Liem’s paradox in parallel trophic diversifications of polyploid fish: from preadaptive polymorphism to trophic specialization

Abstract

The polyploid lineage of the cyprinid genus Labeobarbus provides an excellent model for studying trophic-driven adaptive radiations. Four recently discovered diversifications in rivers of the Ethiopian Highlands (East Africa) show independent repeated evolutions of mouth polymorphisms each represented by four mouth phenotypes: (1) generalized, (2) thick-lipped, (3) scraping, and (4) large-mouthed. Using stable isotope and gut content analyses, we tested hypothesis on the partitioning of trophic resources within each radiation and revealed differences in degree of diversification between radiations. Three out of four radiations showed partitioning of trophic resources within five trophic niches: (1) detritophagy, (2) macrophytophagy, (3) benthophagy, (4) periphyton feeding, and (5) piscivory. The radiations are likely to be at different stages of diversification. One radiation with a similar set of mouth phenotypes was not trophically divergent and showed a remarkable decoupling of form and function. A case of ecologically non-functional mouth polymorphism is a bright example of the Liem’s paradox and supports a concept of the plasticity-first evolution. This might be based on pre-existing genomic templates inherited from ancestral lineages that participated in the polyploidization of the Labeobarbus lineage. Predetermined and preadaptive mouth polymorphism can be considered a key innovation of Labeobarbus that promotes to resource-based diversification.