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Comparative genomics of parallel evolution in repeated adaptive radiations

Final Report Summary - GENADAP (Comparative genomics of parallel evolution in repeated adaptive radiations)

This ERC advanced grant, GenAdap dealt with the comparative genomics of parallel evolution and speciation in repeated adaptive radiations of crater lake cichlid fish.
Biological diversity is created through the formation of new species, and adaptive radiations (groups of closely related species) that arose by ecological speciation are seen as a major source of biodiversity. Even more than 150 years after the publication of the Origin of Species much about speciation and adaptation still is debated – such as the role of natural selection that Darwin not only saw for adaptation, but also speciation. Replicate instances of repeated adaptive radiations that arose by divergent natural selection are one of the most informative biological contexts in which to investigate how adaptive traits and new species evolve. In particular, repeated radiations with parallel adaptations provide rigor to infer the genetic basis of species differences and adaptations. But, in only a small handful of examples have genes involved in speciation (those, which cause some form of reproductive isolation) and adaptations been identified so far. Therefore, understanding debated fundamental issues on the genetics of adaptation, and speciation under sympatric geographic conditions will benefit from knowing how much and what portions of the genome are involved in adaptive speciation and what kind of genes, and what kind of genetic changes result in (parallel) adaptations. Speciation can occur even in the absence of geographic barriers, but the dynamics of gene flow and recombination versus divergent selection affect how like it is to happen. The role of the genetic architecture of traits under divergent selection during the formation of species with gene flow remains hotly debated. Information about genomics of adaptations and of species formation requires direct measurements of selection on the genome. Based on almost 500 sequenced genomes of 19 populations from the young parallel adaptive radiations of the Nicaraguan Midas cichlid crater lake species complex (Amphilophus cf. citrinellus), we discovered the genomic bases of divergent traits that play a role in ecological divergence and sexual selection. We found that hypertrophied lips and a color polymorphism are each caused by single genetic loci, while changes in body form and dentition are polygenic and loci dispersed throughout the genome. Genome-wide differentiation was found to be surprisingly extremely small except for those genomic regions that are associated with those monogenic traits. Peculiarly, genomic differentiation is ten-fold more pronounced between species that phenotypically differ in those traits with a polygenic genetic basis. Contrary to common expectation simple trait architectures are apparently not always as conducive to stable speciation-with-gene-flow as previously thought, whereas polygenic trait architectures can promote rapid speciation in sympatry.