Tracing reinforcement through asymmetrical partner preference in the European common vole Microtus arvalis

Abstract

BackgroundThe mechanistic basis of speciation and in particular the contribution of behaviour to the completion of the speciation process is often contentious. Contact zones between related taxa provide a situation where selection against hybridization might reinforce separation by behavioural mechanisms, which could ultimately fully isolate the taxa. One of the most abundant European mammals, the common vole Microtus arvalis, forms multiple natural hybrid zones where rapidly diverging evolutionary lineages meet in secondary contact. Very narrow zones of hybridization spanning only a few kilometres and sex-specific gene flow patterns indicate reduced fitness of natural hybrids and incipient speciation between some of the evolutionary lineages. In this study, we examined the contribution of behavioural mechanisms to the speciation process in these rodents by fine-mapping allopatric and parapatric populations in the hybrid zone between the Western and Central lineages and experimental testing of the partner preferences of wild, pure-bred and hybrid female common voles.ResultsGenetic analysis based on microsatellite markers revealed the presence of multiple parapatric and largely non-admixed populations at distances of about 10 km at the edge of the area of natural hybridization between the Western and Central lineages. Wild females from Western parapatric populations and lab-born F1 hybrids preferred males from the Western lineage whereas wild females of Central parapatric origin showed no measurable preference. Furthermore, wild and lab-born females from allopatric populations of the Western or Central lineages showed no detectable preference for males from either lineage.ConclusionsThe detected partner preferences are consistent with asymmetrical reinforcement of pre-mating reproductive isolation mechanisms in the European common vole and with earlier results suggesting that hybridization is more detrimental to the Western lineage. As a consequence, these differences in behaviour might contribute to a further geographical stabilization of this moving hybrid zone. Such behavioural processes could also provide a mechanistic perspective for frequently-detected asymmetrical introgression patterns in the largely allopatrically diversifying Microtus genus and other rapidly speciating rodents.

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

“…Beysard and Heckel (2014) concluded that the divergence times between lineages play an important role in the level of gene introgression between them. A recent study by Beysard et al (2015) demonstrated that female common voles from the Western mtDNA lineage preferentially selected males from their own lineage under lab conditions in preference to Central lineage males. At present, we do not know if there is such a preference between voles of the Central and Eastern lineages present in Poland (which diverged more recently than the Central and Western lineages; Stojak et al 2015) or between lineages in the field vole (Beysard et al 2012).…”

Geographic patterns of postzygotic isolation between two closely related widespread dung fly species (Sepsis cynipseaandSepsis neocynipsea; Diptera: Sepsidae)

“…Contrary to a number of precopulatory behavioural traits (Giesen et al, 2017), we obtained only weak evidence for such reinforcement in sympatric areas (the Swiss Alps) for the (postcopulatory) fecundity traits assessed here (egg production only). It thus appears that precopulatory behavioural traits, which are inherently plastic and can potentially evolve fast, are of overriding importance in preventing hybridisation in nature in this and other systems (Eberhard, 1996;Puniamoorthy, 2014;Puniamoorthy et al, 2009;Beysard, Krebs-Wheaton, & Heckel, 2015;Schmidt & Pfennig, 2016).…”

Linking intra- and interspecific assortative mating: Consequences for asymmetric sexual isolation

“…4; see also While et al 2015). This explanation for sexual isolation asymmetry does of course not exclude other models, such as asymmetric postzygotic isolation (Alipaz et al 2005a, b), reinforcement (Coyne and Orr 2004), female preferences for heterospecific males (Ryan and Wagner 1987;Pfennig 2007;Beysard et al 2015), genetic drift (Kaneshiro 1980), sex differences in species recognition , or a transient stage in Fisherian runaway sexual selection (Arnold et al 1996).…”

“…, b), reinforcement (Coyne and Orr ), female preferences for heterospecific males (Ryan and Wagner ; Pfennig ; Beysard et al. ), genetic drift (Kaneshiro ), sex differences in species recognition (Svensson et al. ), or a transient stage in Fisherian runaway sexual selection (Arnold et al.…”