Deep genetic substructure within bonobos

Abstract

Establishing the genetic and geographic structure of populations is fundamental, both to understand their evolutionary past and preserve their future. Nevertheless, the patterns of genetic population structure are unknown for most endangered species. This is the case for bonobos (Pan paniscus), which, together with chimpanzees (Pan troglodytes), are humans' closest living relatives. Chimpanzees live across equatorial Africa and are classified into four subspecies,¹ with some genetic population substructure even within subspecies. Conversely, bonobos live exclusively in the Democratic Republic of Congo and are considered a homogeneous group with low genetic diversity,² despite some population structure inferred from mtDNA. Nevertheless, mtDNA aside, their genetic structure remains unknown, hampering our understanding of the species and conservation efforts. Mapping bonobo genetic diversity in space is, however, challenging because, being endangered, only non-invasive sampling is possible for wild individuals. Here, we jointly analyze the exomes and mtDNA from 20 wild-born bonobos, the whole genomes of 10 captive bonobos, and the mtDNA of 136 wild individuals. We identify three genetically distinct bonobo groups of inferred Central, Western, and Far-Western geographic origin within the bonobo range. We estimate the split time between the central and western populations to be ∼145,000 years ago and genetic differentiation to be in the order of that of the closest chimpanzee subspecies. Furthermore, our estimated long-term N_e for Far-West (∼3,000) is among the lowest estimated for any great ape lineage. Our results highlight the need to attend to the bonobo substructure, both in terms of research and conservation.

Keywords: bonobo; conservation; divergence; endangered species; exome; genetic diversity; genome; great ape; pan paniscus; population substructure.