Matt A. M. Renner

World checklist of hornworts and liverworts

Abstract A working checklist of accepted taxa worldwide is vital in achieving the goal of developing an online flora of all known plants by 2020 as part of the Global Strategy for Plant Conservation. We here present the first-ever worldwide checklist for liverworts (Marchantiophyta) and hornworts (Anthocerotophyta) that includes 7486 species in 398 genera representing 92 families from the two phyla. The checklist has far reaching implications and applications, including providing a valuable tool for taxonomists and systematists, analyzing phytogeographic and diversity patterns, aiding in the assessment of floristic and taxonomic knowledge, and identifying geographical gaps in our understanding of the global liverwort and hornwort flora. The checklist is derived from a working data set centralizing nomenclature, taxonomy and geography on a global scale. Prior to this effort a lack of centralization has been a major impediment for the study and analysis of species richness, conservation and systematic research at both regional and global scales. The success of this checklist, initiated in 2008, has been underpinned by its community approach involving taxonomic specialists working towards a consensus on taxonomy, nomenclature and distribution.

Molecular phylogeny of the leafy liverwort Lejeunea (Porellales): evidence for a neotropical origin, uneven distribution of sexual systems and insufficient taxonomy.

Background Lejeunea is a largely epiphytic, subcosmopolitan liverwort genus with a complex taxonomic history. Species circumscriptions and their relationships are subject to controversy; biogeographic history and diversification through time are largely unknown. Methodology and Results We employed sequences of two chloroplast regions (trnL-trnF, rbcL) and the nuclear ribosomal ITS region of 332 accessions to explore the phylogeny of the Harpalejeunea-Lejeunea-Microlejeunea complex. Lejeunea forms a well-supported clade that splits into two main lineages corresponding to L. subg. Lejeunea and L. subg. Crossotolejeunea. Neotropical accessions dominate early diverging lineages of both main clades of Lejeunea. This pattern suggests an origin in the Neotropics followed by several colonizations from the Neotropics into the Paleotropics and vice versa. Most Afro-Madagascan clades are related to Asian clades. Several temperate Lejeunea radiations were detected. Eighty two of the 91 investigated Lejeunea species could be identified to species level. Of these 82 species, 54 were represented by multiple accessions (25 para- or polyphyletic, 29 monophyletic). Twenty nine of the 36 investigated species of L. subg. Lejeunea were monoicous and 7 dioicous. Within L. subg. Crossotolejeunea, 15 of the 46 investigated species were monoicous and 31 dioicous. Some dioicous as well as some monoicous species have disjunct ranges. Conclusions/Significance We present the first global phylogeny of Lejeunea and the first example of a Neotropical origin of a Pantropical liverwort genus. Furthermore, we provide evidence for the Neotropics as a cradle of Lejeunea lineages and detect post-colonization radiations in Asia, Australasia, Afro-Madagascar and Europe. Dioicy/monoicy shifts are likely non-randomly distributed. The presented phylogeny points to the need of integrative taxonomical studies to clarify many Lejeunea binomials. Most importantly, it provides a framework for future studies on the diversification of this lineage in space and time, especially in the context of sexual systems in Lejeuneaceae.

Evolution of sexual systems, dispersal strategies and habitat selection in the liverwort genus Radula.

• Shifts in sexual systems are among the most common and important transitions in plants and are correlated with a suite of life-history traits. The evolution of sexual systems and their relationships to gametophyte size, sexual and asexual reproduction, and epiphytism are examined here in the liverwort genus Radula. • The sequence of trait acquisition and the phylogenetic correlations between those traits was investigated using comparative methods. • Shifts in sexual systems recurrently occurred from dioecy to monoecy within facultative epiphyte lineages. Production of specialized asexual gemmae was correlated to neither dioecy nor strict epiphytism. • The significant correlations among life-history traits related to sexual systems and habitat conditions suggest the existence of evolutionary trade-offs. Obligate epiphytes do not produce gemmae more frequently than facultative epiphytes and disperse by whole gametophyte fragments, presumably to avoid the sensitive protonemal stage in a habitat prone to rapid changes in moisture availability. As dispersal ranges correlate with diaspore size, this reinforces the notion that epiphytes experience strong dispersal limitations. Our results thus provide the evolutionary complement to metapopulation, metacommunity and experimental studies demonstrating trade-offs between dispersal distance, establishment ability, and life-history strategy, which may be central to the evolution of reproductive strategies in bryophytes.

Integrative taxonomy resolves the cryptic and pseudo-cryptic Radula buccinifera complex (Porellales, Jungermanniopsida), including two reinstated and five new species

Abstract Molecular data from three chloroplast markers resolve individuals attributable to Radula buccinifera in six lineages belonging to two subgenera, indicating the species is polyphyletic as currently circumscribed. All lineages are morphologically diagnosable, but one pair exhibits such morphological overlap that they can be considered cryptic. Molecular and morphological data justify the re-instatement of a broadly circumscribed ecologically variable R. strangulata, of R. mittenii, and the description of five new species. Two species Radula mittenii Steph. and R. notabilis sp. nov. are endemic to the Wet Tropics Bioregion of north-east Queensland, suggesting high diversity and high endemism might characterise the bryoflora of this relatively isolated wet-tropical region. Radula demissa sp. nov. is endemic to southern temperate Australasia, and like R. strangulata occurs on both sides of the Tasman Sea. Radula imposita sp. nov. is a twig and leaf epiphyte found in association with waterways in New South Wales and Queensland. Another species, R. pugioniformis sp. nov., has been confused with Radula buccinifera but was not included in the molecular phylogeny. Morphological data suggest it may belong to subg. Odontoradula. Radula buccinifera is endemic to Australia including Western Australia and Tasmania, and to date is known from south of the Clarence River on the north coast of New South Wales. Nested within R. buccinifera is a morphologically distinct plant from Norfolk Island described as R. anisotoma sp. nov. Radula australiana is resolved as monophyletic, sister to a species occurring in east coast Australian rainforests, and nesting among the R. buccinifera lineages with strong support. The molecular phylogeny suggests several long-distance dispersal events may have occurred. These include two east-west dispersal events from New Zealand to Tasmania and south-east Australia in R. strangulata, one east-west dispersal event from Tasmania to Western Australia in R. buccinifera, and at least one west-east dispersal from Australia to New Zealand in R. australiana. Another west-east dispersal event from Australia to Norfolk Island may have led to the budding speciation of R. anisotoma. In contrast, Radula demissa is phylogeographically subdivided into strongly supported clades either side of the Tasman Sea, suggesting long distance dispersal is infrequent in this species.

The Lejeunea tumida species group is positively polyphyletic (Lejeuneaceae: Jungermanniopsida)

A phylogeny based on nrITS1 and trnL-F sequences resolves the Lejeunea tumida species group polyphyletic with individuals belonging in two clades either side of the basal-most node within Lejeunea. It is impossible for the Lejeunea tumida species group to be more polyphyletic and still be attributed to the same genus under the existing generic classification. A simulation-based approach to testing the null hypothesis of group monophyly rejects this at the P < 0.01 level of significance. Bayesian tests find very strong support for polyphyly, given the data. The monophyly of L. tumida s.s.+L. colensoanais fully supported; however, althoughLejeunea tumida s.s.is nested within L. colensoana, this position is not supported. Both L. oracola and L. rhigophila are resolved as monophyletic. Whereas there is moderate support for the monophyly of L. rhigophila, there is no support for the monophyly of L. oracola. Neither is the monophyly of L. oracola+L. rhigophila supported in Bayesian or parsimony analysis.

Crown Group Lejeuneaceae and Pleurocarpous Mosses in Early Eocene (Ypresian) Indian Amber

Cambay amber originates from the warmest period of the Eocene, which is also well known for the appearance of early angiosperm-dominated megathermal forests. The humid climate of these forests may have triggered the evolution of epiphytic lineages of bryophytes; however, early Eocene fossils of bryophytes are rare. Here, we present evidence for lejeuneoid liverworts and pleurocarpous mosses in Cambay amber. The preserved morphology of the moss fossil is inconclusive for a detailed taxonomic treatment. The liverwort fossil is, however, distinctive; its zig-zagged stems, suberect complicate-bilobed leaves, large leaf lobules, and small, deeply bifid underleaves suggest a member of Lejeuneaceae subtribe Lejeuneinae (Harpalejeunea, Lejeunea, Microlejeunea). We tested alternative classification possibilities by conducting divergence time estimates based on DNA sequence variation of Lejeuneinae using the age of the fossil for corresponding age constraints. Consideration of the fossil as a stem group member of Microlejeunea or Lejeunea resulted in an Eocene to Late Cretaceous age of the Lejeuneinae crown group. This reconstruction is in good accordance with published divergence time estimates generated without the newly presented fossil evidence. Balancing available evidence, we describe the liverwort fossil as the extinct species Microlejeunea nyiahae, representing the oldest crown group fossil of Lejeuneaceae.

The Lejeunea tumida species group (Lejeuneaceae: Jungermanniopsida) in New Zealand

Plants attributed to Lejeunea tumida comprise a heterogeneous aggregate of four morphologically distinct species, each circumscribed by subtle yet significant differences in perianth morphology, oil bodies, lobule morphology and lobe ornamentation. Size and shape also have utility in delimiting species, despite morphological overlap. We employ geometric morphometric methods to quantify and communicate diagnostic differences in lobule shape. Two new species, Lejeunea oracola M.A.M.Renner and Lejeunea rhigophila M.A.M.Renner are described, and a previously described species of Taxilejeunea reinstated as a new combination, Lejeunea colensoana (Steph.) M.A.M.Renner. Descriptions and illustrations of these three species and Lejeunea tumida Mitt. are presented. All four species occur in New Zealand. Although L. tumida has been reported for New South Wales, Victoria, and Tasmania, the identities of Australian plants comprising these records are largely unresolved, and require further investigation.

Chapter Nine: Early Land Plants Today: Liverwort Species Diversity and the Relationship with Higher Taxonomy and Higher Plants

Abstract Liverworts (Marchantiophyta) form a conspicuous and important component in many terrestrial ecosystems throughout the world. Despite of their significance and abundance, studies of various aspects on global plant species richness and distribution patterns have almost exclusively focused on vascular plants. Yet, comprehensive studies of liverwort plant diversity have many implications and broad applications. We use a preliminary dataset that unites liverwort nomenclature, taxonomy, and geography based on some 60,000 records. Global maps are produced for the taxonomic ranks of species, genus, and family to provide a rapid guide of diversity across political units worldwide. The usefulness of higher level taxon analyses was investigated at the genus and family level to test the relationship with species richness. A reduced set of taxonomic ranks other than species has been proved to be useful for rapid and cost-effective assessment of biodiversity. We provide the first examination of how well this method performs for liverworts. Generic richness was slightly more accurately related to species richness than that of families, indicating surrogacy at this taxonomic level as a promising approach for the prediction of liverwort species richness. Finally, given the fact that vascular plant diversity and distribution patterns are often given high consideration in evaluating global networks of protected areas and biodiversity hotspots, we present a comparison of centers of species richness between liverworts and vascular plants. Several regions of high liverwort species richness lie outside the highest centers of vascular plant species richness. We conclude with ideas for future studies of the dataset, which has many exciting implications and applications for the study of liverwort distribution and diversity patterns.

By how much do we underestimate species diversity of liverworts using morphological evidence? An example from Australasian Plagiochila (Plagiochilaceae: Jungermanniopsida)

As a framework for revisionary study of the leafy liverwort Plagiochila in Australia, two methods for species delimitation on molecular sequence data, General Mixed Yule Coalescence model (GMYC) and Automatic Barcode Gap Discovery (ABGD) were applied to a dataset including 265 individuals from Australia, New Zealand, and the Pacific. Groups returned by GMYC and ABGD were incongruent in some lineages, and ABGD tended to lump groups. This may reflect underlying heterogeneity in the history of diversification within different lineages of Plagiochila. GMYC from trees calculated using three different molecular clocks were compared, in some lineages different primary species hypotheses were returned by analyses of trees estimated under different clock models, suggesting clock model selection should be a routine component of phylogeny reconstruction for tree-based species delimitation methods, such as GMYC. Our results suggest that a minimum of 71 Plagiochilaceae species occur in Australasia, 16 more than currently accepted for the region, comprising 8 undetermined species and 8 synonyms requiring reinstatement. Despite modern taxonomic investigation over a four decade period, (1) real diversity is 29% higher than currently recognized; and (2) 12 of 33, or 36%, of currently accepted and previously untested Australasian species have circumscription issues, including polyphyly, paraphyly, internal phylogenetic structure, or combinations of two or more of these issues. These both reflect the many challenges associated with grouping decisions based solely on morphological data in morphologically simple yet polymorphic plant lineages. Our results highlight again the critical need for combined molecular-morphological datasets as a basis for resolving robust species hypotheses in species-rich bryophyte lineages.

New records, replacements, reinstatements and four new species in the Radula parvitexta and R. ventricosa species groups (Jungermanniopsida) in Australia: cases of mistaken identity

Abstract. Various published hypotheses regarding circumscription and relationships of species within the Radula parvitexta and R. ventricosa species groups were tested using molecular data from three chloroplast markers. The phylogeny resolves five clades within the R. parvitexta species group in Australia, which proves polyphyletic across two subgenera, or three subgenera if R. madagascariensis is included. One clade represents an undescribed species, R. psychosis sp. nov., one corresponds to R. madagascariensis, a new record for Australia, the others to R. ratkowskiana, R. tasmanica and R. robinsonii. R. ratkowskiana is reinstated from synonymy of R. tasmanica, and R. parvitexta is placed into synonymy of R. robinsonii. A second new species belonging to the R. parvitexta species group, R. kilgourii sp. nov., is described; however, it was not included in the phylogeny. Three clades were resolved within the R. ventricosa species group in Australia, which is nested within subg. Metaradula. These clades corresponded to R. jovetiana, R. loriana, which is reinstated from synonymy of R. ventricosa, and two new species, namely, R. myriopoda sp. nov. and R. forficata sp. nov. R. ventricosa is excluded from the Australian flora, because all material is referrable to R. loriana. R. forficata and R. kilgourii had not been collected before the present study. R. myriopoda and R. jovetiana exhibit overlap in morphology of the sterile gametophyte and can be reliably separated only on characters associated with the perianth mouth. They can be considered semicryptic species, and would not have been recognised independent of fieldwork and molecular investigations conducted as part of the present study.