Mitochondrial sequences show diverse evolutionary histories of African hominoids

Abstract

Phylogenetic trees for the four extant species of African hominoids are presented, based on mtDNA control region-1 sequences from 1,158 unique haplotypes. We include 83 new haplotypes of western chimpanzees and bonobos. Phylogenetic analysis of this enlarged database, which takes intraspecific geographic variability into account, reveals different patterns of evolution among species and great heterogeneity in species-level variation. Several chimpanzee and bonobo clades (and even single social groups) have retained substantially more mitochondrial variation than is seen in the entire human species. Among the 811 human haplotypes, those that branch off early are predominantly but not exclusively African. Neighbor joining trees provide strong evidence that eastern chimpanzee and human clades have experienced reduced effective population sizes, the latter apparently since the Homo sapiens-neanderthalensis split. Application of topiary pruning resolves ambiguities in the phylogenetic tree that are attributable to homoplasies in the data set. The diverse patterns of mtDNA sequence variation seen in today's hominoid taxa probably reflect historical differences in ecological plasticity, female-biased dispersal, range fragmentation over differing periods of time, and competition among social groups. These results are relevant to the origin of zoonotic diseases, including HIV-1, and call into question some aspects of the current taxonomic treatment and conservation management of gorillas and chimpanzees.

Figure 1

Unrooted phylogram of the neighbor-joining tree of 1,158 different CRI sequences before (A) and after (B) after topiary pruning to level P_L = 8 to remove homoplasies. Bootstrap values ≥50% for the primary internodes are shown. Position of the midpoint root is indicated by arrow. Different colors indicate species (humans, bonobos, and gorillas) and subspecies (chimpanzees). Symbols indicate individuals belonging to the same social group: □, Taï Forest, Côte d’Ivoire; ■, Solo, Mali; ○, Eyengo, Lomako, Democratic Republic of Congo; ●, E-group, Wamba, Democratic Republic of Congo; ∗, Kasakela, Gombe, Tanzania.

Figure 2

Pairwise sequence divergence in humans and other African hominoids.

Figure 3

Effects of topiary pruning. (A) Progressive effect of pruning of the whole data set on the hominid clade from P_L = 0–8. Exclusively African (red), non-African (black), one Indian (orange), neanderthal (blue), and numt (gray) haplotypes are shown. (B) Pruning results in an increase in phylogenetic information, measured as change in negative skew of the length distribution of 10,000 random trees at each pruning level (●), relative to the random removal of the same number of bases (□).