vestiges), resulting in a loss of attachment sites
for fins. This radical shell reduction results in increased
body plasticity. As their life habitat clearly shows, benthic
octopods are capable of moving through minute crevices in
rocks.
Conclusions
This review of cephalopod origins demonstrates that a
synoptic approach is a valuable way to test observed patterns
and search for congruence. The trajectories of some morpho-
logical changes carry their legacy in both embryological
development and the fossil record. We expect that new fossil
finds and improved molecular methods will help refine our
interpretations, but overall we believe the new molecular
results are remarkably congruent with our previous knowl-
edge. Relaxed molecular clocks provide an independent
means to evaluate the fossil record, and choose between
markedly differing hypotheses. Growing evidence demon-
strates that modern cephalopods originated from straight-
shelled orthocerids in the late Silurian (416 Ma). The
putative coleoid fossils in the Carboniferous had a debated
affinity with extant groups, but are arguably stem groups. The
molecular clock suggests that the divergence of the coleoids
was in the Permian, well before the appearance of accepted
members of the coleoids.
Several gaps are still present in our knowledge of ceph-
alopod evolution and this review should serve as food for
thought for students interested in cephalopod evolutionary
studies. We see the basal origin and relationship of
decabrachians as one of several potential major ventures
for future research for both molecular biologists and
paleontologists.
Acknowledgments
We are grateful to Peter Ward (U. Washington) and Michele
Nishiguchi (U. New Mexico) for the gift of Nautilus and
Euprymna RNA extractions, Erik Sperling (Harvard) collected
tissue samples of Nautilus as well as Enteroctopus at Friday
Harbor, assisted by Meghan Rock (Columbia College). The
Carlsberg Foundation funded the molecular work of JV.
Daniel J. Field and Allison Hsiang assisted JV in the molecular
lab. Brian Roach (Yale) generously took time to make most of
the drawings. Daniel J. Field (Yale), Úna Farrell (Yale), Marc
Laflamme (Yale) and Kenneth De Baets (U. of Zürich,
Switzerland) provided invaluable comments on the manu-
script. The reconstruction of the Plectronoceras soft body
benefited from discussions and support from Vyacheslav
Bioessays 33: 602–613,ß 2011 WILEY Periodicals, Inc.
B. Kröger et al.
Bizikov (Moscow U.). Mark Florence facilitated the loan of
P. cambria.
Review essays
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