Molecular Phylogenetic Reconstructions of the Marchantioid Liverwort Radiation

Abstract

Molecular phylogenies of the complex-thalloid liverworts (Marchantiales) were reconstructed using independent nuclear and plastid data sets to explore relative age, relationships, and character evolution in this ancient group. The sample includes 10 carpocephalate taxa and 24 acarpocephalate taxa (emphasizing Riccia) within Marchantiales sensu stricto. In addition, Monoclea, Sphaerocarpos, Riella, three Metzgeriales (Fossombronia, Pellia, and Blasia), the hornwort Anthoceros, four mosses, and outgroup Coleochaete are also sampled. Two nucleotide sequence alignments were used 1) partial nuclear-encoded Large Subunit rDNA (LSU rDNA) for all 48 taxa and 2) the plastid-encoded trnL-F region for the marchantioids and outgroup Blasia. Alignment-ambiguous regions of each alignment were culled. A combined matrix consisting of concatenated nuclear and plastid culled alignments was assembled for marchantioids and Blasia. The two alignments were utilized in four analyses: 1) nuclear LSU rDNA for all taxa, 2) nuclear LSU rDNA for marchantioids + Blasia, 3) plastid trnL-F region for marchantioids plus Blasia, and 4) combined nuclear and plastid data for marchantioids plus Blasia. Selected pairwise comparisons reveal significant rate heterogeneity in the nuclear LSU rDNA data; metzgerioid liverworts, hornworts and primitive mosses evolve significantly slower than other taxa relative to the outgroup Coleochaete. The LSU rDNA genes of some marchantioid taxa and sampled bryalean mosses are apparently evolving relatively fast. Rate heterogeneity is also documented within Marchantiales. Lunularia positions as the most basal of sampled Marchantiopsida; Sphaerocarpales, Marchantia, and Corsinia represent early diverging lines. A monophyletic Aytoniaceae, Cleveaceae, and Riccia are indicated. Topologies imply that extant acarpocephalate taxa are derived from carpocephalate forms. Monoclea positions well within Marchantiales sensu stricto. A well-supported long branch (Decay Index = 19) unites all sampled Marchantiopsida and isolates this clade from other liverworts and bryophytes. This long branch may suggest extensive extinction of proto- and eomarchantioid forms that led to modern taxa. A recurring theme in the topologies presented here is the unresolved marchantioid polytomy that follows well-supported basal nodes. A similar polytomy results from either independent data set and may correspond to a rapid radiation of marchantioid forms (e.g., Aytoniaceae, Cleveaceae, Targionia, Monoclea, and riccioids) coincident with extreme conditions and ecological reorganizations of the Permo-Triassic. The origin of Marchantiopsida probably occurred long before; amidst, perhaps, a series of long-extinct Blasia-like ancestors that colonized and innovated on any of various xeric surfaces (either cool or warm) that were available throughout embryophyte history in the Paleozoic.