The divergence of chimpanzee species and subspecies as revealed in multipopulation isolation-with-migration analyses

Abstract

The divergence of bonobos and three subspecies of the common chimpanzee was examined under a multipopulation isolation-with-migration (IM) model with data from 73 loci drawn from the literature. A benefit of having a full multipopulation model, relative to conducting multiple pairwise analyses between sampled populations, is that a full model can reveal historical gene flow involving ancestral populations. An example of this was found in which gene flow is indicated between the western common chimpanzee subspecies and the ancestor of the central and the eastern common chimpanzee subspecies. The results of a full analysis on all four populations are strongly consistent with analyses on pairs of populations and generally similar to results from previous studies. The basal split between bonobos and common chimpanzees was estimated at 0.93 Ma (0.68-1.54 Ma, 95% highest posterior density interval), with the split among the ancestor of three common chimpanzee populations at 0.46 Ma (0.35-0.65), and the most recent split between central and eastern common chimpanzee populations at 0.093 Ma (0.041-0.157). Population size estimates mostly fell in the range from 5,000 to 10,000 individuals. The exceptions are the size of the ancestor of the common chimpanzee and the bonobo, at 17,000 (8,000-28,000) individuals, and the central common chimpanzee and its immediate ancestor with the eastern common chimpanzee, which have effective size estimates at 27,000 (16,000-44,000) and 32,000 (19,000-54,000) individuals, respectively.

FIG. 1.

Geographic distribution of chimpanzee species and subspecies (Schwartz 1934; Hill 1969; Gonder et al. 2006).

FIG. 2.

Histories for all six population pairs are represented as boxes (for sampled and ancestral populations), horizontal lines (for splitting times) and curved arrows (for migration). Time is represented on the vertical axis in each figure, with the sampled species and subspecies names given at the top of each figure at the most recent time point. (A–C) Comparisons among common chimpanzee subspecies, with a common scaling of the vertical axis for splitting time comparisons. (D–F) Comparisons between the bonobo and common chimpanzee populations with a common scaling of the vertical axis for splitting time comparisons. For all figures, the 95% highest posterior density intervals are shown with arrows in gray for population sizes (i.e., box widths) and splitting times (dotted lines). Migration arrows represent the population migration rate (i.e., 2NM) from the source population to the receiving population (i.e., forward in time). Only those population migration rates that were found to be statistically significant using a likelihood-ratio test are shown in which case the estimated value of 2NM is given as well as the significance level. Asterisks identify curves that are statistically significant by the test of Nielsen and Wakeley (2001): *P < 0.05; **P < 0.01, and ***P < 0.001.

FIG. 3.

IM analyses for the three subspecies of common chimpanzee. Results are shown for an upper bound on the migration parameter, m, of 1.0 (A) and an upper bound of 2.0 (fig. 3B). See figure 2 for further explanation of the meaning of symbols.

FIG. 4.

Estimated marginal posterior densities for m and 2NM for period 1 in three-population models for the common chimpanzee. Curves for m are shown on the left and for 2NM on the right. Curves generated under a uniform prior with an upper bound of m′ = 1 are shown on the top and curves generated with m′ = 2 are shown on the bottom.

FIG. 5.

Four populations in IM analyses with an upper bound on the migration parameter, m′ = 1. See figure 2 for further explanation of the meaning of symbols.

FIG. 6.

Results for four-population models under different prior distributions for m. (A) Uniform prior with m′ = 2. (B) Uniform prior with m′ = 5. (C) Exponential prior with . See figure 2 for further explanation of the meaning of symbols.