Phylogeny, molecular dating and zoogeographic history of the titi monkeys (Callicebus, Pitheciidae) of eastern Brazil

Abstract

The titi monkeys belong to a genus of New World primates endemic to South America, which were recently reclassified in three genera (Cheracebus, Plecturocebus and Callicebus). The genus Callicebus, which currently includes five species, is endemic to eastern Brazil, occurring in the Caatinga, Savanna, and Atlantic Forest biomes. In the present study, we investigated the validity of these species and inferred their phylogenetic relationships, divergence times, and biogeographic patterns based on the molecular analysis of a concatenated sequence of 11 mitochondrial and nuclear DNA markers, derived from 13 specimens. We ran Maximum Likelihood (ML) and Bayesian Inference (BI) analyses, and estimated genetic distances, divergence times. Ancestral areas were estimated on BioGeoBears. Our results suggest that at about twelve million years ago, the ancestor of all titi monkeys inhabited a wide area that extended from the Amazon forest to the South of the Atlantic forest. A first vicariant event originated Cheracebus in the West of the Amazon and the ancestor of Callicebus and Plectorocebus which, later were separated by a second one. The diversification of Callicebus occurred during the Plio-Pleistocene (beginning at 5 Ma) probably influenced by climatic fluctuations and geological events. Therefore, the results of the present work confirmed the existence of five species that currently inhabit forested areas under increasing threat from human activities. Thus, a reliable diagnosis of the taxonomic status of species living in endangered environments is extremely important for the development of conservation measures.

Geographical patterns and current and short‐term historical correlates of phylogenetic diversity and endemism for New World primates

“…and robust capuchins (Sapajus spp. ), there are also lineages that have diversified and their occurrence is restricted to the Atlantic Forest (Carneiro et al, 2018;Kiesling et al, 2015;Lima et al, 2017;Lynch Alfaro et al, 2015); including lion tamarins (Leontopithecus spp. ), woolly spider monkeys (Brachyteles spp.)…”

Duetting Patterns of Titi Monkeys (Primates, Pitheciidae: Callicebinae) and Relationships with Phylogeny

“…The form and structure of titi monkey loud calls examined in the present study raise important questions with respect to the current callicebine taxonomy [ 62 , 63 , 64 , 65 , 66 ]. First, within the donacophilus group, sensu largo , we found the pattern of duetting of the two Peruvian endemics P. oenanthe and P. urubambensis to differ substantially from the other four members of the donacophilus lineage.…”

“…Compared with the continental distribution of the callicebine monkeys, the study was conducted over a relatively small geographic scale (~10%) so that additional patterns of duetting may be found in other regions of the Amazon Basin and in eastern Brazil. In particular, with the exception of C. nigrifrons [ 48 ], little is known on the duetting patterns in the personatus lineage for which recent molecular studies have shed the light on the time of divergence, and the phylogenetic and biogeographic relationships among all five Callicebus species [ 66 ].…”

“…Titi monkeys (Pitheciidae; subfamily Callicebinae) are a monophyletic clade of pair-bonded species exhibiting biparental care [ 52 , 53 , 54 , 55 ] and in which the taxonomy remains contentious [ 56 , 57 , 58 , 59 , 60 , 61 , 62 , 63 , 64 , 65 , 66 ], with several taxa being re-evaluated and/or newly described within last two decades [ 59 , 67 , 68 , 69 , 70 , 71 , 72 ]. Until recently, our understanding of the taxonomy and phylogeny of titi monkeys was based mainly on biogeographical, morphological, and anatomical criteria complemented by chromosome analysis [ 73 , 74 , 75 , 76 ].…”

“…Until recently, our understanding of the taxonomy and phylogeny of titi monkeys was based mainly on biogeographical, morphological, and anatomical criteria complemented by chromosome analysis [ 73 , 74 , 75 , 76 ]. However, recent molecular studies involving multiple genetic markers [ 62 , 63 , 64 , 65 , 66 ] have prompted a reassessment of phylogenetic and biogeographic relationships among the various titi taxa, leading Byrne et al [ 62 ] to split the former genus Callicebus into three genera, including Plecturocebus (with 22 species) and Cheracebus (with six species), which together are distributed in the Amazon and Chaco ecoregions, and Callicebus (with five species), which is endemic to eastern Brazil. These authors, in addition, provide genetic evidence for the existence of four major lineages within the subfamily: the moloch and donacophilus groups (both within the genus Plecturocebus ), the personatus group (genus Callicebus ), and the torquatus group (genus Cheracebus ), which is the most basal lineage within the callicebine radiation ( Figure 1 ).…”