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.

doi:10.1093/molbev/msab063

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

Journal Article · Tue Mar 02 23:00:00 EST 2021 · Molecular Biology and Evolution (Online)

DOI:https://doi.org/10.1093/molbev/msab063· OSTI ID:1815542

^[1]; Martin, Michael D. ^[2]; Korneliussen, Thorfinn Sand ^[3]; Schröck, Christian ^[4]; Lamkowski, Paul ^[5]; Schmutz, Jeremy ^[6]; Healey, Adam ^[7]; ^[8]; Shaw, A. Jonathan ^[9]; Weston, David J. ^[10]; Flatberg, Kjell Ivar ^[2]; Szövényi, Péter ^[11]; Hassel, Kristian ^[2]; Stenøien, Hans K. ^[2]

Norwegian Univ. of Science and Technology, Trondheim (Norway). NTNU Univ. Museum. Dept. of Natural History; OSTI
Norwegian Univ. of Science and Technology, Trondheim (Norway). NTNU Univ. Museum. Dept. of Natural History
Natural History Museum of Denmark, Copenhagen (Denmark). Centre for GeoGenetics
Biology Centre of the Upper Austrian State Museum, Linz (Austria)
Univ. of Greifswald (Germany). Inst. of Botany and Landscape Ecology
USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); HudsonAlpha Inst. for Biotechnology, Huntsville, AL (United States)
HudsonAlpha Inst. for Biotechnology, Huntsville, AL (United States)
Duke Univ., Durham, NC (United States). Dept. of Biology
Department of Biology, Duke University, Durham, NC, USA
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Climate Change Science Inst.
Univ. of Zurich (Switzerland). Zurich-Basel Plant Science Center. Dept. of Systematic and Evolutionary Botany

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.

View Accepted Manuscript (DOE)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1815542

Journal Information:: Molecular Biology and Evolution (Online), Journal Name: Molecular Biology and Evolution (Online) Journal Issue: 7 Vol. 38; ISSN 1537-1719

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

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Powerful Inference with the D-Statistic on Low-Coverage Whole-Genome Data Soraggi, Samuele; Wiuf, Carsten; Albrechtsen, Anders G3 Genes\|Genomes\|Genetics, Vol. 8, Issue 2 https://doi.org/10.1534/g3.117.300192	journal	February 2018
The Concordance of Gene Trees and Species Trees at Two Linked Loci Slatkin, Montgomery; Pollack, Joshua L. Genetics, Vol. 172, Issue 3 https://doi.org/10.1534/genetics.105.049593	journal	March 2006
Estimating Individual Admixture Proportions from Next Generation Sequencing Data Skotte, Line; Korneliussen, Thorfinn Sand; Albrechtsen, Anders Genetics, Vol. 195, Issue 3 https://doi.org/10.1534/genetics.113.154138	journal	September 2013
Quantifying Population Genetic Differentiation from Next-Generation Sequencing Data Fumagalli, Matteo; Vieira, Filipe G.; Korneliussen, Thorfinn Sand Genetics, Vol. 195, Issue 3 https://doi.org/10.1534/genetics.113.154740	journal	August 2013
A phylogenetic monograph of the Sphagnum subsecundum complex (Sphagnaceae) in eastern North America Shaw, A. Jonathan; Shaw, Blanka; Ricca, Mariana The Bryologist, Vol. 115, Issue 1 https://doi.org/10.1639/0007-2745-115.1.128	journal	March 2012
High morphological diversity in remote island populations of the peat moss Sphagnum palustre: glacial refugium, adaptive radiation or just plasticity? Stenøien, Hans K.; Hassel, Kristian; Segreto, Rossana The Bryologist, Vol. 117, Issue 2 https://doi.org/10.1639/0007-2745-117.2.095	journal	May 2014
Invisible in plain sight: recurrent double allopolyploidy in the African Sphagnum ×planifolium (Sphagnaceae) Karlin, Eric F.; Temsch, Eva M.; Bizuru, Elias The Bryologist, Vol. 117, Issue 2 https://doi.org/10.1639/0007-2745-117.2.187	journal	May 2014
Is interspecific gene flow and speciation in peatmosses ( Sphagnum ) constrained by phylogenetic relationship and life-history traits? Meleshko, Olena; Stenøien, Hans K.; Speed, James D. M. Lindbergia, Vol. 41, Issue 1 https://doi.org/10.25227/linbg.01107	journal	January 2018
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The rare peat moss Sphagnum wulfianum (Sphagnaceae) did not survive the last glacial period in northern European refugia Kyrkjeeide, Magni Olsen; Hassel, Kristian; Flatberg, Kjell I. American Journal of Botany, Vol. 99, Issue 4 https://doi.org/10.3732/ajb.1100410	journal	April 2012
Divergent evolution and niche differentiation within the common peatmoss Sphagnum magellanicum Yousefi, Narjes; Hassel, Kristian; Flatberg, Kjell Ivar American Journal of Botany, Vol. 104, Issue 7 https://doi.org/10.3732/ajb.1700163	journal	July 2017

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incomplete lineage sorting
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peatmoss
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rapid diversification
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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

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