Journal of Biogeography (J. Biogeogr.) (2012) 39, 272–288 ORIGINAL Explosive Pleistocene range expansion ARTICLE leads to widespread Amazonian sympatry between robust and gracile capuchin monkeys Jessica W. Lynch Alfaro1*, Jean P. Boubli2, Link E. Olson3, Anthony Di Fiore4, Bryan Wilson5, Gustavo A. Gutie´rrez-Espeleta6, Kenneth L. Chiou4,7, Meredith Schulte8, Sarah Neitzel5, Vanessa Ross8, Doreen Schwochow1,9, Mai T.T. Nguyen1,9, Izeni Farias10, Charles H. Janson11 and Michael E. Alfaro9 1Center for Society and Genetics, University of ABSTRACT California, Los Angeles, CA, USA, 2Wildlife Aim Capuchin monkey species are widely distributed across Central and South Conservation Society, Rio de Janeiro, Brazil, 3University of Alaska Museum, University of America. Morphological studies consistently divide the clade into robust and Alaska Fairbanks, Fairbanks, AK, USA, gracile forms, which show extensive sympatry in the Amazon Basin. We use 4Department of Anthropology, New York genetic data to test whether Miocene or Plio-Pleistocene processes may explain University, New York, NY, USA, 5School of capuchin species’ present distributions, and consider three possible scenarios to Biological Sciences, Washington State explain widespread sympatry. 6 University, Pullman, WA, USA, Escuela de Location The Neotropics, including the Amazon and Atlantic Coastal Forest. Biologı´a, University of Costa Rica, San Jose´, Costa Rica, 7Department of Anthropology, Methods We sequenced the 12S ribosomal RNA and cytochrome b genes from Washington University, St Louis, MO, USA, capuchin monkey specimens. The majority were sampled from US museum 8Department of Anthropology, Washington collections and were wild-caught individuals of known provenance across their State University, Pullman, WA, USA, distribution. We applied a Bayesian discrete-states diffusion model, which 9Department of Ecology and Evolutionary reconstructed the most probable history of invasion across nine subregions. We Biology, University of California, Los Angeles, used comparative methods to test for phylogeographic association and dispersal 10 CA, USA, Departamento de Biologia, rate variation. Universidade Federal do Amazonas, Manaus, AM, Brazil, 11Division of Biological Sciences, Results Capuchins contained two well supported monophyletic clades, the University of Montana, Missoula, MT, USA morphologically distinct ‘gracile’ and ‘robust’ groups. The time-tree analysis estimated a late Miocene divergence between Cebus and Sapajus and a subsequent Plio-Pleistocene diversification within each of the two clades. Bayesian analysis of phylogeographic diffusion history indicated that the current wide-ranging sympatry of Cebus and Sapajus across much of the Amazon Basin was the result of a single explosive late Pleistocene invasion of Sapajus from the Atlantic Forest into the Amazon, where Sapajus is now sympatric with gracile capuchins across much of their range. Main conclusions The biogeographic history of capuchins suggests late Miocene geographic isolation of the gracile and robust forms. Each form diversified independently, but during the Pleistocene, the robust Sapajus expanded its range from the Atlantic Forest to the Amazon, where it has now encroached substantially upon what was previously the exclusive range of gracile Cebus. The genus Cebus, as currently recognized, should be split into two genera to reflect the Miocene divergence and two subsequent independent Pliocene *Correspondence: Jessica W. Lynch Alfaro, radiations: Cebus from the Amazon and Sapajus from the Atlantic Forest. Center for Society and Genetics, 1321 Rolfe Hall, Keywords University of California, Los Angeles, CA 90095, USA. Amazon Basin, Atlantic Forest, Cebus, Neotropical primates, Platyrrhini, E-mail: [email protected] Pleistocene expansion, Sapajus, sympatry. 272 http://wileyonlinelibrary.com/journal/jbi ª 2011 Blackwell Publishing Ltd doi:10.1111/j.1365-2699.2011.02609.x Biogeography of Neotropical capuchin monkeys Capuchin taxonomy is contentious (Hill, 1960; Rylands INTRODUCTION et al., 2000), due in part to extreme intraspecific and even Capuchin monkeys are widely distributed across Central and within-population variation in phenotypes (Hill, 1960; Torres South America. Elliot (1913, p. 77) separated them into two de Assumpc¸a˜o, 1983; Rylands et al., 2005) and also to extended groups: those with ‘heads without tufts on male’ (Group A) life history, with delayed maturation and distinct differences in and those with ‘heads with tufts or ridges on male’ (Group B). appearance among age and sex classes (Izawa, 1980). All This turned into a division of so-called ‘untufted’ and ‘tufted’ treatments based on morphology, however, recognize the capuchins, adopted by Hershkovitz (1949), Hershkovitz (1955) division of robust and gracile forms (Hill, 1960; Rylands et al., and Hill (1960), and used ever since. Hershkovitz (1949) 2000; Groves, 2001; Silva, 2001). Here we refer to Cebus for the recognized four species, one tufted (Cebus apella) and three gracile (or untufted) capuchins and Sapajus for the robust (or untufted [Cebus albifrons, Cebus capucinus and Cebus nigri- tufted) capuchins, for clarity. vittatus (= olivaceus)]. Not all ‘tufted’ capuchins actually have Both forms are found throughout much of the Amazon hair tufts, however (for example, Cebus xanthosternos), and Basin. Robust species also extend into the dry Caatinga and some members of the ‘untufted’ group (A) have tufts (for Cerrado of Brazil, the Atlantic Forest, and as far south as example, female Cebus olivaceus). What, in fact, best divides Paraguay and northern Argentina, while the gracile species these two groups is their anatomy: Elliot’s Group A is more extend across the Andes in western Ecuador, northern slender and gracile compared with Group B, which is more Colombia and north-western Venezuela, into Central America robust in both cranial and postcranial morphology (Silva, (Fig. 1). The area of sympatry between the robust and gracile 2001). Groves (2001) used coat colour variation and tuft shape forms is strikingly large, exceeding that found in any other to divide the tufted or ‘robust’ capuchins into four species: genus of Neotropical primate, but there have been no well C. apella, C. libidinosus, C. xanthosternos and C. nigritus. Silva supported hypotheses to explain the current geographic (2001) placed this group in its own subgenus, Sapajus Kerr, distribution or extent of sympatry of capuchins. While it has 1792, with seven species: Cebus (Sapajus) macrocephalus and been assumed that capuchins originated in the Amazon C. (Sapajus) apella in the Amazon, C. (Sapajus) libidinosus and (Kinzey, 1982), there has been no attempt to indicate the C. (Sapajus) cay in the Caatinga, Cerrado and Chaco habitats, timing of capuchin invasions, either north-west across the and C. (Sapajus) xanthosternos, C. (Sapajus) robustus and Andes and into Central America, or south-east into the dry C. (Sapajus) nigritus in the Atlantic Coastal Forest (Fig. 1b). Cerrado and the Atlantic Coastal Forest. Marcgrave’s capuchin, Cebus flavius (Schreber, 1774), also a Here we develop several hypotheses regarding the chronol- robust capuchin, was recently rediscovered in north-east Brazil ogy and biogeography underlying present-day capuchin (Mendes Pontes et al., 2006; Oliveira & Langguth, 2006). distributions. One of the longest-standing explanations is that (a) (b) Cebus olivaceus Cebus capucinus Cebus kaapori Sapajus apella Sapajus libidinosus Sapajus flavius Cebus albifrons Sapajus macrocephalus Sapajus xanthosternos Sapajus robustus Sapajus cay Sapajus nigritus km km 0 1,000 2,000 0 1,000 2,000 Figure 1 Approximate distribution of (a) Cebus and (b) Sapajus species in the Neotropics. Species distributions follow IUCN Red List maps (IUCN, 2011), with minor corrections, using the taxonomy of Silva (2001, 2002), with the addition of the newly rediscovered Sapajus flavius. Hashes symbolize intrageneric sympatry. Note the extreme overlap between (a) Cebus and (b) Sapajus species in the Amazon Basin. Journal of Biogeography 39, 272–288 273 ª 2011 Blackwell Publishing Ltd J. W. Lynch Alfaro et al. they have colonized their present ranges as a result of dispersal north and south of the Rio Amazonas, with (1) gracile forms from Pleistocene forest refugia (Kinzey, 1982). Diverse lines of diversifying north of the Amazon, and later north into the evidence suggest that during much of the Pleistocene (1.64 Ma Andes, Central America, and northern Venezuela, as well as to 10 ka), arid climates prevailed in the Neotropics, although south of the Amazon; and (2) the robust form diversifying there is also evidence against this conclusion (Knapp & Mallet, south of the Amazon, eventually radiating south-east to the 2003). Schneider et al. (2001) estimated that divergence within Cerrado and Atlantic Forest, as well as north across the each extant platyrrhine genus occurred sometime during the Amazon. Note that the lack of samples from south of Rio Plio-Pleistocene, and Kinzey (1982) argued for the importance Amazonas (in Southern Amazonia) limits our ability to test of Pleistocene forest refugia in influencing distributions of the this hypothesis. species seen today. 2. ‘Atlantic versus Amazon’. A second possibility is that There have been strong arguments against Pleistocene rain vicariance between the Brazilian Atlantic coastal forest and forest fragmentation and refugia in the Amazon and beyond Amazon Basin is the major force shaping capuchin monkey (Colinvaux et al., 2000). Molecular