De Novo Mutation and Rapid Protein (Co-)evolution during Meiotic Adaptation in Arabidopsis arenosa.

Magdalena Bohutínská,Pirita Paajanen,Vinzenz Handrick,Filip Kolář,Levi Yant,Kirsten Bomblies,Roswitha Schmickl,Jian Lu

doi:10.1093/molbev/msab001

Magdalena Bohutínská, Pirita Paajanen + Show 6 more

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https://doi.org/10.1093/molbev/msab001

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Abstract

A sudden shift in environment or cellular context necessitates rapid adaptation. A dramatic example is genome duplication, which leads to polyploidy. In such situations, the waiting time for new mutations might be prohibitive; theoretical and empirical studies suggest that rapid adaptation will largely rely on standing variation already present in source populations. Here, we investigate the evolution of meiosis proteins in Arabidopsis arenosa, some of which were previously implicated in adaptation to polyploidy, and in a diploid, habitat. A striking and unexplained feature of prior results was the large number of amino acid changes in multiple interacting proteins, especially in the relatively young tetraploid. Here, we investigate whether selection on meiosis genes is found in other lineages, how the polyploid may have accumulated so many differences, and whether derived variants were selected from standing variation. We use a range-wide sample of 145 resequenced genomes of diploid and tetraploid A. arenosa, with new genome assemblies. We confirmed signals of positive selection in the polyploid and diploid lineages they were previously reported in and find additional meiosis genes with evidence of selection. We show that the polyploid lineage stands out both qualitatively and quantitatively. Compared with diploids, meiosis proteins in the polyploid have more amino acid changes and a higher proportion affecting more strongly conserved sites. We find evidence that in tetraploids, positive selection may have commonly acted on de novo mutations. Several tests provide hints that coevolution, and in some cases, multinucleotide mutations, might contribute to rapid accumulation of changes in meiotic proteins.

Highlights

IntroductionAs populations face new challenges, positive selection can act on alleles recruited from standing variation or on de novo mutations (Barrett and Schluter 2008)
Sometimes an abrupt change in circumstances forces a rapid evolutionary response
Meiosis Protein Evolution in A. arenosa Lineages We investigated the patterns of evolution of meiosis proteins across all currently known A. arenosa lineages, including samples of four additional diploid lineages in which meiosis protein evolution was not investigated in our previous study (Wright et al 2015)

Summary

Introduction

As populations face new challenges, positive selection can act on alleles recruited from standing variation or on de novo mutations (Barrett and Schluter 2008). Though in long-term macroevolution, de novo mutations clearly play a role, evolution from standing variation may be especially important in facilitating rapid adaptation, because it eliminates the waiting time needed for novel mutations (Hermisson and Pennings 2005; Prezeworski et al 2005; Barrett and Schluter 2008). There are numerous reports of rapid adaptation to novel environments that utilize standing genetic variation (Jones et al 2012; Van Belleghem et al 2018; Haenel et al 2019; Lai et al 2019), whereas reports of de novo mutations in such instances are rare and often include loss of function mutations (Messer and Petrov 2013; ExpositoAlonso et al 2018; Wu et al 2018; Xie et al 2019). The relative importance of de novo mutations may be greater when extensive functional restructuring is needed

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