The population genetics of wild chimpanzees in Cameroon and Nigeria suggests a positive role for selection in the evolution of chimpanzee subspecies

Abstract

Background: Chimpanzees (Pan troglodytes) can be divided into four subspecies. Substantial phylogenetic evidence suggests that these subspecies can be grouped into two distinct lineages: a western African group that includes P. t. verus and P. t. ellioti and a central/eastern African group that includes P. t. troglodytes and P. t. schweinfurthii. The geographic division of these two lineages occurs in Cameroon, where the rages of P. t. ellioti and P. t. troglodytes appear to converge at the Sanaga River. Remarkably, few population genetic studies have included wild chimpanzees from this region.

Results: We analyzed microsatellite genotypes of 187 wild, unrelated chimpanzees, and mitochondrial control region sequencing data from 604 chimpanzees. We found that chimpanzees in Cameroon and eastern Nigeria comprise at least two, and likely three populations. Both the mtDNA and microsatellite data suggest that there is a primary separation of P. t. troglodytes in southern Cameroon from P. t. ellioti north and west of the Sanaga River. These two populations split ~200-250 thousand years ago (kya), but have exchanged one migrant per generation since separating. In addition, P. t. ellioti consists of two populations that split from one another ~4 kya. One population is located in the rainforests of western Cameroon and eastern Nigeria, whereas the second population appears to be confined to a savannah-woodland mosaic in central Cameroon.

Conclusions: Our findings suggest that there are as many as three genetically distinct populations of chimpanzees in Cameroon and eastern Nigeria. P. t. troglodytes in southern Cameroon comprises one population that is separated from two populations of P. t. ellioti in western and central Cameroon, respectively. P. t. ellioti and P. t. troglodytes appear to be characterized by a pattern of isolation-with-migration, and thus, we propose that neutral processes alone can not explain the differentiation of P. t. ellioti and P. t. troglodytes.

Figure 1

Distribution and current phylogeny of Pan. (A) Major rainforest biomes of tropical Africa. (B) Phylogeny of chimpanzees, bonobos and humans using whole genome data, adapted from Prado-Martinez et al. [8]. (C) Distribution of chimpanzee subspecies and bonobos across tropical Africa.

Figure 2

Sample locations of chimpanzees. Locations spanned Cameroon and eastern Nigeria. Probable distributions of P. t. ellioti (purple) and P. t. troglodytes (orange) ranges are shown. Circles denote both hair and fecal samples were collected at the location. Squares denote only hair samples were collected.

Figure 3

mtDNA haplotype network and map. (A) Median-joining haplotype network of mtDNA HVRI locus generated using Network 4.5. Each cluster is color coded to display the inferred geographic origin of individuals; (i) purple representing western Cameroon and eastern Nigeria (north of the Sanaga River and west of the Mbam River), (ii) green representing central Cameroon (north of the Sanaga and east of the Mbam), and (iii) orange representing southern Cameroon (south of the Sanaga). Haplotypes cluster into two main groups (1 and 2), and 4 sub-groups (1A, 1B, 2A and 2B). (B) Pie charts show the frequency distribution of mtDNA haplogroups (1A, 1B, 2A and 2B) across the study area.

Figure 4

Isolation-by-distance. Results of a Mantel test performed to identify a correlation between genetic differentiation and the geographic distance between sampling locations (Figure 2). Points on the chart represent pairwise comparisons and the trend line represents linear correlation (p = 0.0045, R² = 0.0186).

Figure 5

Principal Components Analysis (PCA). PCA generated on the basis of individual genotypes. Individuals are color coded according to geographic origin; (i) purple – western Cameroon and eastern Nigeria, (ii) green – central Cameroon, and (iii) orange – southern Cameroon. PCs 1 and 2 (shown) represent the eigenvectors that accounted for 71 and 21%, respectively, of the total extracted variation.

Figure 6

Cluster analysis and spatial interpolations. (A and B) TESS bar plots for K = 2-3. Each vertical line represents an individual, and colors represent their inferred ancestry from K ancestral populations. Individuals are ordered by their geographic sampling location. (C and D) Spatial interpolations of the Q matrices generated by the program TESS Ad-Mixer for K = 2-3. Spatial interpolations were plotted on probable extents of chimpanzee ranges in Nigeria and Cameroon.