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

Olena Meleshko,Christian Schröck,Paul Lamkowski,Péter Szövényi,Thorfinn Sand Korneliussen,Jeremy Schmutz,A Jonathan Shaw,David J Weston,Kjell Ivar Flatberg,Kristian Hassel,Adam Healey,Hans K Stenøien,Bryan T Piatkowski,Michael D Martin

doi:10.1093/molbev/msab063

Abstract

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.

Highlights

After a long history of rejecting the plausibility of speciation with gene flow in sympatry, it is generally accepted that speciation does occur without complete geographical and reproductive isolation (Morjan and Rieseberg 2004; Sousa and Hey 2013; Ravinet et al 2017)
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 incomplete lineage sorting (ILS) and introgression
We found evidence for ancient introgression among the ancestral populations likely followed by ILS, whereas levels of postspeciation gene flow were surprisingly low

Summary

Introduction

After a long history of rejecting the plausibility of speciation with gene flow in sympatry, it is generally accepted that speciation does occur without complete geographical and reproductive isolation (Morjan and Rieseberg 2004; Sousa and Hey 2013; Ravinet et al 2017). Mounting evidence for postspeciation introgression between closely related species has shifted the discussion toward a debate of the relative importance of gene flow for speciation. How important is gene flow per se in speciation, in comparison with other evolutionary forces? Case studies show that gene exchange between closely related species can trigger adaptive radiation (Dasmahapatra et al 2012; Fontaine et al 2015), whereas selective processes are more important for the divergence of lineages into separate species (Ma et al 2018).

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Discussion

Conclusion