Male behaviour drives assortative reproduction during the initial stage of secondary contact

Abstract

Phenotypic divergence in allopatry can facilitate speciation by reducing the likelihood that individuals of different lineages hybridize during secondary contact. However, few studies have established the causes of reproductive isolation in the crucial early stages of secondary contact. Here, we establish behavioural causes of assortative reproduction between two phenotypically divergent lineages of the European wall lizard (Podarcis muralis), which have recently come into secondary contact. Parentage was highly assortative in experimental contact zones. However, despite pronounced divergence in male phenotypes, including chemical and visual sexual signals, there was no evidence that females discriminated between males of the two lineages in staged interactions or under naturalistic free-ranging conditions. Instead, assortative reproduction was driven by male mate preferences and, to a lesser extent, male-male competition. The effects were more pronounced when the habitat structure promoted high lizard densities. These results emphasize that assortative reproduction can occur in the absence of female choice and that male behaviour may play an important role in limiting hybridization during the initial stages of secondary contact.

Genomic evidence for asymmetric introgression by sexual selection in the common wall lizard

“…Populations with exaggerated sexual characters have been designated to the subspecies Podarcis muralis nigriventris (Bonaparte , considered by Gruschwitz & Böhme, ; Böhme, ), but this taxonomic unit is not supported genetically (see Results). Morphology and coloration are positively correlated with aggressive behaviour and dominance, and individuals with more exaggerated phenotypes have higher reproductive success, both in competition with males from the same region (MacGregor, While, & Uller, ) and in competition with males from western Europe with the ancestral phenotype (Heathcote et al., ; MacGregor, While et al., ; While et al., ). Females do not discriminate between males of different origins, and there is no female choice on male quantitative characters (Heathcote et al., ; While & Uller, ; While et al., ).…”

“…Morphology and coloration are positively correlated with aggressive behaviour and dominance, and individuals with more exaggerated phenotypes have higher reproductive success, both in competition with males from the same region (MacGregor, While, & Uller, ) and in competition with males from western Europe with the ancestral phenotype (Heathcote et al., ; MacGregor, While et al., ; While et al., ). Females do not discriminate between males of different origins, and there is no female choice on male quantitative characters (Heathcote et al., ; While & Uller, ; While et al., ). As a consequence, hybridization in experimental contact zones mainly involves males of the dominant lineage, despite that males prefer to court females that belong to their own genetic lineage (Heathcote et al., ; MacGregor, While et al., ).…”

“…Females do not discriminate between males of different origins, and there is no female choice on male quantitative characters (Heathcote et al., ; While & Uller, ; While et al., ). As a consequence, hybridization in experimental contact zones mainly involves males of the dominant lineage, despite that males prefer to court females that belong to their own genetic lineage (Heathcote et al., ; MacGregor, While et al., ). The phenotypic differences between lizards with the sexually selected syndrome and lizards with the ancestral phenotype persist in non‐native populations in England and in captivity (e.g., MacGregor, While, & Uller, ; While et al., ), strongly suggesting that the influence of phenotypic plasticity on lineage differences is minor.…”

Chemical communication, sexual selection, and introgression in wall lizards

“…However, these associations were not always consistent between the lineages and in some instances were even reversed. Furthermore, previous work suggests that neither Italian nor Western European females discriminate based on male quantitative traits or lineage (Heathcote et al 2016). Indeed, behavioral studies of P.muralis and closely related species suggest females can discriminate between males based on the composition of their femoral secretions (e.g., Lopez et al 2003;López 2006b, Heathcote et al 2014).…”

“…These lineages are native to north-central Italy and Western Europe, and have come together in several zones of secondary contact as a result of natural and human-mediated range expansion (While et al 2015). Phenotypic divergence between the lineages is indicative of differences in the strength of sexual selection on morphology, coloration, and behavior (Heathcote et al 2016;MacGregor et al 2017). Hybridization is asymmetric, with evidence for adaptive introgression of visual sexual characters from the dominant Italian lineage into the Western European lineage (While et al 2015).…”