Biol. Rev. (2010), 85, pp. 471–487.

471
doi: 10.1111/j.1469-185X.2009.00111.x

The ghosts of Gondwana and Laurasia

in modern liverwort distributions
Alain Vanderpoorten1∗ , S. Robbert Gradstein2 , Mark A. Carine3 and Nicolas Devos1
1 Institute of Botany, University of Liège, B22 Sart Tilman, 4000 Liège, Belgium
2
Institute of Plant Sciences, University of Göttingen, Untere Karspüle 2, 37073 Göttingen, Germany
3 Natural History Museum, Department of Botany, Cromwell Rd, London SW7 5BD, England

(Received 18 June 2009; revised 26 October 2009; accepted 03 November 2009)

ABSTRACT

Recent advances in phylogenetics and, in particular, molecular dating, indicate that transoceanic dispersal has played an
important role in shaping plant and animal distributions, obscuring any effect of tectonic history. Taxonomic sampling
in biogeographic studies is, however, systematically biased towards vertebrates and higher plants and the possibility
remains that a much stronger signature of ancient vicariance might be evident among other organisms, particularly
among basal land plants. Here, an explicit Bayesian model-based approach was used to investigate global-scale
biogeographic patterns among liverwort genera and to determine whether the patterns identified are consistent with
the expectations of vicariance or dispersal scenarios. The distribution of each genus was mapped onto the phylograms
describing the floristic affinities among areas in order to define the synapomorphic transitions supporting the observed
groupings. The probabilities of change in a branch were calculated by implementing the Markov model of BayesTraits.
The consistent ambiguity in ancestral state reconstructions returned by the unconstrained, two-rate model indicated that
the overall signal in the data was weak, leading us to test the performance of competing, explicit models. The analyses
resolved clades of geographic areas that are mostly consistent with the kingdoms traditionally identified for plants and
animals, but with strikingly lower rates of endemism. The major split observed in the phylograms is into almost entirely
Laurasian and Gondwanan clades. Other patterns recovered by the analyses, including Wallace’s line and the South
Atlantic Disjunction, have also traditionally been interpreted in terms of vicariance. These observations contrast with
the idea that, in spore-dispersed organisms like bryophytes and pteridophytes, dispersal obscures evidence of vicariance.
However, some discrepancies between the liverwort trees and expectations from a continental drift scenario were
observed, such as the sister-group relationship of the Australian and New Zealand floras, which is supported by the
co-occurrence of many genera, often endemic to these two areas. Together with an interpretation of the results within
a phylogenetic context, our analyses suggest that patterns, which are at first sight consistent with an ancient vicariance
hypothesis, may, in fact, conceal a complex mixture of relictual distributions and more recent, asymmetrical dispersal
events. Our results provide a framework for testing specific evolutionary hypotheses concerning the extremely low levels
of endemism in bryophytes and in particular, the significance of dispersal and cryptic diversification.

Key words: biogeography, bryophytes, liverwort, vicariance, dispersal, distribution patterns, Bayesian inference,
BayesTraits.

CONTENTS
I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 472
II. Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 473
(1) Distribution data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 473
(2) Data analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 475
(a) Area relationships and tests of hypotheses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 475
(b) Taxon optimizations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 476

* Address for correspondence: (Tel: ++32 43 663842; Fax ++32 4 366 29 25; E-mail: a.vanderpoorten@ulg.ac.be)

Biological Reviews 85 (2010) 471–487 © 2009 The Authors. Journal compilation © 2009 Cambridge Philosophical Society
472 Alain Vanderpoorten and others

III. Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 477

(1) Worldwide patterns of liverwort distributions at the genus level . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 477
(2) Biogeographic patterns in the world liverwort flora . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 477
(3) Taxon optimizations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 479
IV. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 479
(1) Endemism in the world liverwort flora . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 479
(2) Relationships among the world liverwort floras: insights into their evolutionary history . . . . . . . . . . . . . . . . 481
V. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 484
VI. Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 484
VII. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 484
VIII. Supporting Information . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 487

I. INTRODUCTION microhabitats where a suitable microenvironment persists,

long after the general climate of the region has changed.
Understanding the mechanisms responsible for generating Consequently, and as Anderson (1963) suggested, ‘the
disjunct distribution patterns has long been a major focus diminutive bryophytes, therefore, potentially offer a better
of biogeography (Upchurch, 2008). For Darwin, biotic clue to the solution of phytogeographical problems than do
distributions were the result of dispersal away from a centre many vascular plants’.
of origin and, on an earth that was thought to be static, A notable feature of bryophytes in this regard is that
the goal of biogeography was to identify the centre of origin many species exhibit the same disjunctions that are well
of a taxon by retracing the steps of genealogical lineages known in flowering plants at the generic level (see Shaw,
through space and time. Every group was assumed to have 2001 and Shaw, Werner & Ros, 2003 for review). For
a unique history and common distribution patterns were example, 43% of the species of mosses that are found in
considered to be the result of the same dispersal processes North America are also found in Europe while 70% of the
(see Ebach, Humphries & Williams, 2003 for review). In the moss species found in Europe also occur in North America
1960s, the reappraisal of the nature of the earth’s crust by (Frahm & Vitt, 1993). By contrast, 48% of genera, but
Wegener’s plate tectonics theory provided a new basis for only 6.5% of the species of vascular plants, are shared
understanding and explaining the biotic similarities among between the North American and European floras (Qian,
regions of the world that are widely separated today (Raven 1999). Given the scarcity of the bryophyte fossil record,
& Axelrod, 1974). Vicariance became viewed as the primary explanations for inter-continental range disjunctions in
process responsible for shaping common distribution patterns bryophytes have long relied on information from other
with dispersal considered irrelevant noise, overwriting, fossil organisms, particularly vascular plants, and upon
in a stochastic fashion, the initial parsimonious pattern reconstructions of past vegetation, climates, continental
established by vicariance (McGlone, 2005). More recently positions and land interconnections (Schofield, 1988). The
however, and with the advance of molecular techniques similarity of range disjunctions observed among bryophyte
and associated dating tools in particular (Renner, 2004; species and angiosperm genera and families has often been
Yoder & Nowak, 2006), the pre-eminence of vicariance attributed to a common factor, namely, continental drift
explanations has become progressively undermined (e.g. (see Devos & Vanderpoorten, 2009, for review). Such
Givnish & Renner, 2004; de Queiroz, 2005; Knapp et al., a vicariance explanation for disjunct species distributions
2005; but see Upchurch, 2008). Dated plant phylogenies among bryophytes is consistent with the traditional view
for many angiosperm families indicate that transoceanic of bryophytes as unmoving, unchanging, sphinxes of the
dispersal has played an important role in shaping their past (Crum, 1972). The limited fossil record of bryophytes is
distributions, obscuring any effect of tectonic history (see somewhat equivocal on this point but it is notable that, whilst
Pennington, Cronk & Richardson, 2004, for review). In some bryophyte fossils exhibit a morphology that is unknown
fact, Sanmartín & Ronquist (2004) failed to detect any among extant taxa (Oostendorp, 1984; Ignatov, 1992), others
signature of Gondwanan break-up from the analysis of 19 are rather similar to modern genera. The oldest bryophyte
southern hemisphere higher plant phylogenies, although they fossil record, the thalloid liverwort Pallaviciniites devonicus, dates
acknowledged that the taxonomic sampling in biogeographic back to the Devonian. Yet, despite its antiquity, Pallaviciniites
studies is systematically biased towards vertebrates and resembles extant genera such as Pallavicinia or Symphyogyna
higher plants and that a much stronger signature of (Krassilov & Schuster, 1984). Tertiary fossils are, in general,
ancient vicariance might be evident among other organisms, similar to the modern flora: virtually all are attributable to
particularly among basal land plants (i.e. bryophytes and extant genera and some even to extant species (Miller, 1984;
pteridophytes). As Schuster (1983) noted, and in contrast to Gradstein, 1993; Grolle & Meister, 2004; Frahm, 2004;
the global equilibrium of higher plant species distributions Frahm & Newton, 2005). Since it is often assumed that
with present climate (see Araujo & Pearson, 2003, for rates of morphological and molecular evolution are highly
review; but see Rull, 2009), bryophytes are able to persist in correlated (Barraclough & Savolainen, 2001; Soltis et al.,

Biological Reviews 85 (2010) 471–487 © 2009 The Authors. Journal compilation © 2009 Cambridge Philosophical Society
The ghosts of Gondwana and Laurasia in modern liverwort distributions
2002), the corollary is that bryophytes are a slow-evolving
and conservative group of plants (Frey, Stech & Meissner,
1999; Frahm, 2000, 2004). This interpretation is consistent
with the recent finding that mosses exhibit slower rates of
molecular evolution than pteridophytes, gymnosperms and
angiosperms (Stenoien, 2008).
Whilst an ancient vicariance explanation for bryophyte
distributions has become the established view, several lines
of evidence are now challenging this hypothesis. Firstly,
bryophytes have high vagility coupled with a remarkable
variety of mechanisms of vegetative reproduction and a wide
range of cellular separation mechanisms whose diversity
is unparalleled among land plants (Duckett & Ligrone,
1992). Whilst the deposition curve of diaspores reveals a
marked decrease in diaspore density with distance from the
source (Longton, 1997; Pohjamo et al., 2006), a moss or
liverwort sporangium may contain millions of spores, while
a single leaf of liverwort may yield more than 500 unicellular
gemmae (Schuster, 1983). It seems likely therefore that every
sporangium and every gametophyte has the potential to
contribute to regional or transcontinental dispersal, even if
a fraction of the spore mass has aborted, as is routinely
the case in many mosses [about 20% on average in the
moss Bryum argenteum (Longton, 1997)]. The recent finding,
that bryophyte distributions in circum-subantarctic islands
are significantly correlated with wind connectivity (Muñoz
et al., 2004), reinforces the hypothesis of a central role for
long-distance dispersal in modern bryophyte distributions.
Furthermore, the marked correlation between species ranges
and survival of spores under the conditions of desiccation
and frost that prevail in high-altitude air currents (van
Zanten, 1976, 1978; van Zanten & Gradstein, 1988) offers
an explanation for the difference in distribution range
observed between restricted and widespread species: those
species restricted to a specific area may have spores that
do not survive trans-oceanic dispersal in high-altitude air
currents, whereas species equipped with drought- and cold-
tolerant spores have the potential to exhibit intercontinental
disjunctions.
Studies on the rates of molecular evolution between
continentally disjunct species (Shaw et al., 2003; Heinrichs
et al., 2005), molecular dating (Hartmann et al., 2006;
Heinrichs et al., 2006; Feldberg et al., 2007; Huttunen et al.,
2008; Devos & Vanderpoorten, 2009), and indirect measures
of gene flow derived from population genetic statistics
(McDaniel & Shaw, 2005), all seem to be incompatible
with an ancient vicariance origin for bryophyte distribution
patterns. If, as such evidence suggests, recent long-distance
dispersal has been the major factor shaping current
bryophyte distributions, then any signal from vicariance
events in the patterning of modern distributions is likely to
have been ‘erased’ due to the intensity and random character
of floristic interchanges among areas (van Zanten & Pócs,
1981). In this scenario, the analysis of taxon distributions
may be expected to show no biogeographic structure.
Hypotheses to explain global patterns of floristic relation-
ships among the world bryophyte floras (continental drift
Biological Reviews 85 (2010) 471–487 © 2009 The Authors. Journal compilation © 2009 Cambridge Philosophical Society
473
versus more recent long-distance dispersal) have not been
tested to date. Indeed, the interpretation of relationships
among the bryophyte floras of the world has until now relied
on the analysis of specific case studies or the interpretation of
distribution patterns without a formal analytical framework
(Schuster, 1983; Schofield, 1992; Tan & Pócs, 2000; although
see Hedenäs, 2007). Within plants in general, very few anal-
yses have been conducted to examine biotic distribution
patterns at a global scale, in part due to the difficulty in com-
piling data matrices for large groups at this scale (Proches,
2001; Proches & Marshall, 2001; Brummitt, 2005; Hedenäs,
2007).
The liverworts are a monophyletic basal land plant group
comprising 5000 species (Gradstein, Churchill & Salazar,
2001). They are traditionally grouped with the mosses and
hornworts in Bryophyta, although the monophyly of the
latter as a group has been increasingly questioned (see
Renzaglia et al., 2007, for review) and most recent molecular
data suggest that the liverworts are sister to all other land
plants (Qiu et al., 2007).
Herein, we aim to use an explicit Bayesian model-
based approach (Lewis, 2001) to investigate global-scale
biogeographic patterns among liverwort genera. Using this
approach, we determine the extent to which the patterns
identified are consistent with those proposed in other analyses
of taxon distributions (e.g. Takhtajan, 1986; Cox, 2001;
Brummitt, 2005; Hedenäs, 2007) or cladistic biogeography
studies (Enghoff, 1995; Sanmartín, Enghoff & Ronquist,
2001; Sanmartín & Ronquist, 2004) and discuss the extent to
which vicariance or alternative evolutionary scenarios may
best explain the floristic biogeographic patterns observed
within liverworts.
II. METHODS
(1) Distribution data
A generic-level analysis of liverwort distributions was
conducted for three main reasons. First, the circumscription
of liverwort genera is arguably more stable than that of
families in the rapidly changing taxonomy of bryophytes.
Second, documenting species distributions is a difficult task.
Many areas, particularly in the tropics, remain largely poorly
collected. Furthermore, recent monographic work is lacking
for many tropical taxa and this is likely to result in the over-
estimation of rates of endemism in liverworts as the same
species may have been described several times under different
names (Gradstein et al., 2001). Third, the ‘ideal’ taxonomic
level for a given biogeographic question is likely to be a group-
specific characteristic, as taxonomic ranks are arbitrarily
defined (Proches, 2001). Biogeographically, genera in one
group may well correspond to families in another. Proches
(2001) emphasized, for example, the similarity of the area
cladograms obtained for bat species and families of Liliiflorae.
In bryophytes, morphology offers many fewer variable
characters for taxonomy than in other groups such as
474 Alain Vanderpoorten and others

angiosperms. In this respect, the fact that some genomic
regions like the internal transcribed spacers of nuclear
ribosomal DNA offer the same or even less variation across
entire orders of mosses than among conspecific accessions in
other groups, potentially suggests that the taxa that are being
compared are not ‘equivalent’ (Vanderpoorten, Goffinet &
Quandt, 2006). The analysis of liverwort distributions at the
genus level results in topologies that are directly comparable
to those obtained with other organisms at different taxonomic
levels (see below), suggesting that this taxonomic level is
indeed appropriate for the issues being addressed.
360 liverwort genera were recognized in the present
analysis. This number corresponds to Crandall-Stotler
& Stotler’s (2000) reference check-list of genera for
liverworts, with some necessary amendments from the recent
literature (see online Appendix 1). A database managed by
M. Wigginton was exploited to document the occurrence of
the liverwort genera in 21 world floristic regions. Although
the database may often include several bibliographic
references for the occurrence of a taxon in a given area, 168 of
the most recent references were selected to provide a synthetic
overview of the literature dealing with the distributions of
the studied genera (see online Appendix 2A, B). Twenty
of the regions used to score distributions correspond
to the biogeographic scheme defined by van der Wijk,
Margadant & Florschütz (1959), who recognized Europe
(EUR), northern Africa (AF1), continental sub-Saharan
Africa (AF2), Mascarene Islands (AF3), southern Africa
(AF4), northern Asia (AS1), eastern Asia (AS2), southern
Asia (AS3), southwestern Asia (AS4), western Asia (AS5),
North America (AM1), Central America (AM2), Caribbean
islands (AM3), northern South America (AM4), Brazil
(AM5), southern South America (AM6), Australia (AU1),
New Zealand (AU2), Antarctica (ANT), and Oceania (OC)
(Fig. 1). Although the boundary between adjacent regions in
some parts of the world has since been refined, the delineation
of those 20 regions is strongly supported by past and present
diversity research and floristic analyses (Tan & Pócs, 2000).
Area AM5 is redefined to include tropical northern Argentina
(Misiones, Cordoba), which was previously included within
AM6. Area AF4 as defined here only includes continental
southern South Africa. ANT includes continental Antarctica
plus the sub-Antarctic islands, with the exception of the
Tristan group, which is included within AM6. In addition,

Fig. 1. Patterns of liverwort genus diversity (number of genera given below regions) and proportion of endemic liverwort genera
(in parentheses) in each of clades identified in Fig. 2 and each of the 21 world biogeographic regions defined by van der Wijk et al.
(1959) with subsequent refinements (Tan & Pócs, 2000): Europe (EUR), northern Africa (AF1), continental sub-Saharan Africa
(AF2), Mascarene Islands (AF3), continental southern Africa (AF4), northern Asia (AS1), eastern Asia (AS2), southern Asia (AS3),
southwestern Asia (AS4), western Asia (AS5), eastern North America (AM1E), western North America (AM1W), Central America
(AM2), Carribean islands (AM3), northern South America (AM4), Brazil (AM5), southern South America (AM6), Australia (AU1),
New Zealand (AU2), Antarctica (ANT), and Oceania (OC).

Biological Reviews 85 (2010) 471–487 © 2009 The Authors. Journal compilation © 2009 Cambridge Philosophical Society
The ghosts of Gondwana and Laurasia in modern liverwort distributions
North America was divided into an eastern (AM1E) and
western (AM1W) area to fit with previous analyses by Enghoff
(1995) and Sanmartín et al. (2001). This division corresponds
to the mid-continental seaway that separated the continent
longitudinally in the late Cretaceous. van der Wijk et al. (1959)
were not followed in recognizing Macaronesia as a specific
African biogeographic element (AF5). In fact, the bryophyte
flora of Macaronesia as traditionally defined is heterogeneous
(Vanderpoorten, Rumsey & Carine, 2007). The flora of the
Cape Verde Islands is closely similar to that of sub-Saharan
Africa and was therefore assimilated with it. By contrast,
the liverwort flora of the Azores, Madeira, and the Canary
Islands is not related to that of Africa but rather to that of
Europe. No liverwort genus is endemic to Macaronesia and
the floristic similarities between Europe and Macaronesia
are so close that identifying the latter as a biogeographic
region on its own would require the recognition of numerous
other biogeographic regions in the world. This would sharply
increase the number of terminal nodes in the analysis and
decrease the size of the areas being used as biogeographic
units. Decreasing the ‘grain size’ of the terminal units is
likely to lead to the definition of discontinuous biogeographic
areas characterized by local ecological conditions rather than
broad-scale patterns (Proches, 2001). The Macaronesian
liverwort flora was therefore merged with that of
Europe. The biogeographic units used here encompass
ecologically heterogeneous regions (e.g. Australia). They are,
however, comparable to those used in previous large-scale
biogeographic analyses to generate general area cladograms
(Sanmartín et al., 2001; Sanmartín & Ronquist, 2004;
Sanmartín, Wanntorp & Winkworth, 2007) and can be
tested against area relationships inferred from phylogenies
or organism distributions.
(2) Data analysis
(a) Area relationships and tests of hypotheses
Floristic relationships among the world biogeographic
regions were examined through an adaptation of Jukes-
Cantor’s substitution model for binary characters (Lewis,
2001). The method was initially designed for modeling
shifts in character states among morphological traits. In
a biogeographic context, ‘gains’, i.e. transition from state
0 to state 1, either represent dispersal from an area into
another or in situ speciation; ‘losses’, i.e. transition from state
1 to state 0, represent either extinction from an area or
failure to colonize it. The resulting cladograms represent
nested sets of areas, in which terminal dichotomies represent
areas between which the most recent biotic interchange has
occurred (Morrone & Crisci, 1995). Although such areas
of non-random distributional congruence among taxa fit
with some definitions of an area of endemism (Morrone,
1994), we refrain from considering them as such since
areas of endemism may be considered historical entities
rather than distributional ones (Harold & Mooi, 1994).
Given that our approach is not historical (i.e. it is not
based on hypotheses of relationships between taxa), the trees
Biological Reviews 85 (2010) 471–487 © 2009 The Authors. Journal compilation © 2009 Cambridge Philosophical Society
475
describing the floristic affinities among areas (hereafter, the
liverwort trees) cannot be considered as area cladograms
(Garron-Orduna, Miranda-Esquivel & Donato, 2008).
Unlike morphological characters, which suffer from a
severe sampling bias because constant characters are never
recorded, leading to an overestimation of the transition
rates and hence the necessity to apply a correction to
the model as initially proposed by Felsenstein (1992) for
the analysis of restriction-site data, no acquisition bias is
present in distribution data. In the present data matrix,
however, the proportion of constant characters is extremely
low due to the lack of all-zero columns and the rarity of
cosmopolitan genera (4.8%), which is not compatible with
the Poisson distribution used to model the probability of
change. Hence, the ‘variable’ coding option of MrBayes
3.1 (Ronquist & Huelsenbeck, 2003), which implements
Felsenstein’s correction, was applied to the data. We also
investigated the performance of a model allowing state
frequencies to differ among genera. Five combinations of
state frequencies were sampled from a discrete uniform
distribution. Bayes factors (BFs) were used to contrast the
performance and choose the most appropriate model for
the data. The Bayes factors represent a summary of the
evidence provided by the data in favour of a certain
model (Kass & Raftery, 1995). The log BF is defined as
minus twice the difference of the log marginal likelihoods
of the two competing models. The marginal likelihoods of
the different models are well approximated by the log of
the harmonic mean of the likelihoods when the Markov
chain is allowed to run for a very large number (millions)
of iterations (Kass & Raftery, 1995; Raftery, 1996). The log
marginal likelihoods were estimated here using the method
of Suchard, Weiss & Sinsheimer (2001) as implemented by
Tracer 1.4 (Rambaut & Drummond, 2007) and threshold
values of 2, 5, and 10 were taken as positive, strong, and
very strong evidence, respectively, for selecting one model
over another (Raftery, 1996). However, before BFs may
be taken as decisive evidence in favour of one hypothesis
over another, estimates of the error involved in the BF
calculation are necessary (Suchard, Weiss & Sinsheimer,
2005). Therefore, the standard error of the log marginal
likelihoods was assessed with Tracer 1.4 and the standard
error of the log BF, i.e. S.E. (x − y), was calculated as
sqrt[S.E.2 (x) + S.E2 .(y)], where S.E.(x) and S.E.(y) are the
standard errors of the log marginal likelihoods returned
by the two competing models, respectively. Because the
standard error of the log marginal likelihoods reached fairly
high values up to 3.00 (Table 1), we conservatively set the
value of the significance of the log BF at 10.
Although such an approach has not traditionally been used
in studies of distribution patterns, it exhibits, together with
parsimony analysis of species assemblages (Trejo-Torres &
Ackerman, 2001, 2002), a series of attractive features over
distance-based approaches (Vanderpoorten et al., 2007). Four
of the most important features of the model-based approach
in the context of the present study include: conservatism,
i.e. the presence of unresolved relations when a conflicting
476 Alain Vanderpoorten and others

Table 1. The most commonly discussed area relationships in the world biogeographic literature (after Sanmartín et al., 2001, and
Sanmartín & Ronquist, 2004) and floral kindgoms as proposed by Takhtajan (1986) and amended by Cox (2001). These hypotheses
were successively used as constraints in the Bayesian analysis of the distribution of the 360 liverwort genera in the 21 world floristic
regions. ML (S.E.) corresponds to the log of the marginal likelihood of the constrained analyses and its standard error. Log marginal
likelihoods that significantly depart from those of the unconstrained analyses are in bold, with a difference of the log Bayes factors of
10 considered as significant. World biogeographic regions are as defined in Fig. 1

Biogeographic pattern Corresponding cladogram References -ML (S.E.)

Gondwana (Antarctica excepted) (AM2-6,AF1-4,AS3-5,OC,AU1-2) Schuster (1983) 3192.51 (0.33)
Laurasia (AM1E,AM1W,EUR,AS1-2) Schuster (1983) 3186.11 (1.27)
Southern Gondwana (AF2,AF4(AU2(AM6,AU1))) Sanmartín & Ronquist (2004) 3161.43 (0.47)
Plant southern (AF2,AF4(AM6(AU2,AU1))) Sanmartín & Ronquist (2004) 3159.06 (1.36)
Inverted southern (AF2,AF4(AU1(AM6,AU2))) Sanmartín & Ronquist (2004) 3164.19 (3.00)
Northern Gondwana (AF2,AF4(AF3(AS3(AS4(OC,AU1))))) Sanmartín & Ronquist (2004) 3235.10 (1.14)
Tropical Gondwana (AF3(AF2,AF4,AM4-5)) Sanmartín & Ronquist (2004) 3212.33 (2.06)
Trans-American (AM6(AM2-5,Holarctic)) Sanmartín & Ronquist (2004) 3232.01 (1.96)
Palearctic/ Nearctic (EUR,AS1-2,AF1) (AM1E,AM1W) Enghoff (1995); Sanmartín et al. (2001) 3264.51 (0.83)
Circum-Atlantic (AM1E,EUR) Enghoff (1995); Sanmartín et al. (2001) 3140.83 (0.61)
South Atlantic disjunction (AM2-6),(AF2-4) McLoughlin (2001) 3133.74 (0.67)
Holarctic (AM1E,AM1W,EUR,AF1,AS1-2) Takhtajan (1986) 3201.93 (1.83)
Neotropics (AM2-5) Takhtajan (1986) 3133.40 (2.12)
Paleotropics (AF2-3,AS3-5) Takhtajan (1986) 3265.03 (1.00)
South America (AM2-6) Cox (2001) 3131.83 (0.71)
Sub-Saharan Africa (AF2-4) Cox (2001) 3132.84 (0.80)
Indo-Pacific (AS3-4,OC) Cox (2001) 3152.90 (1.71)
Australia (AU1,AU2) Cox (2001) 3133.76 (1.26)
Australasia (AU1-2,OC,AS4) Tangney (2007) 3130.52 (0.87)

signal is present in the data; the possibility to assess the
strength of the floristic relationships among areas through the
posterior probabilities; the lower sensitivity to long-branch
attraction than maximum parsimony (MP) (Bergsten, 2005);
and the possibility to test statistically specific hypotheses
of area relationships. Thus, apparent conflict between
the resulting phylogram and expectations from alternative
hypotheses derived from other analyses of taxon distributions
or cladistic biogeographic analyses can be explicitely tested.
This is especially important since the outcome of analyses of
distribution data seems to be highly method-dependent (e.g.
Szumik & Goloboff, 2004; Moline & Linder, 2006; Carine
et al., 2009).
Under MP, the test of Kishino & Hasegawa (1989) was
shown to be strongly biased when the trees compared are
not derived independently of the data sets used for testing
(Goldman, Anderson & Rodrigo, 2000). Because corrected
tests, such as that of Shimodaira & Hasegawa (1999), have not
yet been implemented in a parsimony context, all the analyses
were therefore performed with likelihood-based methods.
Lewis’s model was implemented in a Bayesian framework.
Four Metropolis-coupled Markov Chain Monte Carlo
(MCMCMC) simulations were run twice independently for
10,000,000 generations with MrBayes 3.1. Trees and model
parameters were sampled every 10,000 generations. The
number of generations needed to reach stationarity in the
algorithm was estimated by visual inspection of the plot of the
log-likelihood score at each sampling point. The trees of the
‘burn-in’ for each run were excluded from the tree set, and
the remaining trees from each run were combined to form
the full sample of trees assumed to be representative of the
posterior probability distribution. All analyses included an
operational, dummy all-zero outgroup to allow topologies to
be rooted (Morrone, 1994; Trejo-Torres & Ackerman, 2002).
Constrained analyses were performed to test whether
alternative scenarios of area relationships were consistent
with the data (Table 1). The analyses described above were
successively re-run under the constraints that correspond to
competing hypotheses of area relationships obtained from
different taxa, as described in Table 1. The results of the
different analyses were compared using the Bayes factors.
(b) Taxon optimizations
The distribution of each individual genus that occurs in
>2 and <20 biogeographic regions was mapped onto the
phylograms generated by MrBayes in order to define the
synapomorphic transitions supporting the observed group-
ings. All reconstructions were performed after pruning of
the operational all-0 outgroup from the trees. The proba-
bilities of change in a branch were calculated by estimating
the instantaneous forward (q01 ) and backward (q10 ) rates
among the two states by implementing the Markov model
of ‘Multistate’ in BayesTraits 1.0 (www.evolution.rdg.ac.uk).
A MCMC was used to visit, at each iteration, the space of rate
parameter values and sample one of the trees generated by
the MrBayes analysis. The likelihood of the new combination
was calculated and this new state of the chain was accepted
or rejected following evaluation by the Metropolis-Hastings
term. The rate at which parameters were changed (‘ratedev’)
was set at the beginning of each run so that the acceptance
rate of the proposed change globally ranges between 20

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The ghosts of Gondwana and Laurasia in modern liverwort distributions
and 40%. In the absence of information on rates, uniform
distributions ranging from 0 to 100 were used as priors. The
chain was run for 10,000,000 generations and was sampled
for rate parameters and state probabilities at the nodes of
interest every 10,000 generations. In order to circumvent
the issue associated with the fact that not all of the trees
necessarily contain the internal nodes of interest, reconstruc-
tions were performed using a ‘most recent common ancestor’
approach. This method identifies, for each tree, the node
subtending a group of areas, reconstructs the state at the
node, and then combines this information across trees (Pagel,
Meade & Barker, 2004). For a given branch, a synapomor-
phic transition was defined when the state probabilities were
recovered with an average probability arbitrarily set at >70%
at each of the flanking nodes. The reconstruction was oth-
erwise considered as ambiguous and the synapomorphy not
defined.
The consistent ambiguity in ancestral state reconstruc-
tions returned by the two-rate model, however, indicated
that the overall signal in the data, although strong enough
for generating unimodal posterior probability distribution of
rates from flat uniform priors, was fairly weak. Everything
happens as if the weakness of the signal in the data would
‘drive’ the sampling by the MCMC to a sub-optimum, thus
precluding the use of methods that ‘jump’ from one model to
another depending on their posterior probabilities (Pagel &
Meade, 2006). In such conditions, explicit models must be
used (Barker, Meade & Pagel, 2007). We therefore con-
trasted the performance of four other competing models.
The first model was the unconstrained, two-rate model (I).
In the second model (II), the root was fixed at state ‘present’
and the forward rate q01 was set to 0. This model corre-
sponds to the ‘ML-root’ model of Barker & Pagel (2005).
In the third model (III), q01 was forced to be very low (i.e.
was sampled from a uniform distribution with a 0–1 range),
whereas no constraint was imposed on q10 (which was sam-
pled from a uniform distribution with a range of 0–100).
In the fourth model (IV), q01 was forced to take high values
and was sampled from a uniform distribution with a 10–100
range, whereas q10 was unconstrained. Finally, q10 was set to
0 in the fifth model (V). An example of the BayesTraits
batch file used for the reconstructions is provided in online
Appendix 3.
Log BFs were used to contrast the fit of the constrained
models as compared to the unconstrained, two-rate model,
and the best-fit model was used to perform the taxon
optimizations. Because the standard error of the log BFs
was consistently found to be <0.5 (see online Appendix 4),
a value of 2 was taken as positive evidence for selecting one
model over another. When the log BFs among competing
models were not conclusive, we checked that the different
models returned identical ancestral state reconstructions. For
that purpose, we calculated the average probabilities at each
node and checked that evidence for the same reconstruction
of state was obtained, i.e. that all competing models returned
a probability of >0.70 for the same state. If the state was
reconstructed with a probability <0.70 by at least one of
Biological Reviews 85 (2010) 471–487 © 2009 The Authors. Journal compilation © 2009 Cambridge Philosophical Society
477
the competing models, or if the competing models returned
conflicting state reconstructions, the state at the node was
considered as ambiguous and no synapomorphic transition
was defined.
III. RESULTS
(1) Worldwide patterns of liverwort distributions
at the genus level
The data matrix of the occurrence of 360 liverwort
genera in 21 biogeographic regions is available online at
www.treebase.org under accession SN4138. The number of
liverwort genera per biogeographic region is given in Fig. 1.
In terms of endemism, the first nine areas exhibiting the
highest rates are all Gondwana fragments, with endemism
rates ranging between 1.3% in Australia (AU1) and 10%
in New Zealand (AU2) (Fig. 1). Endemism rates in the
Laurasian fragments are much lower, ranging from 0%
in eastern North America (AM1E), North Africa (AF1),
northern Asia (AS1) to 3.6% in western North America
(AM1W) (Fig. 1).
79% of liverwort genera span at least two geographic
regions and 25% are distributed across more than 10 regions.
Six genera (Aneura, Calypogeia, Chiloscyphus, Fossombronia, Junger-
mannia, and Riccia) occur in all of the 21 floristic regions and
thus exhibit a completely cosmoplitan range with respect to
the areas defined here.
(2) Biogeographic patterns in the world liverwort
flora
The model allowing state frequencies to differ among
genera to infer the floristic relationships among the
world biogeographic regions significantly improved the
log marginal likelihoods over a model assuming equal
state frequencies [log marginal likelihood (and standard
error) of 3138.19 (1.38) versus 3192.98 (1.02)]. The model
allowing heterogeneity in state frequencies among genera
was therefore selected for subsequent analyses.
The 50% majority-rule consensus of the trees resulting
from the analysis (available from www.treebase.org under
accession SN4138) is presented in Fig. 2. The trees depicting
the biogeographic patterns in the world liverwort flora
exhibits varying degrees of congruence with previous
biogeographic classifications based on analyses of endemicity
(Schofield, 1992, for bryophytes, largely inspired from
Takhtajan, 1986 and subsequent amendments by Cox,
2001; Morrone, 2002, for angiosperms) or global biocenotic
similarities (Hedenäs, 2007 for mosses; Brummitt, 2005, for
angiosperms).
The analysis resolves a main clade, labeled as Gondwana,
and a paracladic grade [the terms ‘paracladic’ and
‘monocladic’ in an analysis of taxon distributions being
analogous to ‘paraphyletic’ and ‘monophyletic’ in phylogeny
(see Trejo-Torres & Ackerman, 2002) and characterize
grade-like or cohesive taxon assemblages, respectively]
478 Alain Vanderpoorten and others

Fig. 2. Patterns of worldwide liverwort genus distributions derived from a Bayesian analysis of the distribution of 360 liverwort
genera in 21 world biogeographic regions (see Fig. 1 for abbreviations). The tree is the 50% majority-rule consensus with branch
length averaged over 2000 trees from the posterior probability distribution. Numbers below the branches correspond to the posterior
probabilities. Each clade, as identified by a specific shading and/or boxing, is labeled as defined in Table 2.

composed of AF1, AS1, AS2, AS5, EUR, AM1E and
AM1W. The paracladic grade corresponds to Laurasia with
the inclusion of areas AS5 and AF1 and is comparable to the
‘temperate’ group in Brummitt’s (2005) angiosperm analysis.
It fits with other broad-scale biogeographical classifications
and analyses (Schofield, 1992; see also Proches, 2005, and
Morrone, 2002, for review) and is very similar to Takhtajan’s
(1986) Holarctic, although the latter excludes Arabia.
The clade including all fragments of Gondwana (except
Antarctica and areas AF1 and AS5) is resolved with 95%
posterior probability (hereafter p.p.). Forcing Gondwana to
monoclady leads to a substantial decrease in log marginal
likelihood (Table 1). In fact, analyses wherein Gondwana is
circumscribed without areas ANT, AF1 and AS5 lead to
an improvement of the log marginal likelihood (−3131.05,
S.E. 0.62).

Biological Reviews 85 (2010) 471–487 © 2009 The Authors. Journal compilation © 2009 Cambridge Philosophical Society
The ghosts of Gondwana and Laurasia in modern liverwort distributions
Within Gondwana, Takhtajan’s (1986) Neotropical
Kingdom (Neotropics on Fig. 2) is recovered with 73%
p.p. The Neotropics are sister to area AM6, forming a clade
labeled as ‘South America’ in Fig. 2 and fully consistent
with the idea of a South American Kingdom as proposed
by Cox (2001). In the unconstrained analyses, the sub-
Saharan African areas form a grade, but constraining them
to monophyly actually leads to an improvement of log
marginal likelihood. Sub-Saharan Africa and South America
are resolved as sister areas and form a clade labeled as the
‘South Atlantic Disjunction’ in Fig. 2 with 76% p.p. The
South Atlantic Disjunction is sister to a clade labeled
as ‘Australasia’ with 95% p.p. Within Australasia, weakly
supported at 57%, areas AU1 and AU2 form a clade (labeled
as ‘Australian’) with 79% p.p., which is consistent with Cox’s
(2001) Australian Kingdom (Table 1), and which is sister to
area OC. The clade including OC and Australia is labeled as
the ‘Oceano-Austral’ clade in Fig. 2 and has 75% p.p. Area
AS4 is finally resolved a sister to the Oceano-Australian
clade, but with no support.
The liverwort trees significantly conflict with the
biogeographic scenarios proposed for other organisms,
notably the Southern Gondwana, Plant southern, Inverted
southern, Northern Gondwana, and Tropical Gondwana
groupings (Table 1). Some of the area relationships proposed
by those scenarios are, however, compatible with the
biogeographic patterns observed in liverworts, for instance
the sister-area relationship between AU1 and AU2 is
consistent with the Plant Southern Pattern, the sister area
relationship between the latter group with Oceania and
southeast Asia is consistent with the northern Gondwana
pattern, and the sister-area relationship between sub-
Saharan Africa and northern South America is consistent
with the tropical Gondwana pattern (Table 1).
(3) Taxon optimizations
The log marginal likelihoods of the taxon optimizations
returned by each of the five models for each of the 268
genera distributed in two or more biogeographic regions are
presented in Appendix 4. Unconstrained models, wherein
q01 and q10 were sampled from uniform [0–100] prior
distributions, returned significantly higher log marginal
likelihoods than constrained models in only 9% of the genera.
The unconstrained runs consistently returned log marginal
likelihoods that were not significantly different than those
returned by the IVth model. In fact, high values of q01
(>10) were sampled during the unconstrained runs, thus
mimicking the IVth model. As a result, the state probabilities
recovered by both models at internal nodes were consistently
ambiguous (i.e. with posterior probabilities of about 50%).
Synapomorphic transitions along internal branches are
described in Table 2. The paracladic condition of Holarctic
as resolved by the present analyses is largely due to the
pivotal position of areas AS2 and AS3, which share a series
of synapomorphies with both the core Holarctic and Gond-
wana clades. For instance, area AS2 exclusively shares with
Gondwana a suite of genera that are absent from Holarctic,
Biological Reviews 85 (2010) 471–487 © 2009 The Authors. Journal compilation © 2009 Cambridge Philosophical Society
479
namely Archilejeunea, Denotarisia, Gottschea, Gottschelia, Isotachis,
Jackiella, Lepidolejeunea, Marsupidium, Notoscyphus, Ptychanthus,
Pycnolejeunea, Schiffneriolejeunea, Schistochila, Stenolejeunea, Syzy-
giella, Thysananthus, and Wiesnerella. At the same time, area
AS2 shares with Holarctic a suite of genera, including Bla-
sia, Cladopodiella, Conocephalum, Gymnocolea, Harpanthus, Mylia,
and Preissia, whose absence is synapomorphic for the clades
Gondwana and G1. The resolution of Arabia within Hol-
arctic is supported by the absence from Arabia of the seven
genera that are synapomorphic for the clades Gondwana and
G1, namely Adelanthus, Conoscyphus, Kymatocalyx, Thysananthus,
Symphyogyna, Symphyogynopsis, and Zoopsidella, whilst sharing
with Holarctic a series of genera (see above) whose absence
is synapomorphic for Gondwana.
Within Gondwana, Australasia is characterized by the
gain of eight genera, three of which are endemic. The
sister relationship of areas AU1 and AU2 is supported by
a large suite of 31 synapomorphic gains, 14 of which are
endemic, and 10 losses. The South Atlantic Disjunction,
which is resolved as sister to Australasia, is characterized
by the gain of six genera, four of which are endemic, and
11 losses. Within the Disjunction, sub-Saharan Africa is
poorly defined by the synapomorphic loss of two genera. By
contrast, South America is supported by the shared presence
of eight synapomorphic genera, six of which are endemic,
and six synapomorphic losses.
IV. DISCUSSION
(1) Endemism in the world liverwort flora
A striking characteristic of liverworts in general is the low
rate of endemism by comparison with angiosperms. 79% of
the liverwort genera span at least two geographic regions
and 25% are distributed across more than 10 regions.
In the Cape Kingdom, no liverwort genus is endemic in
comparison with the 16.2% of endemic angiosperm genera
(Born, Linder & Desmet, 2006). In Australia, the 1% of
generic endemism in liverworts pales in comparison with
the 22.6% in angiosperms (Orchard, 1999). Even in the
Neotropics, which display the highest rate of endemic genera
amongst the world’s liverwort flora (24.6%), rates of generic
endemism in the angiosperm flora [65–82% depending
on taxonomic concepts (Takhtajan, 1986)] are considerably
higher. Only in New Zealand do liverworts and angiosperms
display comparable levels of generic endemism of about 10%
(Moreira-Muñoz, 2007).
Although it is evident that the liverwort flora is still
much less well known than its angiosperm counterpart,
and although new liverwort taxa undoubtedly remain to
be discovered, particularly in poorly collected tropical
areas, the increase in the number of new genera resulting
from new discoveries is likely to be counter-balanced by
new data from molecular systematics leading to generic
recircumscriptions and the synonymisation of genera. In the
Neotropics for example, where the highest endemism rate in
480 Alain Vanderpoorten and others

Table 2. Synapomorphic transitions of presence-absence of liverwort genera characteristic for the biogeographic clades identified
in Fig. 2. Synapomorphies were defined based upon the reconstructions of the presence or absence of each genus at each internal
node from a model of genus gain and loss (see online Appendix 4 for model selection) implemented by a Markov Chain Monte
Carlo visiting the space of rate parameters across the trees from the posterior probability distribution. Synapomorphic transitions
along a branch were identified for nodes supported by >70% posterior probabilities. Genera endemic to a clade are in bold. World
biogeographic regions are as defined in Fig. 1

Clade Synapomorphies
Neotropics (AM2 AM3 AM4 AM5) Gains: Anoplolejeunea, Cephaloziopsis, Cyclolejeunea, Dicranolejeunea,
Hypoisotachis, Macrocolura, Micropterygium, Monodactylopsis,
Mytilopsis, Neurolejeunea, Omphalanthus, Oryzolejeunea, Symbiezidium
Losses: Gottschea, Schistochila
South America (AM2 AM3 AM4 AM5 AM6) Gains: Blepharolejeunea, Cronisia, Monoclea, Neesioscyphus,
Noteroclada, Paracromastigum
Losses: Conoscyphus, Gottschelia, Notoscyphus, Ptychanthus, Symphyogynopsis,
Wiesnerella
Holarctic (AF1 AS1 AS2 AS5 EUR AM1E Gains: Moerckia
AM1W)
H1 (EUR AS1 AS2 AS3 AS4 AS5 OC AU1 AU2 Gains: Apometzgeria, Harpanthus, Ptilidium
AF2 AF3 AF4 AM1E AM1W AM2 AM3 AM4
AM5 AM6)
H2 (EUR AS1 AS2 AS3 AS4 OC AU1 AU2 AF2 Gains: Anastrepta, Anastrophyllum, Apotreubia, Arnellia, Bucegia,
AF3 AF4 AM1E AM1W AM2 AM3 AM4 Cryptocolea, Eocalypogeia, Eremonotus, Geocalyx, Herbertus,
AM5 AM6) Hygrobiella, Kurzia, Mesoptychia, Metacalypogeia, Odontoschisma,
Peltopsis, Pleurocladula, Sphenolobopsis, Tetralophozia
H3 (EUR AS2 AS3 AS4 OC AU1 AU2 AF2 AF3 Gains: Acanthocoleus, Cheilolejeunea, Drepanolejeunea, Dumortiera,
AF4 AM1E AM2 AM3 AM4 AM5 AM6) Harpalejeunea, Microlejeunea, Telaranea, Trichocolea
H4 (AS2 AS3 AS4 OC AU1 AU2 AF2 AF3 AF4 Gains: Acrolejeunea, Caudalejeunea, Ceratolejeunea, Cylindrocolea,
AM1E AM2 AM3 AM4 AM5 AM6) Diplasiolejeunea, Leptolejeunea, Leucolejeunea, Lopholejeunea,
Mastigolejeunea
H5 (AS2 AS3 AS4 OC AU1 AU2 AF2 AF3 AF4 Gains: Archilejeunea, Colura, Delavayella, Denotarisia, Gottschea,
AM2 AM3 AM4 AM5 AM6) Gottschelia, Heteroscyphus, Isotachis, Jackiella, Lepicolea,
Lepidolejeunea, Marsupidium, Monosolenium Notoscyphus Ptychanthus,
Pycnolejeunea, Schiffneria, Schiffneriolejeunea, Schistochila,
Spruceanthus, Stenolejeunea, Stictolejeunea, Syzygiella,
Thysananthus, Tuyamaella, Wiesnerella, Xenochila
Losses: Arnellia, Bucegia, Cryptocolea, Mesoptychia
Gondwana (AM2 AM3 AM4 AM5 AM6 AF2 Gains: Conoscyphus
AF3 AF4 AS3 AS4 OC AU1 AU2)
Losses: Cladopodiella, Eremonotus, Gymnocolea, Harpanthus, Hygrobiella, Moerckia,
Peltopsis, Pleurocladula
G1 (AM2 AM3 AM4 AM5 AM6 AF2 AF3 AF4 Gains: Adelanthus, Kymatocalyx, Symphyogyna, Symphyogynopsis, Tylimanthus,
AS4 OC AU1 AU2) Zoopsidella
Losses: Blasia, Conocephalum, Delavayella, Eocalypogeia, Monosolenium, Mylia,
Preissia, Ptilidium, Xenochila
South Atlantic disjunction (AM2 AM3 AM4 Gains: Brachiolejeunea, Frullanoides, Lethocolea, Odontolejeunea
AM5 AM6 AF2 AF3 AF4) Prionolejeunea Xylolejeunea
Losses: Anastrepta, Apometzgeria, Apotreubia, Denotarisia, Jackiella, Metacalypogeia,
Pedinophyllum, Schiffneria, Stenolejeunea, Tuyamella, Spruceanthus
Sub-Saharan Africa (AF2 AF3 AF4) Losses: Trichocolea, Zoopsidella
Australasia (AS4 OC AU1 AU2) Gains: Andrewsianthus, Austroscyphus, Balantiopsis, Dendrolejeunea,
Mastigopelma, Psiloclada, Temnoma, Treubia
Oceano-Austral (OC AU1 AU2) Gains: Acrochila, Goebelobryum, Hymenophyton, Lepidolaena, Lethocolea
Losses: Acanthocoleus, Apotreubia, Kymatocalyx, Schiffneria, Sphenolobopsis,
Tetralophozia
Australia (AU1 AU2) Gains: Allisioniella, Anomoclada, Blepharidophyllum, Brevianthus, Calyptrocolea,
Cephalomitrion, Chaetophyllopsis, Chandonanthus, Clandarium,
Cyanolophocolea, Dendromastigophora, Dinckleria, Drucella,
Eoisotachis, Eotrichocolea, Gackstroemia, Hepatostolonophora, Herzogobryum,
Isophyllaria, Isolembidium, Leptophyllopsis, Neogrollea,
Nothogymnomitrion, Pachyglossa, Paracromastigum, Pseudocephalozia, Seppeltia,
Siphonolejeunea, Triandrophyllum, Trichotemnoma, Wettsteinia
Losses: Anastrepta, Apometzgeria, Cylindrocolea, Mastigopelma, Metacalypogeia, Nardia,
Odontoschisma, Symphyogynopsis, Syzygiella, Wiesnerella

Biological Reviews 85 (2010) 471–487 © 2009 The Authors. Journal compilation © 2009 Cambridge Philosophical Society
The ghosts of Gondwana and Laurasia in modern liverwort distributions
liverwort genera is observed, most of the endemic genera are
stenotypic (1–3 species each) and highly apomorphic (e.g.
Zoopsidella, Pteropsiella, Schusterolejeunea, and Cephalantholejeunea).
These genera, which, for the most part, are assumed to
have diverged during the Tertiary owing to the long period
(60 million years) of isolation since the opening of the South
Atlantic and continuous tectonic activity, are characterized
by extreme morphological reductions (Schuster, 1990).
It is precisely such mono-or stenotypic genera that are
increasingly shown to have been given an inflated taxonomic
rank owing to their peculiar morphology. For example,
Metzgeriopsis, one of the most remarkable liverworts with
a uniquely unistratose thallus that is often interpreted as
an enlarged protonema and leafy sexual branches arising
from thallus margins, was most recently shown to be a
highly modified member of the widespread genus Cololejeunea
(Gradstein et al., 2006).
This typical tendency for bryophytes to display low
endemism rates, shown here at the genus level in continental
floras, also holds true at the species level in areas like
islands, which are typically characterized by high rates
of endemism in other organisms. In the Galapagos for
example, species endemism is 13% in liverworts (Gradstein,
2009) and 6% in mosses (Gradstein & Weber, 1982), against
about 50% in the native angiosperm flora. In the Canary
Islands, the 1.5% of bryophyte species endemism pales
in comparison with the 40% endemism rates observed in
angiosperms (Vanderpoorten et al., 2010). In the western
Mediterranean, Corsica and Sardinia, which harbour nearly
10% species endemism in angiosperms, a single endemic
bryophyte species has been described (Sotiaux et al., 2009).
Even in Hawaii, one of the world’s richest hot-spots of
endemism, 29.4% and 48.6% of the moss and liverwort
species, respectively, are endemic to the archipelago (Staples
et al., 2004; Staples & Imada, 2006), whereas the rate
of species endemism in angiosperms reaches 90% (Sakai,
Wagner & Mehroff, 2002).
The low rate of endemism among bryophytes is at first
sight consistent with a traditional interpretation in which
the disjunct distributions exhibited by many species are
the result of a combination of ancient vicariance and low
evolutionary rates (see Shaw, 2001, for review). In particular,
the interpretation of an ancient origin of the disjunctions
observed in the distributions of liverwort genera fits well with
the striking difference in endemism rates between Laurasia
and Gondwana. In Laurasia, substantial range disjunctions
and the creation of ‘relicts’ have traditionally been thought
to result from extensive Pleistocene glaciations. By contrast,
in Gondwana, they are thought to have occurred much
earlier and would have been primarily induced by plate
migration and tectonic instability (Schuster, 1982). Such
an interpretation would explain why, among the 21 world
floristic regions examined here, the nine regions with the
highest rates of endemism are former Gondwana fragments.
The limited fossil record that is available tends to support the
relictual nature of the laurasian disjunctions. For example,
the presence of fossil material of the Japanese endemic
Biological Reviews 85 (2010) 471–487 © 2009 The Authors. Journal compilation © 2009 Cambridge Philosophical Society
481
liverwort Nipponolejeunea subalpina in Baltic amber from the
European Eocene unambiguously attests that the distribution
of the species, and of the genus (currently restricted to eastern
Asia) as a whole, was much broader in the Tertiary (Grolle &
Meister, 2004). Additional Baltic amber fossils, although
sometimes incomplete and difficult to assign taxonomically,
also attest to the Paleoendemic nature of an array of taxa
currently restricted to eastern Asia (Frahm, 2000, 2004).
The low rates of endemism observed in bryophytes
may also result from our failure to recognize cryptic
taxa. Instances of cryptic speciation are, in fact, becom-
ing increasingly well known (Shaw, 2001; McDaniel &
Shaw, 2003; Buczkowska, 2004; Feldberg et al., 2004;
Fernandez et al., 2006, Wachowiak et al., 2007). However,
this explanation alone cannot serve to explain the sharp dif-
ferences observed between bryophytes and angiosperms,
especially at higher taxonomic levels, suggesting that
bryophytes may genuinely exhibit low rates of lineage
diversification.
Finally, it is also possible that bryophytes disperse more
effectively than angiosperms and that extensive gene flow
among populations prevents divergence, as suggested by
the lack of or low partitioning of genetic variation at
different spatial scales in bryophytes (Cronberg, Molau &
Sonesson, 1997; van der Velde & Bijlsma, 2000; Werner &
Guerra, 2004; Freitas & Brehm, 2001; Korpelainen,
Pohjamo & Laaka-Lindberg, 2005; Grundmann et al., 2007;
Vanderpoorten et al., 2008).
(2) Relationships among the world liverwort floras:
insights into their evolutionary history
Evidence for the significance of dispersal as the major
mechanism shaping the distribution of liverwort genera is
not, at first sight, obvious from the results of the present
analysis. Many of the biogeographic relationships resolved in
the present analyses were already observed in other groups of
organisms where they have traditionally been interpreted in
terms of ancient vicariance. In fact, the major split observed
is into almost entirely Laurasian and Gondwanan areas. The
Laurasia-Gondwana disjunction has typically been identified
in ‘old groups’ [e.g. in conifers (Proches, 2006) and beetles
(Sequeira & Farrell, 2001; Cabrero-Sanudo & Lobo, 2009)],
whereas in ‘modern’ groups, the most striking disjunction
occurs between Old and New World assemblages (Cristoffer
& Peres, 2003; Proches, 2006). Although Holarctic is resolved
here as a paracladic grade owing to the pivotal position of
areas AS2 and AS3, it is tempting to see in the mix of floras
from both Gondwana and Holarctic origin characteristic of
these two areas a signature of the northwards migration of
China towards Laurasia in Devonian and Permian times
and of several other terrains derived from the northern
Gondwanan border during the late Jurassic-late Triassic
(Metcalfe, 1999). The major difference found here among
Gondwanan and Laurasian areas suggests a substantial role
for the Tethys seaway as a biogeographic barrier that was
reinforced during the Cretaceous by the emergence and
radiation of a dense angiosperm belt in the tropics (Proches,
482
2006). Despite its fairly narrow channel, this barrier has
been considered significant in limiting dispersal of many
conifers between Laurasia and Gondwana and a major
impediment to Jurassic and perhaps Triassic migration of
many bryophytes as well (Schuster, 1983; Frey, 1990).
Other narrow stretches of water are believed to have
generated substantial range disjunctions in bryophytes. For
example, the resolution of an Australasian group in the
present analyses fits with the recognition of a large Australian
Kingdom as defined for animals. Conversely, it contrasts with
the idea of an Indo-Pacific Kingdom defined for plants based
on the assumption that the much greater dispersal power of
plants than animals has allowed those of Southeast Asia to
spread, not only through the East Indies to New Guinea,
but also across the vast reaches of the Pacific to even the
most distant of the Pacific Island groups (Cox, 2001). In
fact, the greater number of eastern than western Malesian
liverwort species in Sulawesi is in support of Wallace’s line
and indicates that this border of Asiatic and Australasian
biogeographic regions, although primarily thought to be, due
to its depth, a barrier to animal migrations, is also relevant
to wind-dispersed organisms such as liverworts (Aryanti &
Gradstein, 2007).
Another apparent signature of ancient vicariance is the
sister relationship between sub-Saharan Africa and South
America. This classical pattern, already documented for
bryophytes by Gradstein, Pócs & Váña (1983), has tradi-
tionally been interpreted in terms of the break-up sequence
of northwest Gondwana and the opening of the South
Atlantic ocean, 110 million years ago (mya) (see Sanmartín &
Ronquist, 2004, for review). Within South America, the long
branch leading to area AM6 serves, however, to empha-
size the substantial floristic differences between the latter
and the Neotropics (see Morrone, 2002, for review). In
particular, southern South America shares with Australia
(and sometimes also New Zealand) and/or Antarctica a
suite of genera that are endemic to these areas (Schus-
ter, 1979), including Acrolophozia, Archeophyllum, Austroleje-
unea, Austrolophozia, Blepharidophyllum, Clandarium, Evansianthus,
Gackstroemia, Hepatostolonophora, Herzogobryum, Isophyllaria, Lep-
idogyna, Neohodgsonia, Nothogymnomitrion, Pedinophyllopsis, Phyl-
lothalia, and Roivainenia, and which are absent from the
Neotropics. These recurrent disjunctions are consistent
with the connection between southern South America and
Australia until the late Eocene (35 mya) and with Antarctica
until the Oligocene (30–38 mya) (Sanmartín & Ronquist,
2004).
All these observations contrast with the idea that, in spore-
dispersed organisms like bryophytes and pteridophytes,
dispersal often obscures evidence of vicariance (van Zanten &
Pócs, 1981; Wolf, Schneider & Ranker, 2001). The corollary
of the acceptance of an ancient origin for the disjunctions
currently observed amongst the world bryophyte floras is
that the low proportion of endemics in the liverwort flora
as compared to angiosperms must originate from the slow
evolution rates of the former. Such a view is particularly
well illustrated by the differences between the bryophyte and
Biological Reviews 85 (2010) 471–487 © 2009 The Authors. Journal compilation © 2009 Cambridge Philosophical Society
Alain Vanderpoorten and others
angiosperm floras of Australia and New Zealand. Whilst the
bryophyte flora of the cool-temperate rainforest of Victoria
and Tasmania is shared with comparable habitats in New
Zealand, the angiosperm floras of these two regions are
very different. Since the isolation of New Zealand dates
back to 80 mya, and since ‘for at least two-thirds of
that time the gap from the rest of Gondwanaland must
have been too great for any but casual colonizers’, this
distribution pattern has been considered evidence for ‘the
relative age and evolutionary stability of many bryophyte
species’ (Scott, 1988). Such an interpretation of ‘resistance
to speciation’ (Catcheside, 1982) served, more recently,
to explain the morphological similarity, or even sequence
identity, among disjunct populations of southern hemisphere
bryophyte species, which apparently lack efficient dispersal
mechanisms (Frey et al., 1999; Pfeiffer, 2000; Schaumann
et al., 2003; Schaumann, Pfeiffer & Frey, 2004; Pfeiffer et al.,
2004; Stech & Frey, 2004; Blöcher, Quandt & Frahm,
2006). In the case of the moss, Pyrrhobryum mnioides, evidence
from molecular dating further supports the hypothesis that
some disjunctions can, in fact, be explained by continental
drift (McDaniel & Shaw, 2003). While refuting the idea of
a complete absence of molecular evolution, McDaniel &
Shaw (2003) confirm the traditional view (e.g. Sharp, 1972;
Schofield & Crum, 1972), that morphological evolution of
bryophytes may involve extremely long periods of stasis over
tens or even hundreds of million years.
Although the existence of true ‘living fossils’ has been
established in rare instances (McDaniel & Shaw, 2003; Aigoin
et al., 2009), evidence from molecular phylogenies tends,
however, to suggest that the levels of molecular divergence
observed in bryophytes are not compatible with the ancient
vicariance hypothesis, even though modern distributions
of taxa fit expectations derived from the continental drift
theory. Within Holarctic for example, the striking similarity
between the bryophyte floras of North America and Europe,
with a common species pool that reaches up to 70% in
geologically very ancient areas such as the Ozark Plateau
(Frahm & Vitt, 1993), would suggest a common origin
dating back to the opening of the North Atlantic rather than
more recent long-distance chance dispersal (Schofield, 1988).
However, the extremely low level of molecular divergence
found among disjunct European and American populations
of several moss species is incompatible with an ancient
vicariance hypothesis (Shaw et al., 2003; Huttunen et al.,
2008) and in fact, phylogeographies of moss species with
trans-Atlantic disjunctions point to substantial transoceanic
dispersal rates (Szövényi et al., 2008; Vanderpoorten et al.,
2008). At the continental scale, gene flow levels have
apparently been sufficient to prevent genetic differentiation
among populations caused by genetic drift and to wipe out
any genetic structure caused by the postglacial recolonization
process (van der Velde & Bijlsma, 2003; Szövényi et al.,
2006). In fact, gene flow intensity has been shown to
be sufficient to homogenize the genetic structure of the
moss, Hylocomium splendens, across Scandinavia (Cronberg
et al., 1997) and to prevent any effect of isolation by
The ghosts of Gondwana and Laurasia in modern liverwort distributions
distance on islands separated from the mainland by tens
to hundreds of kilometres (Cronberg, 2002; Grundmann
et al., 2007). This is consistent with recent observations on
the dispersal ability of bryophytes at the landscape scale,
which suggests that many species have the ability to travel at
a rate of several tens of kilometres within a few decades or
centuries (Miller & McDaniel, 2004; Sundberg, Hansson &
Rydin, 2006; Hutsemekers, Dopagne & Vanderpoorten,
2008a).
Given this, the strong biogeographic patterns revealed
by the present analysis are surprising because long-distance
dispersal has long been assumed to generate chaotic, wide-
ranging and pattern-limited relationships in area cladograms
(e.g. McCarthy, 2003). In bryophytes, observations of
repeated vicariance patterns have recently been interpreted
as evidence for the in situ evolution of taxa following
continental drift (Schofield, 1988; Tangney, 2007). It remains
assumed that ‘giving priority to dispersal as the means by
which distributions are formed has several undesirable effects’
because it devalues distribution data since the possibility
of the reliability of patterns in distributions is lessened
if dispersal is assumed to be a major determining factor
(Tangney, 2007). Recent evidence, however, suggests that,
constrained by prevailing wind, asymmetrical dispersal may
produce predictable, repeated distribution patterns that
are likely to account for many of the range disjunctions
currently observed (Cook & Crisp, 2005; McGlone, 2005;
Sanmartín et al., 2007). Event-based tree-fitting methods
applied across a sample of 23 southern hemisphere plant
groups suggested that easterly moving weather systems,
probably often associated with forest fires in eastern Australia
causing massive updraft and carrying plants and animals
with it (McGlone, 2005), has played a major role in
establishing present distributions. Eastward circumpolar
currents thus seem to have constrained the dispersal of plants
between Australia and New Zealand (Sanmartín et al., 2007;
McDowall, 2008). The trees depicting the biogeographic
patterns of liverwort distributions worldwide obtained here,
wherein Australia and New Zealand are resolved as sister
areas, in agreement with previous observations of the
striking similarity of their bryophyte flora (Catcheside,
1982; Scott, 1988; Piippo, 1992), certainly fit with such
a hypothesis. A vicariance hypothesis, which suggests a
sister area relationship between southern South America
and Australia since New Zealand was the first landmass
to break away about 80 mya, while Australia and South
America remained connected across Antarctica until the
opening of the South Tasman sea (35–30 mya) and the Drake
Passage (30–28 mya) (see Trewick, Paterson & Campbell,
2006, for review), is not consistent with this scenario.
Similarly, phylogenies for Southern Hemisphere plants often
indicate close relationships between species from Australia
and New Zealand (Linder & Crisp, 1995; Winkworth
et al., 2002; Wanntorp & Wanntorp, 2003). To explain the
close relationship between Australia and New Zealand by
vicariance, it would be necessary to argue that extinction
of Australian and/or closely related South American species
Biological Reviews 85 (2010) 471–487 © 2009 The Authors. Journal compilation © 2009 Cambridge Philosophical Society
483
has occurred (Linder & Crip, 1995). Although such evidence
is still lacking for bryophytes, molecular divergence times in
other groups have, in many cases, suggested that the current
species diversity has arisen too recently to be explained by
drift (see Waters & Craw, 2006, and Trewick et al., 2006, for
review).
Asymmetrical wind dispersal is expected to favour, in the
long term, the evolution of endemism in the sink area. A sig-
nature of the floristic asymmetry generated by unidirectional
wind currents from Australia towards New Zealand can,
in fact, be found in their respective patterns of endemism.
Despite its comparatively much smaller size, New Zealand
indeed contains four times more strict endemic genera (20)
than Australia. Everything thus happens as if any new
Australian taxon would be more easily transported towards
New Zealand than the reverse. The consequences of asym-
metrical wind dispersal on the evolution of endemism in the
sink area are also nicely illustrated by the liverwort flora of
Macaronesia, wherein recent phylogenetic evidence points
to an American origin of endemism owing to the existence
of frequent depressions moving rapidly eastwards from the
American coasts and the existence of tropical cyclones of
west Carribean origin (Vanderpoorten & Long, 2006). As
mentioned above, endemism rates in bryophytes are, how-
ever, comparatively low. Furthermore, the neo-endemics
originating from such long-distance dispersal events act as
‘autapomorphies’ in global analyses of area relationships
as presented here. As a result, and provided that muta-
tion rates are not substantially higher than dispersal rates
between the source and sink areas, the evolution of genetic
innovations in the latter is unlikely to alter the global pic-
ture of strong floristic affinities between the source and sink
areas.
Furthermore, in addition to wind-dispersal, other trans-
portation mechanisms can help to explain the regularity in
the distribution patterns observed. In particular, the signif-
icance of zoochory for bryophyte dispersal has become
increasingly acknowledged. Despite the lack of specific
means of ensuring attachment, like seed ornamentation in
angiosperms, the adhesive transportation of unspecialized
bryophyte fragments is likely to be enhanced by various
morphological characters, including small size, numerous
branches, and erect or squarrose leaves. Epizoochory seems
especially important in habitats such as woodland, where
animal dispersal agents are common and wind velocity is
low (Heinken et al., 2001). The correlation between the dis-
tribution of some species, such as Timmia megapolitana, and
bird migratory routes, further suggests that birds may also
play an important role in trans-oceanic dispersal (Porley &
Ellis, 2002). In fact, recurrent observations of fragile shoot
apices attached to bird feet were made, for example, on skuas
and penguins in Antarctica (Lewis Smith, 1999). Accidental
ingestion may also occur, so that viable fragments can be dis-
persed over long distances via passage through the digestive
tract of highly mobile vertebrates such as flying foxes and
birds (Proctor, 1961; Parsons et al., 2007).
484
V. CONCLUSIONS
(1) At first sight, the biogeographic patterns of liverwort
distributions observed here lend support to the idea
that world-wide distributions in the bryophyte flora
have been mainly shaped by ancient vicariance rather
than by dispersal and extant climatic conditions.
Several of the observed patterns, and in particular the
main divergence between Gondwana and Laurasia,
could be interpreted as signatures of ancient vicariance.
Acceptance of the ancient vicariance hypothesis,
however, raises the question of why global rates of
endemism are so low in bryophytes. One explanation
that can be proposed to explain the low rates of
endemism observed in the bryophyte flora is that
strong floristic interchanges prevent diversification.
However, if such interchanges are indeed frequent, a
clear biogeographic pattern, such as that observed
in this study, would not be expected. The other
explanation is that bryophyte diversification rates are
much lower than those of angiosperms.
(2) Recent evidence from molecular phylogenies tends to
suggest that patterns which appear to be consistent
with ancient vicariance may have resulted from
much more recent dispersal. As noted by McDowall
(2004), dispersal, although perhaps stochastic in
timing, may be surprisingly regular and enduring in
source, direction and target areas. This regularity
may generate patterns of distribution that resemble
vicariance patterns in general appearance and may,
or may not, be congruent with those vicariance
patterns. This observation, coupled with the fact that
some patterns in the liverwort trees, particularly the
sister-group relationship between Australia and New
Zealand, are best explained by dispersal, tends to
suggest that dispersal may actually be the rule rather
than the exception in generating modern liverwort
distribution patterns. To take this conclusion to the
extreme, and based on the observation that the
most divergent populations of the moss, Ceratodon
purpureus, are those of North versus South hemisphere
(McDaniel & Shaw, 2005), one might even make
the hypothesis, that the main Laurasian/Gondwanan
disjunction observed in the liverwort flora also results
from asymmetrical dispersal promoted by the main
direction of the trade winds of the temperate latitudes
coupled with the high atmospheric pressure in the
Equatorian area.
(3) While the answer to such a question cannot be found in
the results of the present analyses, our results provide a
framework for testing specific hypotheses regarding the
evolutionary significance of dispersal in bryophytes.
Further taxonomic work is necessary to refine the
values of endemism. The latter are, in fact, mostly
from morphological-based taxon circumscriptions that
are becoming increasingly challenged. In this regard,
the question of the status of the handful of monotypic,
Biological Reviews 85 (2010) 471–487 © 2009 The Authors. Journal compilation © 2009 Cambridge Philosophical Society
Alain Vanderpoorten and others
highly apomorphic genera that are characteristic for
areas like the Neotropics, is particularly relevant.
An important molecular phylogenetic effort would
also allow for the significance of ancient vicariance
in area cladograms to be tested. For instance,
under the main hypothesis that differences in lineage
diversification between Gondwana and Laurasia result
from the comparatively young history of the latter
(Schuster, 1983), one would expect that Laurasian
lineages exhibit much shorter branch lengths than
Gondwanan ones. Ideally, those phylogenies should
be analyzed within an absolute time frame. In view
of the scarcity of the fossil record in bryophytes, one
promising solution is to use instances of island neo-
endemic speciation to provide geographic calibration
points (Wall, 2005; Devos & Vanderpoorten, 2009).
Calibrated phylogenies would, in turn, allow for
comparisons of rate diversification between bryophytes
and angiosperms to be made to test the hypothesis of
a slower diversification rate in the former. Finally, the
hypothesis of a high dispersal ability of bryophytes
remains to be tested by measuring the difference
in mutation versus dispersal rates among disjunct
populations. In the context of the issues posed by
multi-copy genes such as ITS, and of the difficulty of
amplifying low-copy nuclear genes (Vanderpoorten
et al., 2006), the increasing development of new
molecular tools such as microsatellites in bryophytes
(see Hutsemekers et al., 2008b for review) is extremely
promising.
VI. ACKNOWLEDGEMENTS
A.V. and N.D. acknowledge financial support from the
Belgian Funds for Scientific Research (FNRS) and the
Leopold III funds. We are very much indebted to
M. Wigginton, who made his database available to us and
rendered this study possible. Many thanks are also due to
C. Raedig, A. Wilson, and T. Orchard, for information
regarding the levels of generic endemism in angiosperms,
and to Andrew Meade, Paul Lewis, and two anonymous
reviewers for their very helpful comments on the manuscript.
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VIII. SUPPORTING INFORMATION
Additional supporting information may be found in the
online version of this article.
Doc. S1. Appendix 1. Amendments to Crandall-Stotler &
Stotler’s (2000) reference check-list of genera for liverworts.
Doc. S2a. Appendix 2A. Distribution matrix of 360
liverwort genera in the 21 world biogeographic regions
(for abbreviations see Fig. 1). Numbers refer to the literature
sources as listed in Appendix 2b.
Doc. S2b. Appendix 2B. Literature references used to
compile the distribution matrix of 360 liverwort genera in 21
world biogeographic regions. Numbers corespond to those
listed in Online Appendix 2A.
Doc. S4. Appendix 4. Log of marginal likelihoods (and
standard error using 1000 bootstrap replicates), mean and
standard deviation of rate parameters q01 and q10 of the five
models used for taxon optimization: (I) q01 and q10 are sam-
pled from a uniform prior distribution ranging from 0 to 100;
(II) q01 = 0; (III) q01 and q10 are sampled from a uniform
prior distribution ranging from 0 to 1 and 0 to 100, respec-
tively; (IV) q01 and q10 are sampled from a uniform prior
distribution ranging from 10 to 100 and 0 to 100, respec-
tively; and (V) q10 = 0 (see text for details). Numbers in bold
correspond to those of the models selected by the Bayes fac-
tors ,with a value of the logBF of 2 considered as significant.
Please note: Wiley-Blackwell are not responsible for the
content or functionality of any supporting materials supplied
by the authors. Any queries (other than missing material)
should be directed to the corresponding author for the
article.