Developmental divergence in gene regulation underlies trophic innovation in Lake Victoria cichlids

Abstract The role of developmental shifts in the emergence of ecological diversity during adaptive radiation remains largely uncharacterized. Here, we investigate the developmental gene regulatory landscape of trophic innovation in the rapid adaptive radiation of cichlid fishes from Lake Victoria (LV), which evolved into hundreds of species in less than 16 000 years. By analysing the whole transcriptomes of functionally decoupled oral and pharyngeal jaws from two life stages, we show that both gene and isoform expression are highly developmentally dynamic in ecologically divergent species. Gene regulation is conserved at the tissue level in the jaws of ecologically distinct species at the early life stage and then diverges into guild-specific developmental programmes in adults. We further show that gene expression and alternative splicing regulate different pathways, particularly in adults, suggesting that these two gene regulatory mechanisms are constrained to perform non-redundant functions, at least at the early stages of adaptive radiation. Interestingly, we found that splicing-mediated exonization of the craniofacial development gene, kaznb, may have contributed to the evolution of herbivory in LV cichlids. Overall, our study suggests that ontogenetic shifts in gene regulation play a key role in the rapid emergence of guild-specific ecological diversity in LV cichlids.