Seeking signatures of reinforcement at the genetic level: a hitchhiking mapping and candidate gene approach in the house mouse

Abstract

Reinforcement is the process by which prezygotic isolation is strengthened as a response to selection against hybridisation. Most empirical support for reinforcement comes from the observation of its possible phenotypic signature: an accentuated degree of prezygotic isolation in the hybrid zone as compared to allopatry. Here, we implemented a novel approach to this question by seeking for the signature of reinforcement at the genetic level. In the house mouse, selection against hybrids and enhanced olfactory-based assortative mate preferences are observed in a hybrid zone between the two European subspecies Mus musculus musculus and M. m. domesticus, suggesting a possible recent reinforcement event. To test for the genetic signature of reinforcing selection and identify genes involved in sexual isolation, we adopted a hitchhiking mapping approach targeting genomic regions containing candidate genes for assortative mating in mice. We densely scanned these genomic regions in hybrid zone and allopatric samples using a large number of fast evolving microsatellite loci that allow the detection of recent selection events. We found a handful of loci showing the expected pattern of significant reduction of variability in populations close to the hybrid zone and showing assortative odour preference in mate choice experiments as compared to populations further away and displaying no such preference. These loci lie close to genes that we pinpoint as testable candidates for further investigation.

Diversity of major urinary proteins (MUPs) in wild house mice

“…Gel-based methods provided the basis for the barcode hypothesis and claims that MUPs are highly polymorphic24 – and therefore, the hypothesis that MUPs mediate individual odour and genetic kin recognition (inbreeding avoidance)234613 also needs to be re-evaluated. The low individual variation of Mup genes and linked microsatellites suggest that these genes are evolving under purifying selection26, perhaps through a selective sweep in this large region40, and the high homology of different Mup loci may be generated by concerted evolution (gene conversion)4142. It is unclear why selection favours low individual variation and high homology of MUP loci, and studies are needed to investigate possible effects on individual survival43, as well as reproductive success (through chemical communication).…”

“…Due to the high sequence similarity of different Mup loci, it is impossible to develop locus-specific primers, and therefore we utilized microsatellite markers to estimate and compare genetic diversity at microsatellite markers inside and outside the MUP cluster40. DNA was extracted from ear punches and other tissue samples using a proteinase K/isopropanol protocol46.…”

Coupling, Reinforcement, and Speciation

“…The idea goes back to Wallace (1889), although the term is much younger (Blair 1955), and it has had a turbulent history (Howard 1993;Butlin 1995;Servedio and Noor 2003). The changing fortunes of reinforcement are largely due to development of theory and accumulation of data (see reviews by Servedio and Noor 2003;Coyne and Orr 2004; and recent work by, e.g., Lemmon and Lemmon 2010;Yukilevich 2012;Smadja et al 2015), but they have also been influenced by redefinition of the term, as with other ideas in speciation biology (Harrison 2012). The current definition originates from Dobzhansky's (1937) first description of the process that focused on secondary contact between populations that have evolved Dobzhansky-Muller incompatibilities, leading to the evolution of prezygotic isolation, and has progressively evolved toward a broader view of reinforcement.…”

Hybridization in Plants: Old Ideas, New Techniques

“…is the only case of reinforcement for which the causal genes have been identified (Hopkins and Rausher, 2011). Yet, comparing genome scans for divergence and selection between allopatric and sympatric populations may suggest new candidate genes underlying reinforcement (Smadja et al, 2015). Once causal genes have been identified, future population genomic analyses can be used to infer when and how the mutations evolved (Barbash et al, 2004;Presgraves and Stephan, 2007;Tang and Presgraves, 2009;Sweigart and Flagel, 2015).…”