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.

Higher genetic diversity on mountain tops: the role of historical and contemporary processes in shaping genetic variation in the bank vole

“…In the present study, we confirmed that the Western and the Basal lineages co-occur in the eastern part of the Swiss Alps, although individuals from the Basal lineage were rare and restricted to a single location. All of these processes were observed in bank voles or closely-related species (Le Galliard et al, 2012;Sutter, Beysard & Heckel, 2013;Boraty nski et al, 2014) and, with the data available, it is difficult to disentangle them in the present study. Indeed, when forcing STRUCTURE to assign populations to two genetic groups based on microsatellite data, the Basal population was not separated from the Western populations.…”

Dobzhansky-Muller incompatibilities, dominance drive, and sex-chromosome introgression at secondary contact zones: A simulation study

“…, Sutter et al. ; Beysard and Heckel ). Along the same line, the occurrence of sharp clines for both X and Y chromosomes relative to autosomes (such as found in rabbits and mice) cannot result from sex differences in migration only, but rather point to DM incompatibilities involving both X and Y chromosomes.…”

ddRAD‐seq data reveal significant genome‐wide population structure and divergent genomic regions that distinguish the mallard and close relatives in North America

“…Although demographic processes can result in skewed ratios (Van Belleghem et al, 2018), modelling of strictly neutral divergence suggests that Φ ST Z:Autosomal ratios > 5 could be generated only if the effective population size of Z-linked loci is 10%-20% the effective size for autosomal loci (as compared to the standard expectation of 75%), which is unlikely in ducks (Lavretsky et al, 2015). Although sex chromosomes are often found to harbour outliers thought to be important in speciation (Dhami, Joseph, Roshier, & Peters, 2016;Ellegren et al, 2012;Lavretsky et al, 2015;Martin et al, 2013;Minvielle, Ito, Inoue-Murayama, Mizutani, & Wakasugi, 2000;Phadnis & Orr, 2009;Pryke, 2010;Ruegg, Anderson, Boone, Pouls, & Smith, 2014;Saether et al, 2007;Sutter, Beysard, & Heckel, 2013), caution is warranted in making conclusions about the relative importance of loci with different modes of inheritance based on data representing a relatively small proportion of the genome. In particular, it is important to consider that higher linkage disequilibrium in sex chromosomes relative to autosomes (Bergero & Charlesworth, 2009) increases the probability of capturing outlier loci when using reduced representation methods (e.g., ddRAD-seq; Samuk et al, 2017).…”