Evolutionary dynamics of gene and isoform regulation underlying rapid and parallel adaptive radiations

Adaptive radiation is a major driver of biodiversity. In some of the largest radiations, the pace of morphological change far outstrips the protein-coding mutation rate, suggesting that gene regulation may be important for diversification. Yet, the specific gene regulatory mechanisms shaping adaptive radiation remain poorly understood. Analysing of 200 transcriptomes from three independent but phylogenetically nested African cichlid adaptive radiations we show that alternative splicing (AS) evolved faster than gene expression (GE), playing a pivotal role in shaping novel trophic adaptations in the youngest and most species rich radiations in Lakes Victoria and Malawi. This divergence was largely driven by ancestral alternative isoforms, which, though present at low levels in related lineages that did not form radiations, increased in frequency during adaptive radiation. In addition, novel isoforms of craniofacial genes - some evolving within just a few thousand years contributed further to adaptation. The rapid turnover of AS is consistent with periods of relaxed selection followed by directional selection on alternative isoforms and splice sites, a dynamic that may have preserved a rich cache of isoform variation in these radiations and enabled ecological diversification as adaptive zones became available. We argue that the interplay between splicing and different forms of selection facilitates the generation and maintenance of protein-coding diversity, promoting evolutionary innovation into many ecologically different species at extremely short timescales. Significance statementAdaptive radiation--when species rapidly diversify to fill new ecological niches--is a key driver of biodiversity but its underlying molecular mechanisms remain unclear. Using comparative transcriptome sequencing across multiple African cichlid fish adaptive radiations, we found that rapid changes in alternative splicing--the process generating different protein-coding isoforms from the same gene--contributed more to early ecological divergence than shifts in gene expression levels. Most adaptive isoforms were present at low levels in the ancestor of these fishes but some new isoforms evolved remarkably fast, shaping diverse ecologies. We show that alternative splice variation, often thought to be biological "noise," can be a powerful and labile source of rapid evolutionary innovation during early stages of adaptive radiation.