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Journal of Systematics and Evolution 47 (5): 497–508 (2009) doi: 10.1111/j.1759-6831.2009.00028.x

Phylogenetic biogeography and taxonomy of disjunctly distributed

bryophytes
1
Jochen HEINRICHS∗ 1
Jörn HENTSCHEL 1 Kathrin FELDBERG 1
Andrea BOMBOSCH
2
Harald SCHNEIDER
1
(Department of Systematic Botany, Albrecht von Haller Institute of Plant Sciences, Georg-August-University, D-37073 Göttingen, 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 ge-
netic 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 migra-
tion 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 dom-
inant photosynthetic active generation. In contrast to
other land plants, the sporophyte is unbranched and not
autonomously viable (Schofield, 1985). Bryophytes dis-
perse frequently both by spores and by propagules that
descend from the gametophyte, or by unspecialized ga-
metophyte fragments with a high potential of regenera-
tion (Correns, 1899). Bryophytes are the progeny of the
first plants that successfully colonized terrestrial habi-
tats (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 typo-
logical species concept where species were defined
as largely invariant units. Many species were known
only from type material (e.g., Stephani, 1898–1925;
Warnstorf, 1911). More recently, authors accepted in-
traspecific morphological variation and lowered numer-
ous local taxa to synonyms of widespread bryophyte
species (Gradstein, 1994; Buck, 1998; Heinrichs, 2002).
Consequently, broad geographical ranges that often span
Received: 11 November 2008 Accepted: 26 February 2009
∗
Author for correspondence. E-mail: jheinri@uni-goettingen.de; Tel.: +49-
551-39-22220; Fax: +49-551-39-22329.
several continents were assigned to many morpholog-
ically circumscribed bryophyte species (Herzog, 1926;
Grolle, 1969; Gradstein et al., 1983; Schofield, 1992;
Tan & Pócs, 2000). The resulting disjunct ranges of
bryophyte species have frequently been explained by
ancient vicariance and slow rates of morphological evo-
lution (Herzog, 1926; Crum, 1972; Frey et al., 1999) but
other authors provided experimental evidence for the al-
ternative 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 taxo-
nomic 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 non-
monophyly and need for a revised taxonomy
An increasing body of published work points to
many taxonomic incongruences of widespread mor-
phologically circumscribed bryophyte species and phy-
logenies derived from molecular markers. Shaw &
Allen (2000) resolved populations of morphologically


C 2009 Institute of Botany, Chinese Academy of Sciences
498 Journal of Systematics and Evolution Vol. 47 No. 5
circumscribed species of the aquatic moss genus
Fontinalis Hedw. in widely diverging clades, as did
Vanderpoorten et al. (2004) for species of Hygroam-
blystegium Loeske and Shaw et al. (2008) for rep-
resentatives of the Sphagnum subsecundum complex.
Stech & Wagner (2005) provided evidence for the poly-
phyly 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 sev-
eral species of the moss Brachytheciastrum Ignatov
& Huttunen as polyphyletic and documented paral-
lel morphological evolution within this genus. Simi-
larly, Cano et al. (2005) found incongruences between
current classification schemes of the Tortula subulata
complex, and a molecular topology. Incongruences be-
tween 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 al-
lowed for a modified appraisal of morphological evi-
dence including new circumscription of taxa or changes
of rank. Vanderpoorten (2004) solved the problem of
non-monophyletic Hygroamblystegium species by intro-
ducing a wide species concept for Hygroamblystegium
varium (Hedw.) Mönk. 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 Pla-
giochila 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 lin-
eage 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
Australasian–South American simple thalloid liverwort
Hymenophyton flabellatum (Labill.) Trev. Based on the
2009
outcome of their molecular phylogenetic analyses and
accompanying morphological studies, they restricted
the range of H. flabellatum to Australasia, and rein-
stated the New Zealand–Tasmanian Hymenophyton lep-
topodum (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) Tre-
vis. from tropical America and proposed the applica-
tion 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 killarnien-
sis 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 tropi-
cal Africa. Hedenäs (2008a) excluded the African An-
titrichia 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 molecu-
lar 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 geo-
graphical 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; Hedenäs, 2008a, b; Hedenäs & Eldenäs, 2007;
Huttunen et al., 2008). Genetic variation without con-
cordant morphological variation has often been re-
garded 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 varia-
tion that has been documented for many morphospecies
of bryophytes always reflects genetically incompatible
units. An apparent lack of interchange of genetic mate-
rial 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

C 2009 Institute of Botany, Chinese Academy of Sciences
 HEINRICHS et al.: Phylogenetic biogeography of bryophytes
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 geo-
graphical 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 lim-
ited morphological differences.
The complex thalloid liverwort Conocephalum
F.H.Wigg. is possibly the most exhaustively studied ex-
ample of a genetically heterogeneous bryophyte species.
Isozyme studies in the Holarctic–temperate Asian
Conocephalum conicum (L.) Dumort. s.l. revealed the
presence of six partly sympatric taxa that were in-
formally 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 salebro-
sum 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 morphologi-
cally indistinct Mediterranean sibling species besides
the European–Asian–American–African complex thal-
loid 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 speci-
ation was also provided for the Holarctic simple thal-
loid liverworts Pellia epiphylla (L.) Corda and Pellia
endiviifolia (Dicks.) Dumort. (Pacak & Szweykowska-
Kulińska, 2000; Fiodorow et al., 2001).
Similar findings are available for several mosses.
Bijlsma et al. (2000) provided evidence for the pres-
ence 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)]. Mc-
Daniel & 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 Califor-
nian populations of the cosmopolitan species Grimmia
laevigata (Bridel) Bridel. They identified two distinct
geographically overlapping clades. Shaw (2000) pub-
lished a nrITS phylogeny of Mielichhoferia elongata
(Hoppe & Hornsch.) Nees & Hornsch. Based on the
outcome of his analyses he proposed two cryptic species

C 2009 Institute of Botany, Chinese Academy of Sciences
499
within the morphologically uniform taxon, one with a
European–North American range, and the other strictly
North American. Hedenäs & Eldenäs (2007) investi-
gated nrITS and chloroplast DNA haplotype variation
of the pleurocarpous moss Hamatocaulis vernicosus
(Mitt.) Hedenäs. Based on their topologies Hedenäs &
Eldenäs (2007) postulated the existence of two cryptic
species, of which one is widespread in Europe, in addi-
tion 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 diver-
sity, potential bottleneck events, and modes of reproduc-
tion. 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 au-
thors 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) con-
cluded that the large Mediterranean islands might func-
tion as “mainland” for bryophytes. Vanderpoorten et al.
(2008) arrived at a similar conclusion when analyz-
ing chloroplast markers of the moss Grimmia montana
Bruch & Schimp. Madeiran and Mediterranean haplo-
types of G. montana were identical or closely related to
European or North American ones.
Grundmann et al. (2008) analyzed diversity pat-
terns of European P. squarrosa using nuclear and
chloroplast DNA sequences, and enzyme electrophore-
sis. These authors provided evidence for sexual repro-
duction, 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 tem-
peratures 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 recombina-
tion. Grundmann et al. (2008) also postulated a post-
glacial recolonization of central Europe from the Iberian
Peninsula and the Balkans. Cronberg (2000) observed
quite similar patterns for the epiphytic moss Leucodon
500 Journal of Systematics and Evolution Vol. 47 No. 5
sciuroides (Hedw.) Schwägr. Mediterranean popula-
tions reproduce sexually and are genetically diverse
whereas more northern populations reproduce vegeta-
tively and are genetically quite uniform. This pattern co-
incides with the expectation of a loss of genetic variation
in populations at the northern limit of the glacial refu-
gia. 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 observa-
tion Hedderson & Nowell (2006) assumed a survival of
Homalothecium sericeum in this region during the last
glacial period.
Szövéni et al. (2006) presented a chloroplast phy-
logeographic analysis of Sphagnum fimbriatum Wilson
and Sphagnum squarrosum Crome. Their haplotype dis-
tribution 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 ge-
nomic variation in ferns and mosses. Their study re-
vealed 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 pop-
ulations of several Polytrichum species (Polytrichum
commune, Polytrichum uliginosum, Polytrichum formo-
sum Hedw., and Polytrichum piliferum Hedw.). The lack
of allozyme and microsatellite variation pointed to ex-
tensive spore dispersal and contradicted the hypothesis
of a recolonization of Europe from southern refugia af-
ter the last glacial period.
Inter- or intraspecific variation of molecular mark-
ers might allow for the reconstruction of range expan-
sion directions. Based on the recent distribution of taxa
and their position in a phylogenetic framework, con-
clusions can be drawn as to the ranges of their an-
cestors. 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 Madagascar–Réunion endemic Bryopteris gau-
2009
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 ori-
gin of a Holarctic Homalothecium clade.
Taxonomic work combined with the reconstruc-
tion 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 Campylo-
pus flora of tropical America and Madeira. This trend is
contradicted by the example Porella with the Macarone-
sian 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 recur-
ring patterns.
4 Intercontinental range expansion versus
conservation
Wegener’s (1915) reconstruction of continental
drift has provided a theory to explain disjunct dis-
tribution 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 underly-
ing 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) con-
tradicts 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 ev-
idence for dispersal or vicariance. One possibility con-
cerning this matter is a critical comparison of phylo-
genies with breakup events of landmasses. Congruence
of ancestral geographical distributions of clades and
the sequence of breakup events rather supports vicari-
ance. However, deviation of a phylogeny and a breakup

C 2009 Institute of Botany, Chinese Academy of Sciences
 HEINRICHS et al.: Phylogenetic biogeography of bryophytes 501

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).


C 2009 Institute of Botany, Chinese Academy of Sciences
502 Journal of Systematics and Evolution Vol. 47 No. 5
sequence supports dispersal (Sanmartin & Ronquist,
2004).
The application of the molecular clock hypothe-
sis 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 de-
termined 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 vari-
ation and the fossil record will provide more reliable in-
sights into the historical biogeography of lineages by en-
abling 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 seri-
ous 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 substitu-
tion rates.
Supraspecific intercontinental ranges are gener-
ally accepted for bryophytes and have been con-
firmed on many occasions (Meissner et al., 1998;
Groth et al., 2003). Several recent studies also con-
firmed the monophyly of intercontinentally distributed
bryophyte species. Neotropical–African 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, Dicra-
noweisa 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). Neotropical–European
disjunctions have been supported for species of the
liverwort genera Lophozia (De Roo et al., 2007) and
2009
Plagiochila (Heinrichs et al., 2004), and Asian–North
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 Pla-
giochila punctata (North America, Neotropics, Africa,
Europe) (Davison et al., 2006).
The observed sequence analogies of different ac-
cessions 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 vi-
cariance 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
Madrean–Tethyan origin of several western North
American–Mediterranean 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 ob-
served distribution ranges. Hentschel et al. (2006) veri-
fied the assumption of a recent introduction of the south-
ern hemispheric Chiloscyphus semiteres (Lehm.) Lehm.
& Lindenb. into Europe (Paton, 1965) by demonstrat-
ing nrITS sequence similarities of accessions from the
Netherlands and Australia. Wall (2005) documented a
clock-like behaviour of the nuclear glyceraldehyde 3-
phosphate dehydrogenase gene of the moss Mitthyrid-
ium H.Rob., and identified clades that were related
to oceanic archipelagos. Using island ages as calibra-
tion 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 Miocene–Pliocene age of a split be-
tween 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 scenar-
ios, and nrITS mutation rates. These authors could
clearly reject western Gondwanan vicariance for the
Neotropical–African range of Bryopteris, and proposed
a dispersal scenario. Heinrichs et al. (2006) recon-
structed 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 diver-
gence time estimates rendered Gondwanan vicariance
unlikely. Heinrichs et al. (2006) explained the observed

C 2009 Institute of Botany, Chinese Academy of Sciences
 HEINRICHS et al.: Phylogenetic biogeography of bryophytes 503

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.


C 2009 Institute of Botany, Chinese Academy of Sciences
504 Journal of Systematics and Evolution Vol. 47 No. 5
distribution patterns as a result of short distance disper-
sal, rare long distance dispersal events, extinction, re-
colonization 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 South-
ern Hemispheric ranges of bryophytes and main wind
directions. Muñoz et al. (2004) found a stronger cor-
relation of floristic similarities with wind connectivity
than with geographic proximities, and therefore favored
wind as a dispersal vector for many Southern Hemi-
spheric biota. However, today’s 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 suffi-
cient 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.
5 State of the art and perspectives
A three-digit number of papers on the molec-
ular phylogeny and phylogenetic biogeography of
bryophytes have been published since Shaw’s review
on biogeographical patterns and cryptic speciation of
bryophytes (Shaw, 2001). On the one hand, these pa-
pers corroborated assumptions of a complex genetic
structure of bryophytes with a uniform morphology, and
raised reservations against many morphologically justi-
fied species concepts, especially within the mosses. On
the other hand, many molecular topologies allowed for
corrections and modifications of morphological classi-
fication schemes.
2009
The relationships of many deep clades of
bryophytes have been clarified using molecular phylo-
genetic approaches plus morphology (Renzaglia et al.,
2007). In contrast, boundaries and relationships of
many species and genera of bryophytes are still un-
clear, as is the genetic structure of most species. Fu-
ture 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 mi-
crosatellites might result in reliable reconstructions of
migration routes and refugia of bryophytes. These stud-
ies 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 vi-
cariance as the preferred explanation of disjunct ranges
of bryophytes. The number of studies is still insuffi-
cient for a general pattern to emerge, or to determine if
there are also patterns that are indicative of geograph-
ical vicariance. Future studies should focus not only
on sequence variation but also on the fossil record of
bryophytes. The search of bryophyte inclusions in Cre-
taceous 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 in-
sights into the chronology of bryophyte diversification
and distribution range formation.
Acknowledgements We thank Jun Wen (Washington
DC), Yin-Long Qiu (Ann Arbor, Michigan) and Yan
Liang (Beijing) for comments on the manuscript. Fi-
nancial support from the German Research Foundation
(grants HE 3584/1-4) is gratefully acknowledged.
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