Inversion invasions: when the genetic basis of local adaptation is concentrated within inversions in the face of gene flow

Abstract

Across many species where inversions have been implicated in local adaptation, genomes often evolve to contain multiple, large inversions that arise early in divergence. Why this occurs has yet to be resolved. To address this gap, we built forward-time simulations in which inversions have flexible characteristics and can invade a metapopulation undergoing spatially divergent selection for a highly polygenic trait. In our simulations, inversions typically arose early in divergence, captured standing genetic variation upon mutation, and then accumulated many small-effect loci over time. Under special conditions, inversions could also arise late in adaptation and capture locally adapted alleles. Polygenic inversions behaved similarly to a single supergene of large effect and were detectable by genome scans. Our results show that characteristics of adaptive inversions found in empirical studies (e.g. multiple large, old inversions that are F ST outliers, sometimes overlapping with other inversions) are consistent with a highly polygenic architecture, and inversions do not need to contain any large-effect genes to play an important role in local adaptation. By combining a population and quantitative genetic framework, our results give a deeper understanding of the specific conditions needed for inversions to be involved in adaptation when the genetic architecture is polygenic. This article is part of the theme issue ‘Genomic architecture of supergenes: causes and evolutionary consequences’.

Genomic architecture of supergenes: connecting form and function

“…For the one inversion that shows clear patterns of local adaptation to the environment (e.g. a supergene), they find it is of a large size and both the capture and accumulation of adaptive variation was important in forming the supergene, findings that are consistent with the predictions of Schaal et al [ 58 ].…”

“…Schaal et al . [ 58 ] use simulated data to explore the dynamics of capture and gain, while Stenløkk et al . [ 59 ] examine the evidence for capture versus gain using data from the Atlantic salmon.…”

“…Schaal et al [ 58 ] address gaps in our understanding of capture and gain with whole-genome simulations of local adaptation with polygenic architectures and supergenes. Focusing on supergenes where recombination suppression is owing to inversions (i.e.…”

“…For some other loci, however, the results suggest that they might have been gained after the formation of the inversions (as modelled in Schaal et al . [ 58 ]).…”

Inversions and parallel evolution

“…If each of the arrangements contains alleles contributing to local adaptation in a specific habitat, arrangement and habitat will become associated due to selection. Then, the inversion provides an efficient means of keeping adaptive allelic combinations intact and preventing the negative effects of recombination in areas of gene flow [ 4 , 5 ]. Inversions should thus be favoured where populations locally adapt to different habitats.…”