High levels of Y-chromosome nucleotide diversity in the genus Pan

Abstract

Although some mitochondrial, X chromosome, and autosomal sequence diversity data are available for our closest relatives, Pan troglodytes and Pan paniscus, data from the nonrecombining portion of the Y chromosome (NRY) are more limited. We examined approximately 3 kb of NRY DNA from 101 chimpanzees, seven bonobos, and 42 humans to investigate: (i) relative levels of intraspecific diversity; (ii) the degree of paternal lineage sorting among species and subspecies of the genus Pan; and (iii) the date of the chimpanzee/bonobo divergence. We identified 10 informative sequence-tagged sites associated with 23 polymorphisms on the NRY from the genus Pan. Nucleotide diversity was significantly higher on the NRY of chimpanzees and bonobos than on the human NRY. Similar to mtDNA, but unlike X-linked and autosomal loci, lineages defined by mutations on the NRY were not shared among subspecies of P. troglodytes. Comparisons with mtDNA ND2 sequences from some of the same individuals revealed a larger female versus male effective population size for chimpanzees. The NRY-based divergence time between chimpanzees and bonobos was estimated at approximately 1.8 million years ago. In contrast to human populations who appear to have had a low effective size and a recent origin with subsequent population growth, some taxa within the genus Pan may be characterized by large populations of relatively constant size, more ancient origins, and high levels of subdivision.

Figure 1

NRY maximum parsimony haplogroup tree. Haplogroup code names are defined in Results. Color coding refers to taxonomic status within Pan. Numbers associated with branches correspond to the number of point mutational events followed by the number of indels in parentheses. Indels were also treated as mutational events in a branch and bound search analysis (55). Dotted lines denote uncertainty associated with Pt?1 and Pt?2.

Figure 2

SPLIT_TIME tree for humans, bonobos, and chimpanzees. The (observed, expected) numbers of mutations are shown on each branch. The total number of expected mutations is random and is not conditional on the total number of observed mutations. Observed mutations on the branches leading to Homo and Pan include a + symbol referring to eight mutations, which could not be assigned to one particular branch. Numbers within boxes correspond to the (observed, expected) numbers of mutations within each taxonomic group. The dotted line indicates the chimpanzee-bonobo divergence time (1.8 million years) estimated with the Pt?1 haplogroup. When the Pt?1 haplogroup was excluded from the analysis, the divergence time remained the same; however, the chimpanzee TMRCA was 610,000 ± 300,000 years and the observed and expected numbers of mutations were 11 and 10.4, respectively.