Explosive Pleistocene range expansion leads to widespread Amazonian sympatry between robust and gracile capuchin monkeys

Journal of Biogeography

Volumn 39, Issue 2, 2012, Pages 272-288

  Lynch Alfaro, Jessica W ^a   Boubli, Jean P ^b   Olson, Link E ^c   Di Fiore, Anthony ^d   Wilson, Bryan ^e   Gutiérrez Espeleta, Gustavo A ^f   Chiou, Kenneth L ^d,g   Schulte, Meredith ^e   Neitzel, Sarah ^e   Ross, Vanessa ^e   Schwochow, Doreen ^a   Nguyen, Mai T T ^a   Farias, Izeni ^h   Janson, Charles H ⁱ   Alfaro, Michael E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b WILDLIFE CONSERVATION SOCIETY   (Brazil)

^c UNIVERSITY OF ALASKA MUSEUM   (United States)

^d NEW YORK UNIVERSITY   (United States)

^e WASHINGTON STATE UNIVERSITY   (United States)

^f UNIVERSIDAD DE COSTA RICA   (Costa Rica)

^g WASHINGTON UNIVERSITY   (United States)

^h FEDERAL UNIVERSITY OF AMAZONAS   (Brazil)

ⁱ UNIVERSITY OF MONTANA   (United States)

Author keywords

Amazon Basin; Atlantic Forest; Cebus; Neotropical primates; Platyrrhini; Pleistocene expansion; Sapajus; Sympatry

Indexed keywords

MIOCENE; MORPHOLOGY; MUSEUM; NEOTROPIC ECOZONE; PHYLOGEOGRAPHY; PLEISTOCENE; PLIOCENE; PRIMATE; RANGE EXPANSION; SYMPATRY;

AMAZON BASIN; ATLANTIC FOREST;

CEBUS; PLATYRRHINI; PRIMATES;

EID: 84855812900     PISSN: 03050270     EISSN: 13652699     Source Type: Journal    
DOI: 10.1111/j.1365-2699.2011.02609.x     Document Type: Article

References (72)

1. Barber, P. (2004) Extraction protocol: Chelex. Available at: (last accessed 13 June 2011).
2. Barroso, C.M.L., Schneider, H., Schneider, M.P.C., Sampaio, I., Harada, M.L., Czelusniak, J. & Goodman, M. (1997) Update on the phylogenetic systematics of New World monkeys: further DNA evidence for placing the pygmy marmoset (Cebuella) within the genus Callithrix. International Journal of Primatology, 18, 651-674.
3. Boubli, J.P. & Ditchfield, A. (2000) The time of divergence between the two species of uacari monkeys, Cacajao calvus and Cacajao melanocephalus. Folia Primatologica, 71, 387-391.
4. Casado, F., Bonvincino, C.R., Nagle, C., Comas, B., Manzur, T.D., Lahos, M.M. & Seuánez, H.N. (2010) Mitochondrial divergence between 2 populations of the hooded capuchin, Cebus (Sapajus) cay (Platyrrhini, Primates). Journal of Heredity, 101, 261-269.
5. Cheviron, Z.A., Hackett, S.J. & Capparella, A.P. (2005) Complex evolutionary history of a Neotropical lowland forest bird (Lepidothrix coronata) and its implications for historical hypotheses of the origin of Neotropical avian diversity. Molecular Phylogenetics and Evolution, 36, 338-357.
6. Chiou, K.L., Pozzi, L., Lynch Alfaro, J.W. & Di Fiore, A. (2011) Pleistocene diversification of living squirrel monkeys (Saimiri spp.) inferred from complete mitochondrial genome sequences. Molecular Phylogenetics and Evolution, 59, 736-745.
7. Colinvaux, P.A., De Oliveira, P.E. & Bush, M.B. (2000) Amazonian and neotropical plant communities on glacial timescales: the failure of the aridity and refuge hypotheses. Quaternary Science Reviews, 191, 141-169.
8. Collins, A.C. & Dubach, J.M. (2000) Biogeographic and ecological forces responsible for speciation in Ateles. International Journal of Primatology, 21, 421-444.
9. Cortés-Ortiz, L., Bermingham, E., Rico, C., Rodríguez-Luna, E., Sampaio, I. & Ruiz-García, M. (2003) Molecular systematics and biogeography of the neotropical monkey genus, Alouatta. Molecular Phylogenetics and Evolution, 26, 64-81.
10. Costa, L.P. (2003) The historical bridge between the Amazon and the Atlantic Forest of Brazil: a study of molecular phylogeography with small mammals. Journal of Biogeography, 30, 71-86.
11. De Oliveira, P.E., Barreto, A.M.F. & Sugiro, K. (1999) Late Pleistocene/Holocene climatic and vegetational history of the Brazilian Caatinga: the fossil dunes of the middle São Francisco River. Palaeogeography, Palaeoclimatology, Palaeoecology, 152, 319-337.
12. Defler, T.R. (1982) A comparison of intergroup behavior in Cebus albifrons and C. apella. Primates, 23, 385-392.
13. Defler, T.R. (1985) Contiguous distribution of two species of cebus monkeys in El Tuparro National Park, Colombia. American Journal of Primatology, 8, 101-112.
14. Defler, T.R. (2004) Primates of Colombia. Conservation International, Bogotá.
15. Di Fiore, A., Link, A., Schmitt, C.A. & Spear, S.N. (2009) Dispersal patterns in sympatric woolly and spider monkeys: integrating molecular and observational data. Behaviour, 146, 437-470.
16. Don, R.H., Cox, P.T., Wainwright, B.J., Baker, K. & Mattick, J.S. (1991) Touchdown PCR to circumvent spurious priming during gene amplification. Nucleic Acids Research, 19, 4008.
17. Drummond, A.J. & Rambaut, A. (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214.
18. Elliot, D.G. (1913) Review of the Primates. Monograph series Vol II. American Museum of Natural History, New York.
19. Ford, S.M. (2006) The biogeographic history of Mesoamerican primates. New perspectives in the study of Mesoamerican primates (ed. by A. Estrada, P.A. Garber, M. Pavelka and L. Luecke ), pp. 81-114. Springer, New York.
20. Gregory-Wodzicki, K.M. (2000) Uplift history of the central and northern Andes: a review. Geological Society of America Bulletin, 112, 1091-1105.
21. Groves, C.P. (2001) Primate taxonomy. Smithsonian Institution Press, Washington, DC.
22. Hartwig, W.C. & Meldrum, D.J. (2002) Miocene platyrrhines of the northern Neotropics. The primate fossil record (ed. by W.C. Hartwig ), pp. 175-188. Cambridge University Press, Cambridge.
23. Haugaasen, T. & Peres, C.A. (2005) Primate assemblage structure in Amazonian flooded and unflooded forests. American Journal of Primatology, 67, 243-258.
24. Haugaasen, T. & Peres, C.A. (2009) Interspecific primate associations in Amazonian flooded and unflooded forests. Primates, 50, 239-251.
25. Hershkovitz, P. (1949) Mammals of northern Colombia. Preliminary report No. 4: Monkeys (Primates) with taxonomic revisions of some forms. Proceedings of the United States National Museum, 98, 323-427.
26. Hershkovitz, P. (1955) Notes on American monkeys of the genus Cebus. Journal of Mammalogy, 36, 449-452.
27. Hill, W.C.O. (1960) Primates: comparative anatomy and taxonomy. IV. Cebidae, Part A. Edinburgh University Press, Edinburgh.
28. Hoorn, C., Wesselingh, F.P., ter Steege, H., Bermudez, M.A., Mora, A., Sevink, J., Sanmartín, I., Sanchez-Meseguer, A., Anderson, C.L., Figueiredo, J.P., Jaramillo, C., Riff, D., Negri, F.R., Hooghiemstra, H., Lundberg, J., Stadler, T., Särkinen, T. & Antonelli, A. (2010) Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science, 330, 927-931.
29. IUCN (2011) IUCN Red List of Threatened Species. Version 2011.1. Available at:
30. Izawa, K. (1980) Social behavior of the wild black-capped capuchin (Cebus apella). Primates, 21, 443-467.
31. Janson, C.H. (1986a) Capuchin counterpoint. Natural History, 95, 44-53.
32. Janson, C.H. (1986b) The mating system as a determinant of social evolution in capuchin monkeys (Cebus). Primate ecology and conservation (ed. by J.G. Else and P.C. Lee ), pp. 169-179. Cambridge University Press, New York.
33. Kay, R.F. & Cozzuol, M.A. (2006) New platyrrhine monkeys from the Solimões Formation (late Miocene, Acre State, Brazil). Journal of Human Evolution, 50, 673-686.
34. Kay, R.F. & Fleagle, J.G. (2010) Stem taxa, homoplasy, long lineages, and the phylogenetic position of Dolichocebus. Journal of Human Evolution, 59, 218-222.
35. Kay, R.F. & Frailey, C.D. (1993) Large fossil platyrrhines from the Rio Acre fauna, late Miocene, western Amazonia. Journal of Human Evolution, 25, 319-327.
36. Kay, R.F., Johnson, D.J. & Meldrum, D.J. (1998) A new pitheciin primate from the middle Miocene of Argentina. American Journal of Primatology, 45, 317-336.
37. Kay, R.F., Johnson, D.J. & Meldrum, D.J. (1999) Proteropithecia, new name for Propithecia Kay, Johnson and Meldrum, 1998 non Vojnits 1985. American Journal of Primatology, 47, 347.
38. Kinzey, W.G. (1982) Distribution of primates and forest refuges. Biological diversification in the tropics (ed. by G.T. Prance ), pp. 455-482. Columbia University Press, New York.
39. Knapp, S. & Mallet, J. (2003) Refuting refugia? Science, 300, 71-72.
40. Lemey, P., Rambaut, A., Drummond, A.J. & Suchard, M.A. (2009) Bayesian phylogeography finds its roots. PLoS Computational Biology, 5, article no. e1000520.
41. Lemmon, A.R. & Lemmon, E.M. (2008) A likelihood framework for estimating phylogeographic history on a continuous landscape. Systematic Biology, 57, 544-561.
42. Lynch, J.D. (1988) Refugia. Analytical biogeography (ed. by A.A. Myers and P.S. Giller ), pp. 311-342. Chapman & Hall, London.
43. Mannu, M. & Ottoni, E.B. (2009) The enhanced tool-kit of two groups of wild bearded capuchin monkeys in the Caatinga: tool making, associative use, and secondary tools. American Journal of Primatology, 71, 242-251.
44. Martinez, R.A., Giudice, A., Szapkievich, V.B., Ascunce, M., Nieves, M., Zunino, G. & Mudry, M.D. (2002) Parameters modeling speciogenic processes in Cebus apella (Primates: Platyrrhini) from Argentina. Mastozoologia Neotropical, 9, 171-186.
45. Mendes Pontes, A.R., Malta, A. & Asfora, P.H. (2006) A new species of capuchin monkey, genus Cebus Erxleben (Cebidae, Primates): found at the very brink of extinction in the Pernambuco endemism centre. Zootaxa, 1200, 1-12.
46. Moritz, C., Patton, J.L., Schneider, C.J. & Smith, T.B. (2000) Diversification of rainforest faunas: an integrated molecular approach. Annual Review of Ecology, Evolution, and Systematics, 31, 533-563.
47. Nores, M. (2004) The implications of Tertiary and Quaternary sea level rise events for avian distribution patterns in the lowlands of northern South America. Global Ecology and Biogeography, 13, 149-161.
48. Oliveira, M.M. & Langguth, A. (2006) Rediscovery of Marcgrave's capuchin monkey and designation of a neotype for Simia flavia Schreber, 1774 (Primates, Cebidae). Boletim do Museu Nacional, Rio de Janeiro: Zoologia, 523, 1-16.
49. Olson, L.E. & Yoder, A.D. (2002) Using secondary structure to identify ribosomal numts: cautionary examples from the human genome. Molecular Biology and Evolution, 19, 93-100.
50. Ottoni, E.B. & Izar, P. (2008) Capuchin monkey tool use: overview and implications. Evolutionary Anthropology, 17, 171-178.
51. Patton, J.L., da Silva, M.N.F. & Malcolm, J.R. (2000) Mammals of the Rio Juruá and the evolutionary and ecological diversification of Amazonia. Bulletin of the American Museum of Natural History, 244, 1-306.
52. Peres, C.A. & Janson, C.H. (1999) Species coexistence, distribution, and environmental determinants of neotropical primate richness: a community-level zoogeographic analysis. Primate communities (ed. by J.G. Fleagle, C.H. Janson and K.E. Reed ), pp. 55-74. Cambridge University Press, Cambridge.
53. Por, F.D. (1992) Sooretama: the Atlantic rain forest of Brazil. SPB Academic Publishing, The Hague.
54. Puorto, G., Salomao, M.G., Theakston, R.D.G., Thorpe, R.S., Warrell, D.A. & Wuster, W. (2001) Combining mitochondrial DNA sequences and morphological data to infer species boundaries: phylogeography of lanceheaded pitvipers in the Brazilian Atlantic Forest, and the status of Bothrops pradoi (Squamata: Serpentes: Viperidae). Journal of Evolutionary Biology, 14, 527-538.
55. Rambaut, A. (1996) Se-Al v2.0a11: sequence alignment editor. Available at:
56. Rambaut, A. & Drummond, A.J. (2007) Tracer v1.5. Available at:
57. Ribas, C.C., Gaban-Lima, R., Miyaki, C.Y. & Cracraft, J. (2005) Historical biogeography and diversification within the Neotropical parrot genus Pionopsitta (Aves: Psittacideae). Journal of Biogeography, 32, 1409-1427.
58. Rosenberger, A.L., Hartwig, W.C., Takai, M., Setoguchi, T. & Shigehara, N. (1991a) Dental variability in Saimiri and the taxonomic status of Neosaimiri fieldsi, an early squirrel monkey from La Venta, Colombia. International Journal of Primatology, 12, 291-301.
59. Rosenberger, A.L., Setoguchi, T. & Hartwig, W.C. (1991b) Laventiana annectens, new genus and species: fossil evidence for the origins of callitrichine New World monkeys. Proceedings of the National Academy of Sciences USA, 88, 2137-2140.
60. Rylands, A.B., da Fonseca, G.A.B., Leite, Y.L.R. & Mittermeier, R.A. (1996) Primates of the Atlantic Forest: origin, distributions, endemism, and communities. Adaptive radiations of Neotropical primates (ed. by M.A. Norconk, A.L. Rosenberger and P.A. Garber ), pp. 21-51. Plenum Press, New York.
61. Rylands, A.B., Schneider, H., Langguth, A., Mittermeier, R.A., Groves, C.P. & Rodríguez-Luna, E. (2000) An assessment of the diversity of New World primates. Neotropical Primates, 8, 61-93.
62. Rylands, A.B., Kierulff, M.C.M. & Mittermeier, R.A. (2005) Some notes on the taxonomy and distributions of the tufted capuchin monkeys (Cebus, Cebidae) of South America. Lundiana, 6(Suppl.), 97-110.
63. Salazar-Bravo, J., Dragoo, J.W., Tinnin, D.S. & Yates, T.L. (2001) Phylogeny and evolution of the neotropical rodent genus Calomys: inferences from mitochondrial DNA sequence data. Molecular Phylogenetics and Evolution, 20, 173-184.
64. Schneider, H., Canavez, F.C., Sampaio, I., Moreira, M.A.M., Tagliaro, C.H. & Seuanez, H.N. (2001) Can molecular data place each neotropical monkey in its own branch? Chromosoma, 109, 515-523.
65. Schrago, C.G. (2007) On the time scale of New World primate diversification. American Journal of Physical Anthropology, 132, 344-354.
66. Silva, J. de S., Jr (2001) Especiação nos macacos-prego e cairaras, gênero Cebus Erxleben, 1777 (Primates, Cebidae). PhD Thesis, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil.
67. Silva, J. de S., Jr (2002) Taxonomy of capuchin monkeys, Cebus Erxleben, 1777. Neotropical Primates, 10, 29.
68. Springer, M. de S. & Douzery, E. (1996) Secondary structure and patterns of evolution among mammalian mitochondrial 12S rRNA molecules. Journal of Molecular Evolution, 43, 357-373.
69. Tagliaro, C.H., Schneider, M.P.C., Schneider, H., Sampaio, I.C. & Stanhope, M.J. (1997) Marmoset phylogenetics, conservation perspectives, and evolution of the mtDNA control region. Molecular Biology and Evolution, 14, 674-684.
70. Takai, M. (1994) New specimens of Neosaimiri fieldsi from La Venta, Colombia: a middle Miocene ancestor of the living squirrel monkeys. Journal of Human Evolution, 27, 329-360.
71. Torres de Assumpção, C. (1983) An ecological study of the primates of southeastern Brazil, with a reappraisal of Cebus apella races. PhD Thesis, University of Edinburgh, Edinburgh.
72. Youlatos, D. (1998) Positional behavior of two sympatric Guianan capuchin monkeys, the brown capuchin (Cebus apella) and the wedge-capped capuchin (Cebus olivaceus). Mammalia, 62, 351-365.