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Theor Popul Biol. 2011 Dec;80(4):272-88. doi: 10.1016/j.tpb.2011.07.002. Epub 2011 Jul 23.

The effects of linkage and gene flow on local adaptation: a two-locus continent-island model.

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Department of Mathematics, University of Vienna, Austria.


Population subdivision and migration are generally considered to be important causes of linkage disequilibrium (LD). We explore the combined effects of recombination and gene flow on the amount of LD, the maintenance of polymorphism, and the degree of local adaptation in a subdivided population by analyzing a diploid, deterministic continent-island model with genic selection on two linked loci (i.e., no dominance or epistasis). For this simple model, we characterize explicitly all possible equilibrium configurations. Simple and intuitive approximations for many quantities of interest are obtained in limiting cases, such as weak migration, weak selection, weak or strong recombination. For instance, we derive explicit expressions for the measures D(=p(AB)-p(A)p(B)) and r(2) (the squared correlation in allelic state) of LD. They depend in qualitatively different ways on the migration rate. Remarkably high values of r(2) are maintained between weakly linked loci, especially if gene flow is low. We determine how the maximum amount of gene flow that admits preservation of the locally adapted haplotype, hence of polymorphism at both loci, depends on recombination rate and selection coefficients. We also investigate the evolution of differentiation by examining the invasion of beneficial mutants of small effect that are linked to an already present, locally adapted allele. Mutants of much smaller effect can invade successfully than predicted by naive single-locus theory provided they are at least weakly linked. Finally, the influence of linkage on the degree of local adaptation, the migration load, and the effective migration rate at a neutral locus is explored. We discuss possible consequences for the evolution of genetic architecture, in particular, for the emergence of clusters of tightly linked, slightly beneficial mutations and the evolution of recombination and chromosome inversions.

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