Extensive Genome-Wide Phylogenetic Discordance Is Due to Incomplete Lineage Sorting and Not Ongoing Introgression in a Rapidly Radiated Bryophyte Genus.

The relative importance of introgression for diversification has long been a highly disputed topic in speciation research and remains an open question despite the great attention it has received over the past decade. Gene flow leaves traces in the genome similar to those created by incomplete lineage sorting (ILS), and identification and quantification of gene flow in the presence of ILS is challenging and requires knowledge about the true phylogenetic relationship among the species. We use whole nuclear, plastid, and organellar genomes from 12 species in the rapidly radiated, ecologically diverse, actively hybridizing genus of peatmoss (Sphagnum) to reconstruct the species phylogeny and quantify introgression using a suite of phylogenomic methods. We found extensive phylogenetic discordance among nuclear and organellar phylogenies, as well as across the nuclear genome and the nodes in the species tree, best explained by extensive ILS following the rapid radiation of the genus rather than by postspeciation introgression. Our analyses support the idea of ancient introgression among the ancestral lineages followed by ILS, whereas recent gene flow among the species is highly restricted despite widespread interspecific hybridization known in the group. Our results contribute to phylogenomic understanding of how speciation proceeds in rapidly radiated, actively hybridizing species groups, and demonstrate that employing a combination of diverse phylogenomic methods can facilitate untangling complex phylogenetic patterns created by ILS and introgression.

Linked Selection and Gene Density Shape Genome-Wide Patterns of Diversification in Peatmosses.

Genome evolution under speciation is poorly understood in nonmodel and nonvascular plants, such as bryophytes-the largest group of nonvascular land plants. Their genomes are structurally different from angiosperms and likely subjected to stronger linked selection pressure, which may have profound consequences on genome evolution in diversifying lineages, even more so when their genome architecture is conserved. We use the highly diverse, rapidly radiated group of peatmosses (Sphagnum) to characterize the processes affecting genome diversification in bryophytes. Using whole-genome sequencing data from populations of 12 species sampled at different phylogenetic and geographical scales, we describe high correlation of the genomic landscapes of differentiation, divergence, and diversity in Sphagnum. Coupled with evidence from the patterns of covariation among different measures of genetic diversity, phylogenetic discordance, and gene density, this provides strong support that peatmoss genome evolution has been shaped by the long-term effects of linked selection, constrained by distribution of selection targets in the genome. Thus, peatmosses join the growing number of animal and plant groups where functional features of the genome, such as gene density, and linked selection drive genome evolution along predetermined and highly similar routes in different species. Our findings demonstrate the great potential of bryophytes for studying the genomics of speciation and highlight the urgent need to expand the genomic resources in this remarkable group of plants.

Short stories from Sphagnum of rare species, taxonomy, and speciation.

Conserving species and their genetic variation are a global priority to safeguard evolutionary potential in a rapidly changing world. Species are fundamental units in research and nature management, but taxonomic work is increasingly undermined. Increasing knowledge on the species genetic diversity would aid in prioritizing conservation efforts. Sphagnum is a diverse, well-known bryophyte genus, which makes the genus suited to study speciation and cryptic variation. The species share specific characteristics and can be difficult to separate in the field. By combining molecular data with thorough morphological examination, new species have recently been discovered. Still, there are taxonomic uncertainties, even for species assessed on the IUCN Red List of threatened species. Here, we use molecular data to examine three rare species within the subgenus Acutifolia described based on morphological characters. All species have narrow distributions and limited dispersability. First, we confirm the genetic origin of S. skyense. Second, we show that S. venustum is a haploid species genetically distinct from morphologically similar species. Lastly, S. nitidulum was found to have a distinct haplotype, but cannot be genetically separated from other red Acutifolia species. We also found high genetic variation within red Acutifolia specimens, indicating the need of further morphological examination and possibly taxonomic revision. Until then, our results have shown that genetic data can aid in prioritizing targets of conservation efforts when taxonomy is unresolved. All three taxa should be further searched for by field biologists to increase knowledge about their distribution ranges.