Understanding geographic origins and history of admixture among chimpanzees in European zoos, with implications for future breeding programmes

Abstract

Despite ample focus on this endangered species, conservation planning for chimpanzees residing outside Africa has proven a challenge because of the lack of ancestry information. Here, we analysed the largest number of chimpanzee samples to date, examining microsatellites in >100 chimpanzees from the range of the species in Africa, and 20% of the European zoo population. We applied the knowledge about subspecies differentiation throughout equatorial Africa to assign origin to chimpanzees in the largest conservation management programme globally. A total of 63% of the genotyped chimpanzees from the European zoos could be assigned to one of the recognized subspecies. The majority being of West African origin (40%) will help consolidate the current breeding programme for this subspecies and the identification of individuals belonging to the two other subspecies so far found in European zoos can form the basis for breeding programmes for these. Individuals of various degree of mixed ancestry made up 37% of the genotyped European zoo population and thus highlight the need for appropriate management programmes guided by genetic analysis to preserve maximum genetic diversity and reduce hybridization among subspecies.

Figure 1

Geographical distribution ranges for Pan troglodytes subspecies (Hill, 1969; Grubb et al., 2003; Oates et al., 2008, 2009). The ranges are colour coded: yellow for P. t. verus, orange for P. t. ellioti, pink for P. t. troglodytes and turquoise for P. t. schweinfurthii. The question mark indicates a dispute about the chimpanzees inhabiting the area west of the Niger River in Nigeria and their phylogenetic grouping with either P. t. verus or P. t. ellioti.

Figure 2

Genetic clusters inferred from genotypic data of Pan troglodytes subspecies with known origin. Proportion of membership to each cluster for every sampled individual is indicated by colours in the vertical bars. The bar plots show the genetic structure among all subspecies when three clusters are assumed. Predefined subspecies origin is indicated below and geographical sampling location above. One individual (Choupette) was registered as P. t. troglodytes, but the analysis revealed it to be of P. t. schweinfurthii origin.

Figure 3

Pairwise comparison of posterior distribution of admixture coefficients (q) between all population pairs based on 25 autosomal loci. The 90% probability intervals are indicated by vertical bars for each individual. Open and full circles indicate population origin for each individual based on its geographical sampling location. Open circles represent individuals from row populations and closed circles denote individuals from column populations. One individual (Choupette) marked with a red asterisk (*) denotes a discrepancy between sampling location and the genotyped subspecies origin (Supplementary Table S2), see also Figure 2 and text.

Figure 4

(a) PCA of chimpanzee individuals from the species distribution range in Africa. Colours: yellow, pink and turquoise for P. t. verus, P. t. troglodytes and P. t. schweinfurthii, respectively. (b) A PCA as above but without P. t. verus is displayed.

Figure 5

Inferred ancestry of Pan troglodytes subspecies with unknown origin based on genetic clustering with sampled individuals from the species natural distribution range. Proportion of membership to each cluster for every sampled individual is indicated by colours in the vertical bars Predefined subspecies origin is indicated below and geographical sampling location above.

Figure 6

(a) PCA of chimpanzee individuals from the species distribution range in Africa and zoo specimens of unknown origin. Colours: yellow, pink, turquoise and green for P. t. verus, P. t. troglodytes, P. t. schweinfurthii and zoo specimens, respectively. The pink dot falling within the outer range of the P. t. schweinfurthii cluster represents the, based on the STRUCTURE analysis, misclassified individual Choupette. In (b), three simulated F1 hybrid populations are included, each consisting of 20 individuals. The populations are colour coded light grey, medium grey and dark grey for P. t. troglodytes/P. t. schweinfurthii, P. t. schweinfurthii/P. t. verus and P. t. verus/P. t. troglodytes, respectively.