Ecological variation drives morphological differentiation in a highly social vertebrate

Animals may respond to ecological heterogeneity by genetic differentiation or phenotypic plasticity. Responses of organisms to their ecology can include adaptation at various levels of organization, including morphology, behaviour and social structure. Adaptations at one level might constrain or enhance adaptations on other levels, which highlights the importance of understanding their interactions. In highly social animals, understanding the influence of their ecological niche on the evolution and maintenance of complex social organization poses an intriguing challenge. Predation risk and habitat characteristics determine social structure in the cooperatively breeding cichlid Neolamprologus pulcher. Here we examine how varying combinations of these ecological factors across eight distinct populations influence morphological differentiation. We investigated the relationship between body shape and ecological parameters for 137 wild-caught individuals from eight distinct populations. Furthermore, we examined the genetic structure and differentiation among these populations using microsatellites. Finally, to disentangle heritable from plastic responses, we raised two successive generations from six populations in the laboratory under common garden conditions and screened 188 individuals for morphological differentiation. We found that body shape of N. pulcher strongly correlates with the measured ecological parameters. Low predation risk, low habitat structure and small shelter size favoured shallow bodies, whereas at the opposite end of these environmental gradients deep body shapes prevail. These consistent morphological differences persisted over two laboratory-reared generations, revealing a heritable basis. In contrast to the significant effect of local ecology on morphological differentiation between populations, both geographical and genetic distance had little explanatory power, suggesting that morphological differentiation between populations is not a simple by-product of genetic isolation. Remarkably, the largest difference in body depth emerged between the two populations located closest to each other, but differing strongly in their ecological niche. These results highlight that morphological variation is a key component of local adaptation in neighbouring populations of a highly social species. Such morphological differentiation has the potential to influence individual cooperative behaviour, which will eventually feed back on group structure and mediate the evolution and maintenance of complex social systems. A free Plain Language Summary can be found within the Supporting Information of this article.

Automated summary

Animals may respond to ecological heterogeneity through genetic differentiation or phenotypic plasticity, adaptation at various levels of organization, and the influence of ecological factors on morphological differentiation can be significant. However, geographical and genetic distance have limited explanatory power for morphological differences between populations.