Population genetic patterns among social groups of the endangered Central American spider monkey (Ateles geoffroyi) in a human-dominated landscape

Abstract

SPIDER MONKEYS (GENUS: Ateles) are a widespread Neotropical primate with a highly plastic socioecological strategy. However, the Central American species, Ateles geoffroyi, was recently re-listed as endangered due to the accelerated loss of forest across the subcontinent. There is inconsistent evidence that spider monkey populations could persist when actively protected, but their long-term viability in unprotected, human-dominated landscapes is not known. We analyzed noninvasive genetic samples from 185 individuals in 14 putative social groups on the Rivas Isthmus in southwestern Nicaragua. We found evidence of weak but significant genetic structure in the mitochondrial control region and in eight nuclear microsatellite loci plus negative spatial autocorrelation in Fst and kinship. The overall pattern suggests strong localized mating and at least historical female-biased dispersal, as is expected for this species. Heterozygosity was significantly lower than expected under random mating and lower than that found in other spider monkey populations, possibly reflecting a recent decline in genetic diversity and a threat from inbreeding. We conclude that despite a long history of human disturbance on this landscape, spider monkeys were until recently successful at maintaining gene flow. We consider the recent decline to be further indication of accelerated anthropogenic disturbance, but also of an opportunity to conserve native biodiversity. Spider monkeys are one of many wildlife species in Central America that is threatened by land cover change, and an apt example of how landscape-scale conservation planning could be used to ensure long-term persistence.

Keywords: Ateles geoffroyi; conservation; human-dominated landscape; inbreeding; microsatellites; spatial genetic structure.

Figure 1

Ateles geoffroyi on the Rivas Isthmus, Nicaragua. Photo credit: Bill Noble. This photo was taken on 8 January 2010 (UTM 16P 637627E 1241983N).

Figure 2

Distribution of the 15 sampling sites or putative social groups of spider monkeys (Ateles geoffroyi) on the Rivas Isthmus, Nicaragua used in this analysis. Site locations reflect the centroid of a 3 ha sampling area. Dark gray shading indicates closed-canopy forest cover, light gray is open-canopy, and lines represent permanent roads and the international border (forest cover derived from Sesnie et al. 2008).

Figure 3

Haplotype network for the restricted dataset of 36 mitochondrial control region haplotypes from 162 spider monkeys (Ateles geoffroyi) on the Rivas Isthmus, Nicaragua.

Figure 4

Pairwise kinship (Loiselle et al. 1995) between 162 spider monkeys (Ateles geoffroyi) across 10 distance classes on the Rivas Isthmus, Nicaragua. Max Distances report the upper limit of distances within each distance class. Line intercept at k = 0 is equivalent to a null probability of identity by descent, k > 0.5 indicates 1st order relatives.