Invalidation of three robust capuchin species (Cebus libidinosus pallidus, C. macrocephalus and C fatuellus; Cebidae, Primates) in the Western Amazon and Orinoco by analyzing DNA microsatellites

We analyzed 163 robust capuchins for eight nuclear DNA microsatellites representing three different "a priori" morphological taxa (47 pallidus individuals from Bolivia, 24 macrocephalus individuals from the Peruvian and Southern Colombian Amazon and 92 fatuellus individuals from the Colombian Eastern Llanos and Northern Colombian Amazon). There were seven main findings to come out of this study. 1-Levels of gene diversity were high for all three populations but the most southern population, pallidus, had the highest whereas the most northern population, fatuellus, showed the lowest; 2- The major part of the microsatellites we used were neutrally dynamic, although some did show evidence of positive natural selection; 3- Deviations from the Hardy-Weinberg equilibrium were detected especially for fatuellus and pallidus (Wahlund effect). We also detected six different populations of widely intermixed individuals. The populations were not related with the morphological taxa traditionally considered by primatologists. 4- Some evidence of significant genetic differentiation was found for different markers among these three taxa. However, the relative genetic heterogeneity found was of a small magnitude but the estimations of gene flow were very high and even superior to those obtained for populations of Cebus capucinus, a unique and recognized species by all primatologists. 5- The assignment analysis showed that a considerable amount of the analyzed individuals were misclassified within their respective taxa (around 33%). 6- No bottleneck events were detected for any of the robust capuchin populations but population expansions were detected which support an explosive expansion of these monkeys during the Pleistocene. 7- None of the different spatial genetic structure analyses detected any significant genetic patches or evidence of gene flow interruption that would be expected if diverse species were living in the same geographical area. In contrast, very smooth monotonic clines were detected which are typical of gradual differentiation without reproductive isolation. Our results do not support the existence of three well-differentiated robust capuchin species within the study area. We propose that these three alleged morphological taxa be classified in two different subspecies within Cebus apella, C. a. macrocephalus and C. a. fatuellus.