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


Meleshko, Olena; Martin, Michael D; Korneliussen, Thorfinn Sand; Schröck, Christian; Lamkowski, Paul; Schmutz, Jeremy; Healey, Adam; Piatkowski, Bryan T; Shaw, A Jonathan; Weston, David J; Flatberg, Kjell Ivar; Szövényi, Péter; Hassel, Kristian; Stenøien, Hans K (2021). Extensive Genome-Wide Phylogenetic Discordance Is Due to Incomplete Lineage Sorting and Not Ongoing Introgression in a Rapidly Radiated Bryophyte Genus. Molecular Biology and Evolution, 38(7):2750-2766.

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.

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.

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Item Type:Journal Article, refereed, original work
Communities & Collections:07 Faculty of Science > Department of Systematic and Evolutionary Botany
07 Faculty of Science > Zurich-Basel Plant Science Center
08 Research Priority Programs > Evolution in Action: From Genomes to Ecosystems
Dewey Decimal Classification:580 Plants (Botany)
Scopus Subject Areas:Life Sciences > Ecology, Evolution, Behavior and Systematics
Life Sciences > Molecular Biology
Life Sciences > Genetics
Uncontrolled Keywords:Genetics, Ecology, Evolution, Behavior and Systematics, Molecular Biology
Language:English
Date:25 June 2021
Deposited On:25 May 2021 14:46
Last Modified:26 Jan 2024 02:47
Publisher:Oxford University Press
ISSN:0737-4038
OA Status:Hybrid
Free access at:PubMed ID. An embargo period may apply.
Publisher DOI:https://doi.org/10.1093/molbev/msab063
PubMed ID:33681996
Project Information:
  • : FunderSNSF
  • : Grant ID310030_184826
  • : Project TitleUnravelling the genetic basis of the Hornwort-Cyanobacteria Symbiosis
  • : FunderSNSF
  • : Grant ID31003A_160004
  • : Project TitleTesting hypotheses on the evolutionary origin of the land plant sporophyte
  • : FunderSNSF
  • : Grant IDPZ00P3_131726
  • : Project TitleGene expression and the evolution of plant alternation of generations
  • Content: Published Version
  • Licence: Creative Commons: Attribution 4.0 International (CC BY 4.0)