Hybrid origins and the earliest stages of diploidization in the highly successful recent polyploidCapsella 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.polyploidy | population genomics | speciation | gene loss

Impact of demography on linked selection in two outcrossing Brassicaceae species

“…Indeed, the recent colonization history of A. lyrata especially in northern Europe has likely been associated with strong population bottlenecks or effective population size reduction (Mattila, Tyrmi, Pyhäjärvi, & Savolainen, 2017;Pyhäjärvi, Aalto, & Savolainen, 2012;Ross-Ibarra et al, 2008;Savolainen & Kuittinen, 2011), which is in contrast to the large and relatively stable population of C. grandiflora (Douglas et al, 2015;Slotte, Foxe, Hazzouri, & Wright, 2010;Slotte et al, 2013;St. We chose these species because they have similar mating systems (both are self-incompatible outcrossers) and genome structure, and because previous research suggests considerable differences in the demographic histories of some populations.…”

Endosperm-based hybridization barriers explain the pattern of gene flow between Arabidopsis lyrata and Arabidopsis arenosa in Central Europe

“…Nevertheless, hybridization has long been recognized to play an important role in plant evolution, with many reported cases of related species that, either punctually or continuously in their life history, have experienced gene flow, leading to introgression of adaptive traits or hybrid speciation (2)(3)(4)(5)(6)(7)(8)(9). Thus, the "tree of life" is considered more as a complex network than an actual tree (10,11).…”

Gene Duplicability of Core Genes Is Highly Consistent across All Angiosperms

“…For instance, it is estimated that ;16% of the genes for Arabidopsis are still present in duplicate following the most recent WGD that occurred ;49 million years ago (mya; Vanneste et al, 2014a), while 75% of the genes are still present in duplicate in soybean (Glycine max), which underwent a WGD ;13 mya (Schmutz et al, 2010). Whether these genes will be retained indefinitely is still an unresolved question (Buggs et al, 2012;McGrath and Lynch, 2012;Douglas et al, 2015), although the lower numbers of retained genes reported for more ancient WGD events seems to suggest that, at least for a subset of genes, dosage constraints eventually get relaxed, leading to functional diversification or loss of these genes.…”