The consequences of gene flow for local adaptation and differentiation: a two-locus two-deme model

DOI10.1007/S00285-013-0660-ZMaRDI QIDQ2447547zbMATH OpenOpenAlexWikidataFDO

Authors Ada Akerman, Reinhard Bürger

Publication date 28 April 2014

Published in Journal of Mathematical Biology (Search for Journal in Brave)

Copyright license Creative Commons Attribution 4.0 International

Full work available at URL https://arxiv.org/abs/1303.1374

zbMATH Keywords

fixation indexgenetic architecturemigrationmultilocus polymorphismpopulation subdivisionrecombinationselection

Mathematics Subject Classification ID

Qualitative investigation and simulation of ordinary differential equation models (34C60) Genetics and epigenetics (92D10) Problems related to evolution (92D15)

Abstract: We consider a population subdivided into two demes connected by migration in which selection acts in opposite direction. We explore the effects of recombination and migration on the maintenance of multilocus polymorphism, on local adaptation, and on differentiation by employing a deterministic model with genic selection on two linked diallelic loci (i.e., no dominance or epistasis). For the following cases, we characterize explicitly the possible equilibrium configurations: weak, strong, highly asymmetric, and super-symmetric migration, no or weak recombination, and independent or strongly recombining loci. For independent loci (linkage equilibrium) and for completely linked loci, we derive the possible bifurcation patterns as functions of the total migration rate, assuming all other parameters are fixed but arbitrary. For these and other cases, we determine analytically the maximum migration rate below which a stable fully polymorphic equilibrium exists. In this case, differentiation and local adaptation are maintained. Their degree is quantified by a new multilocus version of $Fst$ and by the migration load, respectively. In addition, we investigate the invasion conditions of locally beneficial mutants and show that linkage to a locus that is already in migration-selection balance facilitates invasion. Hence, loci of much smaller effect can invade than predicted by one-locus theory if linkage is sufficiently tight. We study how this minimum amount of linkage admitting invasion depends on the migration pattern. This suggests the emergence of clusters of locally beneficial mutations, which may form `genomic islands of divergence'. Finally, the influence of linkage and two-way migration on the effective migration rate at a linked neutral locus is explored. Numerical work complements our analytical results.

Review text

The purpose of this paper is to improve the understanding of how genetic architecture (recombination and locus effects) as well as the pattern and amount of migration determine polymorphism, local adaptation, and differentiation in a subdivided population inhabiting a heterogeneous environment. Two linked, diallelic loci and the migration between two demes are considered. If the alleles are beneficial in only one environment and detrimental in the other, local adaptation of subpopulations, and differentiation between them can be obtained only if a (multilocus) polymorphism is maintained. Therefore, the authors prove the existence and stability of polymorphic equilibrium and the dependence of the equilibrium configurations on the model parameters (migration rates, selection coefficients, recombination rate). Three evolutionarily stable states occur: (i) existence of a single specialist optimally adapted to one deme and poorly to the other, (ii) existence of a single generalist type which has higher average fitness in the whole population than than any of the specialists, and (iii) existence of a set of specialists each adapted to its deme, i.e., coexistence in a polymorphism then local adaptation and differentiation occur only in case (iii). The analytical results presented complement the numerical findings by \textit{S. Yeaman} and \textit{M. C. Whitlock} [``The genetic architecture of adaptation under migration-selection balance, Evolution 65, No. 7, 1897--1911 (2011; \url{doi:10.1111/j.1558-5646.2011.01269.x})] for a multilocus quantitative-genetic model with clusters of locally adaptive mutations, or concentrated genetic architectures, build up in spatially structured populations with opposing selection pressures in two demes. Because tighter linkage is required for invasion under increasingly asymmetric migration rates, more concentrated architectures and a greater advantage for recombination-reducing mechanisms (such as chromosome inversions) should be expected for highly asymmetric migration. In finite populations, invasion of new mutants occurs only with a certain probability, and the genetic drift may erase polymorphism. In the absence of epistasis and under the present form of balancing selection, reduced recombination between selected loci is favored, except when migration rates are sufficiently symmetric and high. Because in the present model, polymorphism at the selected loci is maintained by balancing selection, the effective migration rate may be greatly reduced compared with the actual migration rate. Therefore, strong barriers against gene flow may build up at such neutral sites and enhance (neutral) differentiation.

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Cited in

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• Establishment in a new habitat by polygenic adaptation
• Adaptive peak shifts in a heterogeneous environment
• Adaptive gene introgression after secondary contact

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