Developmental divergence in gene regulation among rapidly radiating cichlid species

Abstract

Developmental shifts in gene regulation underlying key innovations remain largely uncharacterized over short evolutionary timescales. Here, we investigate the gene regulatory landscape of trophic innovations in the fastest vertebrate adaptive radiation: cichlid fishes from Lake Victoria. By analyzing the whole-transcriptomes of the oral and pharyngeal jaws from two life stages in five species adapted to divergent trophic niches, we find that both gene and isoform expression are developmentally dynamic. Expression signatures are most similar across jaws at the early stage and then diverge into species-specific developmental programs in adults. However, even at the early stage, expression in the oral jaws of species adapted to herbivory is distinct from those of carnivores, a pattern not observed for the pharyngeal jaws. We further show that differentially expressed and spliced genes between herbivorous and carnivorous species regulate different genes and pathways, particularly in adults. Interestingly, we find that splicing-mediated exonization of a craniofacial development gene, kaznb, may have contributed to the evolution of herbivory in Lake Victoria cichlids. Overall, our results contribute to our understanding of how ontogenetic shifts in gene regulation can facilitate rapid adaptive evolution.