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.

Origin of the chromosomal radiation of Madeiran house mice: a microsatellite analysis of metacentric chromosomes

“…It should be noted that the centromeric region is expected to show reduced recombination in general (for example, Carneiro et al, 2009;Geraldes et al, 2011;Nachman and Payseur, 2012), and that this has been documented for metacentric chromosomes in the house mouse (Dumas and Britton-Davidian, 2002). As the extent of genetic differentiation in the three chromosome regions was essentially the same among races sharing the same disposition of chromosomes (3.8 or 3.14 and 8.11), as well as within races, it seems unlikely that solely a 'centromeric effect' is responsible for the significant divergence observed at proximal loci between karyotypic groups (that is, 3.8 versus 3.14 and 8.11).…”

“…Thus, Panithanarak et al (2004) compared chromosomes that did and did not differ between chromosomal races in Northern Italy and showed that centromeric regions of rearranged chromosomes showed less introgression than non-rearranged chromosomes. Such a study would be worthwhile on the Madeiran mice, to rule out the possibility that the reduced gene flow associated with proximal markers of metacentric 3.8 is a purely centromeric effect, rather than an impact of the chromosomal rearrangement (Carneiro et al, 2009;Geraldes et al, 2011;Nachman and Payseur, 2012). Such work is currently being carried out, using a suite of centromeric microsatellites that includes three loci per chromosome (total 60 loci: three for each of the 19 autosomes, plus three on the X chromosome).…”

Genomic impacts of chromosomal inversions in parapatricDrosophilaspecies

“…Reduced recombination, in general, can contribute to divergence during the speciation process (reviewed in Nachman & Payseur [58]). Further, genomic scans and experimental approaches have identified regions with greater differentiation than expected under neutrality that are clustered but not associated with inversions (reviewed in earlier studies [1,59,60]).…”

A linkage disequilibrium perspective on the genetic mosaic of speciation in two hybridizing Mediterranean white oaks

“…Several nonexclusive factors can potentially contribute to the genetic mosaic that is created during the process of population divergence and speciation. These include exogenous and/or endogenous drivers of divergent selection (Rundell and Price, 2009;Schluter, 2009); genetic drift (Ohta, 1992); variable mutation and recombination rates (Hedrick, 2005;Noor and Feder, 2006;Nachman and Payseur, 2012); chromosomal structure (Rieseberg, 2001;Strasburg et al, 2012); or the genomic distribution and size effects of genes under selection (Orr, 2005;Rogers and Bernatchez, 2007;Michel et al, 2010).…”

“…One of the most controversial issues, from both theoretical expectations and empirical results, is the creation and maintenance/ growth of the genomic regions of divergence during speciation with gene flow (Hoffmann and Rieseberg, 2008;Feder and Nosil, 2010;White et al, 2010;Yeaman and Whitlock, 2011;Nachman and Payseur, 2012;Nosil and Feder, 2012;Feder et al, 2012b;Narum et al, 2013). Via (2009Via ( , 2012, proposed that strong divergent selection acting on a few loci generates an inter-population process, which she called divergence hitchhiking (DH), that is characterized by reduced inter-population recombination and gene flow.…”