Highly modular genomic architecture underlies combinatorial mechanism of speciation and adaptive radiation

Hybridisation can fuel rapid adaptive radiation, but how it enables the formation of phenotypically highly dimensional species-rich radiations remains unclear. We investigated this by analysing genotype-phenotype associations for 14 ecological (trophic, body patterns) and mating traits (nuptial colour) across 107 species of Lake Victoria cichlid fishes. We find weak trait covariance across the radiation, with many different trait combinations constituting different species. Across the radiation, polygenic, redundant, and lowly pleiotropic genomic architectures of hybrid origin underlie the repeated evolution of key traits. Such independent genomic modules can be reshuffled and recombined like Lego bricks, generating diverse trait combinations from a finite number of elements. During speciation, dispersed oligogenic trait modules become coupled through long-range linkage disequilibrium. We propose that this genomic and phenotypic modularity emerged from repeated cycles of past hybridisation, enabling superfast adaptive radiation through combinatorial speciation.