Interspecific introgression mediates adaptation to whole genome duplication

Sarah Marburger,James D Higgins,Magdalena Bohutínská,Roswitha Schmickl,Jordan Koch,Paul J Seear,Patrick Monnahan,Pirita Paajanen,Levi Yant,Simon H Martin

doi:10.1038/s41467-019-13159-5

Abstract

Adaptive gene flow is a consequential phenomenon across all kingdoms. Although recognition is increasing, there is no study showing that bidirectional gene flow mediates adaptation at loci that manage core processes. We previously discovered concerted molecular changes among interacting members of the meiotic machinery controlling crossover number upon adaptation to whole-genome duplication (WGD) in Arabidopsis arenosa. Here we conduct a population genomic study to test the hypothesis that adaptation to WGD has been mediated by adaptive gene flow between A. arenosa and A. lyrata. We find that A. lyrata underwent WGD more recently than A. arenosa, suggesting that pre-adapted alleles have rescued nascent A. lyrata, but we also detect gene flow in the opposite direction at functionally interacting loci under the most extreme levels of selection. These data indicate that bidirectional gene flow allowed for survival after WGD, and that the merger of these species is greater than the sum of their parts.

Highlights

Adaptive gene flow is a consequential phenomenon across all kingdoms
Our results reveal the molecular basis by which whole-genome duplication (WGD) has been stabilised in both species and indicate that WGD-facilitated hybridisation allowed for stabilisation of meiosis in nascent autotetraploids by highly specific, bidirectional adaptive gene flow
STRUCTURE and principal component analysis (PCA) showed a clear species-specific clustering for diploids, whereas tetraploids exhibited a gradient of relatedness between species (Fig. 1a, b)

Summary

Introduction

Adaptive gene flow is a consequential phenomenon across all kingdoms. recognition is increasing, there is no study showing that bidirectional gene flow mediates adaptation at loci that manage core processes. A targeted resequencing effort focused on patterns of differentiation between diploid and autotetraploid A. arenosa, revealing evidence of highly localised selective sweeps directly overlapping eight loci whose gene products interact during prophase I of meiosis[13]. These eight loci physically and functionally interact to control crossover designation and interference, strongly implying that a modulation of crossover distribution was essential for polyploid establishment in A. arenosa[14,15]. Our results reveal the molecular basis by which WGD has been stabilised in both species and indicate that WGD-facilitated hybridisation allowed for stabilisation of meiosis in nascent autotetraploids by highly specific, bidirectional adaptive gene flow

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Conclusion