Positive Darwinian Selection Drives the Evolution of the Morphology-Related Gene, EPCAM, in Particularly Species-Rich Lineages of African Cichlid Fishes

Abstract

The study of genetic evolution within the context of adaptive radiations offers insights to genes and selection pressures that result in rapid morphological change. Cichlid fishes are very species-rich and variable in coloration, behavior, and morphology, and so provide a classical model system for studying the genetics of adaptive radiation. In this study, we researched the evolution of the epithelial cell adhesion molecule (EPCAM), a candidate gene for the adaptive evolution of morphology broadly, and skin development specifically, in fishes. We compared EPCAM gene sequences from a rapidly speciating African cichlid lineage (the haplochromines), a species-poor African lineage (Nile tilapia Oreochromis niloticus), and a very young adaptive radiation in the Neotropics (sympatric crater lake Midas cichlids, Amphilophus sp.). Our results, based on a hierarchy of evolutionary analyses of nucleotide substitution, demonstrate that there are different selection pressures on the EPCAM gene among the cichlid lineages. Several waves of positive natural selection were identified not only on the terminal branches, but also on ancestral branches. Interestingly, significant positive or directional selection was found in the haplochromine cichlids only but not the comparatively species-poor tilapia lineage. We hypothesize that the strong signal of selection in the ancestral African cichlid lineage coincided with the transition from riverine to lacustrine habitat. The two neotropical species for which we collected new sequence data were invariant in the EPCAM locus. Our results suggest that functional changes promoted by positive Darwinian selection are widespread in the EPCAM gene during African cichlid evolution.