Sex-specific clines support incipient speciation in a common European mammal

Abstract

Hybrid zones provide excellent opportunities to study processes and mechanisms underlying reproductive isolation and speciation. Here we investigated sex-specific clines of molecular markers in hybrid zones of morphologically cryptic yet genetically highly-diverged evolutionary lineages of the European common vole (Microtus arvalis). We analyzed the position and width of four secondary contact zones along three independent transects in the region of the Alps using maternally (mitochondrial DNA) and paternally (Y-chromosome) inherited genetic markers. Given male-biased dispersal in the common vole, a selectively neutral secondary contact would show broader paternal marker clines than maternal ones. In a selective case, for example, involving a form of Haldane's rule, Y-chromosomal clines would not be expected to be broader than maternal markers because they are transmitted by the heterogametic sex and thus gene flow would be restricted. Consistent with the selective case, paternal clines were significantly narrower or at most equal in width to maternal clines in all contact zones. In addition, analyses using maximum likelihood cline-fitting detected a shift of paternal relative to maternal clines in three of four contact zones. These patterns suggest that processes at the contact zones in the common vole are not selectively neutral, and that partial reproductive isolation is already established between these evolutionary lineages. We conclude that hybrid zone movement, sexual selection and/or genetic incompatibilities are likely associated with an unusual unidirectional manifestation of Haldane's rule in this common European mammal.

Figure 1

Map of Switzerland showing the sampling localities of Microtus arvalis samples included in cline analyses of the three transects. Transects are described in Table 1. Localities are designated according to the cytb lineage they harbour (white=Central, grey=Western, black=Italian). The Valais transect along the Rhone valley contains a double transition from the Central through the Western to the Italian lineage. Mixed populations (Figure 2) are indicated by bi-coloured circles. Localities closer than two kilometres to each other were merged for this figure.

Figure 2

Plots of lineage frequencies in populations versus position (km) along the transects Jura, Grisons and Valais for mtDNA (white circles) and Y-chromosomal (grey triangles) markers. Sizes of symbols are proportional to the log number of samples. Bold lines are fitted clines for mtDNA and dashed lines for Y-chromosomal markers. Despite a sampling gap in the Valais transect, an admixed population was detected at km 78, pointing to at least partial contact between the Western and the Central lineage in this transect. See Table 2 for cline properties and statistical comparisons.