Theory suggests that speciation with gene flow is most likely when both sexual and ecological selection are divergent or disruptive. Divergent sexual and natural selection on the visual system have been demonstrated before in sympatric, morphologically similar sister species of Lake Victoria cichlids, but this does not explain the subtle morphological differences between them. To investigate the significance of natural selection on morphology during speciation, we here ask whether the prevalence of disruptive ecological selection differs between sympatric sister species that are at different stages of speciation. Some of our species pairs do () and others do not () differ distinctively in sexually selected male nuptial coloration. We find that (i) evidence for disruptive selection, and for evolutionary response to it, is prevalent in traits that are differentiated between sister species; (ii) prevalence of both predicts the extent of genetic differentiation; and (iii) genetic differentiation is weaker in species pairs with conserved male nuptial coloration. Our results speak to the existence of two different mechanisms of speciation with gene flow: speciation mainly by sexual selection tightly followed by ecological character displacement in some cases and speciation mainly by divergent ecological selection in others.
Adaptive radiation research typically relies on the study of evolution in retrospective, leaving the predictive value of the concept hard to evaluate. Several radiations, including the cichlid fishes in the East African Great Lakes, have been studied extensively, yet no study has investigated the onset of the intraspecific processes of niche expansion and differentiation shortly after colonization of an adaptive zone by cichlids. Haplochromine cichlids of one of the two lineages that seeded the Lake Victoria radiation recently arrived in Lake Chala, a lake perfectly suited for within-lake cichlid speciation. Here, we infer the colonization and demographic history, quantify phenotypic, ecological and genomic diversity and diversification, and investigate the selection regime to ask if the population shows signs of diversification resembling the onset of adaptive radiation. We find that since their arrival in the lake, haplochromines have colonized a wide range of depth habitats associated with ecological and morphological expansion and the beginning of phenotypic differentiation and potentially nascent speciation, consistent with the very early onset of an adaptive radiation process. Moreover, we demonstrate evidence of rugged phenotypic fitness surfaces, indicating that current ecological selection may contribute to the phenotypic diversification.
Cichlids of the genus Oreochromis ("Tilapias") are intensively used in aquaculture around the world. In many cases when "Tilapia" were introduced for economic reasons to catchments that were home to other, often endemic, Oreochromis species, the loss of native species followed. Oreochromis hunteri is an endemic species of Crater Lake Chala on the slopes of Mount Kilimanjaro, and is part of a small species flock in the upper Pangani drainage system of Tanzania. We identified three native and three invasive Oreochromis species in the region. Reconstructing their phylogeography we found that O. hunteri is closely related to, but distinct from the other members of the upper Pangani flock. However, we found a second, genetically and phenotypically distinct Oreochromis species in Lake Chala whose origin we cannot fully resolve. Our ecological and ecomorphological investigations revealed that the endemic O. hunteri is currently rare in the lake, outnumbered by each of three invasive cichlid species. It is mitochondrially, phenotypically and trophically distinct from all others. The occurrence of the formerly abundant O. hunteri in such small numbers, its narrow habitat restriction and its limited morphological variability suggest recent population decline and loss of niche breadth in this critically endangered endemic cichlid species.
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