Structure and dynamics of hybrid zones at different stages of speciation in the common vole (Microtus arvalis)

Abstract

The genetic structure and dynamics of hybrid zones provide crucial information for understanding the processes and mechanisms of evolutionary divergence and speciation. In general, higher levels of evolutionary divergence between taxa are more likely to be associated with reproductive isolation and may result in suppressed or strongly restricted hybridization. In this study, we examined two secondary contact zones between three deep evolutionary lineages in the common vole (Microtus arvalis). Differences in divergence times between the lineages can shed light on different stages of reproductive isolation and thus provide information on the ongoing speciation process in M. arvalis. We examined more than 800 individuals for mitochondrial (mtDNA), Y-chromosome and autosomal markers and used assignment and cline analysis methods to characterize the extent and direction of gene flow in the contact zones. Introgression of both autosomal and mtDNA markers in a relatively broad area of admixture indicates selectively neutral hybridization between the least-divergent lineages (Central and Eastern) without evidence for partial reproductive isolation. In contrast, a very narrow area of hybridization, shifts in marker clines and the quasi-absence of Y-chromosome introgression support a moving hybrid zone and unidirectional selection against male hybrids between the lineages with older divergence (Central and Western). Data from a replicate transect further support non-neutral processes in this hybrid zone and also suggest a role for landscape history in the movement and shaping of geneflow profiles.

Contrasting and congruent patterns of genetic structuring in two Microtus vole species using museum specimens

“…We can also determine whether geographic structure revealed by microsatellites is in agreement with the mtDNA lineage distributions across Poland found in previous studies (Herman et al 2014, Stojak et al 2015. For one of these species, the common vole, studies from other regions in Europe have already found general congruence in patterns of genetic structure between mtDNA and microsatellites at contacts between lineages (Heckel et al 2005;Braaker and Heckel 2009;Beysard and Heckel 2014). For the field vole, Beysard et al (2012) demonstrated an overall pattern of congruence between mtDNA, microsatellites and Laboratory procedures were repeated three times for each sample and each locus.…”

“…1). Beysard and Heckel (2014) analysed the genetic structure and dynamics of three contact zones between mitochondrial lineages of the common vole located in Switzerland and Bavaria. They found very narrow zones of hybridization (using microsatellites) between the Central and Western lineages and a much wider hybrid zone between the Central and Eastern lineages (which are the lineages present in Poland; Stojak et al 2015).…”

“…The Eastern and Central lineages are grouped within the same clade and have an estimated time to most recent common ancestor (tMRCA) of approximately 28 ka BP, whereas the Central and Western lineages belong to separate clades, with a tMRCA at approximately 56 ka BP (Stojak et al 2015). Given that the Central and Eastern lineages are less divergent than the Western and Central lineages, it is perhaps not surprising that Beysard and Heckel (2014) found stronger evidence for reproductive isolation for the Western and Central lineages. Our results are in general agreement with the aforementioned study because the microsatellites employed here demonstrate that individuals generally belong to a single genetic cluster (Western group) across the Central and Eastern mtDNA lineage contact zone in Poland (Fig.…”

“…The application of genetic markers such as microsatellites will allow an assessment of contemporary patterns of gene flow and differentiation in areas where different mtDNA lineages come into contact (Heckel et al 2005;Godinho et al 2008;Beysard et al 2012). For the common vole, mtDNA and microsatellites have been used in other regions in Europe to find general congruence in patterns of genetic structure between the two types of marker (Heckel et al 2005;Braaker and Heckel 2009;Beysard and Heckel 2014), including in an area of contact involving the same mtDNA lineages as found in Poland (Eastern and Central) but along the German-Czech Republic border (Beysard and Heckel 2014). Given that differences in genetic structure might be expected between mtDNA and microsatellite markers, because of differences in mutation rate, effective population sizes and inheritance, the congruent patterns for the two types of marker in the previous studies in the common vole indicate that a degree of contemporary reproductive isolation exists between mtDNA lineages in this species.…”

Coupling, Reinforcement, and Speciation

“…Comparisons among examples with different overall barriers and different combinations of barrier effects, as well as comparative analyses of replicated and independent events of contact in a given system can also help this reconstruction (e.g., Nadeau et al 2014;Vijay et al 2017). In general, it will be important to identify more systems offering multiple hybrid zones to compare situations where coupling may not be at the same stage across the distribution range (e.g., in common voles [Beysard and Heckel 2014], Hyla frogs [Dufresnes et al 2015], or green toads [Dufresnes et al 2014]). Combining genomic analysis of such systems with analysis of phenotypes and the types of barrier effects (one allele vs. two allele) is the most likely route toward understanding of coupling processes.…”