Valderrama Aramayo María Ximena Corina (2002). Reproductive Success and Genetic Population Structure in Wedge-Capped Capuchin Monkeys. Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the Graduate School of Arts and Sciences. Columbia University 2002
Abstract
The central question in this study was whether an unusual breeding system observed in wedge-capped capuchin monkeys would be supported by genetic paternity analysis. Alpha males were observed to have a monopoly of sexual access to fertile females, suggesting an extreme skew in male reproductive output. If all females bred with the alpha male, why did other immigrant males remain in the group for many years, even cooperating in group defense, predator repulsion, and infact care? Long- term demographic data for a large capuchin group were incorporated with neutral autosomal markers. The dataset was used to examine the relative influence of male dominance rank and female preference on reproductive output. Each alpha male sired more offspring than did other males, and two consecutive alpha males collectively sired slightly more than half the offspring. This result indicated an important role of discreet mating and sexual coercion as reproductive strategies by subordinate and extragroup males. In addition, the alpha male sired an increasing proportion of offspring in lower-ranking matrilines. These females may have targeted alpha males as strategy to offset higher rates of offspring loss in these matrilines.
Estimates of genetic relatedness and variability, together with rates of demographic parameters, were used to examine how kin, group, and genetic structure may be associated with social behavior. For example, fewer breeders in a group would be expected to result in high level of relatedness within the group, which may facilitate nepotism. At the same time, capuchin matrilines within groups were highly differentiated in agonistic dominance rank, which determined martilineage sorting over time. The two groups had different proportions of natal and immigrant members, which generated varying levels of relatedness. Reproductive and matrilineage losses were catalyzed by climatic fluctuation. Levels of genetic variability were greater in matrilines than offspring cohorts, therefore matrilineal loss resulted in greater genetic erosion. There was possible evidence for kin selection among male immigrants and among group females, although individual selection could have a greater influence in felames.
The above demographic and genetic information was incorporated with mitochondrial DNA haplotypes to assess local and regional genetic diversity and the demographic history of capuchins in the Llanos of Venezuela. Relatedness within hierarchical demographic units reflected breeding and dispersal patterns. Spatial distribution of uncommon autosomal alleles also showed an association with dispersal patterns within the local population. In contrast, there was lack of phylogenetic resolution and absence of mutation- drift equilibrium in the regional population. In addition, mitochondrial DNA haplotypes were depauperate in variability within and among populations, only showing structure across a riverine dispersal barrier. These results indicated a recent founder event followed by rapid population expansion.
Incorporating genetic information into the long-term demographic study of capuchins was essential for testing models of male reproductive variance. The combined dataset also showed that short-term results could not be extrapolated over the long- term, for example in male reproductive variance and in martineal relatedness estimates.
Information regarding dominance rank differentiation was critical fot understanding how it led to female reproductive differentiation and lineage sorting, a principal mechanism of microevolution in this capuchin population. Similarly, collecting genetic data from two genomes proved indispensable for identifying the demographic and genetic determinants of the regional population’s current genetic structure.