Journal of Systematics and Evolution

47 (5): 497508 (2009)

doi: 10.1111/j.1759-6831.2009.00028.x

Phylogenetic biogeography and taxonomy of disjunctly distributed

bryophytes
1

Jochen HEINRICHS
1

Jorn HENTSCHEL 1 Kathrin FELDBERG

2
Harald SCHNEIDER

Andrea BOMBOSCH

(Department of Systematic Botany, Albrecht von Haller Institute of Plant Sciences, Georg-August-University, D-37073 Gottingen, Germany)
2

(Botany Department, Natural History Museum, London SW7 5BD, UK)

Abstract More than 200 research papers on the molecular phylogeny and phylogenetic biogeography of bryophytes
have been published since the beginning of this millenium. These papers corroborated assumptions of a complex genetic structure of morphologically circumscribed bryophytes, and raised reservations against many morphologically
justified species concepts, especially within the mosses. However, many molecular studies allowed for corrections
and modifications of morphological classification schemes. Several studies reported that the phylogenetic structure
of disjunctly distributed bryophyte species reflects their geographical ranges rather than morphological disparities.
Molecular data led to new appraisals of distribution ranges and allowed for the reconstruction of refugia and migration routes. Intercontinental ranges of bryophytes are often caused by dispersal rather than geographical vicariance.
Many distribution patterns of disjunct bryophytes are likely formed by processes such as short distance dispersal,
rare long distance dispersal events, extinction, recolonization and diversification.
Key words bryophytes, cryptic speciation, disjunctions, divergence time estimates, Diversity Arrays Technology,
DNA sequence variation, isozymes, molecular phylogeny.
Bryophytes (liverworts, mosses and hornworts)
comprise the three lineages of land plants with a life
cycle in which the haploid gametophyte is the dominant photosynthetic active generation. In contrast to
other land plants, the sporophyte is unbranched and not
autonomously viable (Schofield, 1985). Bryophytes disperse frequently both by spores and by propagules that
descend from the gametophyte, or by unspecialized gametophyte fragments with a high potential of regeneration (Correns, 1899). Bryophytes are the progeny of the
first plants that successfully colonized terrestrial habitats (Qiu, 2008). Their evolution in space and time is
still insufficiently known.
In the nineteenth and early twentieth centuries,
bryologists preferred to use a geographical or typological species concept where species were defined
as largely invariant units. Many species were known
only from type material (e.g., Stephani, 18981925;
Warnstorf, 1911). More recently, authors accepted intraspecific morphological variation and lowered numerous local taxa to synonyms of widespread bryophyte
species (Gradstein, 1994; Buck, 1998; Heinrichs, 2002).
Consequently, broad geographical ranges that often span


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Received: 11 November 2008 Accepted: 26 February 2009

Author for correspondence. E-mail: jheinri@uni-goettingen.de; Tel.: +49551-39-22220; Fax: +49-551-39-22329.

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several continents were assigned to many morphologically circumscribed bryophyte species (Herzog, 1926;
Grolle, 1969; Gradstein et al., 1983; Schofield, 1992;
Tan & Pocs, 2000). The resulting disjunct ranges of
bryophyte species have frequently been explained by
ancient vicariance and slow rates of morphological evolution (Herzog, 1926; Crum, 1972; Frey et al., 1999) but
other authors provided experimental evidence for the alternative scenario of successful long distance dispersal
of bryophytes by spores (van Zanten, 1978; van Zanten
& Gradstein, 1988).
The increasing availability of DNA sequence data
now enables the testing of morphology-based taxonomic and biogeographic concepts and the disclosure
of the genotype structure of species. DNA sequence
data also allow for an evaluation of different hypotheses
concerning biogeographical patterns and processes.

1 Morphological species concepts in the light

of molecular phylogenies: indications of nonmonophyly and need for a revised taxonomy
An increasing body of published work points to
many taxonomic incongruences of widespread morphologically circumscribed bryophyte species and phylogenies derived from molecular markers. Shaw &
Allen (2000) resolved populations of morphologically

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circumscribed species of the aquatic moss genus

Fontinalis Hedw. in widely diverging clades, as did
Vanderpoorten et al. (2004) for species of Hygroamblystegium Loeske and Shaw et al. (2008) for representatives of the Sphagnum subsecundum complex.
Stech & Wagner (2005) provided evidence for the polyphyly of several species of Campylopus Brid. Werner
& Guerra (2004) resolved Tortula vahliana (Schultz)
Mont. nested within Tortula muralis Hedw. Draper et al.
(2007) showed the non-monophyly of the pleurocarpous
moss species Isothecium alopecuroides (Dubois) Isov.,
Isothecium holtii Kindb. and Isothecium myosuroides
Brid. Vanderpoorten & Goffinet (2006) identified several species of the moss Brachytheciastrum Ignatov
& Huttunen as polyphyletic and documented parallel morphological evolution within this genus. Similarly, Cano et al. (2005) found incongruences between
current classification schemes of the Tortula subulata
complex, and a molecular topology. Incongruences between morphology-based classifications and molecular
topologies have also been shown for several liverwort
genera including Bryopteris (Nees) Lindenb. (Hartmann
et al., 2006), Chiloscyphus Corda (Hentschel et al.,
2006), Herbertus Gray (Feldberg et al., 2004), Lophozia
(Dumort.) Dumort. (Vilnet et al., 2008), Plagiochila
(Dumort.) Dumort. (Rycroft et al., 2004), and Porella
L. (Hentschel et al., 2007b).
As a consequence of the numerous observations
of species polyphyly, Vanderpoorten & Goffinet (2006)
raised reservations regarding current species definitions.
However, in many cases the molecular topologies allowed for a modified appraisal of morphological evidence including new circumscription of taxa or changes
of rank. Vanderpoorten (2004) solved the problem of
non-monophyletic Hygroamblystegium species by introducing a wide species concept for Hygroamblystegium
varium (Hedw.) Monk. Cano et al. (2005) proposed the
binomen Tortula schimperi Cano et al. for a taxon that
was usually treated as a variety of T. subulata Hedw.
Rycroft et al. (2004) reinstated the leafy liverwort Plagiochila maderensis Steph. that was earlier placed in the
synonymy of Plagiochila spinulosa (Dicks.) Dumort.
Attempts to establish monophyletic entities may
be hampered by reticulate evolution (Shaw & Goffinet,
2000; Natcheva & Cronberg, 2004, 2007; Shaw et al.,
2008). Introgression, hybridization and incomplete lineage sorting may contradict a taxonomy that is strictly
based on the monophyly concept.
Redefinitions of species are often connected with
changes of distribution range concepts. Pfeiffer et al.
(2004) showed phylogeographic structure within the
AustralasianSouth American simple thalloid liverwort
Hymenophyton flabellatum (Labill.) Trev. Based on the

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outcome of their molecular phylogenetic analyses and

accompanying morphological studies, they restricted
the range of H. flabellatum to Australasia, and reinstated the New ZealandTasmanian Hymenophyton leptopodum (Hook.f. & Taylor) A.Evans as well as the
southern South American Hymenophyton pedicellatum
Steph. Based on molecular evidence, Feldberg et al.
(2004, 2007) excluded Herbertus dicranus (Taylor) Trevis. from tropical America and proposed the application of the name Herbertus sendtneri (Nees) A.Evans,
a taxon that was previously assigned to European and
Asian populations only. Heinrichs et al. (1998, 2004,
2005a, b) lowered the European Plagiochila killarniensis Pearson to a synonym of the Neotropical Plagiochila
bifaria (Sw.) Lindenb., included several African and
Neotropical binomia in the European taxon Plagiochila
punctata (Taylor) Taylor, and extended the range of
the Neotropical Plagiochila boryana Steph. to tropical Africa. Hedenas (2008a) excluded the African Antitrichia kilimandscharica Broth. and the western North
American Antitrichia gigantea (Sull. & Lesq.) Kindb.
from the synonymy of Antitrichia curtipendula (Hedw.)
Brid.
It is assumed that ongoing studies into the molecular phylogeny of bryophytes will lead to numerous new
appraisals of ranges.

2 Internal structure of bryophyte species:

molecular variation versus morphological
stasis
Sequencing of variable nuclear or chloroplast
markers of multiple accessions of bryophytes usually
reveals a phylogenetic structure that follows a geographical rather than a morphological pattern (Shaw
& Allen, 2000; Skotnicki et al., 2004; Grundmann
et al., 2006; Hartmann et al., 2006; Vanderpoorten &
Long, 2006; Feldberg et al., 2007; Hentschel et al.,
2007b; Hedenas, 2008a, b; Hedenas & Eldenas, 2007;
Huttunen et al., 2008). Genetic variation without concordant morphological variation has often been regarded as an indication of cryptic speciation (Shaw,
2001; Fernandez et al., 2006; Bickford et al., 2007).
However, it is not yet clear if the molecular variation that has been documented for many morphospecies
of bryophytes always reflects genetically incompatible
units. An apparent lack of interchange of genetic material could also be a result of a geographic or ecological
separation of populations that still hold the potential
to interbreed successfully. If future studies allow for a
more definite decision on hybridization capability of

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bryophyte populations, a refined taxonomy including a

partial return to the geographical species concept seems
possible, especially in taxa in which different clades can
be assigned to clear-cut ranges. Application of the geographical species concept is contradicted by indications
of infrequent long distance dispersal events in many
bryophyte lineages (Skotnicki et al., 2001; McDaniel &
Shaw, 2005; Hentschel et al., 2007b; Huttunen et al.,
2008). Even more difficult is the formal recognition of
different sympatric genotypes that show no or very limited morphological differences.
The complex thalloid liverwort Conocephalum
F.H.Wigg. is possibly the most exhaustively studied example of a genetically heterogeneous bryophyte species.
Isozyme studies in the Holarctictemperate Asian
Conocephalum conicum (L.) Dumort. s.l. revealed the
presence of six partly sympatric taxa that were informally named using a letter system (Odrzykoski
& Szweykowski, 1991). Subsequent detailed study of
morphological and ecological traits led to the formal
recognition of one of them as Conocephalum salebrosum Szweyk. et al. (Szweykowski et al., 2005). This
species occurs sympatrically with C. conicum s.str. but
tends to grow in dryer habitats. Boisselier-Dubayle
et al. (1998) reported the presence of a morphologically indistinct Mediterranean sibling species besides
the EuropeanAsianAmericanAfrican complex thalloid liverwort Reboulia hemisphaerica (L.) Raddi s.str.
Similarly, the subcosmopolitan simple thalloid liverwort
Aneura pinguis (L.) Dumort. s.l. seems to include at least
three reproductively isolated, sympatric cryptic species
(Wachowiak et al., 2007). Evidence for cryptic speciation was also provided for the Holarctic simple thalloid liverworts Pellia epiphylla (L.) Corda and Pellia
endiviifolia (Dicks.) Dumort. (Pacak & SzweykowskaKulinska, 2000; Fiodorow et al., 2001).
Similar findings are available for several mosses.
Bijlsma et al. (2000) provided evidence for the presence of two reproductively isolated cryptic species in
the acrocarpous moss Polytrichum commune Hedw.
[P. commune s.str., Polytrichum uliginosum (Wallr.)
Schriebl, see also van der Velde & Bijlsma, 2004)]. McDaniel & Shaw (2003) recovered a deep split between
the two morphologically weakly separated subspecies
of the trans-Antarctic moss Hymenodontopsis mnioides
(Hook.) N.E.Bell et al. Fernandez et al. (2006) analyzed
amplified fragment length polymorphisms of Californian populations of the cosmopolitan species Grimmia
laevigata (Bridel) Bridel. They identified two distinct
geographically overlapping clades. Shaw (2000) published a nrITS phylogeny of Mielichhoferia elongata
(Hoppe & Hornsch.) Nees & Hornsch. Based on the
outcome of his analyses he proposed two cryptic species

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within the morphologically uniform taxon, one with a

EuropeanNorth American range, and the other strictly
North American. Hedenas & Eldenas (2007) investigated nrITS and chloroplast DNA haplotype variation
of the pleurocarpous moss Hamatocaulis vernicosus
(Mitt.) Hedenas. Based on their topologies Hedenas &
Eldenas (2007) postulated the existence of two cryptic
species, of which one is widespread in Europe, in addition to a few North American records. The other cryptic
species was found south of the boreal zone in Europe, in
northern-most Asiatic Russian Federation, and Peru.

3 Phylogeographic patterns, migration

routes, and modes of reproduction as revealed
from molecular data
Studies of haplotype variation do not only allow
for the recognition of putative cryptic taxa but also for a
reconstruction of the spatial structure of genetic diversity, potential bottleneck events, and modes of reproduction. Grundmann et al. (2007) studied DNA sequence
and allozyme variation to resolve the spatial structure
of Mediterranean accessions of the dioecious Holarctic
moss Pleurochaete squarrosa (Brid.) Lindb. These authors observed a decline of intraspecific variation from
west to east but no difference in gene diversity among
populations from islands and mainland areas. Based on
the latter observation, Grundmann et al. (2007) concluded that the large Mediterranean islands might function as mainland for bryophytes. Vanderpoorten et al.
(2008) arrived at a similar conclusion when analyzing chloroplast markers of the moss Grimmia montana
Bruch & Schimp. Madeiran and Mediterranean haplotypes of G. montana were identical or closely related to
European or North American ones.
Grundmann et al. (2008) analyzed diversity patterns of European P. squarrosa using nuclear and
chloroplast DNA sequences, and enzyme electrophoresis. These authors provided evidence for sexual reproduction, that is, recombination, of P. squarrosa in the
Mediterranean Basin and the Kaiserstuhl Mountains in
southwestern Germany, a region that is well known for
its unusual climate with high monthly average temperatures and short, mild winter. In other regions of
central and northwest Europe P. squarrosa disperses
predominantly by vegetative propagules, a finding that
is corroborated by a lack of evidence of recombination. Grundmann et al. (2008) also postulated a postglacial recolonization of central Europe from the Iberian
Peninsula and the Balkans. Cronberg (2000) observed
quite similar patterns for the epiphytic moss Leucodon

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sciuroides (Hedw.) Schwagr. Mediterranean populations reproduce sexually and are genetically diverse
whereas more northern populations reproduce vegetatively and are genetically quite uniform. This pattern coincides with the expectation of a loss of genetic variation
in populations at the northern limit of the glacial refugia. Glacial survival in southern Europe is obviously not
a general pattern in bryophytes. Hedderson & Nowell
(2006) recognized several unique Homalothecium
sericeum (Hedw.) Schimp. haplotypes in the British
Isles and adjacent mainland. Based on this observation Hedderson & Nowell (2006) assumed a survival of
Homalothecium sericeum in this region during the last
glacial period.
Szoveni et al. (2006) presented a chloroplast phylogeographic analysis of Sphagnum fimbriatum Wilson
and Sphagnum squarrosum Crome. Their haplotype distribution patterns seem to support different dispersal
scenarios for these species. S. fimbriatum seems to have
survived the last glacial period along the Atlantic coast
of Europe, and rapidly colonized Europe after the last
glacial maximum. In contrast, S. squarrosum obviously
had numerous scattered refugia throughout Europe.
Although most studies referring to the internal
structure of widespread bryophyte species revealed
molecular variation, a few examples contradicted this
tendency. James et al. (2008) introduced the Diversity
Arrays Technology, a hybridization-based genotyping
method, to reproducibly detect largely low-copy genomic variation in ferns and mosses. Their study revealed a lack of phylogenetic pattern in the Australian
moss Garovaglia elegans (Dozy & Molk.) Bosch &
Sande Lac. Similarly, van der Velde & Bijlsma (2003)
found nearly no genetic structure among European populations of several Polytrichum species (Polytrichum
commune, Polytrichum uliginosum, Polytrichum formosum Hedw., and Polytrichum piliferum Hedw.). The lack
of allozyme and microsatellite variation pointed to extensive spore dispersal and contradicted the hypothesis
of a recolonization of Europe from southern refugia after the last glacial period.
Inter- or intraspecific variation of molecular markers might allow for the reconstruction of range expansion directions. Based on the recent distribution of taxa
and their position in a phylogenetic framework, conclusions can be drawn as to the ranges of their ancestors. Heinrichs et al. (2005a) resolved an African
accession of Plagiochila sect. Hylacoetes Carl within
several tropical American accessions. Based on this
topology, these authors proposed a Neotropical origin
of the African Plagiochila sect. Hylacoetes populations.
Hartmann et al. (2006) arrived at the same conclusion
for the MadagascarReunion endemic Bryopteris gau-

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dichaudii Gottsche. Feldberg et al. (2007) studied the

phylogenetic biogeography of Herbertus and provided
evidence for a colonization of Africa from Neotropical
and Asian populations (Fig. 1). Huttunen et al. (2008)
discovered evidence for a western North American origin of a Holarctic Homalothecium clade.
Taxonomic work combined with the reconstruction of migration routes provided new insights into the
relationships between floristic regions. Contrary to the
earlier belief, the Atlantic European and Macaronesian
Plagiochila taxa are connected with Neotropical rather
than Asiatic taxa (Heinrichs et al., 2006). Vanderpoorten
& Long documented relationships of Macaronesian and
Neotropical Leptoscyphus Mitt. Similarly, Stech et al.
(2007) showed the close relationships of the Campylopus flora of tropical America and Madeira. This trend is
contradicted by the example Porella with the Macaronesian endemic Porella inaequalis Perss. closely related
to the Asian Porella grandiloba Lindb. rather than to
Neotropical species (Hentschel et al., 2007b). Clearly
more case studies are necessary to decide whether each
species has its own history or whether there are recurring patterns.

4 Intercontinental range expansion versus

conservation
Wegeners (1915) reconstruction of continental
drift has provided a theory to explain disjunct distribution patterns of plants. Some bryologists (Stotler
& Crandall-Stotler, 1974; Gradstein et al., 1983;
Schuster, 1979; Frey et al., 1999) linked ranges of
bryophytes to continental movement. The underlying assumption of geographical vicariance predicts
an origin of many disjunctly distributed bryophyte
species/genera at least in the late Mesozoic. However,
accurate morphology-based insights into the historical
biogeography of bryophytes would require a continuous
fossil record that is not available (Krassilov & Schuster,
1984). The long-distance dispersal ability of bryophytes
(van Zanten, 1978; van Zanten & Gradstein, 1988) contradicts strict vicariance scenarios, as does the frequent
occurrence of widespread bryophyte species on oceanic
islands (Heinrichs et al., 2006; Vanderpoorten et al.,
2007).
Molecular phylogenies enable us to scrutinize evidence for dispersal or vicariance. One possibility concerning this matter is a critical comparison of phylogenies with breakup events of landmasses. Congruence
of ancestral geographical distributions of clades and
the sequence of breakup events rather supports vicariance. However, deviation of a phylogeny and a breakup

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Fig. 1. Molecular phylogeny of the leafy liverwort Herbertus with the reconstruction of putative migration routes and dispersal events. The distribution
of accessions within clade A indicates a dispersal event from tropical America to Africa. An ancestral area reconstruction points to an Asian origin of
clade B (Reproduced from Feldberg et al., 2007 with permission from Wiley-Blackwell).


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sequence supports dispersal (Sanmartin & Ronquist,

2004).
The application of the molecular clock hypothesis allows for a transformation of a phylogram into a
chronogram. Sequences usually do not exactly evolve
at a constant rate but the tempo of mutations within a
molecular marker seems to move in a more or less determined range. Accordingly, a comparison of sequence
variation with that of dated phylogenies may shed some
light on the likelihood of different scenarios (Les et al.,
2003).
Divergence time estimates based on sequence variation and the fossil record will provide more reliable insights into the historical biogeography of lineages by enabling differentiation between coinciding events in time
and pseudo-congruent patterns (Donoghue & Moore,
2003; Renner, 2005). The poor Paleozoic and Mesozoic
fossil record of bryophytes (Oostendorp, 1987) is a serious challenge to any study on the timescale of bryophyte
diversification. Cenozoic fossils are often preserved in
the form of amber inclusions (Grolle & Meister, 2004;
Frahm & Newton, 2005). Amber has not been formed
continuously throughout the history of plants on land
(Grimaldi, 1996). The infrequent generation of amber
inclusions makes it difficult to use them as calibration
points for dating approaches (Hartmann et al., 2006).
Therefore we rely heavily on the variation of substitution rates.
Supraspecific intercontinental ranges are generally accepted for bryophytes and have been confirmed on many occasions (Meissner et al., 1998;
Groth et al., 2003). Several recent studies also confirmed the monophyly of intercontinentally distributed
bryophyte species. NeotropicalAfrican ranges have
been supported by molecular data, for example, for
species of the liverwort genera Chiloscyphus (Hentschel
et al., 2007a), Herbertus (Feldberg et al., 2007),
Pallavicinia Gray (Schaumann et al., 2005), Plagiochila
(Heinrichs et al., 2005a), and Porella (Hentschel et al.,
2007b), and the moss Campylopus (Stech & Wagner,
2005). Similar results are available for North American
European disjunctions, for example, for species of the
moss genera Anacolia Schimp. (Werner et al., 2003),
Claopodium (Lesq. & James) Renauld & Cardot, Dicranoweisa Milde, Scleropodium Bruch & Schimp. (Shaw
et al., 2003), Homalothecium (Huttunen et al., 2008),
and species of the liverwort genera Frullania Raddi
(Hentschel et al., 2009), Herbertus (Feldberg et al.,
2007), Pallavicinia (Schaumann et al., 2005), Porella
(Hentschel et al., 2007b), and Scapania (Dumort.)
Dumort. (De Roo et al., 2007). NeotropicalEuropean
disjunctions have been supported for species of the
liverwort genera Lophozia (De Roo et al., 2007) and

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Plagiochila (Heinrichs et al., 2004), and AsianNorth

American ranges for Porella species (Hentschel et al.,
2007b). The monophyly of even broader species ranges
has been shown, for example, for the moss Tortella
humilis (Hedw.) Jenn. (Neotropics, North America,
Europe) (Werner et al., 2005) or the liverwort Plagiochila punctata (North America, Neotropics, Africa,
Europe) (Davison et al., 2006).
The observed sequence analogies of different accessions of intercontinentally distributed bryophytes led
many authors to assume long distance dispersal as a
feasible explanation for the disjunct ranges (Shaw et al.,
2003, 2008; Forrest et al., 2005; Heinrichs et al., 2005a;
Feldberg et al., 2007; Hentschel et al., 2007b; Huttunen
et al., 2008). A few authors insisted on geographical vicariance and explained similar sequences from different
parts of a disjunct range with stenoevolution, that is,
slow rates of molecular evolution (Frey et al., 1999).
Shaw et al. (2003) tested the likelihood of a
MadreanTethyan origin of several western North
AmericanMediterranean disjunctions of mosses.
These authors stated that no plausible mutation rate
would link the disjunctions to early Miocene times, and
favored recent dispersal as an explanation of the observed distribution ranges. Hentschel et al. (2006) verified the assumption of a recent introduction of the southern hemispheric Chiloscyphus semiteres (Lehm.) Lehm.
& Lindenb. into Europe (Paton, 1965) by demonstrating nrITS sequence similarities of accessions from the
Netherlands and Australia. Wall (2005) documented a
clock-like behaviour of the nuclear glyceraldehyde 3phosphate dehydrogenase gene of the moss Mitthyridium H.Rob., and identified clades that were related
to oceanic archipelagos. Using island ages as calibration points, he provided evidence for a diversification
of Mitthyridium within less than ten million years.
Huttunen et al. (2008) used a mean nrITS substitution
rate to deduce a late MiocenePliocene age of a split between North American and Eurasian Homalothecium.
Hartmann et al. (2006) published a chronogram for
the liverwort Bryopteris and provided hypothetical
timescales based on assumptions of different scenarios, and nrITS mutation rates. These authors could
clearly reject western Gondwanan vicariance for the
NeotropicalAfrican range of Bryopteris, and proposed
a dispersal scenario. Heinrichs et al. (2006) reconstructed the molecular phylogeny of the cosmopolitan
leafy liverwort Plagiochila and presented timescales
based on putative fossil assignments. The results did not
contradict a Gondwanan origin of Plagiochila, but the
geographical distribution of clades (Fig. 2) and divergence time estimates rendered Gondwanan vicariance
unlikely. Heinrichs et al. (2006) explained the observed

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Fig. 2. Molecular phylogeny of the leafy liverwort Plagiochila. Distribution of species is indicated at branches. 1, Australasia; 2, Southern South
America; 3, Subantarctics; 4, Neotropics; 5, Asia; 6, Western Holarctics; 7, Eastern Holarctics; 8, Africa; 9, Hawaiian Islands. Modified from Heinrichs
et al. (2006). BT, bootstrap.


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distribution patterns as a result of short distance dispersal, rare long distance dispersal events, extinction, recolonization and diversification. It is not yet clear if the
situation in Plagiochila represents a general pattern but
several other studies seem to support this combination
of mechanisms (Feldberg et al., 2007; Huttunen et al.,
2008). Support also comes from comparisons of Southern Hemispheric ranges of bryophytes and main wind
directions. Munoz et al. (2004) found a stronger correlation of floristic similarities with wind connectivity
than with geographic proximities, and therefore favored
wind as a dispersal vector for many Southern Hemispheric biota. However, todays disjunct ranges of some
Southern Hemispheric taxa such as Monoclea Hook.
(Meissner et al., 1998) could be a result of short distance
dispersal before the final disassembly of Gondwana, and
subsequent range fragmentation as a result of climate
changes (Schuster, 1979).
Dated chronograms, based on sequence variation
plus the bryophyte fossil record, have been published
for bryophytes in general (Newton et al., 2007, with a
strong focus on the pleurocarpous moss lineage), the
leafy liverworts (Heinrichs et al., 2007) and the leafy
liverwort family Lejeuneaceae (Wilson et al., 2007).
However, sampling within these studies was not sufficient to decide on species level disjunctions, and the
results supported the idea of a reformation of bryophyte
diversity throughout the Cretaceaous and Early Tertiary.
Many recent genera seem to have originated not before
the Late Cretaceous, rendering Gondwanan vicariance
rather unlikely.
Although most current authors favor the adoption
of infrequent long distance dispersal for disjunct ranges,
this hypothesis needs to be tested by further studies
that should focus both on a better understanding of the
bryophyte fossil record and a more comprehensive taxon
sampling.

The relationships of many deep clades of

bryophytes have been clarified using molecular phylogenetic approaches plus morphology (Renzaglia et al.,
2007). In contrast, boundaries and relationships of
many species and genera of bryophytes are still unclear, as is the genetic structure of most species. Future studies should focus strongly on genus or species
level relationships, and shed more light on reproduction
modes of populations that are still insufficiently known.
Population genetic studies using isozymes and microsatellites might result in reliable reconstructions of
migration routes and refugia of bryophytes. These studies could also shed more light on the justification of
assumptions of intercontinental ranges of bryophyte
species.
Phylogenetic studies based on variable molecular
markers and using divergence time estimates usually
support dispersal scenarios rather than geographical vicariance as the preferred explanation of disjunct ranges
of bryophytes. The number of studies is still insufficient for a general pattern to emerge, or to determine if
there are also patterns that are indicative of geographical vicariance. Future studies should focus not only
on sequence variation but also on the fossil record of
bryophytes. The search of bryophyte inclusions in Cretaceous amber deposits may be a promising approach
to our understanding of the origin of extant bryophyte
diversity. Progress in the interpretation of the bryophyte
fossil record is essential to achieve more reliable insights into the chronology of bryophyte diversification
and distribution range formation.

References

State of the art and perspectives

A three-digit number of papers on the molecular phylogeny and phylogenetic biogeography of

bryophytes have been published since Shaws review
on biogeographical patterns and cryptic speciation of
bryophytes (Shaw, 2001). On the one hand, these papers corroborated assumptions of a complex genetic
structure of bryophytes with a uniform morphology, and
raised reservations against many morphologically justified species concepts, especially within the mosses. On
the other hand, many molecular topologies allowed for
corrections and modifications of morphological classification schemes.

Acknowledgements We thank Jun Wen (Washington

DC), Yin-Long Qiu (Ann Arbor, Michigan) and Yan
Liang (Beijing) for comments on the manuscript. Financial support from the German Research Foundation
(grants HE 3584/1-4) is gratefully acknowledged.

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