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.

Highlights

  • The mechanistic basis of speciation and in particular the contribution of behaviour to the completion of the speciation process is often contentious

  • We have suggested that hybridization should be more detrimental to the Western lineage, as this lineage lost ground to the Central lineage since the initial secondary contact but it remains unknown if potential asymmetrically-acting pre-mating mechanisms are involved in the dynamics of the hybrid zone [25]

  • Our analyses show a stronger partner preference of female common voles from the Western edge of the secondary contact zone compared to females of allopatric origin

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Summary

Introduction

The mechanistic basis of speciation and in particular the contribution of behaviour to the completion of the speciation process is often contentious. 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. 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. The recolonization of Europe from their allopatric glacial refugia has led to multiple secondary contacts where hybrid zones have formed which differ in the age of divergence between the evolutionary lineages involved and the level of gene flow between them [18,19,20, 25]. We have suggested that hybridization should be more detrimental to the Western lineage, as this lineage lost ground to the Central lineage since the initial secondary contact but it remains unknown if potential asymmetrically-acting pre-mating mechanisms are involved in the dynamics of the hybrid zone [25]

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