Phylogenetic relationships among Capuchin (Cebidae, Platyrrhini) lineages: An old event of sympatry explains the current distribution of Cebus and Sapajus

Abstract

Capuchin monkeys are currently represented by four species of Cebus and eight of Sapajus. This group is taxonomically complex and several questions still need to be clarified. In the current study, using mtDNA markers and a larger sample representation than in previous studies, we seek to understand the phylogenetic relationships among the capuchin lineages and their historical biogeography. All 12 species of capuchins were analyzed for the mitochondrial Control Region and Cytochrome b to test two biogeographical hypotheses: "Reinvasion of the Amazon (ROA)" and "Sympatric Evolution (SEV)". The phylogenetic relationships among distinct lineages within genera is consistent with an evolutionary diversification pattern probably resulting from an explosive process of diversification and dispersal between 2.0 Ma and 3.0 Ma. Also, the analyses show that the ancestral capuchins were distributed in a wide area encompassing the Amazon and Atlantic Forest. Our results support the SEV hypothesis, showing that the current syntopic distribution of Cebus and Sapajus can be explained by a sympatric speciation event in the Amazon. We also indicate that the recently proposed species taxonomy of Cebus is not supported, and that S. cay and S. macrocephalus are a junior synonym of S. apella.

Figure 1. Geographical distribution of robust (Sapajus) and gracile (Cebus) capuchins species. Map constructed based on information provided by Silva Jr (2001), Lynch Alfaro et al. (2012), and IUCN (2016).

Figure 2. Biogeographic zones analyzed (gray spots) and the collection sites of the Cebus and Sapajus samples. A = samples 1-4; B = samples 5-11; C = 17-57.

Figure 3. Divergence time tree of capuchins estimated on BEAST 1.8.3. Nodes were calibrated using the age of four Platyrrhini fossils. The blue bars above the nodes indicate the Highest Posterior Density of the estimated ages. Arrows 1, 2, 3 and 4 represent the split of the crown capuchins, the first split of the crown Sapajus, a recent split within Sapajus (~ 1.0 Ma) and the first split of the crown Cebus, respectively. The lower boxes indicate the geological times of the Cenozoic era.

Figure 4. Maximum Clade Credibility (MCC) gene tree estimated on BEAST 1.8.3 from DS2. Circles with Arabic numbers inside represent collapsed samples (see Table S1). The numbers above the nodes are statistical supports provided by, from left to right, Maximum Likelihood bootstrap, Bayesian credibility and Maximum Parsimony bootstrap. The dots show the polytomy in both genera. The meaning of arrows 1, 2, 3 and 4 is described in Figure 3. Except for the nodes indicated by the arrows, only support values greater than 70% are shown.

Figure 5. DS2 time consensus tree with the estimates of ancestral areas of the capuchin monkeys made in `BioGeoBEARS’ through the DEC-J model. CN = Central America + North Andes; WM = West Amazon; NM = North Amazon + Coastal Venezuela; SM = South Amazon; SE = Southeast Amazon; CE = Cerrado; PA = Paraguay/Argentina; AF = South and North Atlantic Forest.