The status and phylogeography of the liverwort genus Apometzgeria Kuwah. (Metzgeriaceae) Author(s): Linda C. Fuselier, Blanka Shaw, John J. Engel, Matt von Konrat, Denise P. Costa, Nicolas Devos and A. Jonathan Shaw Source: The Bryologist, Vol. 114, No. 1 (Spring 2011), pp. 92-101 Published by: American Bryological and Lichenological Society Stable URL: http://www.jstor.org/stable/41289759 Accessed: 10-08-2016 20:29 UTC REFERENCES Linked references are available on JSTOR for this article: http://www.jstor.org/stable/41289759?seq=1&cid=pdf-reference#references_tab_contents You may need to log in to JSTOR to access the linked references. Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at http://about.jstor.org/terms JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact support@jstor.org. American Bryological and Lichenological Society is collaborating with JSTOR to digitize, preserve and extend access to The Bryologist This content downloaded from 107.0.125.4 on Wed, 10 Aug 2016 20:29:00 UTC All use subject to http://about.jstor.org/terms The status and phylogeography of the liverwort genus Apometzgeria Kuwah. (Metzgeriaceae) Linda C. Fuselier1'5, Blanka Shaw2, John J. Engel3, Matt von Konrat3, Denise P. Costa4, Nicolas Devos2, and A. Jonathan Shaw2 1 Minnesota State University, Moorhead, Biosciences Department, Moorhead, MN USA; 2 Duke University, Department of Biology, Durham, NC USA; 3 Department of Botany, Field Museum, Chicago, IL USA; 4 Instituto de Pesquisas Jardim Botanico do Rio de Janeiro, Rio de Janeiro, RJ, Brazil Abstract. Three species have been formerly segregated from Metzgeria in the genus Apometzgeria . One of the species, A. frontipilis , is endemic to South America but the second, A. pubescens , is currently understood as having a bipolar range with populations across the Holarctic and in southern South America. The third species, A. longifrondis , was described from China (and is not included in this study). Species of bryophytes that range across continents and have little or no morphological variation among populations may nevertheless harbor morphologically cryptic genetic lineages. We used nuclear and plastid sequence data to examine the phylogenetic relationship between Apometzgeria and Metzgeria , and phylogeographic patterns in taxa assigned to Apometzgeria . Two species often assigned to Apometzgeria are phylogenetically embedded within Metzgeria in two separate clades, one comprising all Holarctic A. pubescens and a second with A. pubescens from South America and all accessions of A. frontipilis. Phylogenetic and haplotype analyses reveal a lack of phylogeographic structure among A. pubescens plants from throughout its Holarctic distribution. However, A. pubescens in South America is more closely related to A. frontipilis and species of Metzgeria from South America than to any A. pubescens from the Northern Hemisphere. Thus, A. pubescens is Holarctic in distribution and morphologically similar plants form a divergent lineage in South America. Our results do not support Apometzgeria as a separate genus in the Metzgeriaceae. Keywords, bryophyte systematics, cryptic speciation, Marchantiophyta, disjunct distributions, Metzgeria. ♦ Like seed across species ♦ ♦ plants,liverwort many bryophyte species with intercontinental ranges have been found to consist of more than one, often continents, but unlike seed rather morphologically cryptic, phylogenetically than genera often tax pla disp differentiated lineages rather than a single wide intercontinental ranges. Recently, ranging species. Cryptic species in bryophytes are 5 Corresponding author e-mail: taxa that are similar morphologically but fuselier@mnstate.edu DOI: 10.1639/0007-2745-114.1.92 phylogenetically divergent to an extent that they appear to be different biological species. More and The Bryologist 114(1), pp. 92-101 0007-2745/1 1 /$ 1 .15/0 Copyright ©2011 by The American Bryological and Lichenological Society, Inc. This content downloaded from 107.0.125.4 on Wed, 10 Aug 2016 20:29:00 UTC All use subject to http://about.jstor.org/terms so Fuselier et al.: Phylogeography of Apometzgeria 93 more cryptic species of bryophytes are being Apometzgeria nor Metzgeria are monophyletic and uncovered (e.g., Feldberg et al. 2004; Fuselier et al. that Apometzgeria species are nested within 2009; Hentschel et al. 2007; Shaw 2001; Wachowiak Metzgeria. Crandall-Stotler et al. (2009) synonymized et al. 2007). Apometzgeria and Austrometzgeria with Metzgeria. Two wide-ranging species with little Recently, based on a morphological study, Furuki & morphological variation in the genus Metzgeria Dalton (2008) expanded the concept of Raddi were shown to harbor cryptic phylogenetic Metzgeriaceae to include Vandiemenia Hewson. species (Fuselier et al. 2009). Metzgeria furcata (L.) Apometzgeria was described as a genus based on Dumort. comprises reciprocally monophyletic sister large cells in the seta, undifferentiated dermal cells of clades, one restricted to North America and two in the midrib, large capsule valve length, the largest Europe. Similarly, two distinct lineages of M midrib and sporophytes among species of Metzgeriay conjugata Lindb. include a northern North and presence of hairs on both surfaces of the thallus American-European lineage and a southern North (Kuwahara 1966, 1978). Schuster (1992) rejected the American lineage. In each case, no morphological generic classification of Apometzgeria and argued that distinctions were detected among lineages but the variation within Apometzgeria is as great as that degree of molecular differentiation strongly suggests between Apometzgeria and Metzgeria. Apometzgeria that they are reproductively isolated and pubescens and A. frontipilis are distinct within the phylogenetically divergent. The genus Metzgeria may Metzgeriaceae because they exhibit a highly include additional cryptic lineages, in particular pubescent dorsal thallus. There are only two other within those taxonomic species with wide, "hairy" species of Metzgeria: M. robinsonii Steph. and intercontinental distributions, but a comprehensive M. hispidissima Steph. (Engel & Kuwahara 1973). phylogenetic analysis of the genus is lacking and Both Schuster (1992) and So (2003) questioned using Metzgeria taxonomy can be challenging. the degree of "hairiness" of the dorsal thallus Two hundred and forty binomials for Metzgeria compared to other "hairy" species as a generic-level are listed in Index Hepaticarum (Geissler & Bischler character. Schuster (1992) acknowledged that the 1985), but the actual number is projected to be much shape of the marginal hairs on the thallus may be a lower (Kuwahara 1986; Schuster 1992). Kuwahara species-defining character, but that this points only (1978, 1986) recognized four genera in the to a morphologically distinct lineage within Metzgeriaceae: Steereella Kuwah., Apometzgeria Metzgeria. Kuwah., Austrometzgeria Kuwah. and Metzgeria. There is a need to further investigate taxonomy Austrometzgeria included only A. saccata, Steereella is of the Metzgeriaceae, and this provides an monospecific, and Apometzgeria included two opportunity to examine the group for potential species: A. pubescens (Schrank.) Kuwah. and A. cryptic species. Here, we examine the generic frontipilis (Lindb.) Kuwah. & J. J. Engel, both of classification of two species assigned to the which were previously assigned to Metzgeria. A third Apometzgeria (as proposed by Kuwahara 1978). Two species of Apometzgeria , A. longifrondis (C. Gao) G.C. species in Apometzgeria (Kuwahara 1978), A. Zhang is recognized as part of the flora of China pubescens and A. frontipilis , are dioicous, neither (http://www.tropicos.org/Name/35 1 9 1 1 24) . produces gemmae, and A. pubescens is rarely found Recently, most authors have rejected this four-genus with sporophytes (Schuster 1992). We were unable to system and adopted only two genera, Austrometzgeria obtain material of the third species assigned to and Metzgeria , with Apometzgeria and Sclerocaulon Apometzgeria , A. longifrondis , and it is not further ( Steereella ) as subgenera of Metzgeria (Costa 2008; considered in this study. Schuster 1992; So 2003), or only one genus, The primary morphological differences between Metzgeria (So, 2002). Grolle and Long (2000) A. frontipilis and A. pubescens are the in-rolled thallus acknowledged Schuster's (1992) proposed margins of A. frontipilis and dense, rather than classification but used that of Kuwahara (1978). sparse, development of hairs on the ventral wing Forrest et al. (2006) presented evidence that neither surface in A. pubescens (Engel 1978; Kuwahara 1973). This content downloaded from 107.0.125.4 on Wed, 10 Aug 2016 20:29:00 UTC All use subject to http://about.jstor.org/terms 94 The Bryologist 114(1): 2011 Apometzgeria frontipilis is restricted to, but common, Vermont, USA (vt), University of Northern in southern South America, and extends northward Alabama, USA (una), Herbarium Gottingen, into the Valdivian zone of southern Chile (Engel Germany (goet) and Fraunhofer Institut fur 1978). Engel and Kuwahara (1973) confirm the co- Bauphysik, were used in this study. We included A. occurrence of A. frontipilis and A. pubescens in pubescens from Europe, China, Nepal, Georgia, southern South America. Thus, A. pubescens is North America, and South America, and A. frontipilis described as bipolar in range with populations from South America. Additional taxa included in throughout Europe, China, Russia, Korea, and Northanalyses were: M. agnewiae Kuwah., M. aurantiaca America (though sparsely) as well as Chile (Engel Steph., M ciliata Raddi, M. claviflora Spruce, M. 1978; Schuster 1992). conjugata Lindb., M. dorsipara (Herzog.) Kuwah., M. Apometzgeria pubescens is characterized by a lack filicina Mitt., M. fur cat a, M. leptoneura Spruce, M of separate asexual propagules, low rates of observed myriopoda Lindb., M. rufula Spruce, and M. violacea sexual reproduction and multi-continent (Ach.) Dumort. We chose Pleurozia purpurea Lindb. distribution. Such a combination makes this species as the outgroup taxon based on Forrest et al. (2006). an excellent candidate for harboring cryptic lineages. Voucher information and GenBank accession We used nuclear and plastid sequence data, numbers are provided in Appendix 1 and the data phylogenetic reconstruction and haplotype analyses matrix is available as a TreeBase accession at http:// to test two hypotheses: 1) that Apometzgeria is a monophyletic group within the genus Metzgeria and, purl.org/phylo/treebase/phylo ws/study/TB2:S 10936. Laboratory protocols for CTAB DNA extraction, thus, not a genus genetically distinct from Metzgeria ,PCR and sequencing were modified from Shaw and 2) A. pubescens includes reciprocally (2003) and were the same as in Fuselier et al. (2009). monophyletic clades that correspond to continental We sequenced one nuclear region, RNA polymerase distributions and provides evidence of II subunit 2 (RPB2; Denton et al. 1998), and three morphologically cryptic lineages that have diverged regions from the plastid genome, psbT (Krellwitz et genetically. Apometzgeria frontipilis has a more al. 2001), transfer RNAGLY (UCC) ( trnG ; Pacak & restricted range, so we focus primarily on uncovering Szweykowska-Kulinska 2000), and the transfer potential cryptic lineages within A. pubescens. We RNALEU (UAA) 5' exon-fr«FPHE (GAA) intergenic also examine the relationship between the two species spacer ( trnL ; Taberlet et al. 1991). Forward and of Apometzgeria and ask whether these taxa representreverse sequences were generated for all regions. sister species as inferences from morphology might Sequences were aligned using ClustalX and suggest. Although Forrest et al. (2006) did not resolve additionally, by hand in PhyDE (Miiller et al. 2007). the two Apometzgeria as a single clade, their taxon Preliminary single gene analyses indicated four cases sampling within the Metzgeriaceae was very limited, of incongruence in inferred relationships for an and Schuster (1992) implied that the hairy thalli of accession between genes. As these (four out of an both Apometzgeria species suggests a close initial sample of 63) could have reflected laboratory relationship. We include enough species of Metzgeriaerror or real incongruence, and because none of the to test the monophyly of Apometzgeria but not samples were central to the analyses presented here necessarily enough to determine the closest relatives (i.e., they represented various taxa randomly selected of A. pubescens or A. frontipilis; that awaits an from across Metzgeria) , they were deleted from the exhaustive phylogenetic study of the entire genus data set. Maximum likelihood (ML) best-fit Metzgeria. substitution models were determined using MrModeltest version 2.3 (Nylander 2004) in Materials and Methods conjunction with PAUP version 4.0 (Swofford 2002) for each locus separately and the entire dataset A total of 59 accessions from Duke University, combined. USA (duke), Herbarium Haussknecht, Germany (je), Phylogenetic analyses were executed on New York Botanical Garden, USA (ny), Field Cipres Portal (Miller et al. 2009). ML analyses were run using Museum of Natural History, USA (f), University of Garli version 0.96 (Zwickl 2006) on the This content downloaded from 107.0.125.4 on Wed, 10 Aug 2016 20:29:00 UTC All use subject to http://about.jstor.org/terms Fuselier et al.: Phylogeography of Apometzgeria 95 Table 1. Loci, optimal substitution models, numbers of taxa and characters for each dataset and combined datasets used in phylogenetic analyses. Substitution models are maximum likelihood best fit substitution models identified using MrModeltest software. Substitution No. of No. of included No. of excluded No. of polymorphic Locus model specimens nucleotide sites nucleotide sites nucleotide sites trnL HKY+ trnG GTR+ psbT GTR+ rpbl entire model 45 V dataset 59 150 120 411 17 567 2005 62 134 0 287 78 52 326 under a from single Fig. 1 as M. pubescens) the Northern optima (HKY+I+r). Optimal substitu Hemisphere forms a clade supported by both analyses MrModeltest Bayesian PP and ML bootstrapping, were and this clade is spec by conducted with resolved as sister to a group of MrBayes accessions Ronquist a 368 659 49 I HKY+I+ identified both 58 51 T SYM+ combined & T T single substitution optimal Hemisphere and Southsubstitution America (top clade in Fig. 1). models specified for The southern South American A. frontipilis (in Fig. 1 heterogeneous analysis; 1). as M. frontipilis ), in contrast,Table is part of a different runs clade that includes South American accessions that four chains and each using trees with default were 3. 2001). The entire representing diverse species from the Northerndatase 10,00 sampled 1,000th pubescensy every and specimens of M. ciliata from Marion Island and Chile. Thus, all Apometzgeria accessions estimated by inspection of the plot of log likelihood were nested within the genus Metzgeria and occur in scores at each sampling point. Support of branches two clades that do not form a monophyletic group. was considered significant with posterior probability The two clades containing Apometzgeria specimens (PP) > 95% in Bayesian analyses and bootstrap values differed by more than 100 substitutions. We refer to > 70% for the ML analyses. We used the freeware TCS all Apometzgeria specimens as M. pubescens or M (Clement et al. 2000) to construct haplotype networksfrontipilis from here onwards. and visualize relationships among populations in the Apometzgeria pubescens clade. One of the two South American accessions that agree morphologically with the Northern Hemisphere M. pubescens was collected in Tierra del Results Fuego, and a second in a more northern region of The final combined dataset included 59 specimens and 2005 nucleotide sites; 326 were Chile (Appendix 1). These two specimens differ from the clade that includes all other M. pubescens , but parsimony-informative. 1438 characters are from the differ only by seven mutations, respectively, from the plastid genome and 567 from the nuclear genome, M. frontipilis group. They are resolved as sister to M. contributing 274 (19%) and 52 (9%) polymorphic frontipilis in our reconstruction (Fig. 1). We renucleotide sites, respectively (Table 1). A total of 287examined these specimens and found that the ventral nucleotide sites, including unique indels, those thallus is densely hairy, and thallus margins are not occurring in only one specimen, were excluded fromincurved, supporting their identification as M. the original dataset. Sequences for all plastid and pubescens. These M. pubescens plants from South nuclear loci were not obtained for every specimen America are more closely related to M. frontipilis and other taxa of Metzgeria from South America and Phylogenetic analyses resolved two major well-Africa than they are to any other M. pubescens supported clades that include specimens of We uniform have been determined priors. morphologically as M. Model number of trees needed to reach burn-in was primarily due to difficulties in amplification. m ea specimens from throughout the Holarctic Apometzgeria (Fig. 1). Apometzgeria pubescens (in distribution of the species. This content downloaded from 107.0.125.4 on Wed, 10 Aug 2016 20:29:00 UTC All use subject to http://about.jstor.org/terms gen 96 The Bryologist 114(1): 2011 j - LF628 M. conjugata Austria ' j ■ _ ' | J ' - LF134 M. viofacea Chile FATOL420 M pubescens Russia FATOL450 M. pubescens Russia LF35 M. pubescens Greece LF100 M. pubescens Spain i LF162 M. pubescens Italy LF166 M. pubescens Germany LF165 M. pubescens Germany LF618 M. pubescens Italy LF184 M. pubescens Germany LF680 M. pubescens Georgia LF706 M. pubescens Russia-Caucasus LF53 M. pubescens Slovakia LF168 M. pubescens Germany LF682 M. pubescens Georgia LF625 M. pubescens Italy LF160 M. pubescens China Xinjiang LF619 M. pubescens Italy LF629 M . pubescens Italy LF622 M. pubescens Austria LF67 M. pubescens China Sichuan LF69 M pubescens Canada BC LF624 M. pubescens Italy 1 j LF55 M. pubescens USA Alaska ■4 LF99 M. pubescens USA Alaska I LF54 M. pubescens USA Alaska - ' LF56 M. pubescens USA Alaska LF167 M. pubescens Germany ■ r LF183 M. pubescens Germany LF620 M. pubescens Austria HLF19 LF20 M. pubescens Nepal HLF19 LF21 M. M. M. pubescens LF21 LF20 M. pubescens Nepal pubescens Nepal Nepal - LF707 M. pubescens Russia Sakhalin 1 LF101 M. cf. pubescens Argentina - ' LF164 M. cf. pubescens Chile LF163 M. frontipilis Chile mm BH1Hi LF496 M. frontipilis Chile LF501 M. frontipilis Chile m LF503 M. frontipilis Chile LF506 M. frontipilis Chile LF490 M. frontipilis Chile ^ - mm j LF498 M. ciliata Chile LF194 M. ciiiata Marion Island j " j ^ ' ' - 0.005 substitutions/site Figure 1. Phylogram derived from a maximum likelihood analysis of the combined dataset for Metzgeria samples, showing support from analyses. The dataset includes sequences from trnL, trnG, psbT , and rpbl plastid and nuclear DNA regions. Thickened branches are supported by > 95% Bayesian posterior probability and > 75% maximum likelihood bootstrap. This content downloaded from 107.0.125.4 on Wed, 10 Aug 2016 20:29:00 UTC All use subject to http://about.jstor.org/terms Fuselier et al.: Phylogeography of Apometzgeria 97 Accessions of M. pubescens from around the comprising plants from South America and the Northern Hemisphere are closely related and other, plants from throughout the Holarctic geographic patterns are poorly resolved. Groups of distribution of M. pubescens. Plants from Nepal, and plants from Alaska and Nepal are, however, each to some degree plants from Alaska, are genetically consistently resolved and strongly supported by differentiated from other populations of M. pubescens single genes and the combined analysis (Fig. 1). The in the Northern Hemisphere. Additional, more Alaskan plants differ from the larger group of M. highly variable markers are needed to further resolve pubescens specimens by seven substitutions, and the genetic relationships within this clade and make Nepal group also differs from other Northern inferences about gene flow among populations. Hemisphere accessions by seven substitutions. Plants Whereas Metzgeria frontipilis occurs in a clade from Nepal are resolved as sister to European plants distinct from almost all accessions of M. pubescens , but the relationship is not supported. two M. pubescens from South America are more Phylogeographic relationships of the Alaskan plants closely related to M. frontipilis than other M. are similarly unsupported. The remaining M. pubescens. Indeed, these M. pubescens are more pubescens plants differ from one another by between closely related to species of Metzgeria from South one and 1 1 nucleotide substitutions and include America and Africa than to M. pubescens from the populations from throughout the Holarctic. Northern Hemisphere. Before the re-discovery of a Relationships among plants in the M. pubescens single M. pubescens specimen from Chile, the species clade were examined further using haplotype networks.was considered Holarctic in distribution (Engel & Fourteen haplotypes were identified among the 33 Kuwahara 1973). Our results indicate that M. plants in the M. pubescens clade; a specimen from pubescens in South America forms a divergent lineage Austria was the most likely outgroup taxon (Fig. 2). that shares a closer phylogenetic history with M. Multilocus haplotypes were shared by the following frontipilis. As such, M. pubescens should be pairs or groups specimens that differed only by missing considered a Holarctic species. or ambiguous nucleotides: Russia and Italy; China, Italy and Canada; three specimens from Italy, and Even when we consider Metzgeria pubescens to be Holarctic in distribution, our results stand in collections from Russia, Greece, Georgia, Germany, contrast to expectations based on previous studies of Slovakia, and Spain. Identical plants from Nepal M. furcata and M. conjugata (Fuselier et al. 2009). formed a group differing by seven mutational steps These species exhibit range disjunctions between from the outgroup (Fig. 2). Otherwise, haplotypes Europe and North America and a clear genetic from the same region were not closely linked. For divergence that is correlated with geographic example, plants of M. pubescens from Italy had theirprovenance rather than morphological similarity closest connections to plants from China and Canada.(Fuselier et al. 2009). Metzgeria furcata is dioicous and plants in North America rarely if ever produce Discussion sexual propagules. However, M. conjugata is Apometzgeria is not a monophyletic group sister monoicous and commonly produces spores, making to the genus Metzgeria as predicted by Kuwahara it more probable that this species would disperse over (1973). Rather, the two species in our analysis that long distances (Van Zanten & Pocs 1981). Despite have been historically assigned to Apometzgeria are the differences in mating systems and dispersal phylogenetically nested within the genus Metzgeria , strategies, both species harbor cryptic lineages in two different clades. This is in agreement with (Fuselier et al. 2009). This pattern is not unusual for Forrest et al. (2006) and supports the rejection bryophytes; of similar cryptic lineages in Apometzgeria as a separate genus of Metzgeriaceae intercontinentally distributed species have been (Crandall-Stotler et al. 2009) or even of subgeneric identified in a range of taxa (e.g., Feldberg et al. 2004; et al. 2009a; Hentschel et al. 2007; Shaw rank within Metzgeria. Metzgeria frontipilis andHeinrichs M. pubescens together do not form a monophyletic 2001; Wachowiak et al. 2007). We expected a similar group within Metzgeria , but occur in two clades, one pattern within the distribution of M. pubescens. This content downloaded from 107.0.125.4 on Wed, 10 Aug 2016 20:29:00 UTC All use subject to http://about.jstor.org/terms 98 The Bryologist 114(l): 2011 Nepal Kaski CLF19, Nepal LF20, Kaski LF2T^' «> CLF54. USA-Alaska LF56TLF9i^N USA-Alaska <' 01F55 USA-Alaska < o <» o » C 4 <> LF707 Russia SakhaEn < > LF620 Austria .. /^FAT0L420( '/ 3 ' VLF629 '/ CNna, Italy, Canada-B^ LF624^^v cr~Lf625lSC~r> <^-f I V LF706 v^Gree Figure 2. Multil Failure to uncover genetic among Instead, adivergence dist populations the of intercontinentally distributed Ho across bryophytes may be related to the genetic markers supported by used. Allozymes, for example, do not always have Presumably, t power sufficient to elucidate divergencerat from resolving high following recent range expansion, compared to more Holarctic dist be hypervariable microsatellite markers. We used more impo sequences from both plastid and nuclear loci, and distributions & although we did not have data for all regions for Vanderpoor Heinrichs et every specimen, the resolving power of these same markers was sufficient to uncover genetic structure in long-distance of other taxa of Metzgeria (Fuselier et al. 2009), and to genetic div reveal genetic divergence between Holarctic and distributed m South American clades of plants formerly assigned to distance dispe Apometzgeria in this study. furcata (Fusel (L.) In summary, our results do not support Pfeiff., Apometzgeria as a distinct genus but rather indicate pubescens is our that species ascribed to that genus are analyses phylogenetically nested within Metzgeriain as reported pubescens collected in a conservation area known to harbor a by Forrest et al. (2006). We provide evidence of a high diversity of lichens (Baniya et al. 2001) at divergent lineage of Metzgeria pubescens in South America that is more closely related to South elevations up to 3300 m. The plants from Alaska were collected primarily on coastal islands. Overall, M. American plants belonging to other taxonomic pubescens displays little phylogeographic structure species than to M. pubescens in the Northern Hemisphere. No nomenclatural changes are across a huge, circum-Northern Hemisphere range. This content downloaded from 107.0.125.4 on Wed, 10 Aug 2016 20:29:00 UTC All use subject to http://about.jstor.org/terms (H m r N Fuselier et al.: Phylogeography of Apometzgeria 99 necessary because all of the species sometimes Furuki, T. 8c P. Dalton. 2008. Vandiemenia ratkowskiana classified in Apometzgeria have previously been Hewson (Marchantiophyta): a revised description and included in Metzgeria. reassessment of its taxonomic status. Journal of Bryology 30: 48-54. 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Kuwahara, Y. 1966. The family Metzgeriaceae in north and (Herbertaceae, Jungermanniopside): range and morphology south east Asia, Pacific Oceania, Australia and New of Herbertus sendtneri inferred from nrlTS. Plant Systematics and Evolution 249: 247-261. Zealand. Revue Bryologique et Lichenologique 34: 191-239. Forrest, L. E., C. Davis, D. Long, B. Crandall-Stotler, A. Clark 8c M. Hollingsworth. 2006. Unraveling the evolutionary Bryologique et Lichenologique 44: 351-410. history of the liverworts (Marchantiophyta): multiple taxa, genomes and analyses. The Bryologist 109: 303-334. Bryophytorum Bibliotheca 28: 1-254. This content downloaded from 107.0.125.4 on Wed, 10 Aug 2016 20:29:00 UTC All use subject to http://about.jstor.org/terms 100 The Bryologist H4(l)' 2011 Miller, M. A., M. T. Holder, R. Vos, P. E. Midford, T. Appendix 1. Accession information and GenBank Liebowitz, L. Chan, P. Hoover & T. Warnow. 2009. The accession numbers for nuclear and chloroplast CIPRES Portals. CIPRES. 2009-08-04. URL: http://www. phylo.org/sub_sections/portal. Accessed: 2009-08-04. sequence data corresponding to specimens used in this study. FIB = Fraunhofer Institut fur Bauphysik (Archived by WebCite(r) at http://www.webcitation.org/ (Stuttgart, Germany). Specimens are listed as: 5imQlJeQa) Milne, R. 2006. Northern hemisphere plant disjunctions: a window on tertiary land bridges and climate change? Annals of Botany 98: 465-472. Miiller, J., K. F. Miiller, C. Neinhuis 8c D. Quandt. 2007. PhyDE - Phylogenetic Data Editor. Accessed October 2009 at species, DNA no., Herbarium, Collector and no. or date, Country, RPB2/ psbT/ trnL/ trnG. Metzgeria cf. pubescens : LF101, ny, Drehwald 22-Mar-97 , Argentina, HQ342541/ HQ342498/ HQ342632, Metzgeria cf. pubescens: LF164, http://www.phyde.de. Nylander, J. 2004. MrModeltest, version 2.3. Available from the author, website: http://www.ebc.uu.se/systzoo/staff/ nylander.html Pacak, A. & Z. Szweykowska-Kulinska. 2000. Molecular data concerning alloploid character and the origin of chloroplast and mitochondrial genomes in the liverwort species Pellia borealis. Journal of Plant Biotechnology 2: 101-108. Schuster, R. M. 1992. The Hepaticae and Anthrocerotae of North America. Field Museum of Natural History, Chicago, jena, Hyvonen et al. 5837 , Chile, -/HQ342506/ HQ342640/HQ342592; Af. frontipilis: LF490, f, Engel 25828 , Chile, HQ342557/HQ3425 1 7/HQ342654/HQ342606; LF496, f, Engel 25835 , Chile, HQ342558/ HQ3425 1 8/HQ342655/HQ342607; LF501, f, Engel 26418 , Chile, -/HQ342520/HQ342657/ HQ342608; LF503, f, Engel 25818 , Chile, HQ342560/ HQ342521/HQ342658/HQ342609; Illinois. Shaw, A. J. 2001. Biogeographic patterns and cryptic speciation in bryophytes. Journal of Biogeography 28: 253-61. LF506, f, Engel 25338 , Chile, HQ342561/ HQ342522/HQ342659/HQ342610; LF163, jena, Hyvonen 5260, t Chile, HQ342547/HQ342505/ Mediterranean disjunct mosses: morphological and HQ342639/HQ34259 1 . molecular patterns. American Journal of Botany 90: M. pubescens: FATOL420, duke, Bakalin 10-Jul-99, 540-550. Russia. , -/HQ342495/HQ342629/HQ342583; FATOL450, duke, Konstantinova & Savchenko (Sphagnum) evolution: who says bryophytes have no roots? 7-Sep-05, Russia, HQ342539/HQ342496/ American Journal of Botany 90: 1777-1787. HQ342630/HQ342584; LF100, Heras & So, M. L. 2003. The genus Metzgeria (Hepaticae) in ny, Asia. Journal of the Hattori Botanical Infante Laboratory 94:HQ342540/HQ342497/ 159-77. 19-May-90y Spain, Swofford, D. L. 2002. PAUP*. Phylogenetic Analysis Using HQ34263 1/HQ342585; LF160, jena, Whittemore Parsimony (*and Other Methods). Version 4. Sinauer 4853, , China, HQ342546/ HQ342503/HQ342637/ Associates, Sunderland, Massachusetts. HQ342589; LF162, jena, Duell 9534/1 , Italy, Taberlet, P., L. Gielly, G. Pautou 8c J. Bouvet. 1991. Universal -/HQ342504/HQ342638/HQ342590; LF165, jena, primers for amplification of three non-coding regions of Schroder 7623/4 , Germany, HQ342548/ chloroplast DNA. Plant Molecular Biology 17: 1105-1109. HQ342507/HQ342641/ HQ342593; LF166, jena, Van Zanten, B. O. 8c T. Pocs. 1981. Distribution and dispersal Schroder 7721/3 , Germany, HQ342549/ of bryophytes. Advances in Bryology 1: 479-562. HQ342508/HQ342642/HQ342594; Wachowiak, W., A. B^cziewicz, E. Chudzinska 8c K. LF167, jena, Buczkowska. 2007. Cryptic speciation in4125/2 liverworts-a case Meinunger , Germany, HQ342550/ study in the Aneura pinguis complex. Botanical Journal HQ342509/HQ342643/HQ342595; LF168,of jena, the Linnean Society 155: 273-282.Meinunger 4725/2, Germany, - /-/HQ342644/ Zwickl, D. J. 2006. Genetic algorithm approaches for the HQ342596; LF183, jena, Schroder 8231/1 , phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Ph.D. dissertation, The University of Texas at Austin. GARLI Germany, HQ342552/HQ34251 1/HQ342646/ HQ342598; LF184, jena, Schroder 21345, version 0.96 available online at http://www.nescent.org/ Germany, HQ342553/HQ3425 12/HQ342647/ informatics/ HQ342599; LF19, vt, Allard 1719 , Nepal, -/HQ3425 1 3/HQ342648/HQ342600; LF20, vt, ms received March 17, 2010; accepted October 27, 2010. Allard 1659 ; Nepal, -/HQ342514/HQ342650/ This content downloaded from 107.0.125.4 on Wed, 10 Aug 2016 20:29:00 UTC All use subject to http://about.jstor.org/terms Fuselier et al.: Phylogeography of Apometzgeria 101 HQ342602; LF21, vt, Allard & Neupane 1683, M. ciliata: LF194, jena, Gremmen, 98-26, South Nepal, HQ342554, -/HQ342651/HQ342603; Africa, -, -/HQ342649/HQ342601; FATOL409, LF35, duke, Sabovljevic 4067, Greece, HQ342555/ duke, Hartmann& Riet, 04-036, French Guiana, HQ3425 1 5/HQ342652/HQ342604; LF53, duke, HQ342537/HQ342493/HQ342627/HQ34258 1 ; Buryova 8852, Slovakia, HQ342562, -/HQ342660/ LF498, f, Engel, 26263, Chile, -/HQ342519 / HQ34261 1; LF54, duke, Schofield & Talbot 112483, USA Alaska, HQ342563/-/HQ342661/ HQ342656, M. claviflora : FATOL369, duke, Pocs, 9726/BJ, Venezuela, -/HQ342490/HQ342624/HQ342578; HQ342612; LF55, duke, Schofield 104355, USA Alaska, HQ342564/HQ342523/HQ342662/ M. conjugata: LF628, fib , AB/Hofbauer, 16, HQ342613; LF56, duke, Schofield 106282, USA Austria, GQ336007/GQ335875/GQ336297/ Alaska, HQ342565/ HQ342663/HQ342614; GQ336152; LF618, fib, Hofbauer 18, Italy, HQ342566 / M. dorsipara: FATOL403, duke, Schafer-Verwimp HQ342524, -/HQ342615; LF619, fib, Hofbauer 21, et al, 24385, Ecuador, HQ342535/HQ342491/ Italy, HQ342567/HQ342525/ HQ342664/ HQ342625/HQ342579; HQ342616; LF620, fib, Hofbauer 13, Austria, M. furcata: LF111, ny, Buck, 40350, USA Arkansas, HQ342568/ HQ342526/HQ342665/ -/; LF622, fib, GQ335933/ GQ33579 1 /GQ3362 1 3/GQ336068; Hofbauer 2, Austria, HQ342569, -/HQ342666/ LF98, duke, Gonzalez-Mancebo & Patino, 15239, HQ342617; LF624, fib, Hofbauer 28, Italy, Canary Islands, GQ335932/GQ335790/ HQ342570/HQ342527, -/HQ342618; LF625, fib, GQ3362 12/GQ336067. Hofbauer 3, Italy, HQ342571/HQ342528/ M. leptoneura: LF102, ny , Steere, 27583, Ecuador, HQ342667/HQ3426 19; LF629, fib, Hofbauer 26, -/HQ342499/HQ342633/HQ342586; LF170, Italy, -/HQ342529 / HQ342668/HQ342620; LF67, jena, Sciifer-Verwimp & Verwimp, 13077, duke, Koponen 47052, China, HQ342572, Brazil, HQ342551/HQ342510/HQ342645/ -/HQ342669/HQ34262 1 ; LF680, duke, Zundorf 23390, Georgia, HQ342573/HQ342530/ HQ342597; LF404, duke, Norris, 67047, Papua New Guinea, HQ342556/HQ342516/ HQ342670/ LF682, duke, Zundorf 23902, HQ342653/HQ342605. Georgia, HQ342574, -/HQ342671, LF69, duke, M. myriopoda: LF388, una , Davison, 2846, USA, Schofield 100944, Canada, HQ342575, GQ335982/ GQ335850/GQ336272/GQ336127; -/HQ342672/HQ342622; LF706, goet, Konstantinova & Savchenko 51, Russia, M. rufula: FATOL410, duke, Sipman, 51415, Ecuador, HQ342538/HQ342494/HQ342628/ HQ342576/HQ342531/HQ342673, LF707, HQ342582. goet, Bakalin 77, Russia, -/HQ342532/HQ34267/ M. filicina: FATOL408, duke, Churchill, 23368, -/; LF99, ny , Schofield 106282, USA, HQ342577/ Bolivia, HQ342536/HQ342492/HQ342626/ HQ342533/HQ342675/HQ342623. HQ342580. M. agnewiae : LF103, ny , Steere 27617, Ecuador, HQ342543/HQ342500/HQ342634/HQ342587. M. aurantiaca: LF132, ny , Wasum 28-Oct-88, Brazil, HQ342544/HQ34250 1 /HQ342635/HQ342588; M. violacea: LF134, ny , Buck, 40911, Chile, HQ342545/HQ342502/HQ342636/-/. Pleurozia purpurea: IBC55, duke, Schofield, 102815, USA, -/AY608019/AY608139/AY608187. 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