Comparative genomic analyses provide new insights into evolutionary history and conservation genomics of gorillas

Abstract

Genome sequencing is a powerful tool to understand species evolutionary history, uncover genes under selection, which could be informative of local adaptation, and infer measures of genetic diversity, inbreeding and mutational load that could be used to inform conservation efforts. Gorillas, critically endangered primates, have received considerable attention and with the recently sequenced Bwindi mountain gorilla population, genomic data is now available from all gorilla subspecies and both mountain gorilla populations. Here, we reanalysed this rich dataset with a focus on evolutionary history, local adaptation and genomic parameters relevant for conservation. We estimate a recent split between western and eastern gorillas of 150,000–180,000 years ago, with gene flow around 20,000 years ago, primarily between the Cross River and Grauer’s gorilla subspecies. This gene flow event likely obscures evolutionary relationships within eastern gorillas: after excluding putatively introgressed genomic regions, we uncover a sister relationship between Virunga mountain gorillas and Grauer’s gorillas to the exclusion of Bwindi mountain gorillas. This makes mountain gorillas paraphyletic. Eastern gorillas are less genetically diverse and more inbred than western gorillas, yet we detected lower genetic load in the eastern species. Analyses of indels fit remarkably well with differences in genetic diversity across gorilla taxa as recovered with nucleotide diversity measures. We also identified genes under selection and unique gene variants specific for each gorilla subspecies, encoding, among others, traits involved in immunity, diet, muscular development, hair morphology and behavior. The presence of this functional variation suggests that the subspecies may be locally adapted. In conclusion, using extensive genomic resources we provide a comprehensive overview of gorilla genomic diversity, including a so-far understudied Bwindi mountain gorilla population, identify putative genes involved in local adaptation, and detect population-specific gene flow across gorilla species.