Charting the genomic landscape of hybridisation and introgression across the Lake Malawi cichlid adaptive radiation
Speciation has classically been viewed as a process requiring complete reproductive isolation between species. However, genomic studies increasingly show that gene flow, the transfer of genetic material between species via hybridization, can promote adaptation and speciation by boosting genetic variation within lineages. For adaptive radiations, where many ecologically diverse species arise rapidly from a common ancestor, gene flow may be an important source of variation for selection to act upon. The adaptive radiations of cichlid fish found in the East African Great Lakes, which show extraordinary species diversity, are an excellent system for studying the effect of gene flow in the evolution of biodiversity. In each of the major radiations, those of Lake Tanganyika, the Lake Victoria region, and Lake Malawi, gene flow has been shown to be a contributing factor in the generation of species. For the Lake Malawi radiation, which consists of around 800 species that evolved within the last 800 thousand years, only one gene flow event was previously known: the ancestral Malawi lineage hybridized with a riverine species related to Astatotilapia sp. "Ruaha blue," forming a ‘hybrid swarm’ that initialized the radiation. Still, little is known about the true extent, impact and genomic footprint of gene flow in the Malawi radiation. Using a whole-genome sequencing dataset of 239 Malawi and 76 non-Malawi African cichlid species, we tested for additional gene flow events that affected the Malawi radiation, both before and after the radiation’s onset. Alongside A. sp. "Ruaha blue," we found that three further lineages, related to the Congo South Africa (CSA), Pseudocrenilabrus, and Orthochromis groups, also likely contributed to the Malawi hybrid swarm. We identified and characterized hundreds of long genomic tracts of foreign CSA and Pseudocrenilabrus ancestry which were segregated amongst Malawi species. We found signals of divergent selection among Malawi species, supporting adaptive contributions from CSA- and Pseudocrenilabrus-derived ancestry. We found complex patterns of ancestry sharing between not just the Malawi radiation and neighbouring riverine species, but also with species from the Lake Victoria region, indicating previously unrecognized genetic connectivity among East African cichlids. Overall, these findings suggest the Malawi radiation formed through repeated intermingling of diverse cichlid lineages and that Malawi genomes are comprised of a complex mosaic of ancestries varying among species and individuals. Our results support the growing recognition that gene flow is an important driver of biodiversity.