Locally adaptive inversions in structured populations

Author:

Mackintosh Carl1234ORCID,Scott Michael F5ORCID,Reuter Max1ORCID,Pomiankowski Andrew12ORCID

Affiliation:

1. Department of Genetics, Evolution, and Environment, University College London , Gower Street, London WC1E 6BT , UK

2. CoMPLEX, University College London , Gower Street, London WC1E 6BT , UK

3. CNRS, UMR7144 Adaptation et Diversité en Milieu Marin, Station Biologique de Roscoff , Roscoff 29680 , France

4. Sorbonne Universités, UPMC Université Paris VI , Roscoff 29680 , France

5. School of Biological Sciences, University of East Anglia , Norwich Research Park, Norwich NR4 7TJ , UK

Abstract

Abstract Inversions have been proposed to facilitate local adaptation, by linking together locally coadapted alleles at different loci. Prior work addressing this question theoretically has considered the spread of inversions in “continent-island” scenarios in which there is a unidirectional flow of maladapted migrants into the island population. In this setting, inversions capturing locally adaptive haplotypes are most likely to invade when selection is weak, because stronger local selection (i) more effectively purges maladaptive alleles and (ii) generates linkage disequilibrium between adaptive alleles, thus lessening the advantage of inversions. We show this finding only holds under limited conditions by studying the establishment of inversions in a more general two-deme model, which explicitly considers the dynamics of allele frequencies in both populations linked by bidirectional migration. In this model, the level of symmetry between demes can be varied from complete asymmetry (continent-island) to complete symmetry. For symmetric selection and migration, strong selection increases the allele frequency divergence between demes thereby increasing the frequency of maladaptive alleles in migrants, favoring inversions—the opposite of the pattern seen in the asymmetric continent-island scenario. We also account for the likelihood that a new inversion captures an adaptive haplotype in the first instance. When considering the combined process of capture and invasion in “continent island” and symmetric scenarios, relatively strong selection increases inversion establishment probability. Migration must also be low enough that the inversion is likely to capture an adaptive allele combination, but not so low as to eliminate the inversion’s advantage. Overall, our analysis suggests that inversions are likely to harbor larger effect alleles that experience relatively strong selection.

Funder

Engineering and Physical Sciences Research Council

Gordon and Betty Moore Foundation

Leverhulme Trust

Natural Environment Research Council

Biotechnology and Biological Sciences Research Council

Publisher

Oxford University Press (OUP)

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