Great-ape Y-Chromosome and mitochondrial DNA phylogenies reflect sub-species structure and patterns of mating and dispersal

Abstract

The distribution of genetic diversity in great-ape species is likely to have been affected by patterns of dispersal and mating. This has previously been investigated by sequencing autosomal and mitochondrial DNA (mtDNA), but large-scale sequence analysis of the male-specific region of the Y Chromosome (MSY) has not yet been undertaken. Here we use the human MSY reference sequence as a basis for sequence capture and read mapping in 19 great-ape males, combining the data with sequences extracted from the published whole genomes of 24 additional males to yield a total sample of 19 chimpanzees, 4 bonobos, 14 gorillas, and 6 orangutans, in which interpretable MSY sequence ranges from 2.61 to 3.80 Mb. This analysis reveals thousands of novel MSY variants and defines unbiased phylogenies. We compare these with mtDNA-based trees in the same individuals, estimating time-to-most-recent common ancestor (TMRCA) for key nodes in both cases. The two loci show high topological concordance and are consistent with accepted (sub)species definitions, but time-depths differ enormously between loci and (sub)species, likely reflecting different dispersal and mating patterns. Gorillas and chimpanzees/bonobos present generally low and high MSY diversity respectively, reflecting polygyny versus multimale-multifemale mating. However, particularly marked differences exist among chimpanzee subspecies: while the western chimpanzee MSY phylogeny has a TMRCA of only 13.2 (10.8-15.8) thousand years, that for central chimpanzees exceeds 1 million years. Cross-species comparison within a single MSY phylogeny emphasises the low human diversity, and reveals species-specific branch length variation that may reflect differences in long-term generation times.