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Subspecies of the Central American Squirrel Monkey (Saimiri oerstedii) as Units for Conservation

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Abstract

The accurate diagnosis of conservation units now typically includes recognition of genetic diversity and unique evolutionary lineages and is necessary to inform the conservation management of endangered species. We evaluated whether the two currently recognized subspecies of the endangered Central American squirrel monkey (Saimiri oerstedii) in Costa Rica are evolutionarily significant units (ESUs) that should be managed separately in conservation efforts. We used previously published sequences of 50 individuals of Saimiri oerstedii for 880 bp of the mtDNA d-loop and genotypes of 244 individuals for 16 microsatellites and conducted novel analyses to characterize genetic differentiation between subspecies of Saimiri oerstedii. We measured sequence differentiation and inferred an intraspecific molecular phylogeny and a haplotype network, and found consistent results supporting statistically significant divergence and reciprocal monophyly between subspecies. A population aggregation analysis also supported Saimiri oerstedii citrinellus and S. o. oerstedii as diagnosably distinct units. These results confirm previous genetic studies with smaller sample sizes and are consistent with other factors including differences in pelage and morphology and divergence at nuclear markers. Conservation managers should manage these subspecies separately to prevent the loss of genetic diversity via artificially induced outbreeding. High levels of genetic diversity may buffer populations against outside extinction pressures, to which Saimiri oerstedii are vulnerable because of their dwindling habitat and small population size.

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References

  • Arauz, J. (1993). Estado de conservación del mono tití (Saimiri oerstedii citrinellus) en su área de distribución original. Costa Rica: Universidad Nacional, Heredia, Costa Rica.

    Google Scholar 

  • Bandelt, H. J., Forster, P., & Rohl, A. (1999). Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37–48.

    Article  PubMed  CAS  Google Scholar 

  • Blair, M. E. (2011). Habitat modification and gene flow in Saimiri oerstedii: Landscape genetics, intraspecific molecular phylogenetics, and conservation. Ph.D. dissertation, New York: Columbia University.

  • Blair, M. E., & Melnick, D. J. (2012a). Genetic evidence for dispersal by both sexes in the Central American squirrel monkey, Saimiri oerstedii citrinellus. American Journal of Primatology, 74, 37–47.

    Article  PubMed  CAS  Google Scholar 

  • Blair, M. E., & Melnick, D. J. (2012b). Scale-dependent effects of a heterogeneous landscape on genetic differentiation in the Central American squirrel monkey (Saimiri oerstedii). PLoS ONE, 7, e43027.

    Article  PubMed  CAS  Google Scholar 

  • Blair, M. E., Sterling, E. J., & Hurley, M. M. (2011). Taxonomy and conservation of Vietnam’s primates: a review. American Journal of Primatology, 73, 1093–1106.

    Article  PubMed  Google Scholar 

  • Boinski, S. (1999). The social organizations of squirrel monkeys: implications for ecological models of social evolution. Evolutionary Anthropology, 8(3), 101–112.

    Article  Google Scholar 

  • Boinski, S., & Cropp, S. J. (1999). Disparate data sets resolve squirrel monkey (Saimiri) taxonomy: implications for behavioral ecology and biomedical usage. International Journal of Primatology, 20(2), 237–256.

    Article  Google Scholar 

  • Boinski, S., & Sirot, L. (1997). Uncertain conservation status of squirrel monkeys in Costa Rica. Folia Primatologica, 68, 181–193.

    Article  Google Scholar 

  • Boinski, S., Jack, K., Lamarsh, C., & Coltrane, J. A. (1998). Squirrel monkeys in Costa Rica: drifting to extinction. Oryx, 32(1), 45–58.

    Google Scholar 

  • Carrillo, E., Wong, G., & Saenz, J. C. (2002). Mammals of Costa Rica, 2nd ed. Santo Domingo de Heredia. Costa Rica: National Institute of Biodiversity.

    Google Scholar 

  • Chen, S., Su, S., Lo, C., Chen, K., Huang, T., Kuo, B., et al. (2009). PALM: A paralleled and integrated framework for phylogenetic inference with automatic likelihood model selectors. PLoS ONE, 4(12), e8116.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Cracraft, J. (1983). Species concepts and speciation analysis. Current Ornithology, 1, 159–187.

    Article  Google Scholar 

  • Crandall, K. A., Bininda-Emonds, O. R. P., Mace, G. M., & Wayne, R. K. (2000). Considering evolutionary processes in conservation biology. Trends in Ecology and Evolution, 15(7), 290–295.

    Article  PubMed  Google Scholar 

  • Cropp, S., & Boinski, S. (2000). The Central American squirrel monkey (Saimiri oerstedii): introduced hybrid or endemic species? Molecular Phylogenetics and Evolution, 16(3), 350–365.

    Article  PubMed  CAS  Google Scholar 

  • Daugherty, C. H., Cree, A., Hay, J. M., & Thompson, M. B. (1990). Neglected taxonomy and continuing extinctions of tuatara (Sphenodon). Nature, 347, 376–389.

    Article  Google Scholar 

  • Davis, J. I., & Nixon, K. C. (1992). Populations, genetic variation, and the delimitation of phylogenetic species. Systematic Biology, 41(4), 421–435.

    Google Scholar 

  • de Queiroz, K. (2007). Species concepts and species delimitation. Systematic Biology, 56, 879–886.

    Article  PubMed  Google Scholar 

  • DeSalle, R., & Amato, G. (2004). The expansion of conservation genetics. Nature Reviews Genetics, 5, 702–712.

    Article  PubMed  CAS  Google Scholar 

  • Ford, S. (2005). The biogeographic history of Mesoamerican primates. In A. Estrada, P. A. Garber, M. Pavelka, & L. Luecke (Eds.), New perspectives in the study of Mesoamerican primates (pp. 81–114). New York: Springer.

    Google Scholar 

  • Hasegawa, M., Kishino, H., & Yano, T. (1985). Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution, 22, 160–174.

    Article  PubMed  CAS  Google Scholar 

  • Hendry, A. P., Lohmann, L. G., Conti, E., Cracraft, J., Crandall, K. A., Faith, D. P., et al. (2010). Evolutionary biology in biodiversity science, conservation, and policy: a call to action. Evolution, 64, 1517–1528.

    PubMed  Google Scholar 

  • Hershkovitz, P. (1984). Taxonomy of squirrel monkeys genus Saimiri (Cebidae, Platyrrhini): a preliminary report with a description of a hitherto unnamed form. American Journal of Primatology, 6, 257–312.

    Article  Google Scholar 

  • IUCN. (2012). IUCN red list of threatened species. Gland: International Union for the Conservation of Nature.

    Google Scholar 

  • Librado, P., & Rozas, J. (2009). DNASP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451–1452.

    Article  PubMed  CAS  Google Scholar 

  • Mace, G. M. (2004). The role of taxonomy in species conservation. Proceedings of the Royal Society of London Series B: Biological Sciences, 359, 711–719.

    Google Scholar 

  • Mayr, E. (1963). Animal species and evolution. Oxford: Oxford University Press.

    Google Scholar 

  • Melnick, D. J., Morales, J. C., & Honeycutt, R. L. (1999). Conservation genetics: Applying molecular methods to maximize the conservation of taxonomic and genetic diversity. In P. Raven & T. Williams (Eds.), Nature and human society: The quest for a sustainable world (pp. 264–275). Washington, DC: National Academies Press.

    Google Scholar 

  • Moritz, C. (1994). Defining 'evolutionarily significant units' for conservation. Trends in Ecology and Evolution, 9(10), 373–375.

    Article  PubMed  CAS  Google Scholar 

  • Moritz, C. (2002). Strategies to protect biological diversity and the evolutionary processes that sustain it. Systematic Biology, 51(2), 238–254.

    Article  PubMed  Google Scholar 

  • Nores, M. (1999). An alternative hypothesis for the origin of Amazonian bird diversity. Journal of Biogeography, 26, 475–485.

    Article  Google Scholar 

  • Nylander, A. A. (2004). MrModeltest v2. Program distributed by the author. Uppsala University: Evolutionary Biology Centre.

  • Ronquist, F., & Huelsenbeck, J. P. (2003). MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1572–1574.

    Article  PubMed  CAS  Google Scholar 

  • Ryder, O. A. (1986). Species conservation and systematics—the dilemma of subspecies. Trends in Ecology and Evolution, 1(1), 9–10.

    Article  Google Scholar 

  • Rylands, A. B., & Mittermeier, R. A. (2008). The diversity of the New World primates (Platyrrhini): An annotated taxonomy. In P. A. Garber, A. Estrada, J. C. Bicca-Marques, E. W. Heymann, & K. B. Strier (Eds.), South American Primates (pp. 23–54). New York: Springer.

    Google Scholar 

  • Sierra, C., Jimenez, I., Altricher, M., Fernandez, M., Gomez, G., Gonzalez, J., et al. (2003). New data on the distribution and abundance of Saimiri oerstedii citrinellus. Primate Conservation, 19, 5–9.

    Google Scholar 

  • Templeton, A. R. (1986). Coadaptation and outbreeding depression. In M. Soule (Ed.), Conservation biology: Science of scarcity and diversity (pp. 105–116). Sunderland, MA: Sinauer.

  • Vogler, A. P., & DeSalle, R. (1994). Diagnosing units of conservation management. Conservation Biology, 8(2), 354–363.

    Article  Google Scholar 

  • Walsh, P. D. (2000). Sample size for the diagnosis of conservation units. Conservation Biology, 14, 1533–1537.

    Article  Google Scholar 

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Acknowledgments

We thank two anonymous reviewers and also M. Losilla for comments that greatly improved this manuscript. We thank the other members of M. Blair’s dissertation advisory committee: A. Di Fiore, M. Cords, R. DeSalle, and T. Disotell. We also thank collaborators, nongovernmental organizations, and representatives from the Ministry of Energy and the Environment and local governments in Costa Rica including G. Wong, M. Schulte, F. Villanea, J. Aguero, M. Cook, L. Leon, J. Bustamante, O. Masis, L. Rubí, and H. Abarca. Field assistants F. Rutka, D. Lake, R. Leon, and W. Chacon helped collect samples in Costa Rica, and we thank K. Desvenain, the Rubí-Brenes family, Hotel Rancho Casa Grande, Hotel Byblos, Hotel Tulemar, Hotel La Posada, and Sky Mountain Canopy Tour for allowing us to search for squirrel monkeys on their property. K. Chiou, M. Montague, A. Morales-Jimenez, C. Bergey, A. Burrell, J. Corush, L. Pozzi, and S. Pickett provided invaluable help in the laboratory. We thank M. Brown, L. Douglas, K. Schmidt, C. Schmitt, J. Hodgson, Z. Liu, K. Guschanski, O. Pineda, A. Goncalves da Silva, J. Munshi-South, and R. Raaum for invaluable advice on data analyses. This research was generously funded by the National Science Foundation (NSF) Award No. BCS-0847912, the American Association of University Women, the Margot Marsh Biodiversity Foundation, Columbia University, the International Primatological Society, the American Society of Primatologists, and the Northwest Primate Conservation Society. M. Blair was supported during her graduate training by the NSF Integrative Graduate Education and Research Traineeship (IGERT) program the New York Consortium in Evolutionary Primatology (NYCEP), Award No. DGE-0333415.

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Blair, M.E., Gutierrez-Espeleta, G.A. & Melnick, D.J. Subspecies of the Central American Squirrel Monkey (Saimiri oerstedii) as Units for Conservation. Int J Primatol 34, 86–98 (2013). https://doi.org/10.1007/s10764-012-9650-z

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  • DOI: https://doi.org/10.1007/s10764-012-9650-z

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