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Genetic characterization and structure of the endemic Colombian silvery brown bare-face tamarin, Saguinus leucopus (Callitrichinae, Cebidae, Primates)

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Abstract

We analyzed 115 Saguinus leucopus, from four Colombian departments (Antioquia, Bolivar, Caldas and Tolima ), for 701 bp of the mt COII gene and at 10 microsatellite loci to estimate gene diversity levels, possible molecular subspecies and historical demographic changes in this species. This endemic Colombian species showed an elevated gene diversity in this gene, although its geographical distribution is very restrictive and extremely threatened by habitat fragmentation. The mt COII gene did not show any geographical structure in the distribution of the haplotypes within this species, but it did show a noteworthy population expansion throughout the history of this species. A Bayesian analysis showed that the haplotype diversification of this species began around 1.6 million years ago (MYA), whilst a haplotype network gave the beginning of this diversification at around 0.5–0.6 MYA. Forty-seven individuals out of the 115 were analyzed for 10 DNA microsatellites. The genetic diversity was relatively elevated for this kind of marker too, and comparable to that found in other Neotropical monkeys with a wider geographical distribution. Two gene pools were detected with the microsatellites, one in the northern distribution area (Antioquia) and the other in the southern distribution area (Tolima). No tests detected any bottleneck affecting this population; however, two procedures (k test and Kimmel et al. 1998 test) detected significant population expansion for the microsatellite markers, like that seen with the mt COII gene.

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References

  • Adkins RM, Honeycutt RL (1991) Molecular phylogeny of the superorder Archonta. Proc Natl Acad Sci USA 88:10317–10321

    CAS  PubMed Central  PubMed  Google Scholar 

  • Adkins RM, Honeycutt RL (1994) Evolution of the primate cytochrome c oxidase subunit II gene. J Mol Evol 38:215–231

    CAS  PubMed  Google Scholar 

  • Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control AC-19:716–723

    Google Scholar 

  • Archie JW (1985) Statistical analysis of heterozygosity data: independent sample comparisons. Evolution 39:623–637

    Google Scholar 

  • Ascunce MS, Hasson E, Mudry MD (2003) COII: a useful tool for inferring phylogenetic relationships among New World monkeys (Primates, Platyrrhini). Zool Scr 32:397–406

    Google Scholar 

  • Ashley MV, Vaughn TA (1995) Owl monkeys (Aotus) are highly divergent in mitochondrial cytochrome c oxidase (COII) sequences. Int J Primatol 5:793–807

    Google Scholar 

  • Badouin L, Lebrun P (2000) An operational Bayesian approach for the identification of sexually reproduced cross-fertilized populations using molecular markers. In: Dore C, Dosba F, Baril C (eds) Proceedings of the international symposium on molecular markers for characterizing genotypes and identifying cultivars in horticulture, 6–9, Montpellier, France

  • Bandelt H-J, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    CAS  PubMed  Google Scholar 

  • Beerli P (1998) Estimation of migration rates and population sizes in geographically structured populations. In: Carvalho G (ed) Advances in molecular ecology. NATO-ASI workshop series. IOS Press, Amsterdam, pp 39–53

    Google Scholar 

  • Beerli P (2006) Comparison of Bayesian and maximum likelihood inference of population genetic parameters. Bioinformatics 22:341–345

    CAS  PubMed  Google Scholar 

  • Beerli P (2007) Estimation of the population scaled mutation rate from microsatellite data. Genetics 177:1967–1968

    PubMed Central  PubMed  Google Scholar 

  • Beerli P (2009) How to use Migrate or why are Markov chain Monte Carlo programs difficult to use? In: Bertorelle G, Bruford MW, Haue HC, Rizzoli A, Vernesi C (eds) Population genetics for animal conservation. Conservation biology, vol 17. Cambridge University Press, Cambridge, pp 42–79

    Google Scholar 

  • Beerli P, Felsenstein J (1999) Maximum-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. Genetics 152:763–773

    CAS  PubMed Central  PubMed  Google Scholar 

  • Beerli P, Felsenstein J (2001) Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proc Natl Acad Sci USA 98:4563–4568

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bennett SE (2003) Los micos de Colombia. Instituto de Investigación de Recursos Biológicos Alexander von Humboldt y Fundación Tropenbos, pp 1–260

  • Brown KS (1982) Paleoecology and regional patterns of evolution in Neotropical forest butterflies. In: Prance GT (ed) Biological diversification in the tropics. Columbia University Press, NY

    Google Scholar 

  • Bruford MW, Wayne RK (1993) Microsatellites and their application to population genetics studies. Curr Opin Genet Dev 3:939–943

    CAS  PubMed  Google Scholar 

  • Bush G (1975) Models in animal speciation. Annu Rev Ecol Syst 6:339–364

    Google Scholar 

  • Bush G, Case SM, Wilson AC, Patton JL (1977) Rapid speciation and chromosomal evolution in mammals. Proc Natl Acad Sci USA 74:3942–3946

    CAS  PubMed Central  PubMed  Google Scholar 

  • Capaldi RA (1990) Structure and function of cytochrome c oxidase. Annu Rev Biochem 59:569–596

    CAS  PubMed  Google Scholar 

  • Carretero-Pinzón X, Ruiz-García M, Defler TR (2009) The taxonomy and conservation status of Saimiri sciureus albigena: a squirrel monkey endemic to Colombia. Primate Conserv 24:89–95

    Google Scholar 

  • Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis: models and estimation procedures. Evolution 21:550–570

    Google Scholar 

  • Clapperton C (1993) Quaternary geology and geomorphology of South America. Elsevier, Amsterdam

    Google Scholar 

  • Clark PU (2002) Early deglaciation in the Tropical Andes. Science 298:7a

    Google Scholar 

  • Climap (1976) The surface of the ice-age Earth. Science 191:1131–1137

  • Collins AC, Dubach JM (2000a) Phylogenetic relationships of spider monkeys (Ateles) based on mitochondrial DNA variation. Int J Primatol 21:381–420

    Google Scholar 

  • Collins AC, Dubach JM (2000b) Biogeographic and ecological forces responsible for speciation in Ateles. Int J Primatol 21:421–444

    Google Scholar 

  • Collins AC, Dubach JM (2001) Nuclear DNA variation in spider monkeys (Ateles). Mol Phylogenet Evol 19:67–75

    CAS  PubMed  Google Scholar 

  • Cornuet JM, Luikart G (1996) Description of power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cornuet JM, Piry S, Luikart G, Estoup A, Solignac M (1999) New methods employing multilocus genotypes to select or exclude populations as origins of individuals. Genetics 153:1989–2000

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cortés-Ortiz L, Bermingham E, Rico C, Rodriguez-Luna E, Sampaio I, Ruiz-García M (2003) Molecular systematics and biogeography of the Neotropical monkey genus, Alouatta. Mol Phylogenet Evol 26:64–81

    PubMed  Google Scholar 

  • Defler TR (2003) Primates de Colombia. Conservación Internacional, Colombia

    Google Scholar 

  • Disotell TR, Honeycutt R, Ruvolo M (1992) Mitochondrial DNA phylogeny of the Old-World 1063 monkey tribe Papioni. Mol Biol Evol 9:1–13

    CAS  PubMed  Google Scholar 

  • Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214

    PubMed Central  PubMed  Google Scholar 

  • Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4:e88

    PubMed Central  PubMed  Google Scholar 

  • Efron B, Tibshirani RJ (1993) An introduction to the bootstrap. Chapman and Hall, New York

    Google Scholar 

  • Ellesworth JA, Hoelzer GA (1998) Characterization of microsatellite loci in a New World Primate, the mantled howler monkey (Alouatta palliata). Mol Ecol 7:657–658

    Google Scholar 

  • Elliot DG (1913) A review of primates. Monograph series. American Museum of Natural History, New York

    Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    PubMed  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003a) Inference of population structure: extensions to linked loci and correlated allele frequencies. Genetics 164:1567–1587

    CAS  PubMed Central  PubMed  Google Scholar 

  • Falush D, Wirth T, Linz B, Pritchard JK, Stephens M et al (2003b) Traces of human migrations in Helicobacter pylori populations. Science 299:1582–1585

    CAS  PubMed  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578

    CAS  PubMed Central  PubMed  Google Scholar 

  • Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376

    CAS  PubMed  Google Scholar 

  • Figueiredo WB, Carvalho-Filho NM, Schneider H, Sampaio I (1998) Mitochondrial DNA sequences and the taxonomic status of Alouatta seniculus populations in Northeastern Amazonia. Neotropical Primates 6:73–77

    Google Scholar 

  • Forman L, Kleiman DG, Bush RM, Dietz JM, Ballou JD, Phillips LG, Coimbra-Filho AF, O’Brien SJ (1986) Genetic variation within and among lion tamarin. Am J Phys Anthropol 71:1–11

    CAS  PubMed  Google Scholar 

  • Fu Y-X (1997) Statistical tests of neutrality against population growth, hitchhiking and background selection. Genetics 147:915–925

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fu Y-X, Li W-H (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709

    CAS  PubMed Central  PubMed  Google Scholar 

  • Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318

    CAS  PubMed  Google Scholar 

  • Goldizen AA, Terborgh J (1986) Cooperative polyandry and helping behavior in saddle-backed tamarins (Saguinus fuscicollis). In: Else JG, Lee PC (eds) Primate ecology and conservation. Cambridge University Press, Cambridge, pp 191–198

    Google Scholar 

  • Goodman SJ (1997) RST Calc: a collection of computer programs for calculating estimates of genetic differentiation from microsatellite data and determining their significances. Mol Ecol 6:881–885

    CAS  Google Scholar 

  • Goudet J, Raymond M, Demeeus T, Rousset F (1996) Testing differentiation in diploid populations. Genetics 144:1933–1940

    CAS  PubMed Central  PubMed  Google Scholar 

  • Haffer J (1969) Speciation in Amazonian forest birds. Science 165:131–137

    CAS  PubMed  Google Scholar 

  • Haffer J (1982) General aspects of the refuge theory. In: Prance GT (ed) Biological diversification in the tropics. Columbia University Press, New York, pp 6–24

    Google Scholar 

  • Haffer J (1997) Alternative models of vertebrate speciation in Amazonia: an overview. Biodivers Conserv 6:451–476

    Google Scholar 

  • Harpending HC (1994) Signature and ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600

    CAS  PubMed  Google Scholar 

  • Harpending HC, Sherry ST, Rogers AR, Stoneking M (1993) Genetic structure of ancient human populations. Curr Anthropol 34:483–496

    Google Scholar 

  • Hernández-Camacho J, Cooper RW (1976) The nonhuman primates of Colombia. In: Thorington RW Jr, Heltne PG (eds) Neotropical primates: field studies and conservation. National Academy of Sciences, Washington, DC, pp 35–69

    Google Scholar 

  • Izawa K (1978) A field study of the ecology and behavior of the black-mantle tamarin (Saguinus nigricollis). Primates 19:241–274

    Google Scholar 

  • Kimmel M, Chakraborty R, King JP, Bamshad M, Watkins WS, Jorde LB (1998) Signatures of population expansion in microsatellite repeat data. Genetics 148:1921–1930

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kinzey WG (1982) Distribution of primates and forest refuges. In: Prance GT (ed) Biological diversification in the tropics. Columbia University Press, New York, pp 455–482

    Google Scholar 

  • Lavergne A, Ruiz-García M, Catzeflis F, Lacote S, Contamin H, Mercerau-Puijalon B, Lacoste V, De Thoisy B (2010) Phylogeny and phylogeography of squirrel monkeys (genus Saimiri) based on cytochrome b genetic analysis. Am J Primatol 72:242–253

    CAS  PubMed  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. doi:10.1093/bioinformatics/btp187

    CAS  PubMed  Google Scholar 

  • Liu K, Colinvaux A (1985) Forest changes in the Amazon basin during the last glacial maximum. Nature 318:556–557

    Google Scholar 

  • Luikart G, Allendorf F, Sherwin B, Cornuet JM (1998) Distortion of allele frequency distribution provides a test for recent population bottleneck. J Hered 86:319–322

    Google Scholar 

  • Mau B (1996) Bayesian phylogenetic inference via Markov chain Monte Carlo methods. University of Wisconsin, Madison

    Google Scholar 

  • Mau B, Newton M, Larget B (1999) Bayesian phylogenetic inference via Markov chain Monte Carlo methods. Biometrics 55:1–12

    CAS  PubMed  Google Scholar 

  • Metivier SP (1998) A reconstruction of glacial extent, temperature and precipitation in South America at the time of the last glacial maximum. PhD thesis, Syracuse University

  • Michalakis Y, Excoffier L (1996) A generic estimation of population subdivision using distances between alleles with special reference to microsatellite loci. Genetics 142:1061–1064

    CAS  PubMed Central  PubMed  Google Scholar 

  • Morales-Jiménez AL, Link A, Stevenson P (2008) Saguinus leucopus. In: IUCN 2011. IUCN red list of threatened species. Version 2011.2. http://www.iucnredlist.org. Accessed 7 May 2013

  • Morral N, Bertrantpetit J, Estivill X (1994) The origin of the major cystic fibrosis mutation (delta F508) in European populations. Nat Genet 7:169–175

    CAS  PubMed  Google Scholar 

  • Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci USA 70:3321–3323

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nei M, Tajima F, Tateno Y (1983) Accuracy of estimated phylogenetic trees from molecular data. II. Gene frequency data. J Mol Evol 19:153–170

    CAS  PubMed  Google Scholar 

  • Paetkau D, Calvert W, Stirling I, Strobeck C (1995) Microsatellite analysis of population structure in Canadian polar bears. Mol Ecol 4:347–354

    CAS  PubMed  Google Scholar 

  • Patkeau D, Slade R, Barden M, Estoup A (2004) Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power. Mol Ecol 13:55–65

    Google Scholar 

  • Perelman P, Johnson WE, Roos C, Seuanez H, Horvath JE, Moreira MAM, Kessing B, Pontius J, Roelke M, Rumpler Y, Schneider MPC, Silva A, O’Brien SJ, Pecon-Slattery J (2011) A molecular phylogeny of living primates. Plos One Genet 7:e1001342

    CAS  Google Scholar 

  • Piry S, Alapetite A, Cornuet JM, Paetkau D, Baudouin L, Estoup A (2004) GENECLASS2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539

    CAS  PubMed  Google Scholar 

  • Plautz HL, Goncalves EC, Ferrari SF, Schneider MPC, Silva A (2009) Evolutionary inferences on the diversity of the genus Aotus (Platyrrhini, Cebidae) from mitochondrial cytochrome c oxidase subunit II gene sequences. Mol Phylogenet Evol 51:382–387

    CAS  PubMed  Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    CAS  PubMed  Google Scholar 

  • Poveda K, Cadena A, Sánchez P (2001) Habitat use of two groups of white footed tamarins (Saguinus leucopus) in Mariquita, Colombia. In: The 18th congress of the International Primatological Society: Primates in the new millennium, Adelaide, Australia, p 58 (abstract)

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100

    CAS  PubMed  Google Scholar 

  • Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci USA 94:9197–9201

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rannala B, Yang Z (1996) Probability distribution of molecular evolutionary trees: a new method of phylogenetic inference. J Mol Evol 43:304–311

    CAS  PubMed  Google Scholar 

  • Reich DE, Goldstein DB (1998) Genetic evidence for a Paleolithic human population expansion in Africa. Proc Natl Acad Sci USA 95:8119–8123

    CAS  PubMed Central  PubMed  Google Scholar 

  • Reich DE, Feldman MW, Goldstein DB (1999) Statistical properties of two tests that use multilocus data sets to detect population expansions. Mol Biol Evol 16:453–466

    CAS  Google Scholar 

  • Rogers AR, Harpending HC (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569

    CAS  PubMed  Google Scholar 

  • Rogers J, Witte SM, Slifer MA (1995) Five new microsatellite DNA polymorphisms in the squirrel monkey (Saimiri boliviensis). Am J Primatol 36:151

    Google Scholar 

  • Rogers AR, Fraley AE, Bamshad MJ, Watkins WS, Jorde LB (1996) Mitochondrial mismatch analysis is insensitive to the mutational process. Mol Biol Evol 13:895–902

    CAS  PubMed  Google Scholar 

  • Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ruivo EB, Carroll JB, Morales-Jiménez AL (2005) The silvery-brown tamarin (Saguinus leucopus) conservation project. Neotropical Primates 13:36–39

    Google Scholar 

  • Ruiz-García M (2005) The use of several microsatellite loci applied to 13 Neotropical primates revealed a strong recent bottleneck event in the woolly monkey (Lagothrix lagotricha) in Colombia. Primate Rep 71:27–55

    Google Scholar 

  • Ruiz-García M, Pinedo-Castro M (2010) Molecular systematics and phylogeography of the genus Lagothrix (Atelidae, Primates) by means of mitochondrial COII gene. Folia Primatol 81:109–128

    PubMed  Google Scholar 

  • Ruiz-García M, Pinedo-Castro M (2013) How many genera and species of woolly monkeys (Atelidae, Platyrrhini, Primates) are there? The first molecular analysis of Lagothrix flavicauda, an endemic Peruvian primate species. Mol Phylogenet Evol (in press)

  • Ruiz-Garcia M, Shostell JM (2013) Molecular population genetics, evolutionary biology and biological conservation of the Neotropical carnivores. Nova Science Publisher, New York, pp 1–720

    Google Scholar 

  • Ruiz-García M, Castillo MI, Álvarez D (2004) Evolutionary trends of Neotropical primates according to the AP68 and AP40 microsatellites. In: Mendes SL, Chiarello AG (eds) A Primatologia no Brasil, volumen 8. Museu de Biologia Prof. Mello Leitão, Santa Teresa, pp 65–100

    Google Scholar 

  • Ruiz-García M, Parra A, Romero-Aleán N, Escobar-Armel P, Shostell JM (2006) Genetic characterization and phylogenetic relationships between the Ateles species (Atelidae, Primates) by means of DNA microsatellite markers and craniometric data. Primate Rep 73:3–47

    Google Scholar 

  • Ruiz-García M, Escobar-Armel P, Alvarez D, Mudry M, Ascunce M, Gutierrez-Espeleta G, Shostell J (2007) Genetic variability in four Alouatta species measured by means of nine DNA microsatellite markers: genetic structure and recent bottlenecks. Folia Primatol 78:73–87

    PubMed  Google Scholar 

  • Ruiz-García M, Castillo MI, Vásquez C, Rodríguez K, Pinedo-Castro M, Shostell J, Leguizamon N (2010) Molecular phylogenetics and phylogeography of the white-fronted capuchin (Cebus albifrons; Cebidae, Primates) by means of mtCOII gene sequences. Mol Phylogenet Evol 57:1049–1061

    PubMed  Google Scholar 

  • Ruiz-García M, Vásquez C, Camargo E, Leguizamon N, Castellanos-Mora LF, Vallejo A, Gálvez H, Shostell J, Alvarez D (2011) The molecular phylogeny of the Aotus genus (Cebidae, Primates). Int J Primatol 32:1218–1241

    Google Scholar 

  • Ruiz-García M, Castillo MI, Lichilin N, Pinedo-Castro M (2012a) Molecular relationships and classification of several tufted capuchin lineages (Cebus apella, C. xanthosternos and C. nigritus, Cebidae), by means of mitochondrial COII gene sequences. Folia Primatol 83:100–125

    PubMed  Google Scholar 

  • Ruiz-García M, Castillo MI, Ledezma A, Leguizamon N, Sánchez R, Chinchilla M, Gutierrez-Espeleta G (2012b) Molecular systematics and phylogeography of Cebus capucinus (Cebidae, Primates) in Colombia and Costa Rica by means of mitochondrial COII gene. Am J Primatol 74:366–380

    PubMed  Google Scholar 

  • Ruiz-García M, Luengas-Villamil K, Leguizamon N, Thoisy B, Galvez H (2013a) Molecular phylogenetics and phylogeography of all the Saimiri taxa (Cebidae, Primates) by means of mtCOII gene sequences. Mol Phylogenet Evol (in press)

  • Ruiz-García M, Vásquez C, Camargo E, Castellanos-Mora LF, Gálvez H, Shostell J (2013b) Molecular genetics analysis of mtDNA COII gene sequences shows illegal traffic of night monkeys (Aotus, Platyrrhini, Primates) in Colombia. J Primatol 2:107. doi:10.4172/2167-6801.1000107

    Google Scholar 

  • Ruiz-García M, Cerón A, Pinedo-Castro M, Gutierrez-Espeleta G (2013b) Phylogenetics and historical genetics of Alouatta palliata (Atelidae, Primates) in Costa Rica, Panama, Colombia and Ecuador by means of mtDNA sequences. Am J Phys Anthropol (submitted)

  • Ruvolo M, Disotell TR, Allard MW, Brown WM, Honeycutt RL (1991) Resolution of the African hominoid trichotomy by use of a mitochondrial gene sequence. Proc Natl Acad Sci USA 88:1571–1574

    Google Scholar 

  • Saillard J, Forster P, Lynnerup N, Bandelt H-J, Norby S (2000) mtDNA variation among Greenland Eskimos: the edge of the Beringian expansion. Am J Hum Genet 67:718–726

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Savage A (1990) The reproductive biology of the cotton-top tamarin (Saguinus oedipus oedipus) in Colombia. PhD thesis, University of Wisconsin, Madison

  • Simonsen KL, Churchill GA, Aquadro CF (1995) Properties of statistical tests of neutrality for DNA polymorphism data. Genetics 141:413–429

    CAS  PubMed Central  PubMed  Google Scholar 

  • Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462

    CAS  PubMed Central  PubMed  Google Scholar 

  • Snow CA (1986) A life history study of the Geoffroy’s tamarin, Saguinus geoffroyi, with emphasis on male-female relationships in captive animals. PhD thesis, Kent State University

  • Soini P (1987) Ecology of the saddle-back tamarin Saguinus fuscicollis illigeri on the río Pacaya, northeastern Peru. Folia Primatol 49:11–32

    Google Scholar 

  • Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony and other methods, pp 1–142. http://paup.csit.fsu.edu

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    CAS  PubMed Central  PubMed  Google Scholar 

  • Terborgh J, Goldizen AW (1985) On the mating system of the cooperatively breeding saddle-backed tamarin (Saguinus fuscicollis). Behav Ecol Sociobiol 16:293–299

    Google Scholar 

  • Van der Hammen T, Duivenvoorden JF, Lips JM, Urrego LE, Espejo N (1991) El cuaternario tardío del área del Medio Caquetá (Amazonia colombiana). Colombia Amazónica 5:63–90

    Google Scholar 

  • Walsh PS, Metzger DA, Higuchi R (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506–513

    CAS  PubMed  Google Scholar 

  • Weber JL, May PE (1989) Abundant class of human DNA polymorphisms which can be typed using the polymerase chain reaction. Am J Hum Genet 44:388–396

    CAS  PubMed Central  PubMed  Google Scholar 

  • Whitmore TC, Prance GT (1987) Biogeography and quaternary history in tropical America. In: Oxford monographs in biogeography, vol 3. Oxford University Press, Oxford

  • Wright S (1951) The genetical structure of populations. Ann Eugen 15:323–354

    CAS  PubMed  Google Scholar 

  • Wright HE Jr (1983) Late-Pleistocene glaciation and climate around the Junin Plain, central Peruvian highlands. Geogr Ann 65A:35–43

    Google Scholar 

  • Zhivotovsky LA, Bennett L, Bowcock AM, Feldman MW (2000) Human population expansion and microsatellite variation. Mol Biol Evol 17:757–767

    CAS  PubMed  Google Scholar 

  • Zhong F, Brady AG, Shi J (1996) Strategy using pooled DNA to identify 56 short tandem repeat polymorphisms for the Bolivian squirrel monkey. Biotechniques 21:580–586

    CAS  PubMed  Google Scholar 

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Acknowledgments

Thanks go to the SDA (Secretaria Distrital Ambiental de Bogotá DC, Colombia) for the project entitled “Fortalecimiento del control y prevención del tráfico ilegal de fauna silvestre, especialmente de Primates, Perezosos y Ardillas, a través de la determinación de zonas sometidas a extracción ilegal utilizando pruebas de genética molecular de poblaciones”, which allowed us to obtain the necessary financial resources to carry out the current study. Thanks to Dr. D. Álvarez and L.F. Castellanos-Mora for their respective help in obtaining Saguinus leucopus samples over the last 10 years. In addition, thanks to Amador Ávila, Claudia Brieva and Carlos del Valle (URRAS, Universidad Nacional de Colombia) as well as to the Natura Foundation for providing S. leucopus samples and financial resources (Natura Foundation). Also, thanks to L.M. Borrero and D.M. Ramírez from the Medellín Zoo, Tinka Plese (UNAU, Medellín) and Cornare (Medellín), for providing Saguinus samples.

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Ruiz-García, M., Escobar-Armel, P., Leguizamon, N. et al. Genetic characterization and structure of the endemic Colombian silvery brown bare-face tamarin, Saguinus leucopus (Callitrichinae, Cebidae, Primates). Primates 55, 415–435 (2014). https://doi.org/10.1007/s10329-014-0418-2

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