On the genetic architecture of an adaptive radiation

How biodiversity evolves is of central interest to evolutionary biology. Adaptive radiations provide prime systems to investigate processes of biological diversification and speciation. The Lake Victoria haplochromine cichlid adaptive radiation stands out due to the exceptional speed with which a spectacular diversity of species have evolved within this lake. Several coinciding factors were likely key to the emergence of this radiation including ecological opportunity, sexual selection, and intrinsic genomic features. Furthermore, the radiation was seeded by a hybrid lineage derived from ancient hybridisation between two divergent species, which fuelled the radiation by providing large amounts of genetic variation. In my thesis, I investigate the ‘genetic architecture’ (the distribution and effects of genetic variants in the genome) that underpin traits or genomic features that may have played key roles in the rapid diversification and in the evolution and maintenance of reproductive barriers in the Lake Victoria cichlid adaptive radiation. In Chapter 1, I compare the genetic architecture of male nuptial colour, a trait under sexual selection, in a sympatric pair that exhibits some gene flow vs a non-sympatric pair. In the sympatric pair, I find the presence of moderate to large effect loci and some evidence for linkage/pleiotropy, which might provide a genetic architecture that is robust to gene flow. The absence of such an architecture in the non-sympatric pair could explain why these species seem to not be able to persist in sympatry. In Chapter 2, I investigate the genetic architecture of a whole suite of traits that distinguish representative species of two different trophic levels. Transition between trophic levels have occurred multiple times and rapidly in this radiation. I find a distributed architecture with little evidence for linkage/pleiotropy (but some moderate to large effect loci). This suggests that at the stage where these transitions occurred, genome-wide LD had to build between multiple unlinked genomic regions underpinning traits that had to change in a concerted fashion, which would have required both divergent selection and reproductive isolation. In Chapter 3, I report a novel sex determining chromosome in African cichlids, that acts as XY in one and ZW in another lineage. This highlights the high evolvability of sex determination in these radiations, which might also play a role in speciation. Finally, Chapter 4 is the first empirical test of the hypothesis that postzygotic intrinsic incompatibilities could be important in speciation from a hybrid swarm, in a process where they become sorted between subpopulations of a hybrid swarm and contribute to reproductive isolation between the emerging species. I screen whole genomes of 94 species of the Lake Victoria radiation and several hybrid crosses for genotype ratio distortions. I find signatures that could be consistent with postzygotic incompatibilities, and significant overlap of putative incompatibility regions with regions of high differentiation between sympatric sister species. I end with a general discussion of my findings and suggestions for future work.