A speciation continuum within repeated origin of hypertrophied lips in cyprinid fish from East Africa

Abstract

Trophic specialization plays a major role in ecological speciation. Multiple adaptive radiations among cyprinid fish of the genus Labeobarbus were recently discovered in riverine environments of the Ethiopian Highlands, East Africa. These radiations contain parallel diversifications of trophic morphology, including thick-lipped or ‘rubberlip’ phenotype, whose trophic function remains largely unexplored. To test the adaptive value of thickened lips, to identify the ecological niche of the thick-lipped ecomorphs, and to test of these ecomorphs are the products of speciation we studied six sympatric pairs of ecomorphs with hypertrophied lips and the normal lip structure from different riverine basins. Trophic morphology, diet, stable isotope (15N and 13C) signatures as well as mtDNA markers and genome-wide SNP variation were analyzed. Our results show that thick-lipped ecomorphs partition trophic resources with generalized ecomorphs in only one half of the examined sympatric pairs despite the pronounced divergence in lip structure. In these thick-lipped ecomorphs that were trophically diverged, the data on their diet along with the elevated 15N values suggest an insectivorous specialization different from the basal omnivorous-detritivouros feeding mode of generalized ecomorphs. Genetic data confirmed an independent and parallel origin of all six lipped ecomorphs. Yet, only one of those six thick-lipped ecomorphs had a notable genetic divergence with sympatric non-lipped ecomorphs based on nuclear SNPs data (FST = 0.21). Sympatric pairs can be sorted by combinations of phenotypic, ecological, and genetic divergence within the speciation continuum from an ecologically non-functional mouth polymorphism via ecologically functional polymorphism to completed speciation via divergent evolution.