title: Hybrid origins and the earliest stages of diploidization in the highly successful recent polyploid Capsella bursa-pastoris.
abstract: Whole-genome duplication (WGD) events have occurred repeatedly during flowering plant evolution, and there is growing evidence for predictable patterns of gene retention and loss following polyploidization. Despite these important insights, the rate and processes governing the earliest stages of diploidization remain poorly understood, and the relative importance of genetic drift, positive selection, and relaxed purifying selection in the process of gene degeneration and loss is unclear. Here, we conduct whole-genome resequencing in Capsella bursa-pastoris, a recently formed tetraploid with one of the most widespread species distributions of any angiosperm. Whole-genome data provide strong support for recent hybrid origins of the tetraploid species within the past 100,000-300,000 y from two diploid progenitors in the Capsella genus. Major-effect inactivating mutations are frequent, but many were inherited from the parental species and show no evidence of being fixed by positive selection. Despite a lack of large-scale gene loss, we observe a decrease in the efficacy of natural selection genome-wide due to the combined effects of demography, selfing, and genome redundancy from WGD. Our results suggest that the earliest stages of diploidization are associated with quantitative genome-wide decreases in the strength and efficacy of selection rather than rapid gene loss, and that nonfunctionalization can receive a "head start" through a legacy of deleterious variants and differential expression originating in parental diploid populations.
authors.affiliation: Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2;
authors.forename: Gavin M
authors.initials: GM
authors.lastname: Douglas
authors.affiliation: Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2;
authors.forename: Gesseca
authors.initials: G
authors.lastname: Gos
authors.affiliation: Department of Ecology and Genetics, Evolutionary Biology Centre, Science for Life Laboratory, Uppsala University, 75236 Uppsala, Sweden;
authors.forename: Kim A
authors.initials: KA
authors.lastname: Steige
authors.affiliation: Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2;
authors.forename: Adriana
authors.initials: A
authors.lastname: Salcedo
authors.affiliation: Department of Ecology and Genetics, Evolutionary Biology Centre, Science for Life Laboratory, Uppsala University, 75236 Uppsala, Sweden;
authors.forename: Karl
authors.initials: K
authors.lastname: Holm
authors.affiliation: Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2;
authors.forename: Emily B
authors.initials: EB
authors.lastname: Josephs
authors.affiliation: Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2;
authors.forename: Ramesh
authors.initials: R
authors.lastname: Arunkumar
authors.affiliation: Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2;
authors.forename: J Arvid
authors.initials: JA
authors.lastname: Ågren
authors.affiliation: Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2; Center for Genomics and Systems Biology, New York University Abu Dhabi, Abu Dhabi, United Arab Emirates 129188;
authors.forename: Khaled M
authors.initials: KM
authors.lastname: Hazzouri
authors.affiliation: Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2;
authors.forename: Wei
authors.initials: W
authors.lastname: Wang
authors.affiliation: McGill Centre for Bioinformatics, McGill University, Montreal, QC, Canada H3G 0B1;
authors.forename: Adrian E
authors.initials: AE
authors.lastname: Platts
authors.affiliation: Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2;
authors.forename: Robert J
authors.initials: RJ
authors.lastname: Williamson
authors.affiliation: Department of Botany, University of Osnabruck, 49076 Osnabruck, Germany; and.
authors.forename: Barbara
authors.initials: B
authors.lastname: Neuffer
authors.affiliation: Department of Ecology and Genetics, Evolutionary Biology Centre, Science for Life Laboratory, Uppsala University, 75236 Uppsala, Sweden; martin.lascoux@ebc.uu.se tanja.slotte@su.se stephen.wright@utoronto.ca.
authors.forename: Martin
authors.initials: M
authors.lastname: Lascoux
authors.affiliation: Department of Ecology and Genetics, Evolutionary Biology Centre, Science for Life Laboratory, Uppsala University, 75236 Uppsala, Sweden; Department of Ecology, Environment, and Plant Sciences, Science for Life Laboratory, Stockholm University, 10691 Stockholm, Sweden martin.lascoux@ebc.uu.se tanja.slotte@su.se stephen.wright@utoronto.ca.
authors.forename: Tanja
authors.initials: T
authors.lastname: Slotte
authors.affiliation: Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2; martin.lascoux@ebc.uu.se tanja.slotte@su.se stephen.wright@utoronto.ca.
authors.forename: Stephen I
authors.initials: SI
authors.lastname: Wright
mesh_terms: D029687:Capsella / Q000235:genetics*; D002678:Chimera / Q000235:genetics*; D019143:Evolution, Molecular; D018745:Genome, Plant / Q000502:physiology*; D055106:Genome-Wide Association Study; D009154:Mutation; D011123:Polyploidy; D012641:Selection, Genetic
keywords: gene loss; polyploidy; population genomics; speciation