American Journal of Botany 98(3): 352369. 2011.

BRYOPHYTE DIVERSITY AND EVOLUTION: WINDOWS INTO THE EARLY EVOLUTION OF LAND PLANTS1
A. Jonathan Shaw2, Pter Szvnyi3, and Blanka Shaw
Department of Biology, Duke University, Durham, North Carolina 27708 USA The bryophytes comprise three phyla of plants united by a similar haploid-dominant life cycle and unbranched sporophytes bearing one sporangium: the liverworts (Marchantiophyta), mosses (Bryophyta), and hornworts (Anthocerophyta). Combined, these groups include some 20 000 species. As descendents of embryophytes that diverged before tracheophytes appeared, bryophytes offer unique windows into the early evolution of land plants. We review insights into the evolution of plant life cycles, in particular the elaboration of the sporophyte generation, the major lineages within bryophyte phyla, and reproductive processes that shape patterns of bryophyte evolution. Recent transcriptomic work suggests extensive overlap in gene expression in bryophyte sporophytes vs. gametophytes, but also novel patterns in the sporophyte, supporting Bowers antithetic hypothesis for origin of alternation of generations. Major lineages of liverworts, mosses, and hornworts have been resolved and general patterns of morphological evolution can now be inferred. The life cycles of bryophytes, arguably more similar to those of early embryophytes than are those in any other living plant group, provide unique insights into gametophyte mating patterns, sexual conicts, and the efcacy and effects of spore dispersal during early land plant evolution. Key words: bryophytes; early land plants; gametophyte evolution; gene expression; peristomes; spore dispersal; sporophyte evolution; tree of life.

The early Paleozoic Era was an exciting period in Earths history, marked by the colonization and diversication of terrestrial organisms, including the ancestral lineages of extant embryophytes (Kenrick and Crane, 1997). As photosynthetic organisms adapted to the higher CO2 levels and diminished UV-B screening of emerging terrestrial habitats (Raven, 2000), a vast array of morphological innovations was developed (Renzaglia et al., 2000), new patterns of genome structure and gene expression evolved (Kofuji et al., 2003; Nishiyama et al., 2003; Tanabe et al., 2005), and novel symbiotic relationships were established (Pirozynski and Malloch, 1975). The bryophytes, which are now important components of virtually all terrestrial ecosystems, were among the earliest of land plants. Traditionally, bryophytes include the mosses, liverworts, and hornworts. Together, these groups comprise some 15 000 20 000 species and as such, are, combined, more diverse than the nonowering vascular plants. The three bryophyte groups share a similar life cycle in which the gametophyte is perennial and dominant in terms of both size and longevity and the sporophyte is unbranched, monosporangiate, and completes its entire development attached to the maternal gametophyte. The sporophyte generation begins as a fertilized egg and eventually produces spores via meiosis in a terminal sporangium, after which, especially in the mosses and liverworts, it ceases
1 Manuscript received 22 August 2010; revision accepted 28 December 2010. Acquisition of supporting data for this paper was funded by NSF grants EF-0531730-002 to A.J.S. and DEB-0918998 to A.J.S. and B.S. 2 Author for correspondence (e-mail: [email protected]); Department of Biology, Duke University, Durham, North Carolina, 27708 USA; fax: 01-919-660-7293 3 Present address: Faculty of Biology, University of Freiburg, Hauptstrasse 1, D-79104 Freiburg, Germany

doi:10.3732/ajb.1000316

to be photosynthetic, dries, and senesces. The sporophytes of many moss species mature over somewhat more than a year but do not continue to grow after spore production and are for the most part essentially annual. Liverwort sporophytes are especially short-lived and generally persist for weeks to months (from fertilization to senescence). The sporophytes of hornworts are potentially indeterminate in life span, but in nature they also appear to rarely persist for more than a year (Bisang, 2003). Although some bryophytes produce spores that develop into genetically determined male or female gametophytes and are sometimes described as heterosporous, they are not heterosporous in the sense of many vascular plants because the male and female spores are produced by the same sporangium rather than in different micro- and megasporangia. Bryophyte species that form male and female spores that are differentiated in size are better described as anisosporous (Mogensen, 1981), but in most species with unisexual gametophytes the spores are indistinguishable. Bryophyte diversity and evolution has been reviewed in two recent books, an edited volume by Gofnet and Shaw (2009) and a text by Vanderpoorten and Gofnet (2009). In this brief review, we address (1) phylogenetic relationships among the three bryophyte phyla and inferences about the evolution of plant life cycles, (2) relationships among major clades within the liverworts, mosses, and hornworts in relation to morphological diversity, and (3) reproductive processes that have signicant impacts on bryophyte diversication. In the last context, we focus on reproductive biology and dispersal because these processes determine the genetic structure of species, which in turn facilitate and modulate speciation. Living bryophytes, like early embryophytes, persist (and disperse) as long-lived gametophytes and rely on spores rather than seeds for reproduction. For these reasons, evolutionary processes in extant bryophytes provide a window into similar processes among colonizing land plants hundreds of millions of years ago.

American Journal of Botany 98(3): 352369, 2011; http://www.amjbot.org/ 2011 Botanical Society of America

352

March 2011]

Shaw et al.Bryophyte diversity and evolution

353

RELATIONSHIPS AMONG BRYOPHYTE GROUPS AND THE EVOLUTION OF EMBRYOPHYTE LIFE CYCLES Phylogenetic relationships among early embryophyte lineages It has been recognized for over a century (e.g., Pringsheim, 1876) that the green algae (Chlorophyta plus streptophyte algae) share signicant structural and biochemical features with land plants (bryophytes and tracheophytes; embryophytes). The green algae, however, are heterogeneous and include taxa in which one or the other or both generations are multicellular, so inferences about the origin of the embryophyte life cycle depend on which group of green algae is sister to the embryophytes (Haig, 2008; Niklas and Kutschera, 2009). Evidence from ultrastructural, biochemical, and molecular data supports the view that the charophycean green algae (including the Charales, Coleochaetales, and other groups) are closely related to the embryophytes, and so their life cycles are informative about the ancestral condition in embryophytes. The charophycean algae themselves include early-diverging unicellular types such as Mesostigma viride Lauterborn. Phylogenetic evidence supports close relationships between embryophytes and several charophycean groups, the Zygnematales (Turmel et al., 2006), Coleochaetales (Graham et al., 1991), and Charales (Karol et al., 2001; Qiu, 2008; Qiu et al., 2006). The modern green algal group most closely related to embryophytes is unclear at the present time (Becker and Marin, 2009). While it is clear that in general multicellularity has evolved multiple times (i.e., among protistan groups), all candidate sister groups to the embryophytes are characterized by a haplobiontic life cycle in which the gametophyte is multicellular and dominant and the sporophyte generation is limited to a unicellular zygote. Thus, the multicellular sporophyte characteristic of all embryophytes appears to have evolved by interpolation of mitotic cell divisions prior to meiosis. This scenario in which the sporophytes of land plants represent an evolutionary innovation corresponds to the so-called antithetic theory concerning the evolution of the embryophyte alternation of generations (Bower, 1890). Nevertheless, signicant questions remain about the nature of the sporophyte in the early ancestors of extant embryophytes (see below). Multiple lines of evidence suggest that the three bryophyte clades (liverworts: Marchantiophyta; mosses: Bryophyta; and hornworts: Anthocerophyta) form a paraphyletic grade basal to the tracheophytes, although some data, including both morphological (Garbary et al., 1993) and molecular (Nishiyama et al., 2004), suggest that either the mosses and liverworts form a monophyletic group, or all three groups form a single clade. Qiu et al. (2006) and Qiu (2008) have shown that the distribution of mitochondrial group II introns across groups, in addition to considerable sequence data, strongly supports the paraphyly hypothesis, and that the branching order at the base of the embryophyte clade is liverworts, then mosses, then hornworts, and then the tracheophyte crown group. This view serves as a well-supported working hypothesis for early land plant relationships (Fig. 1). Spore and tubular remains with apparent liverwort afnities from the Ordovician Period some 470 million years ago (Ma) suggest that at least some of the earliest land plants may have had a heteromorphic haploid-dominant alternation of generations like modern liverworts (reviewed by Gensel, 2008; Niklas and Kutschera, 2009). Spore diads that appear to be intermediate between those of extant Coleochaete species and embryophytes are known from the Cambrian Period (Taylor and Strother, 2009). Later, morphologically similar axial gametophytes

and sporophytes from Devonian strata of the Rhynie Chert (ca. 410 Ma) suggest that there was a period in early land plant history when sporophyte and gametophyte generations were isomorphic (Kenrick and Crane, 1997; Taylor et al., 2005). The fossil evidence is thus consistent with a scenario in which plant life cycles may have followed a trajectory from haploid- to diploid-dominant via an isomorphic transitional stage. But what was the nature of the sporophyte generation in the common ancestors of liverworts, mosses, and hornworts? We still do not know how complex the sporophyte was in the common ancestor of extant liverworts, mosses, or hornworts, nor of subsequent ancestors prior to the origin of tracheophytes (Fig. 1). Stated differently, questions remain about the homology of sporophytic structures in these groups. It is possible, for example, that the common ancestor of all embryophytes had a very simple, even if multicellular, sporophyte and that the sporophytes of living bryophyte phyla, with more or less differentiated vegetative and sporangial tissues, represent independent evolutionary innovations. Conversely, there is paleobotanical evidence that the common ancestor of tracheophytes was characterized by equally complex gametophyte and sporophyte generations (i.e., an isomorphic alternation of generations), and it could be that complex sporophytes evolved early in embryophyte evolution with parallel reduction in liverworts, mosses, and hornworts (Fig. 1). The history of plant life cycle evolution probably lies somewhere between these extremes wherein sporophytes of the bryophyte phyla represent independent innovations from ancestors of intermediate complexity, and the degree of homology depends on the extent to which sporophyte elaboration used a common genomic toolkit, vs. truly independent evolution from scratch. The sporophytes of mosses, liverworts, and hornworts are very different, despite the fact that in all three groups they are unbranched and monosporangiate. Those of liverworts, for example, lack stomata and have no specialized photosynthetic tissues (although epidermal cells contain chloroplasts at early stages of development). The setae of liverworts are very simple in structure and highly ephemeral (usually lasting only days). The sporophytes of mosses typically persist for longer periods, have greater anatomical complexity, and the sporangium usually has specialized photosynthetic tissues and stomata. The linear sporophytes of hornworts lack differentiated setae but have photosynthetic tissues and stomata. Sporangial dehiscence also differs among the three groups, and the sporophytes develop in radically different ways; by diffuse cell divisions in liverworts, apical and intercalary growth in mosses, and a basal intercalary meristem in hornworts. Water-conducting cells occur in the sporophyte of mosses but not liverworts (Ligrone et al., 2000). Thus, despite (presumably plesiotypic) similarities, it is conceivable that the multicellular sporophytes of liverworts, mosses, and hornworts evolved largely in parallel from ancestors with less complex sporophytes. Gene expression and the evolution of plant life cycles The most intriguing aspect of the alternating sporophyte and gametophyte generations of land plants is their extreme morphological and functional divergence despite having shared genomes. Although the two generations differ in their ploidal level, this difference alone does not lead to the development of different structures. That other factors are involved is well shown by early evidence of apogamy and apospory (Farlow, 1874; Pringsheim, 1876) in which abrupt switches between generation-typical morphologies and function are not associated with ploidal changes brought about by syngamy or meiosis.

354

American Journal of Botany

[Vol. 98

Fig. 1. Working hypotheses for relationships among major clades of land plants. Alternative scenarios for the evolution of land plant sporophytes are shown on the gure. A at each node represents a relatively undifferentiated but multicellular sporophyte; B shows an unbranched, monosporangiate sporophyte; C shows a dichotomously branched sporophyte. The key (upper left) suggests three general scenarios that could have occurred; for example, ancestral states for the three nodes (a, b, c) could be A-A-A, which implies independent evolution of complex sporophytes from ancestors with little differentiated but multicellular sporophytes. Other possible scenarios, including various reversals, are of course also possible.

Phenotypic and functional divergences between the two generations clearly arise by differential usage of the same genetic material. Accumulating evidence suggests that morphological and functional transitions between sporophyte and gametophyte are achieved by drastic reprogramming of gene expression patterns through generation-specic transcription factors (reviewed by Singer and Ashton, 2007; Langdale, 2008; Dolan, 2009). The evolutionary origin of diplobiontic life cycles from a purely haplobiontic life cycle required the evolution of regulatory mechanisms governing developmental and physiological processes of the new generation, the multicellular sporophyte. Similarly, the transition from a haploid- to diploid-dominant alternation of

generations must have been accompanied by radical changes in regulatory mechanisms enabling large-scale changes in function and morphology of both generations. Genomic mechanisms underlying sporophyte development could have evolved de novo or by the partial or full transfer of preformed gametophytic programs to the sporophyte generation (Nishiyama et al., 2003; Dolan, 2009; Niklas and Kutschera, 2009). Studies investigating the effect of major regulatory gene homologs of Arabidopsis thaliana in the model moss Physcomitrella patens are consistent with the transfer of gametophytic developmental programs to the sporophyte generation. An impressive example is provided by ROOT HAIR DEFECTIVE 6 (RHD6)like transcription factors regulating root hair development

March 2011]

Shaw et al.Bryophyte diversity and evolution

355

in Arabidopsis thaliana and rhizoid development in the moss Physcomitrella patens (Menand et al., 2007). Here a complete regulatory toolkit appears to have been recruited from the gametophyte for similar functions in sporophytes. Genes and genetic networks involved in the development of reproductive structures across land plants appear to have followed a similar evolutionary path. MADS box genes are preferentially expressed in gametangia and in the basal part of the moss sporophyte. Furthermore, their defect leads to abnormalities related to the development of reproductive structures in mosses (Quodt et al., 2007; Zobell et al., 2010; reviewed in Singer and Ashton, 2009). In Arabidopsis, MADS box genes have similar functions and expression patterns as key regulators of the reproductive phase, with expression restricted to the formation of reproductive structures (Coen and Meyerowitz, 1991). Similar expression patterns and functions suggest that MADS box genes are conserved across land plants and that gametophyte developmental programs were recruited to the sporophyte to perform similar functions. Regulatory genes and networks underlying critical adaptations to the terrestrial environment may have rst appeared in the dominant gametophyte generation and later transferred as the sporophyte was elaborated. Comparative analyses of desiccation and salt tolerance across land plants have revealed conserved regulatory networks acting in the moss gametophyte and angiosperm sporophyte, providing further evidence for the genomic transfer of gametophytic programs to the sporophyte (Khandelwal et al., 2010; Richardt et al., 2010). Comparative analyses of regulatory genes expressed mainly in the sporophyte generation of Arabidopsis thaliana and Physcomitrella patens shed light on regulatory mechanisms that likely evolved de novo during the course of land plant evolution. Class I KNOX genes are expressed only in the sporophyte generation of mosses, ferns, and angiosperms, and in the latter two groups, they are important in the development and maintenance of the shoot apical meristem (Hay and Tsiantis, 2009). In Physcomitrella patens, they are expressed in the developing sporophyte, and their defect leads to the abortion of the sporophyte, but they cause no detectable abnormalities in gametophytes (Sano et al., 2005; Singer and Ashton, 2007). Another example is provided by LEAFY/FLORICAULA genes that have an important role in the formation of the oral meristem in angiosperms (Ng and Yanofsky, 2000). LEAFY homologs in the moss Physcomitrella patens are key regulators of the sporophytic stage by regulating the rst division of the zygote. Although these genes are expressed in both generations, they have no detectable effect on the development of gametophytes in Physcomitrella patens (Tanahashi et al., 2005). Auxin-regulated axis development also appears to have evolved de novo in connection with the origin of the sporophyte generation. Polar auxin transport is only present in the sporophytes of bryophytes and angiosperms (Poli et al., 2003; Fujita et al., 2008; Fujita and Hasebe, 2009). Finally, genes in the Prc2 complex (FIE, CLF) of Arabidopsis thaliana and their moss homologs prevent parthenogenetic formation of sporophytic tissues, and this role appears to be conserved across land plants (Mosquna et al.., 2009; Okano et al., 2009). Although studies on the evolution of developmental programs across basal and derived groups of land plants has signicantly increased during the last 10 years, available information is still fragmentary and is focused on relatively few developmental genes with major effects in angiosperms. The proportions of regulatory genes and gene networks acquired by sporophytes via functional transfer from gametophytes, vs. de novo evolution in the embryophyte sporophyte, are poorly known.

Monitoring transcriptional changes associated with the gametophytesporophyte transition could help to understand how generation-specic morphologies and functions are achieved by the reorganization of gene regulatory networks. Moreover, comparative analysis of generation-biased gene expression across land plants can provide critical insights into the origin of embryophytes and the evolution of plant life cycles on a genome-wide scale. Toward this end, we are currently investigating genome-wide, generation-biased gene expression patterns in Funaria hygrometrica (a close relative of the model, Physcomitrella patens) using next-generation sequencing of mRNA and conducting comparative analysis of generationbiased gene expression across land plants (Szvnyi et al., 2010). In a comparison of expression proles from the gametophytes and attached isogenic sporophytes derived from intragametophytic selng, genes in Funaria fell into three natural groups. (1) Genes with generation-specic expression; (2) those with generation-biased expression; and (3) those with similar expression in both generations. From the 558 differentially expressed genes, similar numbers were differentially expressed toward the two generations; there were 277 gametophyte- and 281 sporophyte-characteristic transcripts (both generation-specic [group 1] and generation-biased [group 2] genes). Overall, ca. 70% and 68% of the generation-characteristic genes fell into the biased category. Comparative analyses of generation-biased gene expression in A. thaliana and F. hygrometrica shed light on crucial questions related to the origin and evolution of land plants and are briey summarized here (Szvnyi et al., 2010). Our ndings show that a large proportion of genes is expressed in both the gametophyte and sporophyte generation in Funaria. In particular, we found that the proportion of transcripts with generationbiased gene expression (2.5% gametophyte, 2.5%, sporophyte) is lower than in Arabidopsis. Furthermore, the similar proportion of sporophyte- and gametophyte-biased genes suggests less gene expression specialization between generations in the bryophyte system compared to angiosperms, where the distribution of generation-specic gene products is unequal (~5% and ~25% in gametophytes and sporophytes, respectively). The extensive overlap and weak specialization in gene expression between the two generations is in agreement with the origin of alternation of generations from an algal ancestor with a purely haplobiontic life cycle. Our data suggest that extensive sharing in gene expression between generations may have been the rule rather than the exception in earliest land plants. We compared expression patterns between Funaria gametophytes and Arabidopsis sporophytes, as well as between sporophytes in the two model systems. Our analyses show that there is limited conservation of generation-biased gene expression between the moss and angiosperm, suggesting extensive intergenerational transfer of genetic networks. Furthermore, extensive overlap in gene expression between bryophyte gametophyte and angiosperm sporophyte generations implies that their morphological and functional similarity is not supercial. It relies on the shared usage of a common set of orthologous genes, indicating that multiple gene networks of the sporophyte generation may have been acquired from the gametophyte by intergenerational transfer. We found poor gene expression conservation between the sporophyte generations of Arabidopsis and Funaria, suggesting that angiosperm and bryophyte sporophytes diverged in an early stage of sporophyte evolution, with subsequent parallel evolution of many important gene networks characterizing the

356

American Journal of Botany

[Vol. 98

sporophytes of extant groups. Nevertheless, the core set of sporophyte-expressed transcripts mainly consists of genes critical for terrestrial life (enhanced osmotic regulation, stress, desiccation and UV tolerance, transporters, and intercellular communication via hormones). Therefore, biological processes underlying molecular adaptation to terrestrial life may have already been used by early sporophytes. These adaptations may have contributed to the successful evolutionary diversication of the sporophytic generation in the terrestrial environment. Our data do show that a signicant proportion of preferentially sporophyte-expressed transcription factors in the model moss have orthologs in A. thaliana known to function in the shoot apical meristem and in development of reproductive structures. This similarity in control mechanisms suggests that in spite of considerable morphological and developmental divergence, similar basic regulatory networks are likely to be involved in growth and reproductive tissue development in the moss and angiosperm sporophyte generation. Moreover, the presence of orthologous transcription factors with putatively shared functions in the developmental processes of both reproductive and vegetative sporophytic tissues/organs implies that both domains may have already been present in the common ancestors sporophyte. Overall, our data suggests that the common ancestor may have possessed a morphologically simple sporophyte nevertheless adapted to terrestrial life and possibly with differentiated vegetative and reproductive tissues (possibly corresponding roughly to the A-A-A sequence of ancestral sporophytes in Fig. 1). PHYLOGENY AND DIVERSITY OF LIVERWORTS, MOSSES, AND HORNWORTS Huge advances have been made during the last 10 years in understanding phylogenetic relationships within the liverwort, moss, and hornwort clades. An exhaustive review of such results is beyond the scope of this essay, but we provide an overview of broad patterns in the context of understanding bryophyte diversity. Liverwort phylogeny and evolution (Marchantiophyta) Phylogenetic studies of liverworts have been progressing at a rapid rate in recent years, in part because of U. S. National Science Foundation support of the Assembling the Tree of Life program (http://www.nsf.gov/funding/pgm_summ.jsp?pims_ id=5129). Phylogenetic results were recently summarized by Crandall-Stotler et al. (2009), along with an updated classication for the phylum. The liverworts have traditionally been divided according to gametophyte growth form: complex thalloids wherein the thallus typically has well-differentiated photosynthetic and storage tissues, with dorsal pores bounded by specialized cells (not stomata); simple thalloids that lack signicant tissue differentiation; and the leafy liverworts, typically with two rows of lateral leaves and a row of ventral amphigastria (often lacking). Several smaller groups (e.g., Haplomitrium, Blasia) fall outside this simple classication of gametophyte body architecture and have been phylogenetically enigmatic. Phylogenetic analyses based on nucleotide sequences have generally supported the major groups, with some renements and surprises. The Haplomitriopsida (three genera) are consistently resolved as sister to the rest of liverworts and include both leafy (Haplomitrium) and more or less thalloid forms (Treubia and Apotreubia)

(Fig. 2). The group is relatively small, with a total of ca. 18 species (Crandall-Stotler et al., 2009). Interestingly, the seven species of Haplomitrium are highly divergent at the molecular level, whereas Treubia and Apotreubia are very uniform between species. Because this group contains both leafy and thallose forms, it is difcult to reconstruct the ancestral state of gametophyte growth form in liverworts from phylogenetic topology alone. Within the sister group to the Haplomitriopsida (i.e., all other liverworts), the complex thalloids are sister to the simple thalloids plus the leaf clades. The genera Blasia and Cavicularia have been controversial because they share gametophyte anatomy, rhizoid structure, and sporophyte anatomy with the simple thalloid groups, but monoplastidic meiosis, gametophyte apical cell morphology, and spermatozoid structure with the complex thalloids (Renzaglia, 1982; Renzaglia and Duckett, 1987; Renzaglia et al., 1994). Molecular phylogenetic analyses place Blasia within the complex thalloid clade, sister to mainstream complex thalloids (Fig. 2). The more or less simple thalloid Sphaerocarpales clade (not explicitly shown in Fig. 2) is nested within the complex thalloid clade. It thus appears that anatomically complex thalli might be derived within the complex thalloid clade (based on the simple structure of Blasia and its sister group relationship to the complex thalloids). Subsequent reduction is a theme within the more derived complex thalloid groups (Crandall-Stotler et al., 2009), and the possibility that Blasia is simplied from a common complex thalloid ancestor for all Marchantiopsida also cannot be eliminated. The simple thalloid liverworts form a paraphyletic grade with the Metzgeriidae sister to leafy liverworts (Fig. 2). Included among the Metzgeriidae is the leafy genus Pleurozia (Davis, 2004; He-Nygren et al., 2004). This placement was one of the biggest early surprises from molecular analyses of liverwort phylogeny because Pleurozia has a gametophyte axis with lateral leaves and had always been classied among the leafy liverworts. Recent morphological information about gametophyte symmetry, apical cell structure, and rhizome morphology have revealed features shared with the simple thalloids (Crandall-Stotler et al., 2009). The Pelliidae is sister to the Metzgeriidae plus the leafy clades (Fig. 2). The two clades of simple thalloids differ in origin and position of antheridia, branching, and other subtle features of the gametophytes, but both are morphologically heterogenous. Two major sister clades of leafy liverworts are resolved repeatedly with different data sets (Davis, 2004; Frey and Stech, 2005; Heinrichs et al., 2005, 2007; Forrest et al., 2006; He-Nygrn et al., 2004): the Porellales and Jungermanniales (Heinrichs et al., 2005). The Porellales include ca. 1500 species and are characterized by endosporic germination, exogenous lateral branches, complicate-bilobed succubous lateral leaves with ventral lobules, clustered rhizoids, and a lack of fungal endosymbionts, among other features (reviewed in Pressel et al., 2010). This clade is especially diverse in the tropics, and the tiny plants frequently occur on the leaves of vascular plants; almost all species are epiphytic. The Jungermanniales include ca. 3000 species, one third to one half of all liverwort species, and occupy a broad range of habitats. They can have incubous or succubous lateral leaves (but lack ventral water sacs) although complicate-bilobed leaves occur in a few groups (e.g., Scapaniaceae), ventral or lateral branches, nonclustered rhizoids, and they have associations with endophytic Ascomycota and Basidiomycota (Pressel et al., 2010). In contrast to the Porellales, species with complicate-bilobed leaves have the dorsal rather than ventral

March 2011]

Shaw et al.Bryophyte diversity and evolution

357

Fig. 2. Synoptic phylogeny of major clades in phylum Marchantiophyta (liverworts), summarized from recent molecular analyses, with exemplars of typical morphology in each clade. Not all sister-group relationships shown here are established with certainty but these patterns appear to represent the consensus view. (A) Jungermannia borealis; (B) Scapania nemorea; (C) Trichocolea tomentella; (D) Frullania selwynii; (E) Pleurozia purpurea (photo provided by D. Holyoak); (F) Metzgeria myriopoda; (G) Moerckia otoviana; (H) Conocephalum sp.; (I) Blasia pusilla; (J) Haplomitrium blumei (photo provided by D. Long, Royal Botanic Garden Edinburgh); (K) Apotreubia hortonae. Unless otherwise noted, photos by B. Shaw.

lobe smaller. Within the Jungermanniales, a clade that includes the Lophocoleaceae, Lepidoziaceae, and Plagiochilaceae (and others), the suborder Lophocoleineae (Crandall-Stotler et al., 2009) is sister to the Cephaloziineae plus Jungermaniinae (Fig. 2). Each of these suborders is characterized by a combination of gametophyte developmental and morphological characters, and the grouping of families largely correspond to previous classications (not withstanding various renements beyond the scope of this summary). In addition to the two major clades of leafy liverworts (Porellales and Jungermanniales), a third group, the Ptilidiales, has been consistently resolved in phylogenetic analyses, but its relationships are still unresolved (Fig. 2). Different analyses have resolved this group alternatively as sister either to the Porellales or to all other leafy liverworts. Additional molecular and morphological data are needed to address this critical issue in leafy liverwort phylogeny. Moss phylogeny and evolution (Bryophyta) Since the turn of the 19th century, morphology of the peristome teeth that

surround the mouth of the capsule (sporangium) has been primary in higher-level classications of mosses (Philibert, 18841890; Fleischer, 19041923; Vitt, 1984; Crosby, 1980). In that regard, peristomes are to mosses as owers and fruits are to angiosperms. Before Philiberts work on comparative peristome morphology, gametophyte growth form was emphasized in 19th century taxonomic treatments (e.g., Mller, 18481851). Although basic peristome types do characterize major clades within the mosses, recent phylogenetic analyses at the familial and shallower levels have frequently shown that gametophyte characters appear to track relationships and that sporophytes, including their peristomial details, can be highly homoplasious. Not surprisingly, molecular data suggest that both gametophyte and sporophyte features should be considered and that any a priori weighting of traits from one generation or the other for phylogenetic inferences may be misleading. Mosses (and to a lesser extent, liverworts and hornworts) are unique among land plants in that both the gametophyte and sporophyte generation have sufcient morphological variability and complexity to be phylogenetically informative.

358

American Journal of Botany

[Vol. 98

Most phylogenetic analyses based on sequences from multiple loci suggest that Takakia plus the Sphagnopsida form a clade sister to other mosses. Takakia and the Sphagnopsida share little morphologically, and Gofnet et al. (2001), Cox et al. (2004), and Shaw et al. (2010) suggest that the apparent sister-group relationship between them may reect phylogenetic artifact. Nevertheless, gene sequences from all three genomes repeatedly resolve them as a clade (Newton et al., 2000; Nickrent et al., 2000; Beckert et al., 2001; Cox et al., 2004; Qiu et al., 2006; Qiu, 2008; Shaw et al., 2010). Neither group has a peristome. The Andreaeopsida and Andreaeobryopsida lack peristomes, as do Takakiopsida and Sphagnopsida; the peristomate mosses are demonstrably monophyletic. One of the unexpected results of moss phylogenetic analyses is that the eperistomate species, Oedipodium griftheanum (Oedipodiopsida), is consistently resolved as sister to all the peristomate mosses (Fig. 3) (Newton et al., 2000; Magombo, 2003; Cox et al., 2004). Whether Oedipodium primitively lacks a peristome, or lost it, cannot be determined by phylogenetic topology alone; in the future, genome and transcriptome data might resolve that question. Early-diverging

groups within the Bryopsida, after Oedipodium, are characterized by nematodontous peristomes, which are formed from whole dead (and empty) cells in four or more concentric layers of amphithecium. The amphithecium and inner endothecium are embryonic layers differentiated at an early stage of sporophyte ontogeny, and all peristomes are formed from amphithecial tissue. Highly divergent nematodontous peristomes characterize the Polytrichopsida, Tetraphidopsida, and Buxbaumiiidae (Bryopsida) (Fig. 3). Interestingly, Bell and Hyvnen (2008) resolved the eperistomate genus Alophozia as sister to the rest of the Polytrichaceae and then a clade with the genera Lyellia and Bartramiopsis, also eperistomate, as sister to the remaining taxa in the family. On this basis, they suggested that the eperistomate condition is plesiotypic in the Polytrichaceae and that the polytrichaceous nematodontous peristome may have evolved independently of other moss peristome teeth. The alternative, at least one loss of the peristome and then one regain, is possible though perhaps less likely. The four massive nematodontous peristome teeth of the Tetraphidaceae (Fig. 3) are unique among mosses, although early cell divisions

Fig. 3. Synoptic phylogeny of major clades in phylum Bryophyta (mosses), summarized from recent molecular analyses, with exemplars of typical morphology in each clade. Not all sister-group relationships shown here are established with certainty, but these patterns appear to represent the consensus view. Phylogenetic relationships among the Funariidae, Timmiidae, Dicranidae, and later lineages are still ambiguous, and this topology shows one possible arrangement. (A) Hylocomium splendens; (B) Hookeria lucens; (C) Splachnum luteum; (D) Bartramia halleriana; (E) Ulota coarctata; (F) Schistidium apocarpum; (G) Funaria hygrometrica; (H) Diphyscium foliosum; (I) Buxbaumia aphylla; (J) Tetraphis pellucida; (K) Pogonatum nanum; (L) Oedipodium grifthianum; (M) Andreaea rupestris; (N) Takakia ceratophylla (from Smith and Davison, 1993, with permission); O. Sphagnum papillosum. Photos AC, E, O by B. Shaw; D, FK, M provided by tepn Koval; L provided by David Holyoak.

March 2011]

Shaw et al.Bryophyte diversity and evolution

359

prior to peristome formation bear similarity to those of more derived arthrodontous mosses (Shaw and Anderson, 1988). Volkmar and Knoop (2010) recently resolved the Polytrichaceae and Tetraphidaceae as sister groups within a clade that is in turn sister to remaining mosses (in contrast to the topology shown in Fig. 3). Future work will determine whether this relationship is supported by additional data. The Buxbaumiidae are characterized by yet another distinctive type of peristome which, unfortunately, has not been subjected to developmental studies. It appears to be intermediate between nemtatondous and arthrodontous types. The three genera currently classied in the Diphysciaceae were generally included previously in the Buxbaumiaceae (e.g., Vitt, 1984), but peristome structure and development (Shaw et al., 1987), nucleotide sequences (Cox et al., 2004; Magombo, 2003), and genomic characters (Gofnet et al., 2005) converge on the conclusion that this group belongs to a clade characterized by arthrodontous peristome structure (Fig. 3). Arthrodontous peristomes in general are formed from the innermost three concentric layers of amphithecial cells, from inside outward, the inner, primary, and outer peristomial layers (IPL, PPL, and OPL, respectively). Development of these layers is remarkably regular, with alternating anticlinal and periclinal divisions (Evans and Hooker, 1913; Shaw and Anderson, 1988; Shaw et al., 1987, 1989a, b). The OPL, for example, consistently has 32 cells around the capsule circumference at maturity and the PPL has 16. It is the IPL that varies most, and that variation pertains to both the numbers of cells in the layer and to the positions of anticlinal IPL walls relative to anticlinal walls in the next outer layer, the PPL. Arthrodontous peristomes are generally considered to comprise three basic types: haplolepideous, diplolepideous-opposite, and diplolepideous-alternate. Haplolepideous peristomes are typically formed from periclinal walls in the inner peristomial layer (IPL) and primary peristomial layer (PPL), whereas diplolepideous peristomes form from walls derived from all three layers (IPL, PPL, OPL). Haplolepideous peristomes typically consist of a single ring of 16 teeth, but diplolepideous peristomes often have two rings, the inner endostome (from adjacent periclinal IPL and PPL cell walls) and the outer exostome (from PPL and OPL cell walls). In diplolepideous peristomes, the inner endostomial teeth (often referred to as segments) may be positioned opposite the exostome teeth or alternate with them. Haplolepideous peristomes form from IPL and PPL cell walls and are therefore homologous in position to the endostomes of diplolepideous peristomes. The name haplolepideous comes from the fact that the outer surface of each tooth is formed from a single column of periclinal cell wall remnants whereas diplolepideous exostome teeth have two columns of cell wall plates on the outer surface (Figs. 4, 5). In addition to differences among peristome types in which cell layers contribute to the formation of teeth, they also differ in sequences of cell divisions during capsule development (Shaw and Anderson, 1988; Shaw et al., 1987, 1989a, b), and consequently the arrangement of cells at maturity (although only the walls persist as teeth). The peristomial formula (Edwards, 1984) has been used to describe in shorthand the numbers and arrangement of cells in the IPL, PPL, and OPL, by convention in 1/8 of the capsule circumference (corresponding to two teeth). Haplolepideous peristomes are characterized by a 4 : 2 : 3 formula, diplolepideous-opposite peristomes 4 : 2 : 4a (where the a indicates that all anticlinal walls in the IPL and PPL are aligned), and diplolepideous-alternate peristomes 4 : 2 : 2-14z (the z indicating that no anticlinal IPL and PPL

walls are aligned at maturity). Peristomial formulae can be surmised from mature peristomes from the patterns of wall remnants on the teeth (Shaw and Rohrer, 1984; Figs. 4, 5). It appears that although mosses with haplolepideous peristome teeth form a monophyletic group, they are nested within the diplolepideous clade probably sister to the group with diplolepideous alternative peristomes (Fig. 3). Diplolepideous peristomes therefore dene a paraphyletic group. The genus Timmia has generally been classied among mosses with diplolepideous-alternate peristomes although the structure of the endostome in Timmia is unique, without clearly dened segments (Fig. 5G, H), and it is therefore impossible to assess whether segments would be opposite or alternate with regard to the exostome teeth (which are typically diplolepideous). Molecular data indicate that Timmia occupies a critical position sister to the haplolepideous plus diplolepideous-opposite clade. Phylogenetic relationships among Timmia species were described by Budke and Gofnet (2006) and peristome development by Budke et al. (2007). All of the early-diverging lineages of Bryopsida (a few variants notwithstanding) have acrocarpous gametophytes wherein the archegonia are formed terminally on the main stems; acrocarps are typically characterized by sparsely or unbranched stems and grow upright (Fig. 3). Pleurocarpous Bryopsida, in contrast, have archegonia borne on short lateral branches such that sporophytes occur laterally along the gametophyte stems. Much attention has been devoted to resolving which group of acrocarps are sister to the pleurocarps, and general answers have been obtained although the specic sister-group has not been identied (Bell and Newton, 2004, 2007; Bell et al., 2007). The terminology of gametophyte growth forms is complex (La Farge-England, 1996) but what might be called the true or core pleurocarps comprise four orders (Hypnodendrales, Ptychomniales, Hookeriales, and Hypnales; Gofnet et al., 2009), and each appears to represent a monophyletic group (Bell et al., 2007). Phylogenetic relationships among family level clades within the pleurocarps have been recalcitrant, likely because these groups appear to have undergone a relatively recent and rapid radiation (Shaw et al., 2003b). Phylogenetic diversity among major moss cladesAlthough diversity is most often measured in terms of species richness, so-called phylogenetic diversity (PD) (Faith, 1994) provides a complementary metric that takes into account the evolutionary distances separating taxa. The rationale for considering PD is straightforward and logical; two geographic areas or clades may have the same numbers of species, but can still differ importantly in diversity if the species in one group (or area) are highly divergent whereas species in the other group are closely related. Phylogenetic diversity may be a good predictor of feature diversity including morphological disparity and ecological/functional heterogeneity. Two groups or clades with similar numbers of species may differ in PD for a number of reasons. A trivial reason is bad taxonomy; if a group is oversplit there can be more species than predicted by the level of PD it contains. More signicantly, low PD despite high numbers of good species may reect a recent radiation. Alternatively, clades may contain high PD relative to the number of species because of extinction, or because of increased rates of molecular evolution relative to speciation. Although the relationship between PD and species richness cannot unambiguously reveal the underlying evolutionary processes, comparisons between biodiversity metrics can be useful for generating testable hypotheses.

360

American Journal of Botany

[Vol. 98

Fig. 4. Cell wall patterns on the insides and outsides of diploleideous-opposite and haplolepideous peristome teeth, and diagrams illustrating peristomial formulae. (AC) Funaria hygrometrica, with diplolepideous-opposite peristome. (A) Light microscope view from inner surface showing opposite segments. (B) SEM view of outer endostomial surface, partially twisted to show inner surface above (partial exostome tooth also shown). (C) SEM view of inner endostomial surface; note inner exostomial surface in backgroundthe protruding horizontal ventral lamellae, developed on many exostome teeth, are derived from PPL cells (B and C from Shaw and Rohrer, 1984, with permission). Funaria has a peristomial formula of 4 : 2 : 4a (Fig. 4G). (D, E) Dicranum scoparium, with haplolepideous peristome. (D) SEM view of whole peristome (from Shaw and Renzaglia, 2004, with permission). The single ring of 16 teeth are derived from PPL and IPL cells. (E) Light microscope view of inner surface showing three cell columns for each pair of teeth, giving a (4) : 2 : 3 formula. (The 4 is listed parenthetically because there are no exostome teeth so the OPL does not actually contribute to the peristome, though it is present.) Integers on image correspond to cells in peristomial diagram (Fig. 4H). Arrows indicate aligned horizontal cell walls that reveal which cells belong to the same column, even when split between adjacent teeth. (F) Drummondia prorepens showing inner endostomial surface and (4) : 2 : 3 cell pattern (from Shaw, 1986, with permission). (G) Peristomial diagram: diplolepideous-opposite. (H) Peristomial diagram: haplolepideous. (I) Peristomial diagram: diplolepideous-alternate with peristomial formula of 4 : 2 : 4z. Note only one column of cells between columns that form the keeled endostomial segments.

March 2011]

Shaw et al.Bryophyte diversity and evolution

361

Patterns of PD relative to species richness have been published for bryopsid mosses and for peatmosses in the genus Sphagnum (Cox et al., 2010; Shaw et al., 2003a, respectively). If there is a linear relationship between PD and taxic diversity, all groups fall along the diagonal of a two-way plot (Fig. 6). In the bryopsid (peristomate) mosses, it is clear that haplolepideous clade and Hookeriales (a largely tropical clade of pleurocarpous taxa) contain higher PD than predicted by the number of genera, whereas the Hypnales (a largely temperate clade of pleurocarpous taxa) contain lower than expected PD. The latter appears to reect the sudden radiation of hypnalian pleurocarps and quanties the small distances separating genera. The diplolepideous-alternate clade, which includes all the pleurocarpous (and many acrocarpous) mosses, has about as much PD as predicted by the level of taxic (generic) diversity. In the genus Sphagnum (peatmosses), taxic diversity (species numbers) suggests that the neotropics comprise a hotspot of diversity, but PD estimates show no such pattern (Table 1). In fact, there is as much or more phylogenetic diversity in the peatmosses of boreal regions than in the tropics and southern hemisphere combined (Shaw et al., 2003a), and this pattern holds for both plastid and nuclear DNA sequences (Table 1). There appears to be no difference in phylogenetic diversity between New World and Old World, in contrast to the high numbers of species attributed to South America. The incongruence between geographic patterns in PD and taxic diversity may reect recent radiations of Sphagnum in South America such that morphologically distinct species are closely related phylogenetically. Hornwort phylogeny and evolution (Anthocerophyta) The hornworts include ca. 14 genera and 200240 species worldwide (Villarreal et al., 2010). All hornworts have thalloid gametophytes that harbor endosymbiotic cyanobacteria in the genus Nostoc. Despite their relatively limited species diversity, the hornworts are of particular phylogenetic interest because they appear to comprise the sister group to tracheophytes (Qiu et al., 2006). Relationships within the hornworts have recently been resolved based on multilocus sequence data; these studies have resulted in drastically new insights into hornwort evolution, but species-level relationships/taxonomy is much in need of work (Duff et al., 2007). The genus Leiosporoceros has been unambiguously resolved as sister to all other hornworts (Duff et al., 2007; Villarreal et al., 2010). The genus lacks RNA editing of the rbcL transcript, its chloroplasts lack pyrenoids (present in most other hornworts but no other embryophytes), the spores are smooth and beanshaped, schizogenous cavities occur only in older thalli, and the gametophytes contain Nostoc endosymbionts in longitudinally oriented canals that elongate as the thallus grows rather than in discrete, spherical colonies (Renzaglia et al., 2009). Some of the species diversity in hornworts appears to be related to geography, and several of the traditional genera are nonmonophyletic (Villarreal et al., 2010). Additional resolution of geographic and phylogenetic patterns can be expected in the coming years

because of in-progress research (J. C. Villarreal, University of Connecticut, unpublished data). Latitudinal gradients in bryophyte diversityA trend of increasing species diversity toward the tropics is nearly universal in plants and animals (Rosenzweig, 1995), but this issue has been somewhat controversial with regard to bryophytes. So-called alpha diversity, species richness within areas, is often comparable in temperate and tropical regions (Shaw et al., 2005; Hedens, 2007). Shaw et al. (2005) found a weak trend of increasing alpha diversity in moss oras of the Americas, but no detectable trend globally. They suggested that the tropics might nevertheless contain higher species richness overall because of regional turnover in species occurrence and indeed Hedens (2007) found that beta diversity (among regions) is higher in pleurocarpous mosses within the tropics than in temperate regions. In particular, pleurocarpous tropical moss oras are more differentiated among continents than are temperate moss oras, where a signicant percentage of species have circumpolar distributions. In general, endemism is far lower in bryophytes than in seed plants, presumably because of dispersal of tiny spores (Vanderpoorten et al., 2009). Studies of dispersal in bryophytes, by spores and other means (e.g., asexual propagules), are critical to understanding biogeographic and biodiversity patterns, as well as evolutionary processes at more local scales. POPULATION PROCESSES AND BRYOPHYTE DIVERSIFICATION Reproductive biology and evolution in bryophyte populations Evolutionary study of bryophytes necessitates rethinking some of the most general and fundamental concepts in biology, including self, parentage, and tness. The bryophyte life cycle is comparable in many ways to that of seed-free tracheophytes such as ferns, including the existence of freeliving gametophytes, the potential for true (intragametophytic) self-fertilization, mitotic production of gametes by gametophytes, and spore reproduction. But the bryophyte life cycle also has features that are unique. Importantly, these include the production of more than one sporophyte on a single gametophyte, multiple paternity of those sporophytes, and, because of these characteristics, the potential for sexual conicts due to competing interests of maternal and paternal gametophyte genomes in sporophytes. Although seed plant biologists use the term self-fertilization for mating between gametophytes produced by the same sporophyte, the term is a misnomer because gametophytes in these plants are genetically distinct individuals produced by meiotic recombination. Application of the term self-fertilization represents baggage from a diploid-biased view of the world; the sporophyte is viewed as the self and gametophytes are seen simply as part of the reproductive apparatus of those sporophytes. Intragametophytic selng produces a completely

(J) Peristomial diagram: diplolepideous-alternate with peristomial formula of 4 : 2 : 8z. Note three columns of cells between columns that form the keeled endostomial segments. From the inside outward, concentric layers of cells are IPL = inner peristomial layer, PPL = primary peristomial layer, and OPL = outer peristomial layer. Note that in diplolepideous-opposite peristomes, all anticlinal walls in the IPL are aligned with anticlinal walls in the OPL (Fig. 4G). In haplolepideous peristomes, every third wall is aligned (Fig. 4H), and in diplolepideous-alternate types, none of the anticlinal IPL walls are aligned with anticlinal walls in the OPL or PPL (Fig. 4I, J). The developmental origins of these different alignment patterns were described by Shaw and Anderson (1988), and Shaw et al. (1987, 1989a, b).

362

American Journal of Botany

[Vol. 98

Fig. 5. Cell wall patterns on the insides and outsides of diplolepideous-alternate peristome teeth, SEM views. (A) Schizymenium sp., outer surface of exostome tooth. Note the vertical line down the center dividing two columns of OPL cells that contributed wall material to the outer surface. (B) Pleuroziopsis ruthenica (from Shaw and Rohrer, 1984, with permission), outer endostomial surface; broken bases of exostome teeth also shown. The endostome

March 2011]

Shaw et al.Bryophyte diversity and evolution

363

Partitioning of phylogenetic diversity in the moss genus Sphagnum between geographic regions. PD values are provided as percentages of total PD in a phylogenetic analysis of 436 accessions from throughout the geographic range of the genus. Sequences were obtained from the nuclear ribosomal ITS region (nrDNA below) and the trnL-trnF plastid region (cpDNA below). Comparisons shown below among boreal, non-Boreal, New and Old World regions are based on equivalent sample sizes (120 and 196 samples, respectively). See Shaw et al. (2003a) for details of sampling and analyses.
Combined 48 44 64 62 nrDNA 49 47 62 67 cpDNA 47 40 68 55

Region Boreal Non-Boreal Old World New World

Fig. 6. Relationship between phylogenetic diversity (PD) and numbers of genera within selected clades of bryopsid mosses, as percentages of total diversity within the Bryophyta class Bryopsida.

homozygous sporophyte in one generation (mutations aside) and is functionally equivalent to asexual reproduction. A diploid individual, be it an oak tree or human, has parents generally considered to be the diploid individuals of the previous generation that mated to form a diploid zygote. In bryophytes, what is the self, and who are the parents of that self? Because the gametophyte is the perennial, free-living plant in nature, the self is generally viewed as that gametophyte. The parents of that gametophyte might be considered the sporophyte from which it was produced meiotically (in which case it has only one parent), or more appropriately, the parents of a freeliving gametophyte are the gametophytes that mated to produce a sporophyte, and through that sporophyte the offspring are produced. The sporophyte is simply part of the reproductive apparatus of the gametophyte (which is in fact no more correct than the reverse, critiqued already). A chicken is just an eggs way of reproducing itself. The tness of a gametophyte is the number of next-generation gametophytes it produces (through the intermediate sporophyte generation); conversely, the tness of the sporophyte is the number of next-generation sporophytes it produces through mating of its gametophyte offspring. The parents of a sporophyte are the gametophytes that mated to produce it. Thus, identifying parentage for a diploid sporophyte (polyploidy ignored for simplicity) means identifying the actual gametes that effected zygote formation. This identication is theoretically possible in seed plants and seed-free tracheophytes, but much more difcult than in bryophytes because the gametophyte generation in bryophytes is macroscopic and readily sampled from natural populations. It is an important and unique feature of the bryophyte life cycle that the reproductive success of a single gametophyte (the number of sporophytes it parents) can be a quantitative trait. In all other groups of plants (with very rare exceptions), a single gametophyte either succeeds in parenting one sporophyte, or it does not. Bryophyte gametophytes,

in contrast, parent one to many sporophytes. Because each sporophyte typically produces hundreds of thousands to millions of spores, tness differences among gametophytes are amplied by variation in mating success. Because most bryophytes have haploid gametophytes and diploid sporophytes (although polyploidy is not uncommon; Sstad 2005), paternity determination for sporophytes is relatively straightforward. Using microsatellite-based genotyping of maternal gametophytes and their attached sporophytes, van der Velde et al. (2001) showed that proximity of male clones to females was the dominant factor determining mating success in a population of Polytrichum formosum, although male clone size (presumably correlated with gamete production) was also a signicant factor. It would be interesting to know whether larger male clones are simply older or have higher growth rates and/or competitive abilities (which would suggest sexual selection is operating). Approximately 98% of sporophytes were fathered by an identiable male clone growing within 5 m of the mother. Individual gametophyte genotypes formed clones ranging from less than 10 cm2 to over 1 m2, and each of three female clones bore at least 2535 sporophytes that were sampled for paternity analysis. One to three male gametophytes fathered the sporophytes attached to each of the females. Sexual conicts appear to be a fact of life in both plants (Haig and Wilczek, 2006) and animals, including humans (Goetz and Shackelford, 2009). The basic prerequisite for sexual conict is multiple paternity of diploid offspring parented by a single female. When multiple sporophytes are borne by a single maternal gametophyte, maternal and paternal genomes in those sporophytes have competing and sometimes contradictory interests. The maternal gametophyte is best served by spreading resources across all sporophytes she supports because they all carry the same maternal genome. When different sporophytes borne by a female gametophyte have different (gametophyte) fathers, it is optimal for each paternal genotype to garner all resources available

consists of a continuous basal membrane below and 16 keeled endostome segments above. Each segment has a vertical line up the center on the outer surface. Note that the keel of each segment alternates with the (broken) exostome teeth. (C, D) Inner endostomial surface showing two narrow columns of cells (a, b) between each keeled segment. This determines the peristomial formula as 4 : 2 : 6. Each column extends upward as a cilium in (C) (Rhizogonium spiniforme (from Shaw and Rohrer, 1984, with permission); this peristome has two cilia between segments. The two cell columns that form cilia above are labeled a and b. The cell columns do not persist as cilia in (D) (Pleuroziopsis ruthenica, from Shaw and Rohrer, 1984, with permission), though the peristomial formula is 4 : 2 : 6, as in (C). (E) Aulacomnium palustre (from Shaw and Rohrer, 1984, with permission), inner endostomial surface showing four narrow columns of cells (ad) between each keeled segment. This determines the peristomial formula as 4 : 2 : 10 (an unusually large number of IPL cells). (G, H) Timmia megapolitana (from Shaw and Rohrer, 1984, with permission). (G) Outer endostomial surface. Note the keeled basal membrane where segments would be formed in diplolepideous-alternate peristomes. (H) Inner endostomial surface. Timmia forms endostomial cilia but no clear segments.

364

American Journal of Botany

[Vol. 98

(Haig and Wilczek, 2006). Multiple paternity sets up the potential for conicts between maternal and paternal genomes. Multiple paternity of sporophytes borne by individual female gametophytes was almost universal in a population of the moss Sphagnum lescurii (Szvnyi et al., 2009b). Indeed, some individual female gametophytes bore sporophytes fathered by as many as 15 different males. Males in the population mated much more faithfully with one or a limited number of females. Sporophyte size (which is correlated with spore number in Sphagnum; Sundberg and Rydin, 1998) is correlated with heterozygosity, suggesting that inbreeding depression (conversely, heterosis) occurs in this species. Inbreeding depression has otherwise been documented in the dioicous moss Ceratodon purpureus, but not in the monoicous species Funaria hygrometrica (Taylor et al., 2007). In Sphagnum, sporophytes lack a seta and are instead raised on pseudopodia of (maternal) gametophyte origin, and highly heterozygous sporophytes of S. lescurii were more likely to be raised on pseudopodia than less heterozygous sporophytes. This raises the intriguing possibility that either female gametophytes are able to differentially provision sporophytes of varying quality or that highly heterozygous sporophytes are better at capturing resources from the mother, although additional work is needed to eliminate other possible explanations (Szvnyi et al., 2009b). If these patterns indicate conicts between maternal and paternal genomes in sporophytes, genomic imprinting is to be expected with regard to sporophyte gene expression (Haig and Wilczek, 2006). By turning off expression of the paternal genome, conicts between maternal and paternal interests can be avoided. Expression of parental alleles in moss sporophytes is a fertile area for future research. Bryophyte dispersal Dispersal is a critically important life history process determining a species current distribution; past, present, and future changes in range; and the standing genetic structure of its populations. Dispersal is also fundamental to metapopulation dynamics, community assembly, responses to habitat fragmentation and climate change, latitudinal biodiversity gradients, as well as to the existence, location, and conservation status of global biodiversity hotspots (Kokko and Lpez-Sepulcre, 2006; Roy and Goldberg, 2007; Grundmann et al., 2008). The genetic consequences of dispersal fundamentally determine the tempo and mode of diversication among populations, metapopulation systems, and deeper clades. Effective long-distance dispersal (LDD) can only be achieved if high numbers of propagules with appropriate environmental tolerances, size, and establishment properties are produced (van Zanten 1976, 1978; van Zanten and Pcs, 1981; Herben and Sderstrm, 1992; Hassel and Sderstrm, 1999). Bryophyte spores appear to fulll these conditions. Individual moss capsules typically produce tens of thousands and sometimes up to millions of spores, and annual spore production can exceed 10 million from just 1 m2 (Longton and Schuster, 1984; Longton 1997; Sderstrm and Herben, 1997; Wiklund, 2002; Sundberg, 2005). Although most spores are deposited near the source (within meters), a signicant number travel longer distances (Stoneburner et al., 1992; Miles and Longton, 1992; Sundberg, 2005). The spores of many species can withstand long periods of desiccation, high levels of UV radiation, and temperature extremes (van Zanten, 1976, 1978; van Zanten and Pcs, 1981). Although establishment probability of spores under natural conditions is low (on the order of 103 to 104), both ecological and theoretical studies indicate that it is sufcient to enable the

persistence of species in a metapopulation landscape (Herben et al., 1991; Longton, 1997; Hassel and Sderstrm, 1999, 2005; Sundberg and Rydin, 2002). Regional- and continental-scale dispersalAs with many previous studies of bryophyte genetic structure based on isozymes, more recent work using DNA ngerprinting methods and sequences have shown that genetic architecture is highly species- and context-dependent (Korpelainen et al., 2005). Nevertheless, a general pattern is emerging in which local and regional dispersal appears to be quite effective in many or most species, at least in those that produce spores regularly (Snll et al., 2004; Zartman and Nasciemento, 2006; Zartman et al., 2006). Analyses of island and mainland populations of Hylocomium splendens showed no detectable pattern of isolation by distance, indicating effective dispersal over hundreds of kilometers (Cronberg et al., 1997; Cronberg, 2002, 2004). Other recent studies using highly polymorphic markers (e.g., microsatellites, AFLP, ISSR) show that dispersal is sufcient even at continental scales to genetically homogenize plants (van der Velde and Bijlsma, 2003; Cronberg, 2002; Grundmann et al., 2007, 2008; Vanderpoorten et al., 2008). An absence or near absence of linkage disequilibrium within the liverwort Frullania asagrayana across a large portion of eastern North America indicates both extensive dispersal and a level of sexual recombination that approaches panmixia (Ramaiya et al., 2010). It should be noted, on the other hand, that few bryophyte species are ubiquitous at regional let alone global scales, and clearly, successful dispersal and establishment are limited. Ecological data also indicate effective dispersal within many bryophyte species across landscape scales. Species richness on islands is generally unrelated to distance of islands from the mainland at spatial scales spanning some 40100 km (Tangney et al., 1990; Nakanishi, 2001; Sundberg et al., 2006). Similarly, comparisons of species composition on newly established substrates with that of local and regional species pools indicate effective dispersal spanning several tens of kilometers for most colonizing bryophyte species (Soro et al., 1999; Miller and McDaniel, 2004; Hutsemkers et al., 2008). Moreover, species composition of isolated island-like substrates may not be explained by relative abundances of potential source species in their immediate surroundings, suggesting that recruitment by LDD is frequent and signicant in most sexually reproducing bryophyte species (Hylander, 2009). Although efcient LDD is certainly an ongoing and detectable process in most bryophyte species it remains to be seen whether it is efcient enough to completely balance the effects of spatial and temporal barriers. Habitat fragmentation affects species composition and richness of bryophyte communities despite effective regional-scale dispersal (Pharo et al., 2004; Zartman and Nascimento, 2006; Pharo and Zartman, 2007; Pohjamo et al., 2008). These effects are likely due to the fact that dispersal efcacy of a signicant proportion of the species cannot balance the temporal and spatial extent of habitat fragmentation. Metapopulation studies indicate that spatial and temporal turnover rates of habitat patches may be higher than can be effectively balanced by dispersal (Snll et al., 2003; Lbel et al., 2006). Dispersal limitation of bryophytes may affect their persistence even on small temporal and spatial scales when habitat dynamics are rapid. Analyses of multiple moss species within Europe have revealed a more or less congruent genetic split between southern

March 2011]

Shaw et al.Bryophyte diversity and evolution

365

and northern populations, a pattern thought to be associated with recolonization of the continent from two Pleistocene refugia (Cronberg, 1998; van der Velde and Bijlsma, 2003; Grundmann et al., 2007, 2008; Szvnyi et al., 2006, 2007). The fact that spatial structuring of genetic lineages is still recognizable suggests the possibility of adaptive divergence between these regional population systems, effectively reducing or eliminating gene ow between them. Indeed, Szvnyi et al. (2009a) found evidence of nonneutral differentiation in the GapC (glyceraldehyde 3-phosphate dehydrogenase) gene between the southern and northern groups in Sphagnum mbriatum. Intercontinental dispersalMany, possibly most, bryophyte species occur on more than one continent. Earlier isozyme analyses rarely revealed genetic differentiation between conspecic populations on different continents, at least in temperate and boreal species. DNA-based markers have more frequently documented differentiation between intercontinentally disjunct populations (Hanssen et al., 2000; Sstad et al., 2000; Szvnyi et al., 2008; Vanderpoorten et al., 2008). Few studies have tried to explicitly distinguish shared polymorphism that reects retention of ancestral variation from ongoing gene ow. Szvnyi et al. (2008), however, found that shared polymorphism between European and North American populations of four Sphagnum species was attributable to both ongoing gene ow and retained polymorphism. Divergence in all four species appeared to reect relatively recent Pleistocene vicariance with retention of polymorphism attributable to low rates of drift in large effective populations. While that study did also evidence intercontinental gene ow, the rate was insufcient to prevent (statistically) signicant, albeit limited differentiation. Recent data are insufcient to make predictions about dispersal processes and their wide-ranging consequences (Ronce, 2007). Studies by Sundberg (2002, 2005, 2010a, b) have made steps toward these goals by providing a detailed description of the spore dispersal curve in bryophytes and by estimating multiple key parameters of the dispersal process. The joint application of mechanistic spore dispersal models (Tackenberg, 2003) with the empirically estimated parameters will open up the way for quantitative predictions about the efcacy and consequences of LDD in bryophytes. Dispersal detected at phylogenetic scalesTo what extent does effective long-distance dispersal impact long-term phylogenetic processes in bryophytes? It was early recognized that most bryophyte species and almost all genera have intercontinental geographic distributions, and until recently vicariance was the preferred explanation because many distributions were interpretable by fragmentation of ancient Gondwanan, Laurasian, or Pangean ranges (e.g., Crum, 1972). Morphologically cryptic genetic differentiation has been documented in a number of widespread species (Shaw, 2001; Heinrichs et al., 2009), and phylogenetic analyses of some groups have revealed allopatric monophyletic groups that turn out to differ in morphological features as well (e.g., the so-called Frullania tamarsci complex: Heinrichs et al., 2010). Recent meta-analyses suggest that the geographic distributions of multiple liverwort genera around the globe may be explained by continental drift events (Vanderpoorten et al., 2009). On the other hand, an increasing number of phylogenetic studies indicate that LDD appears to be responsible for many intercontinental disjunctions previously interpreted as ancient vicariance events (reviewed in Frahm, 2008; Heinrichs et al., 2009). Phylogenetic analyses, for example,

have repeatedly resolved African and South American liverwort species as sister taxa, demonstrating recurrent dispersal between continents. Only a few recent studies have applied molecular dating to explicitly test whether patterns are best explained by vicariance or long-distance dispersal, and the latter has generally been supported as the most likely explanation (e.g., McDaniel and Shaw, 2003; Heinrichs et al., 2007; Devos and Vanderpoorten, 2009; Aigoin et al., 2009). In general, phylogenetic analyses indicate that intercontinental dispersal has occurred repeatedly during bryophyte diversication, but is not so rampant that allopatric differentiation is precluded. PROSPECTUS We identify several areas where research on bryophyte diversity is poised to make signicant progress in the coming years toward a better understanding of evolution in the earliest lineages of embryophytes. It is important to state that oristic and monographic studies provide the foundation for all other efforts by dening the units of evolutionary change (species and deeper clades), and their phylogenetic relationships to one another. And it is equally important to note that without curated herbarium collections and robust informatic tools for efciently extracting information from them, taxonomic efforts are much reduced in value. The outstanding phylogenetic issue in moss systematics pertains to relationships among pleurocarpous groups. Because the pleurocarpous mosses are relatively uniform at the molecular level, resolution of relationships will likely require data from many genes and not from 10 or even 15; genomic resources will have to be tapped to identify 25 or more loci. Because almost half of moss species diversity is in the pleurocarps, this endeavor is well worth the effort. Studies of dispersal and establishment in bryophyte populations provide a window into biogeographic processes in early (pre-seed) land plants. The overall picture from bryophytes includes effective dispersal at regional scales with signicant, though not unlimited, connectivity among populations, and at least occasional intercontinental movements. Intercontinental migration, even within extant species, is certainly more common than in seed plants. Because the life cycles, mating patterns, and dispersal mechanisms of early land plants such as bryophytes differ from those in the more recent seed plants, predominant patterns of population structure have likely evolved through time and bryophytes provide insight into some of the evolutionary processes of early embryophytes. The application of genome and especially transcriptome sequencing to understand the evolution of plant life cycles is one of the most exciting avenues for research in the next few years. We now have the unprecedented ability to investigate differential gene expression in gametophytes and sporophytes and, thereby, the evolution of multicellular sporophytes in plants. Transcriptomics also provides powerful new tools for addressing fundamental questions in bryophyte reproductive biology and evolution, including changes in gene expression associated with speciation, genomic imprinting, and sexual conicts as determinants of reproductive processes and with gene expression in relation to environmental heterogeneity and climate change. Molecular techniques have been enthusiastically applied to deep phylogenetic problems in bryophytes and other plants, and we hope that in the future, old biosystematic issues that fall at the interface of population genetics and systematics will be increasingly addressed using genomic resources in bryophytes.

366 LITERATURE CITED

American Journal of Botany

[Vol. 98

Aigoin, D. A., N. Devos, S. Huttunen, M. Ignatov, J. M. GonzlezMancebo, and A. Vanderpoorten. 2009. And if Engler was not completely wrong? Evidence for multiple evolutionary origins in the moss ora of Macaronesia. Evolution 63: 32483257. Becker, B., and B. Marin. 2009. Streptophyte algae and the origin of embryophytes. Annals of Botany 103: 9991004. Beckert, S., H. Muhle, D. Pruchner, and V. Knoop. 2001. The mitochondrial nad2 gene as a novel marker locus for phylogenetic analysis of early land plants: A comparative analysis in mosses. Molecular Phylogenetics and Evolution 18: 117126. Bell, N. E., and J. Hyvnen. 2008. Rooting the Polytrichopsida: The phylogenetic position of Atrichopsis and the independent origin of the polytrichopsid peristome. In H. Mohamed, B. B. Baki, A. NasrulhaqBoyce, and P. K. Y. Lee [eds.], Bryology in the New Millennium, 227239. University of Malaya, Kuala Lumpur, Malaysia. Bell, N. E., and A. E. Newton. 2004. Systematic studies of non-hypnanaean pleurocarps: Establishing a phylogenetic framework for investigating the origins of pleurocarpy. In B. Gofnet, V. Hollowell, and R. Magill [eds.], Molecular systematics of bryophytes. Monographs in Systematic Botany vol. 98, 290319. Missouri Botanical Garden Press, St. Louis, Missouri, USA. Bell, N. E., and A. E. Newton. 2007. Pleurocarpy in the Rhizogoniaceous grade. In A. E. Newton and R. S. Tangney [eds.], Pleurocarpous mosses: Systematics and evolution. Systematics Association Special Volume 71, 4164. Bell, N. E., D. Quandt, T. J. OBrien, and A. E. Newton. 2007. Taxonomy and phylogeny in the earliest diverging pleurocarps: Square holes and bifurcating pegs. Bryologist 110: 533560. Bisang, I. 2003. Population development, demographic structure, and life cycle aspects of two hornworts in Switzerland. Lindbergia 28: 105112. Bower, F. O. 1890. On antithetic as distinct from homologous alternation of generations in plants. Annals of Botany 4: 347370. Budke, J. M., and B. Goffinet. 2006. Phylogenetic analyses of Timmiaceae (Bryophyta: Musci) based on nuclear and chloroplast sequence data. Systematic Botany 31: 633641. Budke, J. M., C. S. Jones, and B. Goffinet. 2007. Development of the enigmatic peristome of Timmia megapolitana (Timmiaceae; Bryophyta). American Journal of Botany 94: 460467. Coen, E. S., and E. M. Meyerowitz. 1991. The war of the whorls: Genetic interactions controlling ower development. Nature 353: 3137. Cox, C. J., B. Goffinet, A. J. Shaw, and S. B. Boles. 2004. Phylogenetic relationships among the mosses based on heterogeneous Bayesian analysis of multiple genes from multiple genomic compartments. Systematic Botany 29: 234250. Cox, C. J., B. Goffinet, N. J. Wickett, S. B. Boles, and A. J. Shaw. 2010. Moss diversity: A molecular phylogenetic analysis of genera. Phytotaxa 9: 175195. Crandall-Stotler, B. J., R. E. Stotler, and D. G. Long. 2009. Morphology and classication of the Marchantiophyta. In B. Gofnet and A. J. Shaw [eds.], Bryophyte biology, 2nd ed., 154. Cambridge University Press, Cambridge, UK. Cronberg, N. 1998. Population structure and interspecic differentiation of the peat moss sister species Sphagnum rubellum and S. capillifolium (Sphagnaceae) in northern Europe. Plant Systematics and Evolution 209: 139158. Cronberg, N. 2002. Colonization dynamics of the clonal moss Hylocomium splendens on islands in a Baltic land uplift area: Reproduction, genet distribution and genetic variation. Journal of Ecology 90: 925935. Cronberg, N. 2004. Genetic differentiation between populations of the moss Hylocomium splendens (Hedw.) Schimp. from low versus high elevation in the Scandinavian mountain range. Lindbergia 29: 6472. Cronberg, N., U. Molau, and M. Sonesson. 1997. Genetic variation in the clonal bryophyte Hylocomium splendens at hierarchical geographic scales in Scandinavia. Heredity 78: 293301. Crosby, M. R. 1980. The diversity and relationships of mosses. In R. J. Taylor and A. E. Leviton [eds.], The mosses of North America, 115

129. Pacic Division, American Association for the Advancement of Science, San Francisco, California, USA. Crum, H. A. 1972. The geographic origin if the mosses of North Americas eastern deciduous forest. Journal of the Hattori Botanical Laboratory 35: 269298. Davis, C. 2004. A molecular phylogeny of leafy liverworts (Jungermanniidae, Marchantiophyta). In B. Gofnet, V. Hollowell, and R. Magill [eds.], Molecular systematics of bryophytes. Monographs in Systematic Botany vol. 98, 6186. Missouri Botanical Garden, St. Louis, Missouri, USA. Devos, N., and A. Vanderpoorten. 2009. Range disjunctions, speciation and morphological transformation rates in the liverwort genus Leptoscyphus. Evolution 63: 779792. Dolan, L. 2009. Body building on landMorphological evolution of land plants. Current Opinion in Plant Biology 12: 48. Duff, R. J., J. C. Villarreal, D. C. Cargill, and K. S. Renzaglia. 2007. Progress and challenges toward developing a phylogeny and classication of the hornworts. Bryologist 110: 214243. Edwards, S. R. 1984. Homologies and inter-relationships of moss peristomes. In R. M. Schuster [ed.], New manual of bryology, vol. 2, 658695. Hattori Botanical Laboratory, Nichinan, Japan. Evans, A. W., and H. D. Hooker Jr. 1913. Development of the peristome in Ceratodon purpureus. Bulletin of the Torrey Botanical Club 40: 97109. Faith, D. P. 1994. Phylogenetic diversity: A general framework for the prediction of feature diversity. In P. L. Forey, C. J. Humphries, and R. I. Vane-Wright [eds.], Systematics and conservation evaluation, 251268. Clarendon, Oxford, UK. Farlow, W. G. 1874. An asexual growth from the prothallus of Pteris cretica. Quarterly Journal of Microscopical Science 14: 266272. Fleischer, M. 19041923. Die Musci der Flora von Buitenzorg (zugleich Laubmoosora von Java), 4 vols. Brill, Leiden, Netherlands. Forrest, L. L., E. C. Davis, B. J. Crandall-Stotler, B. A. Clark, and M. L. Hollingsworth. 2006. Unraveling the evolutionary history of the liverworts (Marchantiophyta): Multiple taxa, genomes and analysis. Bryologist 109: 303334. Frahm, J. P. 2008. Diversity, dispersal and biogeography of bryophytes (mosses). Biodiversity and Conservation 17: 277284. Frey, W., and M. Stech. 2005. A morpho-molecular classication of the liverworts (Hepaticophytina, Bryophyta). Nova Hedwigia 81: 5578. Fujita, T., and M. Hasebe. 2009. Convergences and divergences in polar auxin transport and shoot development in land plant evolution. Plant Signaling & Behavior 4: 313315. Fujita, T., H. Sakaguchi, Y. Hiwatashi, S. J. Wagstaff, M. Ito, H. Deguchi, T. Sato, and M. Hasebe. 2008. Convergent evolution of shoots in land plants: Lack of auxin polar transport in moss shoots. Evolution & Development 10: 176186. Garbary, D. J., K. S. Renzaglia, and J. G. Duckett. 1993. The phylogeny of land plants: A cladistic analysis based on male gametogenesis. Plant Systematics and Evolution 188: 237269. Gensel, P. G. 2008. The earliest land plants. Annual Review of Ecology, Evolution, and Systematics 39: 459477. Goetz, A. T., and T. K. Shackelford. 2009. Sexual conict in humans: Evolutionary consequences of asymmetric parental investment and paternity uncertainty. Animal Biology 59: 449456. Goffinet, B., W. R. Buck, and A. J. Shaw. 2009. Morphology, anatomy, and classication of the Bryophyta. In B. Gofnet and A. J. Shaw [eds.], Bryophyte biology, 2nd ed., 53138. Cambridge University Press, Cambridge, UK. Goffinet, B., C. J. Cox, A. J. Shaw, and T. A. J. Hedderson. 2001. The Bryophyta (mosses): Systematic and evolutionary inferences from an rps4 gene (cpDNA) phylogeny. Annals of Botany 87: 191208. Goffinet, B., and A. J. Shaw [eds.]. 2009. Bryophyte biology. Cambridge University, Press, Cambridge, UK. Goffinet, B., N. J. Wickett, A. J. Shaw, and C. J. Cox. 2005. Phylogenetic signicance of the rpoA loss in the chloroplast genome of mosses. Taxon 54: 353360. Graham, L. E., C. F. Delwiche, and B. D. Mishler. 1991. Phylogenetic connections between the green algae and the bryophytes. Advances in Bryology 4: 213244.

March 2011]

Shaw et al.Bryophyte diversity and evolution

367

Grundmann, M., S. W. Ansell, R. J. Russell, M. A. Koch, and J. C. Vogel. 2007. Genetic structure of the widespread and common Mediterranean bryophyte Pleurochaete squarrosa (Brid.) Lindb. (Pottiaceae)Evidence from nuclear and plastidic DNA sequence variation and allozymes. Molecular Ecology 16: 709722. Grundmann, M., S. W. Ansell, R. J. Russell, M. A. Koch, and J. C. Vogel. 2008. Hotspots of diversity in a clonal worldThe Mediterranean moss Pleurochaete squarrosa in Central Europe. Molecular Ecology 17: 825838. Haig, D. 2008. Homologous versus antithetic alternation of generations and the origin of sporophytes. Botanical Review 74: 395418. Haig, D., and A. Wilczek. 2006. Sexual conict and the alternation of haploid and diploid generations. Philosophical Transactions of the Royal Society of London, B, Biological Sciences 361: 335343. Hanssen, L., S. M. Sstad, and K. I. Flatberg. 2000. Population structure and taxonomy of Sphagnum cuspidatum and S. viride. Bryologist 103: 93103. Hassel, K., and L. Sderstrm. 1999. Spore germination in the laboratory and spore establishment in the eld in Pogonatum dentatum (Brid.) Brid. Lindbergia 24: 310. Hassel, K., and L. Sderstrm. 2005. The expansion of the alien mosses Orthodontium lineare and Campylopus introexus in Britain and continental Europe. Journal of the Hattori Botanical Laboratory 97: 183193. Hay, A., and M. Tsiantis. 2009. A KNOX family TALE. Current Opinion in Plant Biology 12: 593598. Hedens, L. 2007. Global diversity patterns among pleurocarpous mosses. Bryologist 110: 319331. Heinrichs, J., S. R. Gradstein, R. Wilson, and H. Schneider. 2005. Towards a natural classication of liverworts (Marchantiophyta) based on the chloroplast gene rbcL. Cryptogamie. Bryologie 26: 131150. Heinrichs, J., J. Hentschel, A. Bombosch, A. Fiebig, J. Reise, M. Edelmann, H.-P. Kreier, et al. 2010. One species or at least eight? Delimitation and distribution of Frullania tamarisci (L.) Dumort. s. l. (Jungermanniopsida, Porellales) inferred from nuclear and chloroplast DNA markers. Molecular Phylogenetics and Evolution 56: 11051114. Heinrichs, J., J. Hentschel, K. Feldberg, A. Bombosch, and H. Schneider. 2009. Phylogenetic biogeography and taxonomy of disjunctly distributed bryophytes. Journal of Systematics and Evolution 47: 497508. 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: 3144. He-Nygrn, X., I. Ahonen, A. Juslen, D. Glenny, and S. Piippo. 2004. Phylogeny of liverwortsBeyond a leaf and a thallus. In B. Gofnet, V. Hollowell, and R. Magill [eds.], Molecular systematics of bryophytes. Monographs in Systematic Botany, vol. 98, 87118. Missouri Botanical Garden Press, St. Louis, Missouri, USA. Herben, T., H. Rydin, and L. Sderstrm. 1991. Spore establishment probability and the persistence of the fugitive invading moss, Orthodontium lineare: A spatial simulation model. Oikos 60: 215221. Herben, T., and L. Sderstrm. 1992. Which habitat parameters are most important for the persistence of a bryophyte species on patchy, temporary substrates? Biological Conservation 59: 121126. Hutsemkers, V., C. Dopagne, and A. Vanderpoorten. 2008. How far and how fast do bryophytes travel at the landscape scale. Diversity & Distributions 14: 483492. Hylander, K. 2009. No increase in colonization rate of boreal bryophytes close to propagule sources. Ecology 90: 160169. Karol, K. G., R. M. Mccourt, M. T. Cimino, and C. F. Delwiche. 2001. The closest living relatives of land plants. Science 294: 23512353. Kenrick, P. R., and P. R. Crane. 1997. The origin and early evolution of plants on land. Nature 389: 3339.

Khandelwal, A., S. H. Cho, H. Marella, Y. Sakata, P. F. Perroud, A. Pan, and R. S. Quatrano. 2010. Role of ABA and ABI3 in desiccation tolerance. Science 327: 546. Kofuji, R., N. Sumakawa, M. Yamasaki, K. Kondo, K. Ueda, M. Ito, and M. Hasebe. 2003. Evolution and divergence of the MADS-box gene family based on genome-wide expression analyses. Molecular Biology and Evolution 20: 19631977. Kokko, H., and A. Lpez-Sepulcre. 2006. From individual dispersal to species ranges: Perspectives for a changing world. Science 313: 789790. Korpelainen, H., M. Pohjamo, and S. Laaka-Lindberg. 2005. How efciently does bryophyte dispersal lead to gene ow? Journal of the Hattori Botanical Laboratory 97: 195205. La Farge-England, C. 1996. Growth form, branching pattern, and perichaetial position in mosses: Cladocarpy and pleurocarpy redened. Bryologist 99: 170186. Langdale, J. A. 2008. Evolution of developmental mechanisms in plants. Current Opinion in Genetics & Development 18: 368373. Ligrone, R., J. G. Duckett, and K. S. Renzaglia. 2000. Conducting tissues and phylogenetic relationships of bryophytes. Philosophical Transactions of the Royal Society of London, B, Biological Sciences 355: 795813. Lbel, S., T. Snll, and H. Rydin. 2006. Species richness patterns and metapopulation processesEvidence from epiphyte communities in boreo-nemoral forests. Ecography 29: 169182. Longton, R. E. 1997. Reproductive biology and life-history strategies. In R. E. Longton [ed.], Advances in bryology, vol 6, Population studies, 65101. J. Cramer, Berlin, Germany. Longton, R. E., and R. M. Schuster. R. M. 1984. Reproductive biology. In R. M. Schuster [ed.], New manual of bryology, 386462. Hattori Botanical Laboratory, Nichinan, Japan. Magombo, Z. L. K. 2003. The phylogeny of basal peristomate mosses: Evidence from cpDNA, and implications for peristome evolution. Systematic Botany 28: 2438. McDaniel, S. F., and A. J. Shaw. 2003. Phylogeographic structure and cryptic speciation in the trans-antarctic moss Pyrrhobryum mnioides. Evolution 57: 205215. Menand, B., K. Yi, S. Jouannic, L. Hoffmann, E. Ryan, P. Linstead, D. G. Schaefer, and L. Dolan. 2007. An ancient mechanism controls the development of cells with a rooting function in land plants. Science 316: 14771480. Miles, C. J., and R. E. Longton. 1992. Deposition of moss spores in relation to distance from parent gametophytes. Journal of Bryology 17: 355368. Miller, N. G., and S. F. McDaniel. 2004. Bryophyte dispersal inferred from colonization of an introduced substratum on Whiteface Mountain, New York. American Journal of Botany 91: 11731182. Mogensen, G. S. 1981. The biological signicance of morphological characters in bryophytes: The spore. Bryologist 84: 187207. Mosquna, A., A. Katz, E. L. Decker, S. A. Rensing, R. Reski, and N. Ohad. 2009. Regulation of stem cell maintenance by the Polycomb protein FIE has been conserved during land plant evolution. Development 136: 24332444. Mller, C. 18481851. Synopsis Muscorum Frondosorum omnium hucusque cognitorum pars prima. Vegetationis Acrocarpicae, pars secunda. Musci Vegetationis Pleurocarpicae. A. Foerstner, Berlin, Germany. Nakanishi, K. 2001. Floristic diversity of bryophyte vegetation in relation to island area. Journal of the Hattori Botanical Laboratory 91: 301316. Newton, A. E., C. J. Cox, J. G. Duckett, J. Wheeler, B. Goffinet, B. D. Mishler, and T. A. J. Hedderson. 2000. Evolution of the major moss lineages. Bryologist 103: 187211. Ng, M., and M. F. Yanofsky. 2000. Three ways to learn the ABCs. Current Opinion in Plant Biology 3: 4752. Nickrent, D. L., C. L. Parkinson, J. D. Palmer, and R. J. Duff. 2000. Multigene phylogeny of land plants with special reference to bryophytes and the earliest land plants. Molecular Biology and Evolution 17: 18851895. Niklas, K. J., and U. Kutschera. 2009. The evolution of the plant life cycle. New Phytologist 185: 2741.

368

American Journal of Botany

[Vol. 98

Nishiyama, T., P. G. Wolf, M. Kugita, R. B. Sinclair, M. Sugita, C. Sugiura, T. Wakasugi, et al. 2004. Chloroplast phylogeny indicates that bryophytes are monophyletic. Molecular Biology and Evolution 21: 18131819. Nishiyama, T., T. Fujita. T. Shin-I, M. Seki, H. Nishide, I. Uchiyama, A. Kamiya, et al. 2003. Comparative genomics of Physcomitrella patens gametophytic transcriptome and Arabidopsis thaliana: Implication for land plant evolution. Proceedings of the National Academy of Sciences, USA 100: 80078012. Okano, Y., N. Aono, Y. Hiwatashi, T. Murata, T. Nishiyama, T. Ishikawa, M. Kubo, and M. Hasebe. 2009. A polycomb repressive complex 2 gene regulates apogamy and gives evolutionary insights into early land plant evolution. Proceedings of the National Academy of Sciences, USA 106: 1632116326. Pharo, E. J., D. B. Lindenmayer, and N. Taws. 2004. The effects of largescale fragmentation on bryophytes in temperate forests. Journal of Applied Ecology 41: 910921. Pharo, E. J., and C. E. Zartman. 2007. Bryophytes in a changing landscape: The hierarchical effects of habitat fragmentation on ecological and evolutionary processes. Biological Conservation 135: 315325. Philibert, H. 18841890. De limportance du pristome pour les afnits naturelles des mousses. Revue Bryologique 11: 4952, 6572. Etudes sur le pristome. Revue Bryologique 11: 8187; 12: 6777, 8185; 13: 1727, 8186; 14: 911, 8190; 15: 612, 2428, 3744, 5056, 6569, 9093; 16: 19, 3944, 6777; 17: 812, 2529, 3842. Pirozynski, K. A., and D. W. Malloch. 1975. The origin of land plants: A matter of mycotropism. Bio Systems 6: 153164. Pohjamo, M., H. Korpelainen, and N. Kalinauskaite. 2008. Restricted gene ow in the clonal hepatic Trichocolea tomentella in fragmented landscapes. Biological Conservation 141: 12041217. Poli, D. B., M. Jacobs, and T. J. Cooke. 2003. Auxin regulation of axial growth in bryophyte sporophytes: Its potential signicance for the evolution of early land plants. American Journal of Botany 90: 14051415. Pressel, S., M. I. Bidartondo, R. Ligrone, and J. G. Duckett. 2010. Fungal symbioses in bryophytes: New insights in the twenty rst century. Phytotaxa 9: 238253. Pringsheim, N. 1876. ber Sprossung der Moosfrchte. Monatsberichte der kniglich Preussischen. Akademie der Wissenschaften zu Berlin 1876: 425429. Qiu, Y.-L. 2008. Phylogeny and evolution of charophytic algae and land plants. Journal of Systematics and Evolution 46: 287306. Qiu, Y.-L., L. B. Li, B. Wang, Z. D. Chen, V. Knoop, M. Groth-Malonek, O. Dombrovska, et al. 2006. The deepest divergences in land plants inferred from phylogenomic evidence. Proceedings of the National Academy of Sciences, USA 103: 1551115516. Quodt, V., W. Faigl, H. Saedler, and T. Mnster. 2007. The MADSdomain protein PPM2 preferentially occurs in gametangia and sporophytes of the moss Physcomitrella patens. Gene 400: 2534. Ramaiya, M., M. G. Johnson, B. Shaw, J. Heinrichs, J. Hentschel, M. Von Konrat, P. G. Davison, and A. J. Shaw. 2010. Morphologically cryptic biological species within the liverwort, Frullania asagrayana. American Journal of Botany 97: 17071718. Raven, J. A. 2000. Land plant biochemistry. Philosophical Transactions of the Royal Society of London, B, Biological Sciences 355: 833846. Renzaglia, K. S. 1982. A comparative developmental investigation of the gametophyte generation in the Metzgeriales (Hepatophyta). Bryophytorum Bibliotheca 24: 1253. Renzaglia, K. S., R. C. Brown, B. E. Lemmon, J. G. Duckett, and R. Ligrone. 1994. The occurrence and phylogenetic signicance of monoplastidic meiosis in liverworts. Canadian Journal of Botany 72: 6572. Renzaglia, K. S., and J. G. Duckett. 1987. Spermatogenesis of Blasia pusilla, from antheridial initial through mature spermatozoid. Bryologist 90: 419449. Renzaglia, K. S., R. J. Duff, D. L. Nickrent, and D. J. Garbary. 2000. Vegetative and reproductive innovations of early land plants: Implications for a unied phylogeny. Philosophical Transactions of the Royal Society of London, B, Biological Sciences 355: 769793. Renzaglia, K. S., J. C. Villarreal, and R. J. Duff. 2009. New insights into morphology, anatomy, and systematics of hornworts. In B.

Gofnet and A. J. Shaw [eds.], Bryophyte biology, 2nd ed., 139171. Cambridge University Press, Cambridge, UK. Richardt, S., G. Timmerhaus, D. Lang, E. Qudeimat, L. G. Correa, R. Reski, S. A. Rensing, and W. Frank. 2010. Microarray analysis of the moss Physcomitrella patens reveals evolutionarily conserved transcriptional regulation of salt stress and abscisic acid signalling. Plant Molecular Biology 72: 2745. Ronce, O. 2007. How does it feel to be like a rolling stone? Ten questions about dispersal evolution. Annual Review of Ecology, Evolution, and Systematics 38: 231253. Rosenzweig, M. L. 1995. Species diversity in space and time. Cambridge University Press, Cambridge, UK. Roy, K., and E. E. Goldberg. 2007. Origination, extinction, and dispersal: Integrative models for understanding present-day diversity gradients. American Naturalist 170: s71s85. Sano, R., C. M. Jurez, B. Hass, K. Sakakibara, M. Ito, J. A. Banks, and M. Hasebe. 2005. KNOX homeobox genes potentially have similar function in both diploid unicellular and multicellular meristems, but not in haploid meristems. Evolution & Development 7: 6978. Sstad, S. M. 2005. Patterns and mechanisms of polyploid speciation in bryophytes. In F. T. Bakker, L. W. Chatrou, B. Gravendeel, and P. Pelser [eds.], Plant species-level systematics: New perspectives on pattern and process. Gantner Verlag, Ruggell, Liechtenstein. Sstad, S. M., K. I. Flatberg, and L. Hanssen. 2000. Origin, taxonomy and population structure of the allopolyploid peat moss Sphagnum majus. Plant Systematics and Evolution 225: 7384. Shaw, A. J. 2001. Biogeographic patterns and cryptic speciation in bryophytes. Journal of Biogeography 28: 253261. Shaw, A. J., C. J. Cox, and S. B. Boles. 2003a. Global patterns of peatmoss biodiversity. Molecular Ecology 12: 25532570. Shaw, A. J., C. J. Cox, W. R. Buck, N. Devos, A. M. Buchanan, L. Cave, R. Seppelt, et al. 2010. Newly resolved relationships in an early land plant lineage: Bryophyta class Sphagnopsida (peat mosses). American Journal of Botany 97: 15111531. Shaw, A. J., C. J. Cox, and B. Goffinet. 2005. Global patterns of moss diversity: Taxonomic and molecular inferences. Taxon 54: 337352. Shaw, A. J., and K. S. Renzaglia. 2004. Phylogeny and diversication of bryophytes. American Journal of Botany 91: 15571581. Shaw, J. 1986. Peristome structure in the Orthotrichaceae. Journal of the Hattori Botanical Laboratory 60: 119136. Shaw, J., and L. E. Anderson. 1988. Peristome development in mosses in relation to systematics and evolution. II. Tetraphis pellucida (Tetraphidaceae). American Journal of Botany 75: 10191032. Shaw, J., L. E. Anderson, and B. D. Mishler. 1987. Peristome development in mosses in relation to systematics and evolution. I. Diphyscium foliosum (Buxbaumiaceae). Memoirs of the New York Botanical Garden 45: 5570. Shaw, J., L. E. Anderson, and B. D. Mishler. 1989a. Peristome development in mosses in relation to systematics and evolution. III. Funaria hygrometrica, Bryum bicolor, and B. pseudocapillare. Systematic Botany 14: 2436. Shaw, J., L. E. Anderson, and B. D. Mishler. 1989b. Peristome development in mosses in relation to systematics and evolution. IV. Haplolepideae: Ditrichaceae and Dicranaceae. Bryologist 92: 314325. Shaw, J., C. J. Cox, S. B. Boles, and B. Goffinet. 2003b. Phylogenetic evidence for a rapid radiation of pleurocarpous mosses (Bryopsida). Evolution 57: 22262241. Shaw, J., and J. Rohrer. 1984. Endostomial architecture in diplolepideous mosses. Journal of the Hattori Botanical Laboratory 57: 4161. Singer, S. D., and N. W. Ashton. 2007. Revelation of ancestral roles of KNOX genes by a functional analysis of Physcomitrella homologues. Plant Cell Reports 26: 20392054. Singer, S. D., and N. W. Ashton. 2009. MADS about moss. Plant Signaling & Behavior 4: 111112. Smith, D. K., and P. G. Davison. 1993. Antheridia and sporophytes in Takakia ceratophylla (Mitt.) Grolle: Evidence for reclassication among the mosses. Journal of the Hattori Botanical Laboratory 73: 263271.

March 2011]

Shaw et al.Bryophyte diversity and evolution

369

Snll, T., J. Fogelqvist, P. J. Ribeiro Jr., and M. Lascoux. 2004. Spatial genetic structure in two congeneric epiphytes with different dispersal strategies analysed by three different methods. Molecular Ecology 13: 21092119. Snll, T., P. J. Ribeiro Jr., and H. Rydin. 2003. Spatial occurrence and colonizations in patch-tracking metapopulations: Local conditions versus dispersal. Oikos 103: 566578. Sderstrm, L., and T. Herben. 1997. Dynamics of bryophyte metapopulations. In R. E. Longton [ed.], Advances in bryology, vol. 6, Population studies, 205240. J. Cramer, Berlin, Germany. Soro, A., S. Sundberg, and H. Rydin. 1999. Species diversity, niche width and species associations in harvested and undisturbed bogs. Journal of Vegetation Science 10: 549560. Stoneburner, A., D. M. Lane, and L. E. Anderson. 1992. Spore dispersal distances in Atrichum angustatum (Polytrichaceae). Bryologist 95: 324328. Sundberg, S. 2002. Sporophyte production and spore dispersal phenology in Sphagnum: The importance of summer moisture and patch characteristics. Canadian Journal of Botany 80: 543556. Sundberg, S. 2005. Sporophyte size positively inuences short-range spore dispersal in Sphagnum, but what happens further away? Oikos 108: 115124. Sundberg, S. 2010a. Size matters for violent discharge height and settling speed of Sphagnum spores: Important attributes for dispersal potential. Annals of Botany 105: 291300. Sundberg, S. 2010b. The Sphagnum air-gun mechanism resurrected. New Phytologist 185: 886889. Sundberg, S., J. Hansson, and H. Rydin. 2006. Colonization of Sphagnum on land uplift islands in the Baltic Sea: Time, area, distance and life history. Journal of Biogeography 33: 14791491. Sundberg, S., and H. Rydin. 1998. Spore number in Sphagnum and its dependence on spore and capsule size. Journal of Bryology 20: 116. Sundberg, S., and H. Rydin. 2002. Habitat requirements for establishment of Sphagnum from spores. Journal of Ecology 90: 268278. Szvnyi, P., Zs. Hock, H. Korpelainen, and A. J. Shaw. 2009a. Spatial pattern of nucleotide polymorphism indicates molecular adaptation in the bryophyte Sphagnum mbriatum. Molecular Phylogenetics and Evolution 53: 277286. Szvnyi, P., Zs. Hock, J. Schneller, and Z. Tth. 2007. Multilocus dataset reveals demographic histories of two peat mosses in Europe. BMC Evolutionary Biology 7: 144. Szvnyi, P., Zs. Hock, E. Urmi, and J. J. Schneller. 2006. Contrasting phylogeographic patterns in Sphagnum mbriatum and S. squarrosum (Bryophyta, Sphagnopsida) in Europe. New Phytologist 172: 784794. Szvnyi, P., S. A. Rensing, D. Lang, G. A. Wray, and A. J. Shaw. 2010. Generation-biased gene expression in a bryophyte model system. Molecular Biology and Evolution . Szvnyi, P., M. Ricca, and A. J. Shaw. 2009b. Multiple paternity and sporophytic inbreeding depression in a dioicous moss species. Heredity 103: 394403. Szvnyi, P., S. Terracciano, M. Ricca, S. Giordano, and A. J. Shaw. 2008. Recent divergence, intercontinental dispersal and shared polymorphism are shaping the genetic structure of amphi-Atlantic peatmoss populations. Molecular Ecology 17: 53645377. Tackenberg, O. 2003. Modeling long-distance dispersal of plant diaspores by wind. Ecological Monographs 73: 173189. Tanabe, Y., M. Hasebe, H. Sekimoto, T. Nishiyama, M. Kitani, K. Henschel, T. Mnster, et al. 2005. Characterization of MADSbox genes in charophycean green algae and its implication for the evolution of MADS-box genes. Proceedings of the National Academy of Sciences, USA 102: 24362441. Tanahashi, T., N. Sumikawa, M. Kato, and M. Hasebe. 2005. Diversication of gene function: Homologs of the oral regulator FLO/ LFY control the rst zygotic cell division in the moss Physcomitrella patens. Development 132: 17271736.

Tangney, R. S., J. B. Wilson, and A. F. Mark. 1990. Bryophyte island biogeography: A study in Lake Manapouri, New Zealand. Oikos 59: 2126. Taylor, P. J., S. M. Eppley, and L. K. Jesson. 2007. Sporophytic inbreeding depression in mosses occurs in a species with separate sexes but not in a species with combined sexes. American Journal of Botany 94: 18531859. Taylor, T. N., H. Kerp, and H. Hass. 2005. Life history biology of early land plants: Deciphering the gametophyte phase. Proceedings of the National Academy of Sciences, USA 102: 58925897. Taylor, W. A., and P. K. Strother. 2009. Ultrastructure, morphology, and topology of Cambrian palynomorphs from the Lone Rock Formation, Wisconsin, USA. Review of Palaeobotany and Palynology 153: 296309. Turmel, M., C. Otis, and C. Lemieux. 2006. The chloroplast genome sequence of Chara vulgaris sheds new light into the closest green algal relatives of land plants. Molecular Biology and Evolution 23: 13241338. 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 35: 654663. Vanderpoorten, A., and B. Goffinet. 2009. Introduction to bryophytes. Cambridge University Press, Cambridge, UK. Vanderpoorten, A., S. R. Gradstein, M. A. Carine, and N. Devos. 2009. The ghosts of Gondwana and Laurasia in modern liverwort distributions. Biological Reviews of the Cambridge Philosophical Society . Van der Velde, M., and R. Bijlsma. 2003. Phylogeography of ve Polytrichum species within Europe. Biological Journal of the Linnean Society 78: 203213. Van der Velde, M., H. J. During, L. Van de Zande, and R. Bijlsma. 2001. The reproductive biology of Polytrichum formosum: Clonal structure and paternity revealed by microsatellites. Molecular Ecology 10: 24232434. Villarreal, J. C., D. C. Cargill, A. Hagborg, L. Sderstrm, and K. S. Renzaglia. 2010. A synthesis of hornwort diversity: Patterns, causes and future work. Phytotaxa 9: 150166. Vitt, D. H. 1984. Classication of the Bryopsida. In R. M. Schuster [ed.], New manual of bryology, vol. 2, 696759. Hattori Botanical Laboratory, Nichinan, Japan. Wiklund, K. 2002. Substratum preference, spore output and temporal variation in sporophyte production in the epixylic moss Buxbaumia viridis. Journal of Bryology 24: 187195. van Zanten, B. O. 1978. Experimental studies on trans-oceanic longrange dispersal of moss spores in the southern hemisphere. Journal of the Hattori Botanical Laboratory 44: 455482. van Zanten, B. O., and T. Pcs. 1981. Distribution and dispersal of bryophytes. In W. Schultze-Motel [ed.], Advances in bryology, vol. 1, 479562. J. Cramer, Berlin, Germany. Volkmar, U., and V. Knoop. 2010. Introducing intron locus cox1i624 for phylogenetic analyses in bryophytes: On the issue of Takakia as sister genus to all other extant mosses. Journal of Molecular Evolution 70: 506518. Zartman, C. E., S. F. McDaniel, and A. J. Shaw. 2006. Experimental habitat fragmentation increases linkage disequilibrium but does not affect genetic diversity or population structure in the Amazonian liverwort Radula accida. Molecular Ecology 15: 23052315. Zartman, C. E., and H. E. Nascimento. 2006. Are habitat-tracking metacommunities dispersal limited? Inferences from abundance occupancy patterns of epiphylls in Amazonian forest fragments. Biological Conservation 127: 4654. Zobell, O., W. Faigl, H. Saedler, and T. Mnster. 2010. MIKC* MADS-box proteins: Conserved regulators of the gametophytic generation of land plants. Molecular Biology and Evolution 27: 12011211.