Recombination rate variation and speciation: theoretical predictions and empirical results from rabbits and mice

Abstract

Recently diverged taxa may continue to exchange genes. A number of models of speciation with gene flow propose that the frequency of gene exchange will be lower in genomic regions of low recombination and that these regions will therefore be more differentiated. However, several population-genetic models that focus on selection at linked sites also predict greater differentiation in regions of low recombination simply as a result of faster sorting of ancestral alleles even in the absence of gene flow. Moreover, identifying the actual amount of gene flow from patterns of genetic variation is tricky, because both ancestral polymorphism and migration lead to shared variation between recently diverged taxa. New analytic methods have been developed to help distinguish ancestral polymorphism from migration. Along with a growing number of datasets of multi-locus DNA sequence variation, these methods have spawned a renewed interest in speciation models with gene flow. Here, we review both speciation and population-genetic models that make explicit predictions about how the rate of recombination influences patterns of genetic variation within and between species. We then compare those predictions with empirical data of DNA sequence variation in rabbits and mice. We find strong support for the prediction that genomic regions experiencing low levels of recombination are more differentiated. In most cases, reduced gene flow appears to contribute to the pattern, although disentangling the relative contribution of reduced gene flow and selection at linked sites remains a challenge. We suggest fruitful areas of research that might help distinguish between different models.

Figure 1.

Comparison of expected patterns of variation in regions of low recombination and regions of high recombination under (a) models of speciation with gene flow and (b) under population-genetic models of selection at linked sites without gene flow. See also legend to table 1.

Figure 2.

(a) Geographical distribution of rabbit subspecies in the Iberian peninsula: Oryctolagus cuniculus algirus (blue) and Oryctolagus cuniculus cuniculus (red). The approximate location of the hybrid zone is shown in purple. (b) Examples of gene genealogies in rabbits for one X-linked locus (SHOX, F_ST = 0.907) and two autosomal loci (GK5, F_ST = 0.120 and TIAM1, F_ST = 0.008). Colours correspond to subspecies of origin.

Figure 3.

(a) Comparison of patterns of differentiation between centromeric loci (presumed to experience low recombination) and telomeric loci (presumed to experience high recombination) between subspecies of rabbits. (b) Comparison of patterns of differentiation between low-recombination loci and high-recombination loci between subspecies of house mice.

Figure 4.

(a) Geographical distribution of house mouse subspecies: Mus musculus domesticus (blue), Mus musculus musculus (red) and Mus musculus castaneus (yellow). Mus musculus molossinus (orange) is found in Japan and is believed to derive from hybridization between M. m. musculus and M. m. castaneus. Ranges reflect inferred distributions before expansions associated with humans during the last few hundred years. (b) Examples of gene genealogies in house mice for one X-linked locus (Ocrl, F_ST = 0.867), one Y-linked locus (Jarid1d, F_ST = 0.907) and one autosomal locus (Clcn6, F_ST = 0.434).