Hybrid origins and the earliest stages of diploidization in the highly successful recent polyploid Capsella bursa-pastoris

• Published in: Proceedings of the National Academy of Sciences - PNAS 2015-03, Vol.112 (9), p.2806-2811
• Main Authors: Douglas, Gavin M, Gos, Gesseca, Steige, Kim A, Salcedo, Adriana, Holm, Karl, Josephs, Emily B, Arunkumar, Ramesh, Ågren, J Arvid, Hazzouri, Khaled M, Wang, Wei, Platts, Adrian E, Williamson, Robert J, Neuffer, Barbara, Lascoux, Martin, Slotte, Tanja, Wright, Stephen I
• Format: Article
• Language: English
• Subjects: Biological Sciences; Capsella - genetics; Capsella bursa-pastoris; Chimera - genetics; Demography; Evolution; Evolution, Molecular; Flowers & plants; gene loss; Genome, Plant - physiology; Genome-Wide Association Study; Genomes; Hybridization; Mutation; Polyploidy; population genomics; Redundancy; Selection, Genetic; speciation
• ISSN: 0027-8424; 1091-6490; 1091-6490
• DOI: 10.1073/pnas.1412277112

Significance Plants have undergone repeated rounds of whole-genome duplication, followed by gene degeneration and loss. Using whole-genome resequencing, we examined the origins of the recent tetraploid Capsella bursa-pastoris and the earliest stages of genome evolution after polyploidization. We conclude the species had a hybrid origin from two distinct Capsella lineages within the past 100,000–300,000 y. Our analyses suggest the absence of rapid gene loss but provide evidence that the species has large numbers of inactivating mutations, many of which were inherited from the parental species. Our results suggest that genome evolution following polyploidy is determined not only by genome redundancy but also by demography, the mating system, and the evolutionary history of the parental species. 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.