Climate and Socio-Sexual Environment Predict Interpopulation Variation in Chemical Signaling Glands in a Widespread Lizard

Many animal species show considerable intraspecific phenotypic variation. For species with broad distributions, this variation may result from heterogeneity in the strength and agents of selection across environments and could contribute to reproductive isolation among populations. Here, we examined interpopulation variation in a morphological trait related to chemical communication, femoral pore number (FP), using 3437 individuals from 55 Pyrenean populations of the common wall lizard (Podarcis muralis). Specifically, we tested the relative roles of genetic relatedness and gene flow, and adaptation to local conditions in generating this variation, with particular interest in the influence of climate and the socio-sexual environment (i.e., the intensity of sexual selection, estimated using sexual size dimorphism [SSD] and adult sex ratio as proxy measures). We found significant interpopulation variation and sexual dimorphism in FP, as well as high genomic differentiation among populations driven by both geographic and environmental distances. Specifically, FP differences across populations were best predicted by a combination of positive allometry and the local intensity of sexual selection, as determined by SSD, or local climatic conditions. Higher FP in more male-competitive environments, or with higher temperature and vegetation complexity, is consistent with adaptation to maintaining signaling efficacy of territorial scent marks. These results suggest that adaptation to local conditions contributes to interpopulation divergence in FP and thus environmental changes can potentially impact the fine-tuning of chemical communication mediating social and sexual behavior.