Evolutionary history of chimpanzees inferred from complete mitochondrial genomes

Abstract

Investigations into the evolutionary history of the common chimpanzee, Pan troglodytes, have produced inconsistent results due to differences in the types of molecular data considered, the model assumptions employed, and the quantity and geographical range of samples used. We amplified and sequenced 24 complete P. troglodytes mitochondrial genomes from fecal samples collected at multiple study sites throughout sub-Saharan Africa. Using a "relaxed molecular clock," fossil calibrations, and 12 additional complete primate mitochondrial genomes, we analyzed the pattern and timing of primate diversification in a Bayesian framework. Our results support the recognition of four chimpanzee subspecies. Within P. troglodytes, we report a mean (95% highest posterior density [HPD]) time since most recent common ancestor (tMRCA) of 1.026 (0.811-1.263) Ma for the four proposed subspecies, with two major lineages. One of these lineages (tMRCA = 0.510 [0.387-0.650] Ma) contains P. t. verus (tMRCA = 0.155 [0.101-0.213] Ma) and P. t. ellioti (formerly P. t. vellerosus; tMRCA = 0.157 [0.102-0.215] Ma), both of which are monophyletic. The other major lineage contains P. t. schweinfurthii (tMRCA = 0.111 [0.077-0.146] Ma), a monophyletic clade nested within the P. t. troglodytes lineage (tMRCA = 0.380 [0.296-0.476] Ma). We utilized two analysis techniques that may be of widespread interest. First, we implemented a Yule speciation prior across the entire primate tree with separate coalescent priors on each of the chimpanzee subspecies. The validity of this approach was confirmed by estimates based on more traditional techniques. We also suggest that accurate tMRCA estimates from large computationally difficult sequence alignments may be obtained by implementing our novel method of bootstrapping smaller randomly subsampled alignments.

FIG. 1.

Amplification of full-length mitochondrial genomic equivalents from chimpanzee fecal DNA. Amplicons are shown in relation to a previously published chimpanzee mitochondrial genome sequence (Genbank accession number: D38113) and are labeled as shown in Table 1.

FIG. 2.

Chimpanzee fecal sample collection sites in sub-Saharan Africa. International borders are shown in brown. Ranges of the four proposed chimpanzee subspecies are highlighted in color. The question mark (?) west of the lower Niger River indicates that the limited mtDNA sequences available to date from this region have clustered phylogenetically with P. t. verus (Gagneux et al. 2001). Collection sites were located in Cameroon (BB, BQ, CP, DP, MT, and WE), Cote d’Ivoire (TA), Republic of Congo (GT), Democratic Republic of Congo (BD, BU, WK), Gabon (LP), Rwanda (NY), and Tanzania (GM), as reported previously (Liu et al. 2008).

FIG. 3.

Phylogenetic reconstruction of the “chimpanzee-plus” mtDNA genomes alignment. mtDNA sequences (10,743 bp) were analyzed using the BMCMC approach in BEAST. The MCC tree is presented, with the Pan troglodytes clade shown boxed and enlarged. The subspecies of each sample was determined by mtDNA haplotype and is indicated by color. Posterior probabilities of well-supported nodes are represented by filled circles (90–99%) or asterisks (100%). Open circles indicate fossil-calibrated nodes. The P. t. troglodytes lineage is paraphyletic, and one of its samples (WE464) was collected in the P. t. ellioti range (see text). Specific details of the node date estimations are included in Table 2.

FIG. 4.

Midpoint-rooted tree demonstrating the “clock-like” nature of chimpanzee mtDNA evolution. Twenty-six P. troglodytes and one P. paniscus sequence were analyzed using the BMCMC approach in MrBayes. The majority-rule consensus tree is presented. Branch tips are colored by species or subspecies. Relationship patterns are the same as in figure 3, but sequence names are removed for clarity. All nodes are well supported, and posterior probabilities of all major nodes are 100%.