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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, bryo-
phytes 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 mor-
phological 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 conflicts, and the effi-
cacy 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 to be photosynthetic, dries, and senesces. The sporophytes of
history, marked by the colonization and diversification of many moss species mature over somewhat more than a year but
terrestrial organisms, including the ancestral lineages of do not continue to grow after spore production and are for the
extant embryophytes (Kenrick and Crane, 1997). As photo- most part essentially annual. Liverwort sporophytes are espe-
synthetic organisms adapted to the higher CO2 levels and cially short-lived and generally persist for weeks to months
diminished UV-B screening of emerging terrestrial habitats (from fertilization to senescence). The sporophytes of horn-
(Raven, 2000), a vast array of morphological innovations worts are potentially indeterminate in life span, but in nature
was developed (Renzaglia et al., 2000), new patterns of ge- they also appear to rarely persist for more than a year (Bisang,
nome structure and gene expression evolved (Kofuji et al., 2003). Although some bryophytes produce spores that develop
2003; Nishiyama et al., 2003; Tanabe et al., 2005), and novel into genetically determined male or female gametophytes
symbiotic relationships were established (Pirozynski and and are sometimes described as heterosporous, they are not
Malloch, 1975). The bryophytes, which are now important heterosporous in the sense of many vascular plants because the
components of virtually all terrestrial ecosystems, were male and female spores are produced by the same sporan-
among the earliest of land plants. gium rather than in different micro- and megasporangia. Bryo-
Traditionally, bryophytes include the mosses, liverworts, phyte species that form male and female spores that are
and hornworts. Together, these groups comprise some 15 000 differentiated in size are better described as anisosporous
20 000 species and as such, are, combined, more diverse than (Mogensen, 1981), but in most species with unisexual gameto-
the nonflowering vascular plants. The three bryophyte groups phytes the spores are indistinguishable.
share a similar life cycle in which the gametophyte is perennial Bryophyte diversity and evolution has been reviewed in
and dominant in terms of both size and longevity and the sporo- two recent books, an edited volume by Goffinet and Shaw
phyte is unbranched, monosporangiate, and completes its (2009) and a text by Vanderpoorten and Goffinet (2009).
entire development attached to the maternal gametophyte. In this brief review, we address (1) phylogenetic relationships
The sporophyte generation begins as a fertilized egg and even- among the three bryophyte phyla and inferences about the
tually produces spores via meiosis in a terminal sporangium, evolution of plant life cycles, (2) relationships among major
after which, especially in the mosses and liverworts, it ceases clades within the liverworts, mosses, and hornworts in rela-
tion to morphological diversity, and (3) reproductive processes
1 Manuscript received 22 August 2010; revision accepted 28 December that have significant impacts on bryophyte diversification.
2010. In the last context, we focus on reproductive biology and dis-
Acquisition of supporting data for this paper was funded by NSF grants persal because these processes determine the genetic structure
EF-0531730-002 to A.J.S. and DEB-0918998 to A.J.S. and B.S. of species, which in turn facilitate and modulate speciation.
2 Author for correspondence (e-mail: shaw@duke.edu); Department of
Living bryophytes, like early embryophytes, persist (and
Biology, Duke University, Durham, North Carolina, 27708 USA; fax:
01-919-660-7293
disperse) as long-lived gametophytes and rely on spores rather
3 Present address: Faculty of Biology, University of Freiburg, Haupt- than seeds for reproduction. For these reasons, evolutionary
strasse 1, D-79104 Freiburg, Germany processes in extant bryophytes provide a window into similar
processes among colonizing land plants hundreds of millions
doi:10.3732/ajb.1000316 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 and sporophytes from Devonian strata of the Rhynie Chert (ca.
THE EVOLUTION OF EMBRYOPHYTE LIFE CYCLES 410 Ma) suggest that there was a period in early land plant his-
tory when sporophyte and gametophyte generations were iso-
Phylogenetic relationships among early embryophyte morphic (Kenrick and Crane, 1997; Taylor et al., 2005). The
lineages It has been recognized for over a century (e.g., fossil evidence is thus consistent with a scenario in which plant
Pringsheim, 1876) that the green algae (Chlorophyta plus strep- life cycles may have followed a trajectory from haploid- to
tophyte algae) share significant structural and biochemical diploid-dominant via an isomorphic transitional stage.
features with land plants (bryophytes and tracheophytes; embryo- But what was the nature of the sporophyte generation in the
phytes). The green algae, however, are heterogeneous and in- common ancestors of liverworts, mosses, and hornworts? We
clude taxa in which one or the other or both generations are still do not know how complex the sporophyte was in the com-
multicellular, so inferences about the origin of the embryophyte mon ancestor of extant liverworts, mosses, or hornworts, nor
life cycle depend on which group of green algae is sister to the of subsequent ancestors prior to the origin of tracheophytes
embryophytes (Haig, 2008; Niklas and Kutschera, 2009). Evi- (Fig. 1). Stated differently, questions remain about the homol-
dence from ultrastructural, biochemical, and molecular data ogy of sporophytic structures in these groups. It is possible, for
supports the view that the charophycean green algae (including example, that the common ancestor of all embryophytes had a
the Charales, Coleochaetales, and other groups) are closely very simple, even if multicellular, sporophyte and that the sporo-
related to the embryophytes, and so their life cycles are infor- phytes of living bryophyte phyla, with more or less differenti-
mative about the ancestral condition in embryophytes. The ch- ated vegetative and sporangial tissues, represent independent
arophycean algae themselves include early-diverging unicellular evolutionary innovations. Conversely, there is paleobotanical
types such as Mesostigma viride Lauterborn. Phylogenetic evi- evidence that the common ancestor of tracheophytes was char-
dence supports close relationships between embryophytes and acterized by equally complex gametophyte and sporophyte gen-
several charophycean groups, the Zygnematales (Turmel et al., erations (i.e., an isomorphic alternation of generations), and it
2006), Coleochaetales (Graham et al., 1991), and Charales could be that complex sporophytes evolved early in embryo-
(Karol et al., 2001; Qiu, 2008; Qiu et al., 2006). The modern phyte evolution with parallel reduction in liverworts, mosses,
green algal group most closely related to embryophytes is un- and hornworts (Fig. 1). The history of plant life cycle evolution
clear at the present time (Becker and Marin, 2009). While it is probably lies somewhere between these extremes wherein
clear that in general multicellularity has evolved multiple times sporophytes of the bryophyte phyla represent independent in-
(i.e., among protistan groups), all candidate sister groups to the novations from ancestors of intermediate complexity, and the
embryophytes are characterized by a haplobiontic life cycle in degree of homology depends on the extent to which sporophyte
which the gametophyte is multicellular and dominant and the elaboration used a common genomic toolkit, vs. truly inde-
sporophyte generation is limited to a unicellular zygote. Thus, pendent evolution from scratch. The sporophytes of mosses, liv-
the multicellular sporophyte characteristic of all embryophytes erworts, and hornworts are very different, despite the fact that in
appears to have evolved by interpolation of mitotic cell divisions all three groups they are unbranched and monosporangiate.
prior to meiosis. This scenario in which the sporophytes of land Those of liverworts, for example, lack stomata and have no spe-
plants represent an evolutionary innovation corresponds to the cialized photosynthetic tissues (although epidermal cells contain
so-called antithetic theory concerning the evolution of the embryo- chloroplasts at early stages of development). The setae of liver-
phyte alternation of generations (Bower, 1890). Nevertheless, worts are very simple in structure and highly ephemeral (usually
significant questions remain about the nature of the sporophyte lasting only days). The sporophytes of mosses typically persist
in the early ancestors of extant embryophytes (see below). for longer periods, have greater anatomical complexity, and the
Multiple lines of evidence suggest that the three bryophyte sporangium usually has specialized photosynthetic tissues and
clades (liverworts: Marchantiophyta; mosses: Bryophyta; and stomata. The linear sporophytes of hornworts lack differentiated
hornworts: Anthocerophyta) form a paraphyletic grade basal to setae but have photosynthetic tissues and stomata. Sporangial
the tracheophytes, although some data, including both morpho- dehiscence also differs among the three groups, and the sporo-
logical (Garbary et al., 1993) and molecular (Nishiyama et al., phytes develop in radically different ways; by diffuse cell divi-
2004), suggest that either the mosses and liverworts form a sions in liverworts, apical and intercalary growth in mosses, and
monophyletic group, or all three groups form a single clade. a basal intercalary meristem in hornworts. Water-conducting
Qiu et al. (2006) and Qiu (2008) have shown that the distri- cells occur in the sporophyte of mosses but not liverworts
bution of mitochondrial group II introns across groups, in (Ligrone et al., 2000). Thus, despite (presumably plesiotypic)
addition to considerable sequence data, strongly supports the similarities, it is conceivable that the multicellular sporophytes
paraphyly hypothesis, and that the branching order at the base of liverworts, mosses, and hornworts evolved largely in parallel
of the embryophyte clade is liverworts, then mosses, then horn- from ancestors with less complex sporophytes.
worts, and then the tracheophyte crown group. This view serves
as a well-supported working hypothesis for early land plant re- Gene expression and the evolution of plant life cycles The
lationships (Fig. 1). most intriguing aspect of the alternating sporophyte and game-
Spore and tubular remains with apparent liverwort affinities tophyte generations of land plants is their extreme morphologi-
from the Ordovician Period some 470 million years ago (Ma) cal and functional divergence despite having shared genomes.
suggest that at least some of the earliest land plants may have Although the two generations differ in their ploidal level, this
had a heteromorphic haploid-dominant alternation of genera- difference alone does not lead to the development of different
tions like modern liverworts (reviewed by Gensel, 2008; Niklas structures. That other factors are involved is well shown by
and Kutschera, 2009). Spore diads that appear to be intermedi- early evidence of apogamy and apospory (Farlow, 1874;
ate between those of extant Coleochaete species and embryo- Pringsheim, 1876) in which abrupt switches between genera-
phytes are known from the Cambrian Period (Taylor and tion-typical morphologies and function are not associated
Strother, 2009). Later, morphologically similar axial gametophytes 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 figure. 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 dif-
ferentiated but multicellular sporophytes. Other possible scenarios, including various reversals, are of course also possible.

Phenotypic and functional divergences between the two generations must have been accompanied by radical changes in
generations clearly arise by differential usage of the same ge- regulatory mechanisms enabling large-scale changes in function
netic material. and morphology of both generations. Genomic mechanisms un-
Accumulating evidence suggests that morphological and derlying sporophyte development could have evolved de novo or
functional transitions between sporophyte and gametophyte are by the partial or full transfer of preformed gametophytic pro-
achieved by drastic reprogramming of gene expression patterns grams to the sporophyte generation (Nishiyama et al., 2003;
through generation-specific transcription factors (reviewed by Dolan, 2009; Niklas and Kutschera, 2009).
Singer and Ashton, 2007; Langdale, 2008; Dolan, 2009). The Studies investigating the effect of major regulatory gene ho-
evolutionary origin of diplobiontic life cycles from a purely hap- mologs of Arabidopsis thaliana in the model moss Physcomitrella
lobiontic life cycle required the evolution of regulatory mecha- patens are consistent with the transfer of gametophytic develop-
nisms governing developmental and physiological processes of mental programs to the sporophyte generation. An impressive
the new generation, the multicellular sporophyte. Similarly, the example is provided by ROOT HAIR DEFECTIVE 6 (RHD6)-
transition from a haploid- to diploid-dominant alternation of 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 Monitoring transcriptional changes associated with the
Physcomitrella patens (Menand et al., 2007). Here a complete gametophytesporophyte transition could help to understand
regulatory toolkit appears to have been recruited from the game- how generation-specific morphologies and functions are
tophyte for similar functions in sporophytes. Genes and genetic achieved by the reorganization of gene regulatory networks.
networks involved in the development of reproductive structures Moreover, comparative analysis of generation-biased gene ex-
across land plants appear to have followed a similar evolutionary pression across land plants can provide critical insights into the
path. MADS box genes are preferentially expressed in gametan- origin of embryophytes and the evolution of plant life cycles on
gia and in the basal part of the moss sporophyte. Furthermore, a genome-wide scale. Toward this end, we are currently inves-
their defect leads to abnormalities related to the development of tigating genome-wide, generation-biased gene expression pat-
reproductive structures in mosses (Quodt et al., 2007; Zobell terns in Funaria hygrometrica (a close relative of the model,
et al., 2010; reviewed in Singer and Ashton, 2009). In Arabidop- Physcomitrella patens) using next-generation sequencing of
sis, MADS box genes have similar functions and expression pat- mRNA and conducting comparative analysis of generation-
terns as key regulators of the reproductive phase, with expression biased gene expression across land plants (Szvnyi et al.,
restricted to the formation of reproductive structures (Coen and 2010). In a comparison of expression profiles from the gameto-
Meyerowitz, 1991). Similar expression patterns and functions phytes and attached isogenic sporophytes derived from intrag-
suggest that MADS box genes are conserved across land plants ametophytic selfing, genes in Funaria fell into three natural
and that gametophyte developmental programs were recruited to groups. (1) Genes with generation-specific expression; (2)
the sporophyte to perform similar functions. those with generation-biased expression; and (3) those with
Regulatory genes and networks underlying critical adapta- similar expression in both generations. From the 558 differ-
tions to the terrestrial environment may have first appeared in entially expressed genes, similar numbers were differentially
the dominant gametophyte generation and later transferred as expressed toward the two generations; there were 277 gameto-
the sporophyte was elaborated. Comparative analyses of desic- phyte- and 281 sporophyte-characteristic transcripts (both gen-
cation and salt tolerance across land plants have revealed con- eration-specific [group 1] and generation-biased [group 2]
served regulatory networks acting in the moss gametophyte and genes). Overall, ca. 70% and 68% of the generation-character-
angiosperm sporophyte, providing further evidence for the ge- istic genes fell into the biased category.
nomic transfer of gametophytic programs to the sporophyte Comparative analyses of generation-biased gene expression
(Khandelwal et al., 2010; Richardt et al., 2010). in A. thaliana and F. hygrometrica shed light on crucial ques-
Comparative analyses of regulatory genes expressed mainly tions related to the origin and evolution of land plants and are
in the sporophyte generation of Arabidopsis thaliana and Phy- briefly summarized here (Szvnyi et al., 2010). Our findings
scomitrella patens shed light on regulatory mechanisms that show that a large proportion of genes is expressed in both the
likely evolved de novo during the course of land plant evolution. gametophyte and sporophyte generation in Funaria. In particu-
Class I KNOX genes are expressed only in the sporophyte gen- lar, we found that the proportion of transcripts with generation-
eration of mosses, ferns, and angiosperms, and in the latter two biased gene expression (2.5% gametophyte, 2.5%, sporophyte)
groups, they are important in the development and maintenance is lower than in Arabidopsis. Furthermore, the similar propor-
of the shoot apical meristem (Hay and Tsiantis, 2009). In Phy- tion of sporophyte- and gametophyte-biased genes suggests
scomitrella patens, they are expressed in the developing sporo- less gene expression specialization between generations in the
phyte, and their defect leads to the abortion of the sporophyte, bryophyte system compared to angiosperms, where the distri-
but they cause no detectable abnormalities in gametophytes bution of generation-specific gene products is unequal (~5%
(Sano et al., 2005; Singer and Ashton, 2007). Another example and ~25% in gametophytes and sporophytes, respectively). The
is provided by LEAFY/FLORICAULA genes that have an impor- extensive overlap and weak specialization in gene expression
tant role in the formation of the floral meristem in angiosperms between the two generations is in agreement with the origin of
(Ng and Yanofsky, 2000). LEAFY homologs in the moss Phy- alternation of generations from an algal ancestor with a purely
scomitrella patens are key regulators of the sporophytic stage by haplobiontic life cycle. Our data suggest that extensive sharing
regulating the first division of the zygote. Although these genes in gene expression between generations may have been the rule
are expressed in both generations, they have no detectable effect rather than the exception in earliest land plants.
on the development of gametophytes in Physcomitrella patens We compared expression patterns between Funaria gameto-
(Tanahashi et al., 2005). Auxin-regulated axis development also phytes and Arabidopsis sporophytes, as well as between sporo-
appears to have evolved de novo in connection with the origin of phytes in the two model systems. Our analyses show that there
the sporophyte generation. Polar auxin transport is only present is limited conservation of generation-biased gene expression
in the sporophytes of bryophytes and angiosperms (Poli et al., between the moss and angiosperm, suggesting extensive inter-
2003; Fujita et al., 2008; Fujita and Hasebe, 2009). Finally, generational transfer of genetic networks. Furthermore, exten-
genes in the Prc2 complex (FIE, CLF) of Arabidopsis thaliana sive overlap in gene expression between bryophyte gametophyte
and their moss homologs prevent parthenogenetic formation of and angiosperm sporophyte generations implies that their mor-
sporophytic tissues, and this role appears to be conserved across phological and functional similarity is not superficial. It relies
land plants (Mosquna et al.., 2009; Okano et al., 2009). Although on the shared usage of a common set of orthologous genes, in-
studies on the evolution of developmental programs across basal dicating that multiple gene networks of the sporophyte gen-
and derived groups of land plants has significantly increased eration may have been acquired from the gametophyte by
during the last 10 years, available information is still fragmen- intergenerational transfer.
tary and is focused on relatively few developmental genes with We found poor gene expression conservation between the
major effects in angiosperms. The proportions of regulatory sporophyte generations of Arabidopsis and Funaria, suggesting
genes and gene networks acquired by sporophytes via functional that angiosperm and bryophyte sporophytes diverged in an
transfer from gametophytes, vs. de novo evolution in the em- early stage of sporophyte evolution, with subsequent parallel
bryophyte sporophyte, are poorly known. evolution of many important gene networks characterizing the
356 American Journal of Botany [Vol. 98

sporophytes of extant groups. Nevertheless, the core set of (Fig. 2). The group is relatively small, with a total of ca. 18
sporophyte-expressed transcripts mainly consists of genes species (Crandall-Stotler et al., 2009). Interestingly, the seven
critical for terrestrial life (enhanced osmotic regulation, stress, species of Haplomitrium are highly divergent at the molecular
desiccation and UV tolerance, transporters, and intercellular level, whereas Treubia and Apotreubia are very uniform be-
communication via hormones). Therefore, biological processes tween species. Because this group contains both leafy and thal-
underlying molecular adaptation to terrestrial life may have al- lose forms, it is difficult to reconstruct the ancestral state of
ready been used by early sporophytes. These adaptations may gametophyte growth form in liverworts from phylogenetic to-
have contributed to the successful evolutionary diversification pology alone.
of the sporophytic generation in the terrestrial environment. Within the sister group to the Haplomitriopsida (i.e., all other
Our data do show that a significant proportion of preferen- liverworts), the complex thalloids are sister to the simple thal-
tially sporophyte-expressed transcription factors in the model loids plus the leaf clades. The genera Blasia and Cavicularia
moss have orthologs in A. thaliana known to function in the have been controversial because they share gametophyte anat-
shoot apical meristem and in development of reproductive omy, rhizoid structure, and sporophyte anatomy with the simple
structures. This similarity in control mechanisms suggests that thalloid groups, but monoplastidic meiosis, gametophyte apical
in spite of considerable morphological and developmental di- cell morphology, and spermatozoid structure with the complex
vergence, similar basic regulatory networks are likely to be in- thalloids (Renzaglia, 1982; Renzaglia and Duckett, 1987;
volved in growth and reproductive tissue development in the Renzaglia et al., 1994). Molecular phylogenetic analyses place
moss and angiosperm sporophyte generation. Moreover, the Blasia within the complex thalloid clade, sister to mainstream
presence of orthologous transcription factors with putatively complex thalloids (Fig. 2). The more or less simple thalloid
shared functions in the developmental processes of both repro- Sphaerocarpales clade (not explicitly shown in Fig. 2) is nested
ductive and vegetative sporophytic tissues/organs implies that within the complex thalloid clade. It thus appears that anatomi-
both domains may have already been present in the common cally complex thalli might be derived within the complex thal-
ancestors sporophyte. Overall, our data suggests that the com- loid clade (based on the simple structure of Blasia and its sister
mon ancestor may have possessed a morphologically simple group relationship to the complex thalloids). Subsequent reduc-
sporophyte nevertheless adapted to terrestrial life and possibly tion is a theme within the more derived complex thalloid groups
with differentiated vegetative and reproductive tissues (possi- (Crandall-Stotler et al., 2009), and the possibility that Blasia is
bly corresponding roughly to the A-A-A sequence of ancestral simplified from a common complex thalloid ancestor for all
sporophytes in Fig. 1). Marchantiopsida also cannot be eliminated.
The simple thalloid liverworts form a paraphyletic grade with
the Metzgeriidae sister to leafy liverworts (Fig. 2). Included
PHYLOGENY AND DIVERSITY OF among the Metzgeriidae is the leafy genus Pleurozia (Davis,
LIVERWORTS, MOSSES, AND HORNWORTS 2004; He-Nygren et al., 2004). This placement was one of the
biggest early surprises from molecular analyses of liverwort phy-
Huge advances have been made during the last 10 years in logeny because Pleurozia has a gametophyte axis with lateral
understanding phylogenetic relationships within the liverwort, leaves and had always been classified among the leafy liverworts.
moss, and hornwort clades. An exhaustive review of such Recent morphological information about gametophyte symme-
results is beyond the scope of this essay, but we provide an try, apical cell structure, and rhizome morphology have revealed
overview of broad patterns in the context of understanding bry- features shared with the simple thalloids (Crandall-Stotler et al.,
ophyte diversity. 2009). The Pelliidae is sister to the Metzgeriidae plus the leafy
clades (Fig. 2). The two clades of simple thalloids differ in origin
Liverwort phylogeny and evolution (Marchantiophyta) and position of antheridia, branching, and other subtle features of
Phylogenetic studies of liverworts have been progressing at a the gametophytes, but both are morphologically heterogenous.
rapid rate in recent years, in part because of U. S. National Sci- Two major sister clades of leafy liverworts are resolved re-
ence Foundation support of the Assembling the Tree of Life peatedly with different data sets (Davis, 2004; Frey and Stech,
program (http://www.nsf.gov/funding/pgm_summ.jsp?pims_ 2005; Heinrichs et al., 2005, 2007; Forrest et al., 2006;
id=5129). Phylogenetic results were recently summarized by He-Nygrn et al., 2004): the Porellales and Jungermanniales
Crandall-Stotler et al. (2009), along with an updated classifica- (Heinrichs et al., 2005). The Porellales include ca. 1500 species
tion for the phylum. and are characterized by endosporic germination, exogenous
The liverworts have traditionally been divided according to lateral branches, complicate-bilobed succubous lateral leaves
gametophyte growth form: complex thalloids wherein the thal- with ventral lobules, clustered rhizoids, and a lack of fungal
lus typically has well-differentiated photosynthetic and storage endosymbionts, among other features (reviewed in Pressel
tissues, with dorsal pores bounded by specialized cells (not sto- et al., 2010). This clade is especially diverse in the tropics, and
mata); simple thalloids that lack significant tissue differentia- the tiny plants frequently occur on the leaves of vascular plants;
tion; and the leafy liverworts, typically with two rows of lateral almost all species are epiphytic.
leaves and a row of ventral amphigastria (often lacking). Sev- The Jungermanniales include ca. 3000 species, one third
eral smaller groups (e.g., Haplomitrium, Blasia) fall outside to one half of all liverwort species, and occupy a broad range
this simple classification of gametophyte body architecture and of habitats. They can have incubous or succubous lateral leaves
have been phylogenetically enigmatic. Phylogenetic analyses (but lack ventral water sacs) although complicate-bilobed
based on nucleotide sequences have generally supported the leaves occur in a few groups (e.g., Scapaniaceae), ventral or
major groups, with some refinements and surprises. The Haplo- lateral branches, nonclustered rhizoids, and they have asso-
mitriopsida (three genera) are consistently resolved as sister to ciations with endophytic Ascomycota and Basidiomycota
the rest of liverworts and include both leafy (Haplomitrium) (Pressel et al., 2010). In contrast to the Porellales, species with
and more or less thalloid forms (Treubia and Apotreubia) 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 flotoviana; (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 surround the mouth of the capsule (sporangium) has been primary
the Lophocoleaceae, Lepidoziaceae, and Plagiochilaceae (and in higher-level classifications of mosses (Philibert, 18841890;
others), the suborder Lophocoleineae (Crandall-Stotler et al., Fleischer, 19041923; Vitt, 1984; Crosby, 1980). In that regard,
2009) is sister to the Cephaloziineae plus Jungermaniinae peristomes are to mosses as flowers and fruits are to angiosperms.
(Fig. 2). Each of these suborders is characterized by a combina- Before Philiberts work on comparative peristome morphology,
tion of gametophyte developmental and morphological charac- gametophyte growth form was emphasized in 19th century taxo-
ters, and the grouping of families largely correspond to previous nomic treatments (e.g., Mller, 18481851). Although basic per-
classifications (not withstanding various refinements beyond istome types do characterize major clades within the mosses,
the scope of this summary). recent phylogenetic analyses at the familial and shallower levels
In addition to the two major clades of leafy liverworts (Porella- have frequently shown that gametophyte characters appear to
les and Jungermanniales), a third group, the Ptilidiales, has been track relationships and that sporophytes, including their peristo-
consistently resolved in phylogenetic analyses, but its relationships mial details, can be highly homoplasious. Not surprisingly,
are still unresolved (Fig. 2). Different analyses have resolved this molecular data suggest that both gametophyte and sporophyte
group alternatively as sister either to the Porellales or to all other features should be considered and that any a priori weighting of
leafy liverworts. Additional molecular and morphological data are traits from one generation or the other for phylogenetic inferences
needed to address this critical issue in leafy liverwort phylogeny. may be misleading. Mosses (and to a lesser extent, liverworts and
hornworts) are unique among land plants in that both the gameto-
Moss phylogeny and evolution (Bryophyta) Since the turn phyte and sporophyte generation have sufficient morphological
of the 19th century, morphology of the peristome teeth that variability and complexity to be phylogenetically informative.
358 American Journal of Botany [Vol. 98

Most phylogenetic analyses based on sequences from multiple groups within the Bryopsida, after Oedipodium, are charac-
loci suggest that Takakia plus the Sphagnopsida form a clade terized by nematodontous peristomes, which are formed from
sister to other mosses. Takakia and the Sphagnopsida share little whole dead (and empty) cells in four or more concentric lay-
morphologically, and Goffinet et al. (2001), Cox et al. (2004), ers of amphithecium. The amphithecium and inner endothe-
and Shaw et al. (2010) suggest that the apparent sister-group re- cium are embryonic layers differentiated at an early stage of
lationship between them may reflect phylogenetic artifact. Nev- sporophyte ontogeny, and all peristomes are formed from
ertheless, gene sequences from all three genomes repeatedly amphithecial tissue. Highly divergent nematodontous peris-
resolve them as a clade (Newton et al., 2000; Nickrent et al., tomes characterize the Polytrichopsida, Tetraphidopsida, and
2000; Beckert et al., 2001; Cox et al., 2004; Qiu et al., 2006; Qiu, Buxbaumiiidae (Bryopsida) (Fig. 3). Interestingly, Bell and
2008; Shaw et al., 2010). Neither group has a peristome. Hyvnen (2008) resolved the eperistomate genus Alophozia as
The Andreaeopsida and Andreaeobryopsida lack peristomes, sister to the rest of the Polytrichaceae and then a clade with the
as do Takakiopsida and Sphagnopsida; the peristomate mosses genera Lyellia and Bartramiopsis, also eperistomate, as sister to
are demonstrably monophyletic. One of the unexpected results the remaining taxa in the family. On this basis, they suggested
of moss phylogenetic analyses is that the eperistomate species, that the eperistomate condition is plesiotypic in the Poly-
Oedipodium griffitheanum (Oedipodiopsida), is consistently re- trichaceae and that the polytrichaceous nematodontous peris-
solved as sister to all the peristomate mosses (Fig. 3) (Newton tome may have evolved independently of other moss peristome
et al., 2000; Magombo, 2003; Cox et al., 2004). Whether Oedi- teeth. The alternative, at least one loss of the peristome and then
podium primitively lacks a peristome, or lost it, cannot be deter- one regain, is possible though perhaps less likely. The four
mined by phylogenetic topology alone; in the future, genome and massive nematodontous peristome teeth of the Tetraphidaceae
transcriptome data might resolve that question. Early-diverging (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 morphol-
ogy in each clade. Not all sister-group relationships shown here are established with certainty, but these patterns appear to represent the consensus view. Phyloge-
netic 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 griffithianum; (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 pro-
vided 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 walls are aligned at maturity). Peristomial formulae can be sur-
derived arthrodontous mosses (Shaw and Anderson, 1988). mised from mature peristomes from the patterns of wall rem-
Volkmar and Knoop (2010) recently resolved the Polytrichaceae nants on the teeth (Shaw and Rohrer, 1984; Figs. 4, 5).
and Tetraphidaceae as sister groups within a clade that is in turn It appears that although mosses with haplolepideous peristome
sister to remaining mosses (in contrast to the topology shown in teeth form a monophyletic group, they are nested within the
Fig. 3). Future work will determine whether this relationship is diplolepideous clade probably sister to the group with
supported by additional data. diplolepideous alternative peristomes (Fig. 3). Diplolepideous
The Buxbaumiidae are characterized by yet another distinctive peristomes therefore define a paraphyletic group. The genus
type of peristome which, unfortunately, has not been subjected to Timmia has generally been classified among mosses with
developmental studies. It appears to be intermediate between diplolepideous-alternate peristomes although the structure of the
nemtatondous and arthrodontous types. The three genera cur- endostome in Timmia is unique, without clearly defined segments
rently classified in the Diphysciaceae were generally included (Fig. 5G, H), and it is therefore impossible to assess whether seg-
previously in the Buxbaumiaceae (e.g., Vitt, 1984), but peristome ments would be opposite or alternate with regard to the exostome
structure and development (Shaw et al., 1987), nucleotide se- teeth (which are typically diplolepideous). Molecular data indicate
quences (Cox et al., 2004; Magombo, 2003), and genomic char- that Timmia occupies a critical position sister to the haplolepideous
acters (Goffinet et al., 2005) converge on the conclusion that this plus diplolepideous-opposite clade. Phylogenetic relationships
group belongs to a clade characterized by arthrodontous peris- among Timmia species were described by Budke and Goffinet
tome structure (Fig. 3). Arthrodontous peristomes in general are (2006) and peristome development by Budke et al. (2007).
formed from the innermost three concentric layers of amphithe- All of the early-diverging lineages of Bryopsida (a few vari-
cial cells, from inside outward, the inner, primary, and outer per- ants notwithstanding) have acrocarpous gametophytes wherein
istomial layers (IPL, PPL, and OPL, respectively). Development the archegonia are formed terminally on the main stems; acro-
of these layers is remarkably regular, with alternating anticlinal carps are typically characterized by sparsely or unbranched
and periclinal divisions (Evans and Hooker, 1913; Shaw and stems and grow upright (Fig. 3). Pleurocarpous Bryopsida, in
Anderson, 1988; Shaw et al., 1987, 1989a, b). The OPL, for ex- contrast, have archegonia borne on short lateral branches such
ample, consistently has 32 cells around the capsule circumfer- that sporophytes occur laterally along the gametophyte stems.
ence at maturity and the PPL has 16. It is the IPL that varies most, Much attention has been devoted to resolving which group of
and that variation pertains to both the numbers of cells in the acrocarps are sister to the pleurocarps, and general answers
layer and to the positions of anticlinal IPL walls relative to anti- have been obtained although the specific sister-group has not
clinal walls in the next outer layer, the PPL. been identified (Bell and Newton, 2004, 2007; Bell et al., 2007).
Arthrodontous peristomes are generally considered to com- The terminology of gametophyte growth forms is complex (La
prise three basic types: haplolepideous, diplolepideous-oppo- Farge-England, 1996) but what might be called the true or
site, and diplolepideous-alternate. Haplolepideous peristomes core pleurocarps comprise four orders (Hypnodendrales, Pty-
are typically formed from periclinal walls in the inner peristo- chomniales, Hookeriales, and Hypnales; Goffinet et al., 2009),
mial layer (IPL) and primary peristomial layer (PPL), whereas and each appears to represent a monophyletic group (Bell et al.,
diplolepideous peristomes form from walls derived from all 2007). Phylogenetic relationships among family level clades
three layers (IPL, PPL, OPL). Haplolepideous peristomes typi- within the pleurocarps have been recalcitrant, likely because
cally consist of a single ring of 16 teeth, but diplolepideous these groups appear to have undergone a relatively recent and
peristomes often have two rings, the inner endostome (from ad- rapid radiation (Shaw et al., 2003b).
jacent periclinal IPL and PPL cell walls) and the outer exos-
tome (from PPL and OPL cell walls). In diplolepideous Phylogenetic diversity among major moss cladesAlthough
peristomes, the inner endostomial teeth (often referred to as diversity is most often measured in terms of species richness,
segments) may be positioned opposite the exostome teeth or so-called phylogenetic diversity (PD) (Faith, 1994) provides a
alternate with them. Haplolepideous peristomes form from IPL complementary metric that takes into account the evolutionary
and PPL cell walls and are therefore homologous in position to distances separating taxa. The rationale for considering PD is
the endostomes of diplolepideous peristomes. The name hap- straightforward and logical; two geographic areas or clades
lolepideous comes from the fact that the outer surface of each may have the same numbers of species, but can still differ im-
tooth is formed from a single column of periclinal cell wall portantly in diversity if the species in one group (or area) are
remnants whereas diplolepideous exostome teeth have two col- highly divergent whereas species in the other group are closely
umns of cell wall plates on the outer surface (Figs. 4, 5). related. Phylogenetic diversity may be a good predictor of
In addition to differences among peristome types in which feature diversity including morphological disparity and eco-
cell layers contribute to the formation of teeth, they also differ logical/functional heterogeneity. Two groups or clades with
in sequences of cell divisions during capsule development similar numbers of species may differ in PD for a number of
(Shaw and Anderson, 1988; Shaw et al., 1987, 1989a, b), and reasons. A trivial reason is bad taxonomy; if a group is over-
consequently the arrangement of cells at maturity (although split there can be more species than predicted by the level
only the walls persist as teeth). The peristomial formula of PD it contains. More significantly, low PD despite high
(Edwards, 1984) has been used to describe in shorthand the numbers of good species may reflect a recent radiation.
numbers and arrangement of cells in the IPL, PPL, and OPL, by Alternatively, clades may contain high PD relative to the num-
convention in 1/8 of the capsule circumference (corresponding ber of species because of extinction, or because of increased
to two teeth). Haplolepideous peristomes are characterized by a rates of molecular evolution relative to speciation. Although
4 : 2 : 3 formula, diplolepideous-opposite peristomes 4 : 2 : 4a the relationship between PD and species richness cannot
(where the a indicates that all anticlinal walls in the IPL and unambiguously reveal the underlying evolutionary processes,
PPL are aligned), and diplolepideous-alternate peristomes comparisons between biodiversity metrics can be useful for
4 : 2 : 2-14z (the z indicating that no anticlinal IPL and PPL 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 peristo-
mial 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 pub- because of in-progress research (J. C. Villarreal, University of
lished for bryopsid mosses and for peatmosses in the genus Connecticut, unpublished data).
Sphagnum (Cox et al., 2010; Shaw et al., 2003a, respectively).
If there is a linear relationship between PD and taxic diversity, Latitudinal gradients in bryophyte diversityA trend of in-
all groups fall along the diagonal of a two-way plot (Fig. 6). In creasing species diversity toward the tropics is nearly universal in
the bryopsid (peristomate) mosses, it is clear that haplolepideous plants and animals (Rosenzweig, 1995), but this issue has been
clade and Hookeriales (a largely tropical clade of pleurocar- somewhat controversial with regard to bryophytes. So-called al-
pous taxa) contain higher PD than predicted by the number of pha diversity, species richness within areas, is often comparable
genera, whereas the Hypnales (a largely temperate clade of in temperate and tropical regions (Shaw et al., 2005; Hedens,
pleurocarpous taxa) contain lower than expected PD. The latter 2007). Shaw et al. (2005) found a weak trend of increasing alpha
appears to reflect the sudden radiation of hypnalian pleurocarps diversity in moss floras of the Americas, but no detectable trend
and quantifies the small distances separating genera. The globally. They suggested that the tropics might nevertheless con-
diplolepideous-alternate clade, which includes all the pleuro- tain higher species richness overall because of regional turnover
carpous (and many acrocarpous) mosses, has about as much PD in species occurrence and indeed Hedens (2007) found that beta
as predicted by the level of taxic (generic) diversity. diversity (among regions) is higher in pleurocarpous mosses
In the genus Sphagnum (peatmosses), taxic diversity (species within the tropics than in temperate regions. In particular, pleuro-
numbers) suggests that the neotropics comprise a hotspot of carpous tropical moss floras are more differentiated among con-
diversity, but PD estimates show no such pattern (Table 1). In tinents than are temperate moss floras, where a significant
fact, there is as much or more phylogenetic diversity in the peat- percentage of species have circumpolar distributions. In general,
mosses of boreal regions than in the tropics and southern hemi- endemism is far lower in bryophytes than in seed plants, presum-
sphere combined (Shaw et al., 2003a), and this pattern holds for ably because of dispersal of tiny spores (Vanderpoorten et al.,
both plastid and nuclear DNA sequences (Table 1). There ap- 2009). Studies of dispersal in bryophytes, by spores and other
pears to be no difference in phylogenetic diversity between New means (e.g., asexual propagules), are critical to understanding
World and Old World, in contrast to the high numbers of species biogeographic and biodiversity patterns, as well as evolutionary
attributed to South America. The incongruence between geo- processes at more local scales.
graphic patterns in PD and taxic diversity may reflect recent ra-
diations of Sphagnum in South America such that morphologically
distinct species are closely related phylogenetically. POPULATION PROCESSES AND BRYOPHYTE
DIVERSIFICATION
Hornwort phylogeny and evolution (Anthocerophyta) The
hornworts include ca. 14 genera and 200240 species world- Reproductive biology and evolution in bryophyte popula-
wide (Villarreal et al., 2010). All hornworts have thalloid game- tions Evolutionary study of bryophytes necessitates rethink-
tophytes that harbor endosymbiotic cyanobacteria in the genus ing some of the most general and fundamental concepts in
Nostoc. Despite their relatively limited species diversity, the biology, including self, parentage, and fitness. The bryo-
hornworts are of particular phylogenetic interest because they phyte life cycle is comparable in many ways to that of seed-free
appear to comprise the sister group to tracheophytes (Qiu et al., tracheophytes such as ferns, including the existence of free-
2006). Relationships within the hornworts have recently been living gametophytes, the potential for true (intragametophytic)
resolved based on multilocus sequence data; these studies have self-fertilization, mitotic production of gametes by gameto-
resulted in drastically new insights into hornwort evolution, but phytes, and spore reproduction. But the bryophyte life cycle
species-level relationships/taxonomy is much in need of work also has features that are unique. Importantly, these include the
(Duff et al., 2007). production of more than one sporophyte on a single gameto-
The genus Leiosporoceros has been unambiguously resolved phyte, multiple paternity of those sporophytes, and, because of
as sister to all other hornworts (Duff et al., 2007; Villarreal these characteristics, the potential for sexual conflicts due to
et al., 2010). The genus lacks RNA editing of the rbcL transcript, competing interests of maternal and paternal gametophyte ge-
its chloroplasts lack pyrenoids (present in most other hornworts nomes in sporophytes.
but no other embryophytes), the spores are smooth and bean- Although seed plant biologists use the term self-fertiliza-
shaped, schizogenous cavities occur only in older thalli, and the tion for mating between gametophytes produced by the same
gametophytes contain Nostoc endosymbionts in longitudinally sporophyte, the term is a misnomer because gametophytes in
oriented canals that elongate as the thallus grows rather than in these plants are genetically distinct individuals produced by
discrete, spherical colonies (Renzaglia et al., 2009). Some of meiotic recombination. Application of the term self-fertilization
the species diversity in hornworts appears to be related to geog- represents baggage from a diploid-biased view of the world; the
raphy, and several of the traditional genera are nonmonophyl- sporophyte is viewed as the self and gametophytes are
etic (Villarreal et al., 2010). Additional resolution of geographic seen simply as part of the reproductive apparatus of those
and phylogenetic patterns can be expected in the coming years sporophytes. Intragametophytic selfing 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) Pleurozi-
opsis 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

Table 1. 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.

Region Combined nrDNA cpDNA

Boreal 48 49 47
Non-Boreal 44 47 40
Old World 64 62 68
New World 62 67 55
Fig. 6. Relationship between phylogenetic diversity (PD) and num-
bers of genera within selected clades of bryopsid mosses, as percentages of
total diversity within the Bryophyta class Bryopsida.
in contrast, parent one to many sporophytes. Because each spo-
rophyte typically produces hundreds of thousands to millions of
homozygous sporophyte in one generation (mutations aside) spores, fitness differences among gametophytes are amplified
and is functionally equivalent to asexual reproduction. A dip- by variation in mating success.
loid individual, be it an oak tree or human, has parents generally Because most bryophytes have haploid gametophytes and
considered to be the diploid individuals of the previous genera- diploid sporophytes (although polyploidy is not uncommon;
tion that mated to form a diploid zygote. Sstad 2005), paternity determination for sporophytes is rela-
In bryophytes, what is the self, and who are the parents of that tively straightforward. Using microsatellite-based genotyping
self? Because the gametophyte is the perennial, free-living plant of maternal gametophytes and their attached sporophytes, van
in nature, the self is generally viewed as that gametophyte. The der Velde et al. (2001) showed that proximity of male clones
parents of that gametophyte might be considered the sporophyte to females was the dominant factor determining mating suc-
from which it was produced meiotically (in which case it has cess in a population of Polytrichum formosum, although male
only one parent), or more appropriately, the parents of a free- clone size (presumably correlated with gamete production)
living gametophyte are the gametophytes that mated to produce was also a significant factor. It would be interesting to know
a sporophyte, and through that sporophyte the offspring are pro- whether larger male clones are simply older or have higher
duced. The sporophyte is simply part of the reproductive appa- growth rates and/or competitive abilities (which would sug-
ratus of the gametophyte (which is in fact no more correct than gest sexual selection is operating). Approximately 98% of
the reverse, critiqued already). A chicken is just an eggs way of sporophytes were fathered by an identifiable male clone grow-
reproducing itself. The fitness of a gametophyte is the number ing within 5 m of the mother. Individual gametophyte geno-
of next-generation gametophytes it produces (through the inter- types formed clones ranging from less than 10 cm2 to over 1
mediate sporophyte generation); conversely, the fitness of the m2, and each of three female clones bore at least 2535 sporo-
sporophyte is the number of next-generation sporophytes it pro- phytes that were sampled for paternity analysis. One to three
duces through mating of its gametophyte offspring. The parents male gametophytes fathered the sporophytes attached to each
of a sporophyte are the gametophytes that mated to produce it. of the females.
Thus, identifying parentage for a diploid sporophyte (polyploidy Sexual conflicts appear to be a fact of life in both plants (Haig
ignored for simplicity) means identifying the actual gametes and Wilczek, 2006) and animals, including humans (Goetz and
that effected zygote formation. This identification is theoreti- Shackelford, 2009). The basic prerequisite for sexual conflict is
cally possible in seed plants and seed-free tracheophytes, but multiple paternity of diploid offspring parented by a single fe-
much more difficult than in bryophytes because the gameto- male. When multiple sporophytes are borne by a single maternal
phyte generation in bryophytes is macroscopic and readily sam- gametophyte, maternal and paternal genomes in those sporo-
pled from natural populations. It is an important and unique phytes have competing and sometimes contradictory interests.
feature of the bryophyte life cycle that the reproductive success The maternal gametophyte is best served by spreading resources
of a single gametophyte (the number of sporophytes it parents) across all sporophytes she supports because they all carry the
can be a quantitative trait. In all other groups of plants (with very same maternal genome. When different sporophytes borne by a
rare exceptions), a single gametophyte either succeeds in par- female gametophyte have different (gametophyte) fathers, it is
enting one sporophyte, or it does not. Bryophyte gametophytes, 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 poten- persistence of species in a metapopulation landscape (Herben
tial for conflicts between maternal and paternal genomes. et al., 1991; Longton, 1997; Hassel and Sderstrm, 1999,
Multiple paternity of sporophytes borne by individual female 2005; Sundberg and Rydin, 2002).
gametophytes was almost universal in a population of the moss
Sphagnum lescurii (Szvnyi et al., 2009b). Indeed, some indi- Regional- and continental-scale dispersalAs with many
vidual female gametophytes bore sporophytes fathered by as previous studies of bryophyte genetic structure based on
many as 15 different males. Males in the population mated isozymes, more recent work using DNA fingerprinting meth-
much more faithfully with one or a limited number of females. ods and sequences have shown that genetic architecture is
Sporophyte size (which is correlated with spore number in Sphag- highly species- and context-dependent (Korpelainen et al.,
num; Sundberg and Rydin, 1998) is correlated with heterozygos- 2005). Nevertheless, a general pattern is emerging in which lo-
ity, suggesting that inbreeding depression (conversely, heterosis) cal and regional dispersal appears to be quite effective in many
occurs in this species. Inbreeding depression has otherwise or most species, at least in those that produce spores regularly
been documented in the dioicous moss Ceratodon purpureus, (Snll et al., 2004; Zartman and Nasciemento, 2006; Zartman
but not in the monoicous species Funaria hygrometrica (Taylor et al., 2006). Analyses of island and mainland populations of
et al., 2007). In Sphagnum, sporophytes lack a seta and are in- Hylocomium splendens showed no detectable pattern of isola-
stead raised on pseudopodia of (maternal) gametophyte origin, tion by distance, indicating effective dispersal over hundreds
and highly heterozygous sporophytes of S. lescurii were more of kilometers (Cronberg et al., 1997; Cronberg, 2002, 2004).
likely to be raised on pseudopodia than less heterozygous Other recent studies using highly polymorphic markers (e.g.,
sporophytes. This raises the intriguing possibility that either microsatellites, AFLP, ISSR) show that dispersal is sufficient
female gametophytes are able to differentially provision sporo- even at continental scales to genetically homogenize plants
phytes of varying quality or that highly heterozygous sporo- (van der Velde and Bijlsma, 2003; Cronberg, 2002; Grundmann
phytes are better at capturing resources from the mother, et al., 2007, 2008; Vanderpoorten et al., 2008). An absence or
although additional work is needed to eliminate other possible near absence of linkage disequilibrium within the liverwort
explanations (Szvnyi et al., 2009b). Frullania asagrayana across a large portion of eastern North
If these patterns indicate conflicts between maternal and pa- America indicates both extensive dispersal and a level of sex-
ternal genomes in sporophytes, genomic imprinting is to be ual recombination that approaches panmixia (Ramaiya et al.,
expected with regard to sporophyte gene expression (Haig and 2010). It should be noted, on the other hand, that few bryo-
Wilczek, 2006). By turning off expression of the paternal phyte species are ubiquitous at regional let alone global
genome, conflicts between maternal and paternal interests can scales, and clearly, successful dispersal and establishment are
be avoided. Expression of parental alleles in moss sporophytes limited.
is a fertile area for future research. Ecological data also indicate effective dispersal within many
bryophyte species across landscape scales. Species richness on
Bryophyte dispersal Dispersal is a critically important life islands is generally unrelated to distance of islands from the
history process determining a species current distribution; past, mainland at spatial scales spanning some 40100 km (Tangney
present, and future changes in range; and the standing genetic et al., 1990; Nakanishi, 2001; Sundberg et al., 2006). Similarly,
structure of its populations. Dispersal is also fundamental to comparisons of species composition on newly established sub-
metapopulation dynamics, community assembly, responses to strates with that of local and regional species pools indicate ef-
habitat fragmentation and climate change, latitudinal biodiver- fective dispersal spanning several tens of kilometers for most
sity gradients, as well as to the existence, location, and conser- colonizing bryophyte species (Soro et al., 1999; Miller and
vation status of global biodiversity hotspots (Kokko and McDaniel, 2004; Hutsemkers et al., 2008). Moreover, species
Lpez-Sepulcre, 2006; Roy and Goldberg, 2007; Grundmann composition of isolated island-like substrates may not be ex-
et al., 2008). The genetic consequences of dispersal fundamen- plained by relative abundances of potential source species in
tally determine the tempo and mode of diversification among their immediate surroundings, suggesting that recruitment by
populations, metapopulation systems, and deeper clades. LDD is frequent and significant in most sexually reproducing
Effective long-distance dispersal (LDD) can only be achieved bryophyte species (Hylander, 2009).
if high numbers of propagules with appropriate environmental Although efficient LDD is certainly an ongoing and detect-
tolerances, size, and establishment properties are produced able process in most bryophyte species it remains to be seen
(van Zanten 1976, 1978; van Zanten and Pcs, 1981; Herben whether it is efficient enough to completely balance the effects
and Sderstrm, 1992; Hassel and Sderstrm, 1999). Bryo- of spatial and temporal barriers. Habitat fragmentation affects
phyte spores appear to fulfill these conditions. Individual moss species composition and richness of bryophyte communities
capsules typically produce tens of thousands and sometimes up despite effective regional-scale dispersal (Pharo et al., 2004;
to millions of spores, and annual spore production can exceed 10 Zartman and Nascimento, 2006; Pharo and Zartman, 2007;
million from just 1 m2 (Longton and Schuster, 1984; Longton Pohjamo et al., 2008). These effects are likely due to the fact
1997; Sderstrm and Herben, 1997; Wiklund, 2002; Sundberg, that dispersal efficacy of a significant proportion of the species
2005). Although most spores are deposited near the source cannot balance the temporal and spatial extent of habitat
(within meters), a significant number travel longer distances fragmentation. Metapopulation studies indicate that spatial and
(Stoneburner et al., 1992; Miles and Longton, 1992; Sundberg, temporal turnover rates of habitat patches may be higher than
2005). The spores of many species can withstand long periods can be effectively balanced by dispersal (Snll et al., 2003;
of desiccation, high levels of UV radiation, and temperature ex- Lbel et al., 2006). Dispersal limitation of bryophytes may
tremes (van Zanten, 1976, 1978; van Zanten and Pcs, 1981). affect their persistence even on small temporal and spatial
Although establishment probability of spores under natural scales when habitat dynamics are rapid.
conditions is low (on the order of 103 to 104), both ecological Analyses of multiple moss species within Europe have re-
and theoretical studies indicate that it is sufficient to enable the vealed 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 have repeatedly resolved African and South American liver-
with recolonization of the continent from two Pleistocene refugia wort species as sister taxa, demonstrating recurrent dispersal
(Cronberg, 1998; van der Velde and Bijlsma, 2003; Grundmann between continents. Only a few recent studies have applied mo-
et al., 2007, 2008; Szvnyi et al., 2006, 2007). The fact that lecular dating to explicitly test whether patterns are best ex-
spatial structuring of genetic lineages is still recognizable sug- plained by vicariance or long-distance dispersal, and the latter
gests the possibility of adaptive divergence between these re- has generally been supported as the most likely explanation
gional population systems, effectively reducing or eliminating (e.g., McDaniel and Shaw, 2003; Heinrichs et al., 2007; Devos
gene flow between them. Indeed, Szvnyi et al. (2009a) found and Vanderpoorten, 2009; Aigoin et al., 2009). In general, phy-
evidence of nonneutral differentiation in the GapC (glyceralde- logenetic analyses indicate that intercontinental dispersal has
hyde 3-phosphate dehydrogenase) gene between the southern occurred repeatedly during bryophyte diversification, but is not
and northern groups in Sphagnum fimbriatum. so rampant that allopatric differentiation is precluded.

Intercontinental dispersalMany, possibly most, bryophyte


species occur on more than one continent. Earlier isozyme anal- PROSPECTUS
yses rarely revealed genetic differentiation between conspecific
populations on different continents, at least in temperate and We identify several areas where research on bryophyte di-
boreal species. DNA-based markers have more frequently doc- versity is poised to make significant progress in the coming
umented differentiation between intercontinentally disjunct years toward a better understanding of evolution in the earliest
populations (Hanssen et al., 2000; Sstad et al., 2000; Szvnyi lineages of embryophytes. It is important to state that floristic
et al., 2008; Vanderpoorten et al., 2008). Few studies have tried and monographic studies provide the foundation for all other
to explicitly distinguish shared polymorphism that reflects re- efforts by defining the units of evolutionary change (species
tention of ancestral variation from ongoing gene flow. Szvnyi and deeper clades), and their phylogenetic relationships to one
et al. (2008), however, found that shared polymorphism between another. And it is equally important to note that without curated
European and North American populations of four Sphagnum herbarium collections and robust informatic tools for efficiently
species was attributable to both ongoing gene flow and retained extracting information from them, taxonomic efforts are much
polymorphism. Divergence in all four species appeared to re- reduced in value.
flect relatively recent Pleistocene vicariance with retention of The outstanding phylogenetic issue in moss systematics per-
polymorphism attributable to low rates of drift in large effective tains to relationships among pleurocarpous groups. Because the
populations. While that study did also evidence intercontinental pleurocarpous mosses are relatively uniform at the molecular
gene flow, the rate was insufficient to prevent (statistically) sig- level, resolution of relationships will likely require data from
nificant, albeit limited differentiation. many genes and not from 10 or even 15; genomic resources will
Recent data are insufficient to make predictions about disper- have to be tapped to identify 25 or more loci. Because almost
sal processes and their wide-ranging consequences (Ronce, half of moss species diversity is in the pleurocarps, this en-
2007). Studies by Sundberg (2002, 2005, 2010a, b) have made deavor is well worth the effort.
steps toward these goals by providing a detailed description of Studies of dispersal and establishment in bryophyte populations
the spore dispersal curve in bryophytes and by estimating mul- provide a window into biogeographic processes in early (pre-seed)
tiple key parameters of the dispersal process. The joint applica- land plants. The overall picture from bryophytes includes effective
tion of mechanistic spore dispersal models (Tackenberg, 2003) dispersal at regional scales with significant, though not unlimited,
with the empirically estimated parameters will open up the way connectivity among populations, and at least occasional interconti-
for quantitative predictions about the efficacy and consequences nental movements. Intercontinental migration, even within extant
of LDD in bryophytes. species, is certainly more common than in seed plants. Because the
life cycles, mating patterns, and dispersal mechanisms of early
Dispersal detected at phylogenetic scalesTo what extent land plants such as bryophytes differ from those in the more recent
does effective long-distance dispersal impact long-term phylo- seed plants, predominant patterns of population structure have
genetic processes in bryophytes? It was early recognized that likely evolved through time and bryophytes provide insight into
most bryophyte species and almost all genera have interconti- some of the evolutionary processes of early embryophytes.
nental geographic distributions, and until recently vicariance The application of genome and especially transcriptome se-
was the preferred explanation because many distributions were quencing to understand the evolution of plant life cycles is one
interpretable by fragmentation of ancient Gondwanan, Laurasian, of the most exciting avenues for research in the next few years.
or Pangean ranges (e.g., Crum, 1972). Morphologically cryptic We now have the unprecedented ability to investigate differen-
genetic differentiation has been documented in a number of tial gene expression in gametophytes and sporophytes and,
widespread species (Shaw, 2001; Heinrichs et al., 2009), and thereby, the evolution of multicellular sporophytes in plants.
phylogenetic analyses of some groups have revealed allopatric Transcriptomics also provides powerful new tools for addressing
monophyletic groups that turn out to differ in morphological fundamental questions in bryophyte reproductive biology and
features as well (e.g., the so-called Frullania tamarsci com- evolution, including changes in gene expression associated
plex: Heinrichs et al., 2010). Recent meta-analyses suggest with speciation, genomic imprinting, and sexual conflicts as de-
that the geographic distributions of multiple liverwort genera terminants of reproductive processes and with gene expression
around the globe may be explained by continental drift events in relation to environmental heterogeneity and climate change.
(Vanderpoorten et al., 2009). On the other hand, an increasing Molecular techniques have been enthusiastically applied to
number of phylogenetic studies indicate that LDD appears to be deep phylogenetic problems in bryophytes and other plants, and
responsible for many intercontinental disjunctions previously we hope that in the future, old biosystematic issues that fall at
interpreted as ancient vicariance events (reviewed in Frahm, the interface of population genetics and systematics will be in-
2008; Heinrichs et al., 2009). Phylogenetic analyses, for example, creasingly addressed using genomic resources in bryophytes.
366 American Journal of Botany [Vol. 98

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