Abstract
The fates of genetic polymorphisms maintained by balancing selection depend on evolutionary dynamics at linked sites. While coevolution across linked, epigenetically-interacting loci has been extensively explored, such supergenes may be relatively rare. However, genes harboring adaptive variation can occur in close physical proximity while generating independent effects on fitness. Here, I present a model in which two linked loci without epistasis are both under balancing selection for unrelated reasons. Using forward-time simulations, I show that recombination rate strongly influences the retention of adaptive polymorphism, especially for intermediate selection coefficients. A locus is more likely to retain adaptive variation if it is closely linked to another locus under balancing selection, even if the two loci have no interaction. Thus, two linked polymorphisms can both be retained indefinitely even when they would both be lost to drift if unlinked. While these results may be intuitive, they have important implications for genetic architecture: clusters of mutually reinforcing genes may underlie phenotypic variation in natural populations, and such genes cannot be assumed to be functionally associated. Future studies that measure selection coefficients and recombination rates among closely linked genes will be fruitful for characterizing the extent of this phenomenon.
Highlights
Balancing selection is an evolutionary process that maintains more than one allele at a locus for longer than would be expected under genetic drift alone (Fijarczyk & Babik, 2015)
All simulations started with 50% allele frequencies, the highly variable allele frequencies observed over the course of most simulations (Fig. 1) suggest that similar results would be obtained for any intermediate initial allele frequency, and probably for rarer initial frequencies as well
When selection was weak (Nes 5), polymorphism was lost relatively quickly in 2–7 Ne generations regardless of recombination rate, whereas if selection was strong (Nes ! 15), polymorphism was typically retained for the duration of the simulated 50 Ne generations (Table S1)
Summary
Balancing selection is an evolutionary process that maintains more than one allele at a locus for longer than would be expected under genetic drift alone (Fijarczyk & Babik, 2015). The deluge of population genomic data from humans, accompanied by new sophisticated methods for detecting balancing selection, has recently revealed numerous candidate polymorphisms maintained by selection in our species (Segurel et al, 2012; Leffler et al, 2013; Key et al, 2014; Teixeira et al, 2015; Bitarello et al, 2018). In taxa such as Drosophila with relatively large population sizes, adaptively maintained polymorphisms may be even more prevalent (Bergland et al, 2014; Croze et al, 2017)
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