Axel Jensen: Genomics of an African primate radiation

Abstract

Rather than presenting as a swarm of continuous trait variation, organisms tend to cluster in discrete groups with similar characteristics. Understanding the emergence and maintenance of these discontinuities, commonly recognized as species, is a fundamental goal in evolutionary biology. In this thesis, I use comparative phylogenomics to elucidate the evolutionary processes shaping the remarkable diversification of guenons (tribe Cercopithecini), a diverse African primate group comprising ~35 species that radiated over the past ~10-12 million years. In Paper I, I present a highly resolved guenon phylogeny, and demonstrate extensive ancestral gene flow, also between deeply divergent lineages with different karyotypes. I found that genomic regions with strong signals of introgression were enriched for immune genes, possibly representing adaptive introgression, and explore potential barriers to gene flow. Paper II focuses on the demography and evolution of the recently described guenon species Cercopithecus lomamiensis, and its sister species C. hamlyni. While both species are listed as vulnerable on the IUCN Red List, I found them to have high genetic diversity, without signs of inbreeding. I also investigate genomic signatures of selection in these species, focusing specifically on putative adaptations to terrestriality, a trait that makes them stand out in the predominantly arboreal genus Cercopithecus. In Paper III, I investigate the prevalence of Y chromosome introgression in guenons, which, in line with the expectations under Haldane’s rule, were rare in this primate group. A notable exception was found in Cercopithecus denti, which carries a Y chromosome that introgressed from C. mitis ~6 million years after their initial divergence. Negligible introgression in autosomal loci suggests that the introgressing Y chromosome reached fixation from a low initial frequency, pointing to a putative selective advantage over the ancestral Y chromosome. Lastly, in Paper IV, I investigate the extensive karyotype diversification among guenons, and whether it played a role in speciation. By assembling the genomes of eight species with different karyotypes, I identified 30 independent chromosomal fission events, and four fusions. I found that introgression was reduced on fissioned relative to conserved chromosomes in a previously identified gene flow event between C. cephus (2n = 66) and C. pogonias (2n = 72), suggesting a potential role of fissions as reproductive barriers. This thesis provides insights into the evolutionary forces that shaped one of the world’s most speciose primate radiations, contributing to a broader understanding of the genetics of species diversification.