More reliable estimates of divergence times in Pan using complete mtDNA sequences and accounting for population structure

Abstract

Here, we report the sequencing and analysis of eight complete mitochondrial genomes of chimpanzees (Pan troglodytes) from each of the three established subspecies (P. t. troglodytes, P. t. schweinfurthii and P. t. verus) and the proposed fourth subspecies (P. t. ellioti). Our population genetic analyses are consistent with neutral patterns of evolution that have been shaped by demography. The high levels of mtDNA diversity in western chimpanzees are unlike those seen at nuclear loci, which may reflect a demographic history of greater female to male effective population sizes possibly owing to the characteristics of the founding population. By using relaxed-clock methods, we have inferred a timetree of chimpanzee species and subspecies. The absolute divergence times vary based on the methods and calibration used, but relative divergence times show extensive uniformity. Overall, mtDNA produces consistently older times than those known from nuclear markers, a discrepancy that is reduced significantly by explicitly accounting for chimpanzee population structures in time estimation. Assuming the human-chimpanzee split to be between 7 and 5 Ma, chimpanzee time estimates are 2.1-1.5, 1.1-0.76 and 0.25-0.18 Ma for the chimpanzee/bonobo, western/(eastern + central) and eastern/central chimpanzee divergences, respectively.

Figure 1.

Maximum-likelihood phylogeny of chimpanzees, human and gorilla. Full mitochondrial genome (excluding the D-loop) and 13 mitochondrial protein-coding genes gave similar results. The geographical location of the chimpanzee populations is shown. Bootstrap values are shown near each node.

Figure 2.

Compilation of estimated divergence times between chimpanzees and bonobos and within chimpanzees from literature (autosomal loci only, filled circle) and this study (MDT, cross; BEAST (2 + 1), square).

Figure 3.

Timetrees obtained from BEAST (2 + 1 model) from 4F degenerate sites. The time scale is in million years (Ma). Both trees used the gorilla/human + chimpanzee calibration (10.0–6.5 Ma). Additionally, the upper tree used the human/chimpanzee (H/C) calibration range of 6.5–4.2 Ma while the lower tree fixed it at 6.5 Ma.