Parallel trophic diversifications in polyploid cyprinid fish from East Africa: from preadaptive polymorphism to trophic specialization

Abstract

Trophic diversification is one of the main mechanisms driving the adaptive radiation. The polyploid lineage of the cyprinid genus Labeobarbus represent an excellent model for studying the trophically-based adaptive radiation in either lacustrine or riverine environments. Recently discovered four diversifications in rivers of the Ethiopian Highlands (East Africa) demonstrate independently evolved repeated mouth polymorphisms each represented by four core mouth phenotypes: (i) generalized, (ii) thick-lipped, (iii) scraping, and iv) large-mouthed. Mouth phenotypes in some radiations can be further divided to subtypes representing from four to eight sympatric ecomorphs. Using the stable isotope and gut content analyses we tested hypothesis on trophic resource partitioning within each radiation, revealed disparity in degree of diversification between radiations and tried to reconstruct the process of trophic diversification. Three of four radiations demonstrated partitioning of trophic resources within five trophic niches: i) detritophagy, ii) macrophytophagy, iii) invertivorous benthophagy, iv) periphyton feeding, and v) piscivory. The studied riverine radiations were likely at the different stages of the diversification. One radiation having a similar set of mouth phenotypes was not trophically divergent displaying a remarkable decouple of form and function. A unique case of ecologically non-functional mouth polymorphism at an incipient stage of trophic diversification supports a concept of the plasticity-first evolution. This phenomenon stems from the pre-existing genomic templates of mouth polymorphism ancestrally inherited upon the allopolyploid origin of the Labeobarbus lineage. The predetermined and preadaptive mouth polymorphism can be considered a key innovation of the Labeobarbus that promoted to resource-based diversification via adaptive radiation.