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Fulltext Geographical structure, narrow species ranges, and Cenozoic diversification in a pantropical clade of epiphyllous leafy liverworts

Bechteler J, Schäfer-Verwimp A, Lee GE, Feldberg K, Pérez-Escobar OA, Pócs T, et al.

Ecol Evol, 2017 01;7(2):638-653.
PMID: 28116059 DOI: 10.1002/ece3.2656

The evolutionary history and classification of epiphyllous cryptogams are still poorly known. Leptolejeunea is a largely epiphyllous pantropical liverwort genus with about 25 species characterized by deeply bilobed underleaves, elliptic to narrowly obovate leaf lobes, the presence of ocelli, and vegetative reproduction by cladia. Sequences of three chloroplast regions (rbcL, trnL-F, psbA) and the nuclear ribosomal ITS region were obtained for 66 accessions of Leptolejeunea and six outgroup species to explore the phylogeny, divergence times, and ancestral areas of this genus. The phylogeny was estimated using maximum-likelihood and Bayesian inference approaches, and divergence times were estimated with a Bayesian relaxed clock method. Leptolejeunea likely originated in Asia or the Neotropics within a time interval from the Early Eocene to the Late Cretaceous (67.9 Ma, 95% highest posterior density [HPD]: 47.9-93.7). Diversification of the crown group initiated in the Eocene or early Oligocene (38.4 Ma, 95% HPD: 27.2-52.6). Most species clades were established in the Miocene. Leptolejeunea epiphylla and L. schiffneri originated in Asia and colonized African islands during the Plio-Pleistocene. Accessions of supposedly pantropical species are placed in different main clades. Several monophyletic morphospecies exhibit considerable sequence variation related to a geographical pattern. The clear geographic structure of the Leptolejeunea crown group points to evolutionary processes including rare long-distance dispersal and subsequent speciation. Leptolejeunea may have benefitted from the large-scale distribution of humid tropical angiosperm forests in the Eocene.
Fulltext An ancient tropical origin, dispersals via land bridges and Miocene diversification explain the subcosmopolitan disjunctions of the liverwort genus Lejeunea

Lee GE, Condamine FL, Bechteler J, Pérez-Escobar OA, Scheben A, Schäfer-Verwimp A, et al.

Sci Rep, 2020 Aug 24;10(1):14123.
PMID: 32839508 DOI: 10.1038/s41598-020-71039-1

Understanding the biogeographical and diversification processes explaining current diversity patterns of subcosmopolitan-distributed groups is challenging. We aimed at disentangling the historical biogeography of the subcosmopolitan liverwort genus Lejeunea with estimation of ancestral areas of origin and testing if sexual system and palaeotemperature variations can be factors of diversification. We assembled a dense taxon sampling for 120 species sampled throughout the geographical distribution of the genus. Lejeunea diverged from its sister group after the Paleocene-Eocene boundary (52.2 Ma, 95% credibility intervals 50.1-54.2 Ma), and the initial diversification of the crown group occurred in the early to middle Eocene (44.5 Ma, 95% credibility intervals 38.5-50.8 Ma). The DEC model indicated that (1) Lejeunea likely originated in an area composed of the Neotropics and the Nearctic, (2) dispersals through terrestrial land bridges in the late Oligocene and Miocene allowed Lejeunea to colonize the Old World, (3) the Boreotropical forest covering the northern regions until the late Eocene did not facilitate Lejeunea dispersals, and (4) a single long-distance dispersal event was inferred between the Neotropics and Africa. Biogeographical and diversification analyses show the Miocene was an important period when Lejeunea diversified globally. We found slight support for higher diversification rates of species with both male and female reproductive organs on the same individual (monoicy), and a moderate positive influence of palaeotemperatures on diversification. Our study shows that an ancient origin associated with a dispersal history facilitated by terrestrial land bridges and not long-distance dispersals are likely to explain the subcosmopolitan distribution of Lejeunea. By enhancing the diversification rates, monoicy likely favoured the colonisations of new areas, especially in the Miocene that was a key epoch shaping the worldwide distribution.
Fulltext Crown Group Lejeuneaceae and Pleurocarpous Mosses in Early Eocene (Ypresian) Indian Amber

Heinrichs J, Scheben A, Bechteler J, Lee GE, Schäfer-Verwimp A, Hedenäs L, et al.

PLoS One, 2016;11(5):e0156301.
PMID: 27244582 DOI: 10.1371/journal.pone.0156301

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.
Comprehensive phylogenomic time tree of bryophytes reveals deep relationships and uncovers gene incongruences in the last 500 million years of diversification

Bechteler J, Peñaloza-Bojacá G, Bell D, Gordon Burleigh J, McDaniel SF, Christine Davis E, et al.

Am J Bot, 2023 Oct 04.
PMID: 37792319 DOI: 10.1002/ajb2.16249

PREMISE: Bryophytes form a major component of terrestrial plant biomass, structuring ecological communities in all biomes. Our understanding of the evolutionary history of hornworts, liverworts, and mosses has been significantly reshaped by inferences from molecular data, which have highlighted extensive homoplasy in various traits and repeated bursts of diversification. However, the timing of key events in the phylogeny, patterns, and processes of diversification across bryophytes remain unclear.
METHODS: Using the GoFlag probe set, we sequenced 405 exons representing 228 nuclear genes for 531 species from 52 of the 54 orders of bryophytes. We inferred the species phylogeny from gene tree analyses using concatenated and coalescence approaches, assessed gene conflict, and estimated the timing of divergences based on 29 fossil calibrations.
RESULTS: The phylogeny resolves many relationships across the bryophytes, enabling us to resurrect five liverwort orders and recognize three more and propose 10 new orders of mosses. Most orders originated in the Jurassic and diversified in the Cretaceous or later. The phylogenomic data also highlight topological conflict in parts of the tree, suggesting complex processes of diversification that cannot be adequately captured in a single gene-tree topology.
CONCLUSIONS: We sampled hundreds of loci across a broad phylogenetic spectrum spanning at least 450 Ma of evolution; these data resolved many of the critical nodes of the diversification of bryophytes. The data also highlight the need to explore the mechanisms underlying the phylogenetic ambiguity at specific nodes. The phylogenomic data provide an expandable framework toward reconstructing a comprehensive phylogeny of this important group of plants.