Capuchin monkey biogeography: understandingSapajusPleistocene range expansion and the current sympatry betweenCebusandSapajus

Abstract

Aim Our aim was to examine gracile capuchin (Cebus) and robust capuchin monkey (Sapajus) diversification, with a focus on recent Sapajus expansion within Amazonia. We wanted to reconstruct the biogeographical history of the clade using statistical methods that model lineages' occupation of different regions over time in order to evaluate recently proposed 'Out of Amazonia' and 'Reinvasion of Amazonia' hypotheses as alternative explanations for the extensive geographical overlap between reciprocally monophyletic gracile (Cebus) and robust (Sapajus) capuchin monkeys.Location Central and South America.Methods We reconstructed a time-calibrated molecular phylogeny for capuchins under Bayesian inference from three mitochondrial genes. We then categorized 12 capuchin clades across four Neotropical centres of endemism and reconstructed the biogeographical history of the capuchin radiation using six models implemented in 'BioGeoBEARS'. We performed a phylogeographical analysis for a robust capuchin clade that spans the Atlantic Forest, Cerrado, Caatinga and Amazonia. ResultsWe find support for a late Miocene vicariant Cebus-Sapajus divergence and a Pleistocene Sapajus invasion of Amazonia from the Atlantic Forest. Our new analyses confirm Sapajus diversified first in the Atlantic Forest, with subsequent range expansion into widespread sympatry with Cebus in Amazonia, as well as multiple expansions into drier savanna-like habitats. We do not find mitochondrial molecular congruence with morphological species distinctions for Sapajus flavius, S. cay, S. macrocephalus, S. libidinosus and S. apella; instead, these five morphological types together form a single widespread clade (Bayesian posterior probability = 1) with geographical substructure and shared ancestry during the Pleistocene.Main conclusions Our results support vicariance dividing ancestral capuchin populations in Amazonia versus the Atlantic Forest, and a Pleistocene 'Amazonian invasion' by Sapajus to explain the present-day sympatry of Cebus and Sapajus.

Biogeographic origins of Darwin's finches (Thraupidae: Coerebinae)

“…Conversely, over-dividing, or inaccurately dividing geographic regions, may produce the opposite effect and could overemphasize dispersal, anagenetically or cladogenetically. Other recent studies of South American biogeography have delineated geographic boundaries similar to our 8-area regime (e.g., Batalha-Filho et al 2014, Lima et al 2017. The results presented here suggest that models such as those run through BioGeoBEARS are sensitive to these delineations and should be considered during future investigation of biogeography in this area.…”

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.)…”

Titi monkey biogeography: Parallel Pleistocene spread byPlecturocebusandCheracebusinto a post‐Pebas Western Amazon

“…Neotropical primates are a diverse, widespread mammalian clade with five families, 21 genera and around 171 species (Byrne et al., ; Estrada et al., ; Mittermeier, Rylands, & Wilson, ; Rylands et al., ). There have been some recent investigations into the biogeographic history of Neotropical primates in a robust phylogenetic framework (e.g., Buckner, Lynch Alfaro, Rylands, & Alfaro, ; Lima et al., ; Lynch Alfaro, Boubli, et al., ). Diversification patterns among capuchin monkeys have been used to test “out of the Amazon” versus “reinvasion of the Amazon” hypotheses to explain sympatry between robust ( Sapajus ) and gracile ( Cebus ) capuchins in the Amazon (Lima et al., ), while squirrel monkey diversification in the Pleistocene has been associated with the transition from a lacustrine to a riverine system in Amazonia and the occupation of a lowland wetland niche (Lynch Alfaro, Boubli, et al., ).…”

“…There have been some recent investigations into the biogeographic history of Neotropical primates in a robust phylogenetic framework (e.g., Buckner, Lynch Alfaro, Rylands, & Alfaro, ; Lima et al., ; Lynch Alfaro, Boubli, et al., ). Diversification patterns among capuchin monkeys have been used to test “out of the Amazon” versus “reinvasion of the Amazon” hypotheses to explain sympatry between robust ( Sapajus ) and gracile ( Cebus ) capuchins in the Amazon (Lima et al., ), while squirrel monkey diversification in the Pleistocene has been associated with the transition from a lacustrine to a riverine system in Amazonia and the occupation of a lowland wetland niche (Lynch Alfaro, Boubli, et al., ). Among all Neotropical primate lineages, however, titi monkeys (Callicebinae; Pitheciidae) are unrivalled in their distribution across space and time, forming one of the most widespread and species‐rich groups, making them an interesting primate model for the study of Amazonian and South American historical biogeography.…”

“…Statistical methods based on maximum likelihood were applied to a time‐calibrated molecular phylogeny, allowing the comparison of models to determine the relative importance of vicariance and dispersal in forming the current distributions of callicebine taxa. This approach has been used to better understand the biogeographic history of other Neotropical primates (e.g., Buckner et al., ; Lima et al., ; Lynch Alfaro, Boubli, et al., ).…”