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

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

Research output: Contribution to journalArticlepeer-review

64 Scopus citations

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.

Original languageEnglish
Pages (from-to)2750-2766
Number of pages17
JournalMolecular Biology and Evolution
Volume38
Issue number7
DOIs
StatePublished - Jul 1 2021

Funding

This study was supported by the Research Council of Norway (Project No. 250541/F20) to K.H., as well as by Swiss National Science Foundation (Grant Numbers 160004, 131726, and 184826), the EU's Horizon 2020 Research and Innovation Programme (PlantHUB No. 722338), the Georges and Antoine Claraz Foundation, the Forschungskredit and the University Research Priority Program "Evolution in Action" of the University of Zurich to P.S., the Research Council of Norway (Project No. 287327) to M.D.M., and by the Carlsberg Foundation Young Researcher Fellowship (CF19-0712) to T.S.K. We thank the Nature Conservation Departments of the provinces of Salzburg and Tyrol for issuing sampling permits, and the Genomics Core Facility (GCF) at NTNU University and the Functional Genomics Center Zurich for sequencing our libraries. The GCF is funded by the Faculty of Medicine and Health Sciences (NTNU) and the Central Norway Regional Health Authority. We thank the Department of Energy Joint Genome Institute for prepublication access to the Sphagnum angustifolium (formerly fallax) genome sequence. The work conducted by the US DOE Joint Genome Institute is supported by the Office of Science of the US Department of Energy under Contract Number DE-AC02- 05CH11231. Seydina I. Diop, Vanessa C. Bieker, and Marcin Gorny are gratefully acknowledged for assistance with bioinformatic processing of the data, and Tommy Prestø for assistance with depositing the collected accessions at the TRH Herbarium. We also thank Erik Boström and Narjes Yousefi for technical support in the molecular laboratory, and Andrew D. Foote for helpful comments during the progression of the study. Last but not least, we thank the editor and the two anonymous reviewers for their helpful comments on the manuscript.

FundersFunder number
Department of Energy Joint Genome Institute
EU's Horizon 2020 Research and Innovation Programme722338
Marcin Gorny
NTNU University
U.S. Department of EnergyDE-AC02- 05CH11231
Office of Science
Norges Teknisk-Naturvitenskapelige Universitet
Fakultet for medisin og helsevitenskap, Norges Teknisk-Naturvitenskapelige Universitet
Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung184826, 160004, 131726
CarlsbergfondetCF19-0712
Helse Midt-Norge
Norges Forskningsråd250541/F20
Universität Zürich287327
Functional Genomics Center Zurich
Georges and Antoine Claraz Foundation

    Keywords

    • incomplete lineage sorting
    • introgression
    • peatmoss
    • phylogenomics
    • rapid diversification
    • speciation

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