Adaptive cellular evolution in the intestine of hyperdiverse cichlid fishes

Abstract The ability of animals to efficiently track down and digest food is crucial for their survival, and the specialization to different diets is a major driver of diversification in this group 1–3 . Although the evolution of feeding structures has been studied extensively in this context 4–6 , the nature and extent of adaptations in the digestive tract remain poorly understood. Here, we examine dietary adaptations in the intestines of one of the largest adaptive radiations in vertebrates, the cichlid fishes of Lake Tanganyika. By generating comprehensive single-cell transcriptomic data for 24 Tanganyikan cichlid species with divergent feeding habits, and integrating this with eco-morphological and genomic information, we uncover that, at the cellular level, dietary adaptations primarily involve anterior enterocytes. In particular, we show that the relative abundances of anterior enterocytes as well as the gene expression profiles in this cell population evolved in response to rapid trophic specializations, and that these diet-related adaptations are driven by fast-evolving, cell-population-specific genes. Overall, our findings show that alterations in intestinal epithelium cell composition and in the cell-type-specific molecular makeup provided the substrate for trophic specializations, demonstrating that ecological adaptations target multiple layers of biological organization.