Ancestral Hybridization Facilitated Species Diversification in the Lake Malawi Cichlid Fish Adaptive Radiation

The adaptive radiation of cichlid fishes in East Afrian Lake Malawi encompasses over 500 species that are believed to have evolved within the last 800 thousand years from a common founder population. It has been proposed that hybridisation between ancestral lineages can provide the genetic raw material to fuel such exceptionally high diversification rates, and evidence for this has recently been presented for the Lake Victoria Region cichlid superflock. Here we report that Lake Malawi cichlid genomes also show evidence of hybridisation between two lineages that split 3-4 million years ago, today represented by Lake Victoria cichlids and the riverine Astatotilapia sp. ‘ruaha blue’. The two ancestries in Malawi cichlid genomes are present in large blocks of several kilobases, but there is little variation in this pattern between Malawi cichlid species, suggesting that the large-scale mosaic structure of the genomes was largely established prior to the radiation. Nevertheless, tens of thousands of polymorphic variants apparently derived from the hybridisation are interspersed in the genomes. These loci show a striking excess of differentiation across ecological subgroups in the Lake Malawi cichlid assemblage, and parental alleles sort differentially into benthic and pelagic Malawi cichlid lineages, consistent with strong differential selection on these loci during species divergence. Furthermore, these loci are enriched for genes involved in immune response and vision, including opsin genes previously identified as important for speciation. Our results reinforce the role of ancestral hybridisation in explosive diversification by demonstrating its significance in one of the largest recent vertebrate adaptive radiations.