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(American Journal of Botany. 2008;95:720-730.) doi: 10.3732/ajb.2007407 © 2008 Botanical Society of America, Inc. |
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Systematics and Phytogeography |
2 Swedish Museum of Natural History, Department of Cryptogamic Botany, Box 50007 SE-104 05 Stockholm, Sweden 3 Main Botanical Garden of Russian Academy of Sciences, Botanicheskaya 4, Moscow 127276, Russia 4 University of Liège, Institute of Botany, B22 Sart Tilman, B-4000 Liège, Belgium
Received for publication 11 December 2007. Accepted for publication 4 March 2008.
ABSTRACT
Competing hypotheses that rely either on a stepping-stone dispersal via the North Atlantic or the Bering land bridges, or more recent transoceanic dispersal, have been proposed to explain the disjunct distribution of Mediterranean flora in southern Europe and western North America. These hypotheses were tested with molecular dating using a phylogeny of the moss genus Homalothecium based on ITS, atpB-rbcL, and rpl16 sequence data. The monophyly of two main lineages in Western Palearctic (Europe, central Asia and north Africa) and North America is consistent with the ancient vicariance hypothesis. The monophyly of Madeiran H. sericeum accessions supports the recognition of the Macaronesian endemic H. mandonii. A range of absolute rates of molecular evolution documented in land plants was used as probabilistic calibration prior by a Bayesian inference implementing a relaxed-clock model to derive ages for the nodes of interest. Our age estimates for the divergence of the American and Western Palearctic Homalothecium clade (5.7 Ma, IC 3.52–8.26) and the origin of H. mandonii (2.52 Myr IC 0.86–8.25) are not compatible with the ancient vicariance hypothesis. Age estimates suggests that species distributions result from rare instances of dispersal and subsequent sympatric diversification. The calibrated phylogeny indicates that Homalothecium has undergone a fast radiation during the last 4 Myr, which is consistent with the low levels of morphological divergence among sibling species.
Key Words: biogeography • Brachytheciaceae • cryptic species • Macaronesia • Mediterranean biota • northern hemisphere disjunctions • phylogeny • rapid radiation
The five Mediterranean climate regions of the world occupy less than 5% of the Earth surface, yet harbor almost 20% of the world’s angiosperm species diversity (Cowling et al., 1996
). In the northern hemisphere, Mediterranean biota are strikingly similar to those found along the Pacific coast of Northwest America, and this disjunct distribution pattern has long gained the attention of paleobiologists, systematists, and ecologists (Donoghue et al., 2001; Sanmartín et al., 2001; Tiffney and Manchester, 2001; Milne, 2006).
Several competing hypotheses, including a split from the common broad-leaved, sclerophyllous evergreen vegetation after the opening of the North Atlantic, the dispersal via the North Atlantic or the Bering land bridges coupled with subsequent regional extinctions, or more recent transoceanic long-distance dispersal, have commonly been proposed to account for the modern distribution of these Mediterranean floras. The first three hypotheses rely on a stepping-stone dispersal model (Schuster, 1983) and differ in the timing of divergence. The North Atlantic ocean opened about 60 million years ago (Ma) and may have caused the vicariance of a previously common sclerophyllous vegetation. North America and Europe remained connected, however, via the North Atlantic land bridge until 25 or possibly even 15 Ma (Milne, 2006). Finally, the Bering Land Bridge hypothesis proposes that the American and European Mediterranean floras have undergone a parallel evolution from a much more recent flora connecting Eurasia and western North America since the sundering of the Bering bridge 5.5–5.4 Ma (Milne, 2006). In either case, massive extinctions, either in eastern North America (North Atlantic Land Bridge) or in eastern Asia (Bering Land Bridge), must have occurred to account for the currently observed disjunct pattern.
The fourth hypothesis relies on a long-distance dispersal model. As Milne (2006, p. 466) has claimed, "Long-distance dispersal has been an unpopular hypothesis among biogeographers because it is highly random in nature, almost impossible to falsify and, unlike vicariance, cannot be linked to specific abiotic events" (see also McGlone, 2005). Recent results derived from molecular dating techniques suggest, however, that long-distance dispersal is a much more important factor for explaining the disjunct distributions of plants than previously thought (e.g., Givnish and Renner, 2004; Sanmartín and Ronquist, 2004; DeQueiroz, 2005; Milne, 2006). Distributions that are consistent with the continental drift model may, in fact, reflect a complex mix of relictualism overlaid by more recent evolution and dispersal (McDowall, 2004).
Bryophytes, a group of early land plants of about 18500 species whose monophyly has been increasingly challenged (see Renzaglia et al., 2007, for review), offer the potential for significant insights into biogeographic patterns and area relationships (Shaw, 2001). It has indeed traditionally been assumed that bryophytes can persist in microhabitats where a suitable microenvironment persists, long after the general climate of the region has changed (Schuster, 1983). In this scenario, bryophytes may be more useful for solving phytogeographical problems than many higher plants (Anderson, 1963) Bryophytes, in particular, provide appropriate models for investigating the origin of the northern hemisphere disjunction in Mediterranean biota because 7% of the European and 6% of the North American moss species and 5% of the European and 4% of the North American hepatic species have this western North American–Mediterranean distribution (Schofield, 1988). It has been increasingly recognized that recurrent, asymmetric dispersal is capable of generating regular distribution patterns that mimic ancient vicariance (Cook and Crisp, 2005; Sanmartín et al., 2007), but the coincidence of so many species having essentially the same disjunction has long been used as evidence to argue against long-distance, chance dispersal (Schofield, 1988). Yet, although it has been suggested on paleontological and phylogenetic ground that bryophyte species can remain unchanged at the morphological (Konopka et al., 1998; McDaniel and Shaw, 2003; Frahm and Newton, 2005) and molecular (Frey et al., 1999; Schaumann et al., 2003, 2004) levels over periods of tens to hundreds of million years, the complete absence of morphological differentiation and the extremely low level of molecular divergence among disjunct European and American populations of several moss species tends rather to indicate that the trans-Atlantic disjunction is of fairly recent origin (Shaw et al., 2003).
In this study, we reconstructed the phylogeny of the moss genus Homalothecium, which has a disjunct distribution between North America and Western Palearctic (Europe, Central Asia, and North Africa), with centers of diversity in the Pacific Northwest and the Mediterranean region, to revisit the origin of the North Atlantic range disjunction. We contrast the phylogeny with the general area cladogram that would be expected under competing biogeographic hypotheses and infer the minimum number of vicariance, dispersal, sympatric speciation, and extinction events that are necessary to reconcile the two. Finally, we used a Bayesian procedure implementing a relaxed-clock model (Drummond et al., 2002, 2006) to test hypotheses regarding the timing of the northern hemisphere disjunction observed in the genus.
MATERIALS AND METHODS
Taxon sampling
All species that belong to Homalothecium according to recent taxonomic revisions (Hoffman, 1998; Ignatov and Huttunen, 2002) were sampled. Several specimens of each species from different parts of their distribution areas were sampled (Appendix 1).
The outgroup included Floribundaria floribunda (Dozy & Molk.) M.Fleisch., a species belonging to the Meteoriaceae, sister family of the Brachytheciaceae (Huttunen et al., 2004) and representatives of different subfamilies of the Brachytheciaceae: Rhynchostegiella tenella (Dicks.) Limpr., Brachythecium rivulare Schimp., Cirriphyllum piliferum (Hedw.) Grout, and Eurhynchiastrum pulchellum (Hedw.) Ignatov & Huttunen. In addition, eight accessions of Brachytheciastrum, which is sister to Homalothecium within the Homalothecioideae (Huttunen and Ignatov, 2004; Vanderpoorten et al., 2005), were also used.
Molecular protocols
Total DNA was extracted using the DNeasy Plant Mini kit (Qiagen Solna, Sweden). On the basis of data from previous projects (Huttunen et al., 2004; Vanderpoorten et al., 2005; Hedenäs and Eldenäs, 2007) we selected three DNA regions (nuclear ITS1-5.8S-ITS2 region, plastid atpB-rbcL spacer, and plastid rpl16 region for sequencing. The ITS1-5.8S-ITS2 region was amplified with primers ITS5_bryo and ITS4_bryo (Stech and Frahm, 1999), the rpl16 region with primers rpl16ant R2 (Hedenäs and Eldenäs, 2007) and F71 (Jordan et al., 1996) and atpB-rbcL with the primers atpB-bryo and rbcL-bryo (Chiang et al., 1998). PCR cycles included an initial denaturation with 5 min at 95°C, followed by 35 cycles of 30 s at 95°C, 30 s at 52°C, 1 min 30 s at 72°C for the ITS region, 35 cycles of 30 s at 95°C, 30 s at 58°C, 1 min 30 s at 72°C for the rpl16, and 30–35 cycles of 45 s at 95°C, 1 min 15 s at 49°C, 1 min 15 s at 72°C for the atpB-rbcL; and a final elongation of 8 min at 72°C. PCR amplicons were sequenced in both directions. Sequencing results were checked and contiguous sequence files compiled with Staden 1–6-0b4 (Staden et al., 2003a, 2003b).
Alignment and phylogenetic analyses
Sequences were aligned manually with BioEdit version 6.0.5. (Hall, 2001). In the ITS alignment, 28 bp were excluded due to ambiguity in positional homology. Phylogenetic information from indel events was included in phylogenetic analyses by coding indel events into a separate data matrix with the program SeqState version 1.25 (Müller, 2006) using the simple indel coding method (Simmons and Ochoterena, 2000). In the latter, all indels are scored as binary characters regardless of their length. All the phylogenetic analyses were first conducted on the chloroplastic (rpl16 and atpB-rbcL) and nuclear (ITS) data separately to detect possible incongruence between partitions by comparing their topologies. No conflicting placement of the same taxon in divergent clades supported with a posterior probability >90% was found. All subsequent analyses were thus carried out on the combined data set.
Phylogenetic analyses were performed with the parsimony ratchet method (Nixon, 1999) using the program TNT version 1.0 (Goloboff et al., 2006) and with Bayesian inference using the program MrBayes (Huelsenbeck and Ronquist, 2001. Parsimony ratchet analyses included 400 random addition series and 1000 ratchet iterations. Cycles with original weights and perturbation phase with a likelihood of 20 for up- and down-weighting alternated. Jackknife support for clades was calculated with TNT using 1000 jackknife replications. Trees for jackknifing were obtained from ratchet with two random addition series and 200 ratchet iterations similar to original ratchet analyses.
For the Bayesian procedure, a specific nucleotide substitution model was selected with the Akaike criterion as implemented by the program MrModeltest version 2.2 (Nylander, 2004), for each of the cpDNA and ITS partitions. A discrete model employing identical rates of forward and backward transitions (Lewis, 2001) was applied to the indel matrix. The rate parameters, base frequencies, and shape parameters of the gamma distributions used to model within matrix heterogeneity were allowed to vary independently in each partition. Two Markov chain Monte Carlo (MCMC) analyses of 3000000 iterations each were run, and trees were sampled every 10000 generations. Stationarity and convergence of the MCMCs were determined by plotting the likelihoods per generation and checking for no average improvement in the likelihood scores. After convergence, the trees from the burn-in phase were removed, and the remaining trees from the two runs were combined to form the full sample of trees assumed to be representative of the posterior probability distribution.
Molecular dating
Divergence times were estimated using an uncorrelated log-normal model of rate variation among branches in the tree (i.e., a relaxed-clock model). The model was implemented in a Bayesian context in the program BEAST v.1.4.3. Win (Drummond et al., 2002, 2006; Drummond and Rambaut, 2007) to sample branch lengths and absolute rates of nucleotides substitution, within the range of a set of priors and according to their posterior probabilities.
An independent model of nucleotide substitution, as identified by MrModeltest, was applied to each of the ITS and cpDNA partitions. Two independent general time reversible models of nucleotide substitution, with among-sites rate variation modeled by a discrete gamma distribution with six rate categories, were applied to the two cpDNA partitions (atpB-rbcL and rpl16), while a Hasegawa–Kishino–Yano (Hasegawa et al., 1985) model of nucleotide substitution with gamma-distributed rates was applied to the ITS partition. Molecular dating was performed on the 50% majority-rule consensus of the trees sampled from the posterior probability distribution generated by the MrBayes analysis. Despite the fact that BEAST can simultaneously estimate the posterior probability distribution of tree topologies and divergence times, only the latter were sampled by the MCMC in our analysis. BEAST does indeed not allow the user to model insertion–deletion evolution, which is a major shortcoming because of the large number of informative indels in our data set. The MrBayes analyses without indel scoring (that is, the data and settings for the analyses are the same as in the BEAST analyses) resulted in a congruent, but less resolved and supported topology than those including the indel data. Therefore, the topology derived from the MrBayes analysis with indel data, which constitutes the best phylogenetic hypothesis currently available for Homalothecium, was used as a constraint in the BEAST analysis. An uncorrelated log-normal model of rate variation was applied independently on each of the partitions, so that the MCMC could sample, for each partition, different rates of nucleotide substitution and degrees of relaxation of the molecular clock.
In the absence of fossil evidence in Homalothecium, a strong prior on the absolute rate of molecular evolution was used on each partition. Estimates of absolute rates of molecular evolution found in the literature were used. Because substitution rates may vary among lineages (Sanderson et al., 2004), uncertainties around those estimates were factored using probabilistic calibration priors. Accordingly, a normal distribution prior on the absolute ITS rate of evolution, with a mean of 0.014 substitutions–1•site–1•Myr and standard deviation of 0.005 substitutions–1•site–1•Myr, was used. This prior is based on the estimation in green algae and land plants of a sequence divergence in the ITS region that ranges from 0.8 to 2.0% Myr–1 (Bakker et al., 1995). A mean prior of 0.014 corresponds to the average between 0.8 and 2.0% Myr–1, and the standard deviation was set so that the normal distribution centered on the mean of 0.014 includes both the minimum and maximum values estimated by Bakker et al. (1995). For the cpDNA data sets, a normal distribution with a mean of 5.0 10–4 and standard deviation of 10–4 substitutions–1•site–1•Myr was used as a prior on the absolute rpl16 and atpB-rbcL rates of evolution. These figures are derived from Palmer (1991) and Schnabel and Wendel (1998), who report average absolute rates of substitutions in noncoding cpDNA of 5.0 10–4 substitutions–1•site–1•Myr across a wide range of algae and land plants. We used here a standard deviation of 10–4 substitutions–1•site–1•Myr so that our prior probability distribution includes a wide range of rates documented for land plants.
A Yule prior on branching rates was employed and four independent MCMC analyses were each run for 10000000 steps. Parameter values were sampled every 1000 cycle over the 10000000 MCMC steps. Convergence and acceptable mixing of the sampled parameters was checked using the program Tracer 1.2 (Rambaut and Drummond, 2003). After discarding the burn-in steps, the four runs were combined to obtain an estimation of the posterior probability distribution of the divergence dates of the ancestral nodes.
To compare the results from the previous analysis, we ran a second analysis to infer the absolute rates of nucleotide substitution if the ancient vicariance hypothesis were to be accepted. In this last analysis, the age of the opening of the North Atlantic Ocean, which occurred around 60 Ma (Tiffney and Manchester, 2001), was used as a calibration point. Accordingly, the age of the node that represents the North American–Eurasiatic disjunction was sampled from a normal prior probability distribution centered at 60 ± 3 Myr (± SD) by the MCMC.
Diversification rate estimates
With a dated phylogeny and under the assumption of a Yule pure-birth process of diversification, the measure 
, defined separately by Kendall (1949) and Moran (1951), can be used to estimate diversification rates in a group of interest. The rate of diversification , which is equal to N – 2/s, where N is the number of extant taxa and s is the sum of the durations of the branches of the phylogeny (Nee, 2001), was calculated at several nodes in the phylogeny to estimate its variability among Homalothecium lineages. To account for uncertainty in the divergence time estimates, we calculated a minimum, maximum, and mean value of using the minimum, maximum, and mean divergence dates estimated by our molecular dating analysis.
Biogeographic inference
Event-based methods that explicitly incorporate all the processes that might explain the observed distribution patterns, including vicariance, speciation within an area, extinction, and dispersal, were employed to reconstruct ancestral distributions and infer the evolutionary mechanisms explaining the observed distribution of Homalothecium species. Each process is assigned a cost and the analysis involves finding the biogeographic scenario with the lowest overall cost (see Sanmartín et al., 2007, for review). Dispersal-vicariance analysis as implemented by the program DIVA version 1.1 (Ronquist, 1997), was used to infer ancestral areas at each internal node. The program TreeFitter version 1.0 (Ronquist, 2001) was then used to determine the number of events of vicariance, speciation within an area, extinction, and dispersal, which are necessary to reconcile the species tree with a general area cladogram derived from the succession of geographic events (Sanmartín and Ronquist, 2004). More recent techniques that directly incorporate information on lineage duration and divergence times (Ree et al., 2005) were not used here because we aimed at testing for the ancient vicariance hypothesis by means of two complementary and independent analyses involving molecular dating on the one hand and event-based tree-fitting on the other. Each Homalothecium species was assigned one or several of four distribution areas, including eastern and western North America, as delimited by the midcontinental seaway that separated the continent longitudinally in the late Cretaceous (see, e.g., Sanmartín et al., 2001), Western Palearctic, and Macaronesia. Outgroup taxa, which are not representative of the distribution of their families (Vilhelmsen, 2004), were excluded from the analysis. TreeFitter analyses were performed by fitting the 50% majority-rule consensus of the trees sampled from the posterior probability distribution to different biogeographic scenarios (Table 1). The analyses were carried out using the default cost settings. The significance of the scenarios inferred was assessed by 1000 random permutations of terminals in the species tree.
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The length of the DNA fragments ranges in the ITS region from 706 to 751 bp, in the rpl16 from 687 to 708 bp, and in the atpB-rbcL from 581 to 602 bp. The proportion of parsimony-informative (PI) positions is highest in the ITS (9.9% of the positions in the alignment used in phylogenetic analyses), while the rpl16 (5.8%) and the atpB-rbcL (4.9%) regions have fairly similar proportions of PI positions. The gap coding added 57 PI characters in ITS, 8 in atpB-rbcL and 21 in rpl16. The majority of these gaps are 1–3 bp long (19 of 21 gaps in the rpl16, 7 of 8 in the atpB-rbcL, and 34 of 57 in the ITS region).
The 50% majority-rule consensus of the trees sampled from the posterior probability distribution from MrBayes analysis (average –ln L = -6934.63) is presented in Fig. 1. MP analyses recovered a single tree (L = 709), which is fully congruent with the consensus from the Bayesian analysis. Homalothecioideae Ignatov & Huttunen, as originally circumscribed (Ignatov and Huttunen, 2002), are not monophyletic in the present analyses. Homalothecium laevisetum was indeed nested among the outgroup species. Within Homalothecioideae, Brachytheciastrum and Homalothecium are resolved as sister with 80% posterior probability. However, Homalothecium s. l. is not monophyletic because H. arenarium appears as sister to the Brachytheciastrum-Homalothecium clade.
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The crown Homalothecium clade includes two of the three sampled accessions of H. megaptilum, which form a fully supported clade that is sister to two strongly supported clades labeled as the ‘Eurasiatic’ and the ‘American’ on Fig. 1. Within the American clade, supported with a 100% posterior probability, the accessions of North American species, H. aeneum, H. nevadense, and H. fulgescens, form monophyletic lineages supported by 99%, 100% and 100% posterior probabilities, respectively. The third sampled accession of H. megaptilum groups with the H. nevadense clade with a 100% posterior probability.
The Eurasiatic clade, with 99% posterior probability, includes H. fallax, H. lutescens, and H. philippeanum, which are distributed in western Eurasia and North Africa, and H. sericeum, which has the same range but is also present in eastern North America. The three Madeiran accessions of H. sericeum form a fully supported clade (100% posterior probability) sister to the remaining European, Central Asiatic, and American accessions of the species (99% posterior probability).
The divergence dates were estimated for each node supported by more than 50% posterior probability values and are given in Fig. 1. The split between the Eurasiatic and American Homalothecium clades (A in Fig. 1) and between the three Madeiran accessions of H. sericeum and the remaining Eurasiatic and American accessions of the species (C in Fig. 1) are estimated at 5.69 (3.52–8.26) and 2.52 (0.86–8.25) Ma, respectively.
Under the assumption that the split between the Eurasiatic and American Homalothecium clades took place following the opening of the North Atlantic ocean, approximately 60 Ma, the absolute rates of nucleotide substitution for the ITS and the atpB-rbcL and rpl16 chloroplast regions are estimated at 1.15 x 10–4 (0.79 x 10–4–1.54 x 10–4), 5.51 x 10–5 (3.57 x 10–5–7.92 x 10–5) and 5.61 x 10–5 (3.59 x 10–5–7.75 x 10–5) substitution–1•nucleotide–1•Myr, respectively.
Using 7.9 (5.02–11.57) Myr as the actual time of origin of the most recent common ancestor to all extant lineages of the core Homalothecium clade, the rate of diversification () is estimated at 0.5 (0.28–1.1) new lineages per million year. The rate of diversification for the various clades within the core Homalothecium clade varies around a mean diversification of 0.56 new lineages per million year. With a rate of diversification of 0.34, the basal Homalothecium clade (Fig. 1) has the slowest diversification rate, while clade C seems to have diversified faster than any other clade, as suggested by a diversification rate of 0.77 lineages per million year.
The reconstruction of ancestral distribution areas is presented in Fig. 2. The different biogeographic scenarios tested all have the same cost of 6, and no random permutation in 1000 of the species tree terminals generated reconstructions with a lower cost (Table 1). This cost corresponds to 46 instances of sympatric diversification, 0–1 vicariance events, 0–2 extinctions, and 2–3 dispersal events. Among the four possible events that are used to reconcile the area cladograms with the species tree, only diversification within the area was more frequent than expected by chance (Table 1).
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Phylogeography of Homalothecium
Besides a few lineages that render Homalothecium polyphyletic and the call for taxonomic changes that we presented elsewhere, the phylogenetic analysis of Homalothecium resolves two main lineages: one including only American species and another with Western Palearctic species. The existence of such a strong phylogeographic signal suggests that long-distance dispersal is less important than mutation for generating patterns of variation on a global scale. This pattern contrasts with that found in species that commonly produce numerous, small spores; for example, in many Polytrichaceae (van der Velde and Bijlsma, 2003) or weedy species such as Tortula muralis (Werner and Guerra, 2004) and Ceratodon purpureus (Hedw.) Brid. (McDaniel and Shaw, 2005). In those cases, little or no intercontinental differentiation was detected. Our data support the view that barriers to gene flow exist at the intercontinental scale in Homalothecium, in agreement with some previous intercontinental moss phylogeographies (Shaw, 2000; McDaniel and Shaw, 2003; Shaw et al., 2003; Grundmann et al., 2006; Vanderpoorten et al., 2008).
Sympatric diversification is the only of the four mechanisms used to reconcile the Homalothecium species tree with the proposed biogeographic scenarios, which is more frequent than expected by chance. Although dispersal was inferred more frequently than vicariance and extinction, none of these events received statistical support. The different biogeographic scenarios proposed to explain modern Homalothecium distributions furthermore all have the same cost, which is not indicative of a strong vicariance signal. Although these observations tend to suggest that modern distributions of Homalothecium species were achieved through rare instances of dispersal followed by sympatric diversification, competing hypotheses regarding the origin of the northern Atlantic range disjunction in the genus cannot be satisfactorily tested without setting a time scale.
Molecular dating in bryophytes is, unfortunately, hampered by the extremely limited availability of the fossil record. The fossil record for bryophytes is, indeed, extremely incomplete, whether through low probability of fossilization due to habitat preferences or poor preservation due to absence of cutinized or woody tissue. Most of the rare pre-Quaternary bryophyte fossils are sterile, and gametophytic evidence is not sufficient to allow for a satisfactory taxonomic placement (Schofield, 1988; Heinrichs et al., 2007). The best source of fossil information for bryophytes comes from tissues preserved in Baltic, Saxon, and Dominican amber because, in contrast to fossils in other deposits, tissues included in amber are usually perfectly conserved (Frahm, 2000, 2004). The percentage of plant fossils in amber is, however, very low. Ninety-nine percent of all fossils from Baltic amber consist of arthropods and, in the remaining percent of plant fossils, bryophytes are extremely rare. To date, only about 100 species are known from the fossil European bryophyte flora (Frahm and Newton, 2005). The problem of fossils is even more acute in pleurocarpous mosses for two reasons. First, the recurrent lack of morphological synapomorphies for defining genera or families, which is probably due to a combination of fast rates of morphological evolution and convergent evolution associated with habitat transitions (Vanderpoorten et al., 2002, 2005; Huttunen et al., 2004), makes it difficult to determine precisely the taxonomic placement of fossils, especially for those that are sterile. Second, the oldest fossils are lacking clear morphological synapomorphies with extant plants, which increases the uncertainty associated with their assignment to an internal node in the phylogeny (Ignatov and Shcherbakov, 2007; Newton et al., 2007).
In the absence of fossil evidence, the divergence of these two lineages was estimated by using absolute rates of molecular evolution found in the literature and factoring uncertainties around those estimates using probabilistic calibration priors. The method can be viewed as uncertain due to rate differences among plant lineages (Sanderson et al., 2004). However, uncertainties were factored as much as possible by using, for each rate, probabilistic priors that were designed to encompass most of the differences found among plant lineages. We are confident that, by taking into account calibration uncertainties, divergence dates can be approximated sufficiently well to place some bounds on the timing of important evolutionary and biogeographic events within Homalothecium. It is noteworthy that our age estimate for the divergence between H. lutescens and H. sericeum (B in Fig. 1, 3.39 Myr, CI 1.76–5.20) is consistent with the age of 1.1–2.6 Myr estimated by Hedderson and Nowell (2006) for the same divergence.
Our dating suggests some phylogenetic patterns that are, at first sight, consistent with a hypothesis of relictualism and ancient vicariance, may actually have originated from recent dispersal. For instance, the monophyly of Madeiran populations of H. sericeum with regard to North American and Western Palearctic populations is consistent with the idea of a Tertiary relictual origin of the Macaronesian flora, as initially proposed by Engler’s and subsequently reiterated by other biogeographers (e.g., Dansereau, 1961; Bramwell, 1972, 1976; Sunding, 1979;Takhtajan, 1986). Yet, the age of the ancestral node of H. sericeum (C in Fig. 1, 2.52 Myr) is not compatible with this scenario. This observation adds to the mounting evidence that Macaronesian endemism in bryophytes may not be relictual of a Tertiary flora that vanished during the glaciations but is of fairly recent, neoendemic origin (Vanderpoorten et al., 2007).
Similarly, our age estimate (5.69 Myr; A in Fig. 1) for the divergence between the American and Eurasiatic clades contradicts the hypothesis of the fragmentation of an ancestral continuous Laurasian range, which was at first sight consistent with the reciprocal monophyly of North American and Eurasiatic lineages. Under the assumption that the split between these clades is, in fact, due to the opening of the North Atlantic ocean (approximately 60 Ma), the analysis produces unrealistic estimates for the absolute rate of nucleotide substitution for both the ITS and chloroplast regions. Acceptation of the ancient vicariance hypothesis would in fact involve that rates of nucleotide substitution in the ITS, atpB-rbcL, and rpl16, are 10–100 times slower than the rates currently reported in land plants (Palmer, 1991; Bakker et al., 1995; Schnabel and Wendel, 1998). Although it has sometimes been suggested that bryophytes are capable of extremely low rates of evolution (Frey et al., 1999; Schaumann et al., 2003, 2004), current evidence based on molecular dating contradicts such an interpretation (McDaniel and Shaw, 2003; Wall, 2005; Newton et al., 2007). Our results are thus congruent with recent analyses (Tiffney and Manchester, 2001; Shaw et al., 2003; Hohmann et al., 2006; Milne, 2006) that challenge the traditional view that the speciation in North American and Eurasiatic clades is a result of the fragmentation of a widespread sclerophyllous vegetation zone and loss of the biotic connection between North America and Europe in the late Oligocene or early Miocene (Axelrod, 1975; Milne, 2006).
Based on our results, the hypothesis of a parallel evolution of the genus from a Beringian flora that diverged after the sundering of the Bering Land Bridge 5.4–5.5 Ma (Milne, 2006) cannot be rejected. However, the cooling of the climate may have broken the biotic connection through the Bering land bridge already earlier (Milne and Abbot, 2002), rendering the Beringian route unlikely. This hypothesis requires, furthermore, the extinction of Homalothecium in East Asia. Such a hypothesis has, however, been challenged on paleobotanical grounds because of limited evidence that sclerophyllous vegetation ever formed a continuous band between presently disjunct regions (Wolfe, 1975). In angiosperm genera like Styrax, which have geographic disjunctions similar to those observed in Homalothecium, such an absence of fossils in the eastern Asian flora was used to argue against the Bering Land Bridge hypothesis (Fritsch, 1996). The absence of fossils in this area could definitely be explained by the low fossilization rate typical of bryophytes. However, signatures of formerly wider distributions in eastern Asia can often be found in extant distributions. For example, Antitrichia curtipendula (Hedw.) Brid. s. l. [including A. gigantea (Sull. & Lesq.) Kindb. and A. formosana Nog.], which has a similar ecology and distribution pattern to Homalothecium, has a few extant occurrences in Taiwan (Hedenäs, 2008).
Alternatively, the North American–European disjunction observed in Homalothecium may result from discrete transoceanic events of long-distance dispersal after the sundering of the land bridges. The dispersal ability of bryophytes has long been debated (see Shaw, 2001, for a review). Several pieces of evidence from experiments on spore durability and tolerance to the harsh climatic conditions prevailing in high altitude air currents (van Zanten, 1978; van Zanten and Gradstein, 1988), correlative analyses between species distributions and air currents (Munoz et al., 2004), interpretation of species distributions in a phylogenetic context (e.g., Shaw et al., 2003; Vanderpoorten and Long, 2006), and genetic inferences of dispersal (McDaniel and Shaw, 2005) all point to an overall good ability of bryophytes for long-distance dispersal. Most recently, Hartmann et al. (2006) and Heinrichs et al. (2006) used molecular dating techniques to reject ancient vicariance as an explanation for transoceanic distribution patterns. Altogether, all these observations converge toward a scenario, wherein long-distance dispersal plays a major role in modern moss distributions.
Consequences for speciation and evolution
The evolutionary corollary of a fairly recent origin of Homalothecium species is that, in contrast with a traditional interpretation according to which mosses are slowly evolving plants (Cummins and Wyatt, 1981), speciation rates in bryophytes can be fairly high. With a diversification rate of 0.5 (0.28–1.1) new lineages per million year, the radiation of Homalothecium is actually comparable to that of Mittyrhidium, a moss genus that originated approximately 8 Ma on Peninsular Malaysia and diversified at a rapid rate of 0.56 ± 0.004 new lineages per million year (Wall, 2005). Those rates are also comparable with other key examples of rapid endemic speciation in angiosperms (Baldwin and Sanderson, 1998; Klak et al., 2004; Hughes and Eastwood, 2006).
The hypothesis of a recent origin of Homalothecium species is consistent with the sometimes subtle morphological differences that exist among species, leading to conflicts regarding the acceptance of such taxa at the species level. Within the H. aureum clade, for example, the American specimens share a suite of characteristics including paraphyses among female gametangia that are longer than in Eurasiatic specimens, smaller spores, a shorter seta, a smaller size, a more rigid, profoundly regularly pinnate and stiff habit, and a dioicous sexual condition contrasting with the phyllodioicous condition of Eurasiatic specimens. These characters have, however, a fairly continuous range of variation, making it difficult to draw a clear limit. As a result, the American populations are, in some instances, treated as a distinct species, H. pinnatifidum (Sull. & Lesq.) Lawton (Grout, 1928; Lawton, 1965; Norris and Shevock, 2004), while being synonymized with H. aureum in others (Hoffman, 1998). Morphometrical analyses did not, however, find any characters to distinguish them (Hoffman, 1997).
Similarly, the position of all Madeiran specimens of H. sericeum as sister to North American and Western Palearctic accessions supports previous taxonomic treatments recognizing the Madeiran endemic species, H. mandonii (Mitt.) Geh. The morphological differences separating these two taxa are, however, unclear, and H. mandonii is often treated in synonymy to H. sericeum (Hedenäs, 1992; Hill et al., 2006). According to Geheeb (1886), H. mandonii differs from H. sericeum only by the shape and serrulation of the branch leaves, characters that are fairly unreliable in Homalothecium. Homalothecium mandonii is morphologically a very variable species (Hedenäs, 1992), and our molecular sampling included three specimens that differed, for example, in size and branch curvature. In most characters, the morphological variation overlaps with that of H. sericeum. We found, however, at least two potential diagnostic features for the Madeiran clade, namely, a relatively short seta and a naked calyptra that lacks paraphyses, which should be further investigated on a broader specimen sampling.
The question of the recognition of such taxa, for which speciation has perhaps not been completed yet, at the species level, remains open. Our opinion is that synonymizing such taxa would ignore the distinctive nature of the lineages under speciation. In line with previous interpretations of recent endemic speciation in the liverwort genus Leptoscyphus (Vanderpoorten and Long, 2006), we therefore argue for the recognition of distinct species, albeit young and not yet morphologically well characterized.
Appendix 1. GenBank accession and herbarium vouchers for sequenced specimens. A dash indicates the region was not sampled. Voucher specimens are deposited in the following herbaria: H—Helsinki, MHA—the Main Botanical Garden of Russian Academy of Sciences Herbarium, Moscow, S—Stockholm, STK—Stuttgart, UBC—Herbarium of the University of British Columbia.
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FOOTNOTES
1 The authors thank the curators of the herbarium of the University of British Columbia (UBC) and the Natural History Museum of Stuttgart (STK) for loans of herbarium material. This research was supported by a Marie Curie Intra-European Fellowship (MEIF-CT-2005-009452) within the 6th European Community Framework Program for S.H. and by the Swedish Foundation for International Cooperation in Research and Higher Education (STINT, Dnr. 05/063). The Swedish Research Council (Vetenskapsrådet project no. 621-2003-3338) supported the participation of L.H. in this project. N.D. and A.V are grateful for financial support from the Belgian Funds for Scientific Research (FNRS). M.I. was partly supported by the Russian Foundation for Basic Research (RFBR 07-04-00013). 
5 Author for correspondence (e-mail: sanna.huttunen{at}nrm.se)
LITERATURE CITED
Anderson, L. E. 1963. Modern species concepts: Mosses. Bryologist 66: 107–119.
Axelrod, D. I. 1975. Evolution and biogeography of Madrea-Tethyan sclerophyll vegetation. Annals of the Missouri Botanical Garden 62: 280–334.[CrossRef][Web of Science]
Bakker, F. T., J. L. Olsen, AND W. T. Stam. 1995. Evolution of nuclear rDNA ITS sequences in the Cladophora albida/sericea clade (Chlorophyta). Journal of Molecular Evolution 40: 640–651.[CrossRef][Web of Science][Medline]
Baldwin, B. G., AND M. J. Sanderson. 1998. Age and rate of diversification of the Hawaiian silversword alliance (Compositae). Proceedings of the National Academy of Sciences, USA 95: 9402–9406.
Bramwell, D. 1972. Endemism in the flora of the Canary Islands. In D. H. Valentine [ed.], Taxonomy, phytogeography and evolution, 141–159. Academic Press, London, UK.
Bramwell, D. 1976. The endemic flora of the Canary Islands: Distribution, relationships and phytogeography. In G. Kunkel [ed.], Biogeography and ecology in the Canary Islands. W. Junk, The Hague, Netherlands.
Chiang, T.-Y., B. A. Schaal, AND C.-I. Peng. 1998. Universal primers for amplification and sequencing a noncoding spacer between the atp B and rbc L genes of chloroplast DNA. Botanical Bulletin of Academica Sinica 39: 245–250.
Cook, L. G., AND M. D. Crisp. 2005. Directional asymmetry of long-distance dispersal and colonization could mislead reconstructions of biogeography. Journal of Biogeography 32: 741–754.[CrossRef][Web of Science]
Cowling, R.-M., P. W. Rundel, B. B. Lamont, M. K. Arroyo, AND M. Arianoutsou. 1996. Plant diversity in Mediterranean-climate regions. Trends in Ecology &Evolution 11: 362–366.[CrossRef][Web of Science]
Cummins, H., AND R. Wyatt. 1981. Genetic variability in natural populations of the moss Atrichum angustatum. Bryologist 84: 30–38.[CrossRef]
Dansereau, P. 1961. Etudes macaronésiennes. I. Géographie des Cryptogames vasculaires. Agronomica Lusitanica 23: 151–181.
de Queiroz, A. 2005. The resurrection of oceanic dispersal in historic biogeography. Trends in Ecology &Evolution 20: 68–73.[CrossRef][Web of Science][Medline]
Donoghue, M. J., C. D. Bell, AND J. Li. 2001. Phylogenetic patterns in northern hemisphere plant geography. International Journal of Plant Sciences 162 (6 supplement): 41–52.
Drummond, A. J., S. Y. W. Ho, M. J. Phillips, AND A. Rambaut. 2006. Relaxed phylogenetics and dating with confidence. PLoS Biology 4: e88.[CrossRef][Medline]
Drummond, A. J., G. K. Nicholls, A. G. Rodrigo, AND W. Solomon. 2002. Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data. Genetics 161: 1307–1320.
Drummond, A. J., AND A. Rambaut. 2007. Bayesian evolutionary analysis sampling trees, version 1.4.3. Website http://beast.bio.ed.ac.uk..
Frahm, J.-P. 2000. New and interesting records of mosses from Baltic and Saxonian amber. Lindbergia 25: 33–39.
Frahm, J.-P. 2004. A new contribution to the moss flora of Baltic and Saxon amber. Review of Palaeobotany and Palynology 129: 81–101.[CrossRef][Web of Science]
Frahm, J.-P., AND A. Newton. 2005. A new contribution to the moss flora of Dominican amber. Bryologist 108: 526–536.[CrossRef]
Frey, W., M. Stech, AND K. Meissner. 1999. Chloroplast DNA-relationship in palaeoaustral Lopidium concinnum (Hypopterygiaceae, Musci). An example of stenoevolution in mosses—Studies in austral temperate rain forest bryophytes 2. Plant Systematics and Evolution 218: 67–75.[CrossRef][Web of Science]
Fritsch, P. 1996. Isozyme analysis of intercontinental disjuncts within Styrax (Styraceae): Implications for the Madrean-Thetyan hypothesis. American Journal of Botany 83: 342–355.[CrossRef][Web of Science]
Geheeb, A. 1886. Bryologische Fragmente. III. A Diverse Notizen. Flora 22: 339–353.
Givnish, T. J., AND S. S. Renner. 2004. Tropical intercontinental disjunctions: Gondwana breakup, immigration from the boreo-tropics, and transoceanic dispersal. International Journal of Plant Sciences 165 (supplement): S1–S6.[CrossRef][Web of Science]
Goloboff, P., J. S. Farris, AND K. Nixon. 2006. TNT: Tree analysis using New Technology, version 1.0. Website http://www.zmuc.dk/public/Phylogeny/TNT.
Grout, A. 1928. Moss flora of North America North of Mexico, vol. III, part I.
Grundmann, M., H. Schneider, S. J. Russell, AND J. C. Vogel. 2006. Phylogenetic relationships of the moss genus Pleurochaete Lindb. (Bryales: Pottiaceae) based on chloroplast and nuclear genomic markers. Organisms, Diversity &Evolution 6: 33–45.[CrossRef][Web of Science]
Hall, T. 2001. BioEdit version 5.0.6. Website http://www.mbio.ncsu.edu/BioEdit/BioDoc.pdf.
Hartmann, F. L., R. Wilson, S. R. Gradstein, H. Schneider, AND J. Heinrichs. 2006. Testing hypothesis on species delimitation and disjunctions in the liverwort Bryopteris (Jungermanniopsida: Lejeuneaceae). International Journal of Plant Sciences 167: 1205–1214.[CrossRef][Web of Science]
Hasegawa, M., H. Kishino, AND T. Yano. 1985. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 26: 132–147.[CrossRef]
Hedderson, T. A., AND T. L. Nowell. 2006. Phylogeography of Homalothecium sericeum (Hedw.) Br. Eur.; toward a reconstruction of glacial survival and post-glacial migration. Journal of Bryology 28: 283–292.[CrossRef][Web of Science]
Hedenäs, L. 1992. Flora of Madeiran pleurocarpous mosses (Isobryales, Hypnobryales, Hookeriales). Bryophytorum Bibliotheca 44: 1–165.
Hedenäs, L. 2008. Molecular variation and speciation in Antitrichia curtipendula s. l. (Leucodontaceae, Bryophyta). Botanical Journal of the Linnean Society 156: 341–354.[CrossRef][Web of Science]
Hedenäs, L., AND P. Eldenäs. 2007. Cryptic speciation, habitat differentiation, and geography in Hamatocalis vernicosus (Calliergonaceae, Bryophyta). Plant Systematics and Evolution 268: 131–145.[CrossRef][Web of Science]
Heinrichs, J., J. Hentschel, R. Wilson, K. Feldberg, AND H. Schneider. 2007. Evolution of leafy liverworts (Jungermanniidae, Marchantiophyta): Estimating divergence times from chloroplast DNA sequences using penalized likelihood with integrated fossil evidence. Taxon 56: 31–44.[Web of Science]
Heinrichs, J., M. Lindner, H. Groth, J. Hentschel, K. Feldberg, C. Renker, J. J. Engler, M. von Konrat, D. G. Long, AND H. Schneider. 2006. Goodbye or welcome Gondwana?—Insights into the phylogenetic biogeography of the leafy liverwort Plagiochila with a description of Proskauera, gen. nov. (Plagiochilaceae, Jungermanniales). Plant Systematics and Evolution 258: 227–250.[CrossRef][Web of Science]
Hill, M. O., N. Bell, M. A. Bruggeman-Nannenga, M. Brugues, M. J. Cano, J. Enroth, K. I. Flatberg, J.-P. Frahm, M. T. Gallego, R. Garilleti, J. Guerra, L. Hedenäs, D. T. Holyoak, J. Hyvönen, M. S. Ignatov, F. Lara, V. Mazimpaka, J. Munos, AND L. Söderström. 2006. An annotated checklist of the mosses of Europe and Macaronesia. Journal of Bryology 28: 198–267.[CrossRef][Web of Science]
Hoffman, H. 1997. Biometrical investigation on Homalothecium aureum, H. pinnatifidum, and related taxa. Journal of Bryology 19: 465–484.
Hoffman, H. 1998. A monograph of the genus Homalothecium (Brachytheciaceae, Musci). Lindbergia 23: 119–159.
Hohmann, S., J. W. Kadereit, AND G. Kadereit. 2006. Understanding Mediterranean-Californian disjunctions: molecular evidence from Chenopodiaceae-Betoideae. Taxon 55: 67–78.[Web of Science]
Huelsenbeck, J. P., AND F. R. Ronquist. 2001. MrBayes: Bayesian inference of phylogeny. Biometrics 17: 754–755.
Hughes, C., AND R. Eastwood. 2006. Island radiation on a continental scale: Exceptional rates of plant diversification after uplift of the Andes. Proceedings of the National Academy of Sciences, USA 103: 10334–10339.
Huttunen, S., AND M. S. Ignatov. 2004. Phylogeny of Brachytheciaceae (Bryophyta) based on morphology and sequence level data. Cladistics 20: 151–183.[CrossRef][Web of Science]
Huttunen, S., M. S. Ignatov, K. Müller, AND D. Quandt. 2004. Phylogeny and evolution of epiphytism in the three moss families Meteoriaceae, Brachytheciaceae and Lembophyllaceae. Monographs in Systematic Botany 98: 328–361.
Ignatov, M. S., AND S. Huttunen. 2002. Brachytheciaceae (Bryophyta)—A family of sibling genera. Arctoa 11: 245–296.
Ignatov, M. S., AND D. E. Shcherbakov. 2007. Did pleurocarpous mosses originate before the Cretaceous? In A. Newton, and R. Tangney [eds.], Pleurocarpous mosses: Systematics and evolution. Systematics Association Special Volume 71: 321–336.
Jordan, W. C., M. W. Courtney, AND J. E. Neigel. 1996. Low levels of interspecific genetic variation at rapidly evolving chloroplast DNA locus in North American duckweeds (Lemnaceae). American Journal of Botany 83: 430–439.[CrossRef][Web of Science]
Kendall, D. G. 1949. Stochastic processes and population growth. Journal of the Royal Statistical Society, B 11: 230–264.
Konopka, A. S., P. S. Herendeen, AND P. R. Crane. 1998. Sporophytes and gametophytes of Dicranaceae from the Santonian (Late Cretaceous) of Georgia, USA. American Journal of Botany 85: 714–723.[Abstract]
Lawton, E. 1965. A revision of the genus Homalothecium in western North America. Bulletin of the Torrey Botanical Club 92: 333–354.[CrossRef]
Lewis, P. O. 2001. A likelihood approach to estimating phylogeny from discrete morphological character data. Systematic Biology 50: 913–925.
McDaniel, S. F., AND A. J. Shaw. 2003. Phylogeographic structure and cryptic speciation in the trans-antarctic moss Pyrrhobryum mnioides. Evolution 57: 205–215.[Web of Science][Medline]
McDaniel, S. F., AND A. J. Shaw. 2005. Selective sweeps and intercontinental migration in the cosmopolitan moss Ceratodon purpureus (Hedw.) Brid. Molecular Ecology 14: 1121–1132.[CrossRef][Medline]
McDowall, R. M. 2004. What is biogeography: A place for process. Journal of Biogeography 31: 345–351.[Web of Science]
McGlone, M. S. 2005. Goodbye Gondwana. Journal of Biogeography 32: 739–740.[CrossRef][Web of Science]
Milne, R. I. 2006. Northern hemisphere plant disjunctions: A window on Tertiary land bridges and climate change? Annals of Botany 98: 465–472.
Milne, R. I., AND R. J. Abbot. 2002. The origin and evolution of Tertiary relict floras. Advances in Botanical Research 38: 281–314.[CrossRef]
Moran, P. A. P. 1951. Estimation methods for evolutive processes. Journal of the Royal Statistical Society, B 13: 141–146.
Müller, K. 2006. Incorporating information from length-mutational events into phylogenetic analyses. Molecular Phylogenetics and Evolution 38: 667–676.[CrossRef][Web of Science][Medline]
Muñoz, J., A. M. Felícisimo, F. Cabezas, A. R. Burgaz, AND I. Martínez. 2004. Wind as long-distance dispersal vehicle in the southern hemisphere. Science 304: 1144–1147.
Nee, S. 2001. Inferring speciation rates from phylogenies. Evolution 55: 661–668.[CrossRef][Web of Science][Medline]
Newton, A. E., N. Wikström, N. Bell, L. L. Forrest, AND M. S. Ignatov. 2007. Dating the diversification of the pleurocarpous mosses. In A. Newton, and R. Tangney [eds.], Pleurocarpous mosses: Systematics and evolution. Systematics Association Special Volume 71: 337–366.
Nixon, K. 1999. The parsimony ratchet, a new method for rapid parsimony analysis. Cladistics 15: 407–414.[CrossRef][Web of Science]
Norris, D. H., AND J. R. Shevock. 2004. Contributions toward a bryoflora of California: A specimen-based catalogue of mosses. Madroño 51: 1–131.
Nylander, J. A. A. 2004. MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, Sweden.
Palmer, J. D. 1991. Plastid chromosome: Structure and evolution. In L. Bogorad, and I. K. Vasil [eds.], The molecular biology of plastids, 5–53. Academic Press, San Diego, California, USA.
Rambaut, A., AND A. J. Drummond. 2003. Tracer, version 1.2 [computer program]. Website http://evolve.zoo.ox.ac.uk [accessed June 2007].
Ree, R. H., B. R. Moore, C. Campbell, AND M. J. Donoghue. 2005. A likelihood framework for inferring the evolution of geographic range on phylogenetic trees. Evolution 59: 2299–2311.[Web of Science][Medline]
Renzaglia, K. S., S. Schuette, R. J. Duff, R. Ligrone, A. J. Shaw, B. D. Mishler, AND J. G. Duckett. 2007. Bryophyte phylogeny: Advancing the molecular and morphological frontiers. Bryologist 110: 179–213.[CrossRef]
Ronquist, F. 1997. Dispersal–vicariance analysis: A new approach to the quantification of historical biogeography. Systematic Biology 46: 195–201.
Ronquist, F. 2001. TreeFitter, version 1.0 [computer program]. Website http://www.ebc.uu.se/systzoo/research/treefitter/treefitter.html.
Sanderson, M. J., J. L. Thorne, N. Wikström, AND K. Bremer. 2004. Molecular evidence on plant divergence times. American Journal of Botany 91: 1656–1665.
Sanmartín, I., H. Enghoff, AND F. Ronquist. 2001. Patterns of animal dispersal, vicariance and diversification in the Holarctic. Biological Journal of the Linnean Society 73: 345–390.[CrossRef][Web of Science]
Sanmartín, I., AND F. Ronquist. 2004. Southern hemisphere biogeography inferred by event-based models: Plant versus animal patterns. Systematic Biology 53: 216–243.
Sanmartín, I., L. Wanntorp, AND R. C. Winkworth. 2007. West Wind Drift revisited: Testing for directional dispersal in the Southern Hemisphere using event-based tree fitting. Journal of Biogeography 34: 398–416.[CrossRef][Web of Science]
Schaumann, F., W. Frey, G. Hässel de Menéndez, AND T. Pfeiffer. 2003. Geomolecular divergence in the Gondwanan dendroid Symphyogyna complex (Pallaviciniaceae, Hepaticophytina, Bryophyta). Studies in austral temperate rain forest bryophytes 22. Flora 198: 404–412.
Schaumann, F., T. Pfeiffer, AND W. Frey. 2004. Molecular divergence patterns within the Gondwanan liverwort genus Jensenia (Pallaviciniaceae, Hepaticophytina, Bryophyta). Studies in austral temperate rain forest bryophytes 25. Journal of the Hattori Botanical Laboratory 96: 231–244.
Schnabel, A., AND J. F. Wendel. 1998. Cladistic biogeography of Gleditsia (Leguminosae) based on ndhf and rpl16 chloroplast gene sequences. American Journal of Botany 85: 1753–1765.
Schofield, W. B. 1988. Bryophyte disjunctions in the northern hemisphere: Europe and North America. Botanical Journal of the Linnean Society 98: 211–224.[CrossRef][Web of Science]
Schuster, R. M. 1983. Phytogeography of the Bryophyta. In R. M. Schuster [ed.], New manual of bryology, vol. 1, 463–626. Hattori Botanical Laboratory, Nichinan, Japan.
Shaw, A. J. 2000. Molecular phylogeography and cryptic speciation in the mosses Mielichhoferia elongata and M. mielichhoferiana (Bryaceae). Molecular Ecology 9: 595–608.[CrossRef][Medline]
Shaw, A. J. 2001. Biogeographic patterns and cryptic speciation in bryophytes. Journal of Biogeography 28: 253–261.[CrossRef][Web of Science]
Shaw, A. J., O. Werner, AND R. M. Ros. 2003. Intercontinental Mediterranean disjunct mosses: Morphological and molecular patterns. American Journal of Botany 90: 540–550.
Simmons, M. P., AND H. Ochoterena. 2000. Gaps as characters in sequence-based phylogenetic analyses. Systematic Biology 49: 349–381.
Staden, R., D. P. Judge, AND J. K. Bonfield. 2003a. Analysing sequences using the Staden package and EMBOSS. In S. A. Krawetz, and D. D. Womble [eds.], Introduction to bioinformatics. A theoretical and practical approach. Human Press, Totawa, New Jersey, USA.
Staden, R., D. P. Judge, AND J. K. Bonfield. 2003b. Managing sequencing projects in the GAP4 environment. In S. A. Krawetz, and D. D. Womble [eds.], Introduction to bioinformatics. A theoretical and practical approach. Human Press, Totawa, New Jersey, USA.
Stech, M., AND J.-P. Frahm. 1999. The status of Platyhypnidium mutatum Ochyra &Vanderpoorten and the systematic value of the Donrichardsiaceae based on molecular data. Journal of Bryology 21: 191–195.[Web of Science]
Sunding, P. 1979. Origins of the Macaronesian flora. In D. Bramwell [ed.], Plants and islands, 13–40. Academic Press, London, UK.
Takhtajan, A. L. 1986. Floristic regions of the world. Univeristy of California Press, Berkeley, California, USA.
Tiffney, B. H., AND S. R. Manchester. 2001. The use of geological and paleontological evidence in evaluating plant phylogeographic hypothesis in the Northern Hemisphere Tertiary. International Journal of Plant Sciences 162 supplement): S3–17.[CrossRef][Web of Science]
Vanderpoorten, A., M. A. Carine, AND F. Rumsey. 2007. Does Macaronesia exist? Conflicting signal in the bryophyte and pteridophyte floras. American Journal of Botany 94: 625–639.
Vanderpoorten, A., N. Devos, O. J. Hardy, B. Goffinet, AND A. J. Shaw. 2008. The barriers to oceanic island radiation in bryophytes: insights from the phylogeography of the moss Grimmia montana. Journal of Biogeography.
Vanderpoorten, A., L. Hedenäs, C. J. Cox, AND A. J. Shaw. 2002. Phylogeny and morphological evolution of the Amblystegiaceae (Bryophyta, Musci). Molecular Phylogenetics and Evolution 23: 1–21.[CrossRef][Web of Science][Medline]
Vanderpoorten, A., M. S. Ignatov, S. Huttunen, AND B. Goffinet. 2005. A molecular and morphological recircumscription of Brachytheciastrum (Brachytheciaceae, Bryopsida). Taxon 54: 369–376.[Web of Science]
Vanderpoorten, A., AND D. G. Long. 2006. Budding speciation and neotropical origin of the Azorean endemic liverwort, Leptoscyphus azoricus. Molecular Phylogenetics and Evolution 40: 73–83.[CrossRef][Web of Science][Medline]
Van der Velde, M., AND R. Bijlsma. 2003. Phylogeography of five Polytrichum species within Europe. Biological Journal of the Linnean Society 78: 203–213.[CrossRef][Web of Science]
Van Zanten, B. O. 1978. Experimental studies on transoceanic long-range dispersal of moss spores in the southern hemiphere. Journal of the Hattori Botanical Laboratory 44: 455–482.
Van Zanten, B. O., AND S. R. Gradstein. 1988. Experimental dispersal geography of neotropical liverworts. Nova Hedwigia Beihefte 90: 41–94.
Vilhelmsen, L. 2004. The old wasp and the tree: Fossils, phylogeny and biogeography in the Orussidae (Insecta, Hymenoptera). Biological Journal of the Linnean Society 82: 139–160.[CrossRef][Web of Science]
Wall, D. P. 2005. Origin and rapid diversification of a tropical moss. Evolution 59: 1413–1424.[Web of Science][Medline]
Werner, O., AND J. Guerra. 2004. Molecular phylogeography of the moss Tortula muralis Hedw. (Pottiaceae) based on chloroplast rps 4 gene sequence data. Plant Biology 6: 147–157.[CrossRef][Medline]
Wolfe, J. A. 1975. Some aspects of plant geography of the northern during the late Cretaceous and Tertiary. Annals of the Missouri Botanical Garden 62: 264–279.[CrossRef][Web of Science]
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