Developmental tinkering of gene regulation facilitated super rapid adaptive radiation

Abstract

AbstractDevelopmental shifts in gene regulation underlying key innovations remain largely uncharacterised at short evolutionary timescales. Here we investigate the gene expression and alternative splicing landscape of trophic innovations in the fastest vertebrate adaptive radiation: cichlid fishes from Lake Victoria. Using whole-transcriptomes of the oral and pharyngeal jaws from two life stages of species adapted to divergent trophic niches, we show that gene and isoform expression were fine-tuned during development to generate specialised species-specific eco-morphologies in adults. This is a striking contrast to mammals where tissue-specific gene expression is conserved across species even after 90 million years of evolution and suggests that gene regulatory programs have evolved rapidly in Lake Victoria cichlids. We show that gene expression during development is highly modular and this developmental modularity may have facilitated trophic diversification. Furthermore, we discovered that retrotransposon mediated exonisation of a craniofacial development gene, KAZNB, has contributed to the evolution of a novel trophic niche. This advocates for the importance of exonisation and the splicing machinery in rapidly expanding the coding capacity of the genome <15,000 years. We also identified a major transcription factor of craniofacial remodelling in Darwin’s finches, ALX3, to have contributed to jaw divergence in Lake Victoria cichlids. Overall, our results suggest that developmental tinkering of gene regulation is a major facilitator of key innovations and diversification during adaptive radiation.