Abstract
Habitat loss and fragmentation, illegal trade, and other anthropogenic activities cause the population decline of wild species including primates. The white-footed tamarin (Saguinus leucopus) is highly affected by habitat loss and illegal traffic in northwest Colombia. Few studies have been carried out on the species levels of genetic diversity and structure as a means to understand the demographic history of this species, identify conservation management units, and prioritize conservation efforts. In this study we evaluate levels of genetic diversity and population structure for S. leucopus and identify historical demographic changes along its entire geographical range employing 12 nuclear microsatellite loci and the mitochondrial Hypervariable Region I. We identified four well-differentiated population clusters and high levels of genetic diversity in some clusters. We also found evidence of a north-to-south diversification process during the Pleistocene (between 718,600 and 284,800 years ago) and a recent decrease in the effective population size overall. We recommend integrating this information into management practices and conservation plans for the species, and information about observed genetic differences among gene pools as a tool to infer the origin of S. leucopus individual rescued from illegal trade.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Allendorf FW (2017) Genetics and the conservation of natural populations: allozymes to genomes. Mol Ecol 26:420–430. https://doi.org/10.1111/mec.13948
Amos W, Hoffman JI, Frodsham A et al (2007) Automated binning of microsatellite alleles: problems and solutions. Mol Ecol Resour 7:10–14. https://doi.org/10.1111/j.1471-8286.2006.01560.x
Arciniegas Vacares JS (2015) Caracterización genética de poblaciones naturales de Saguinus leucopus (Primates: Callitrichidae) a lo largo de su rango de distribución. MSc thesis, Universidad Nacional de Colombia, Bogota. https://repositorio.unal.edu.co/handle/unal/56720
Arroyave FJA, Goyeneche OYR, Gómez MAB et al (2014) Tráfico ilegal de tortugas continentales (Testudinata) en Colombia: una aproximación desde el análisis de redes. Acta Biol Colomb 19:381–392. https://doi.org/10.15446/abc.v19n3.41590
Bairrão Ruivo E, Wormell D (2012) The international conservation programme for the White-footed tamarin Saguinus leucopus in Colombia. Int Zoo Yearb 46:46–55. https://doi.org/10.1111/j.1748-1090.2012.00173.x
Baker PA, Fritz SC, Battisti DS et al (2020) Beyond refugia: new insights on quaternary climate variation and the evolution of biotic diversity in tropical South America. In: Rull V, Carnaval AC (eds) Neotropical diversification: patterns and processes. Springer, Cham, pp 51–70
Bensasson D, Feldman MW, Petrov DA (2003) Rates of DNA duplication and mitochondrial DNA insertion in the human genome. J Mol Evol 57:343–354. https://doi.org/10.1007/s00239-003-2485-7
Böhle UR, Zischler H (2002) Polymorphic microsatellite loci for the mustached tamarin (Saguinus mystax) and their cross-species amplification in other New World monkeys. Mol Ecol Resour 2:1–3. https://doi.org/10.1046/j.1471-8278.2001.00113.x
Buckner JC, Alfaro JWL, Rylands AB et al (2015) Biogeography of the marmosets and tamarins (Callitrichidae). Mol Phylogenet Evol 82:413–425. https://doi.org/10.1016/j.ympev.2014.04.031
Burrell AS, Disotell TR, Bergey CM (2015) The use of museum specimens with high-throughput DNA sequencers. J Hum Evol 79:35–44. https://doi.org/10.1016/j.jhevol.2014.10.015
Cotton A, Clark F, Boubli JP et al (2016) IUCN red list of threatened primate species. In: Wich S, Marshall A (eds) An introduction to primate conservation. Oxford University Press, New York, pp 31–38
Cuartas-Calle (2004) Distribución histórica y actual, uso del hábitat y estimación del estado de conservación de Saguinus leucopus (Tití gris) en el área de la jurisdicción de Corantioquia. Contrato 4910. Informe final
Darriba D, Taboada GL, Doallo R et al (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9(8):772. https://doi.org/10.1038/nmeth.2109
Díaz-Muñoz SL (2011) Paternity and relatedness in a polyandrous nonhuman primate: testing adaptive hypotheses of male reproductive cooperation. Anim Behav 82:563–571. https://doi.org/10.1016/j.anbehav.2011.06.013
Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7(1):214. https://doi.org/10.1186/1471-2148-7-214
Estrada A, Garber PA, Chaudhary A (2020) Current and future trends in socio-economic, demographic and governance factors affecting global primate conservation. PeerJ 8:e9816. https://doi.org/10.7717/peerj.9816
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x
Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10(3):564–567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
Falla AC (2017) Studbook nacional y plan de manejo Tití gris (Saguinus leucopus-Günter 1876), 4th edn. ACOPAZOA, Bogota
Frankham R, Ballou JD, Briscoe DA (2010) Introduction to conservation genetics, 2nd edn. Cambridge University Press, Cambridge
Fulton TL, Wagner SM, Shapiro B (2012) Case study: recovery of ancient nuclear DNA from toe pads of the extinct passenger pigeon. In: Shapiro B, Hofreiter M (eds) Ancient DNA: methods and protocols. Humana Press, Totowa, pp 29–35
Funk WC, McKay JK, Hohenlohe PA et al (2012) Harnessing genomics for delineating conservation units. Trends Ecol Evol 27(9):489–496. https://doi.org/10.1016/j.tree.2012.05.012
Garber PA, Porter LM, Spross J et al (2016) Tamarins: insights into monogamous and non-monogamous single female social and breeding systems. Am J Primatol 78:298–314. https://doi.org/10.1002/ajp.22370
García R (1997) Rehabilitación, reproducción y reintroducción de un grupo de Tití Gris cautivo (Saguinus leucopus. Orden: Primates. Familia: Callithrichidae) a un ambiente natural. Tesis de Pregrado, Universidad de Antioquia, Medellín
Goudet J (2003) Fstat (ver. 2.9. 4), a program to estimate and test population genetics parameters. http://www.unil.ch/izea/softwares/fstat. Html Updated from Goudet (1995)
Grant WS (2015) Problems and cautions with sequence mismatch analysis and Bayesian skyline plots to infer historical demography. J Hered 106:333–346. https://doi.org/10.1093/jhered/esv020
Heller R, Chikhi L, Siegismund HR (2013) The confounding effect of population structure on Bayesian skyline plot inferences of demographic history. PLoS One 8(5):e62992. https://doi.org/10.1371/journal.pone.0062992
Henao Díaz F, Stevenson P, Carretero-Pinzón X et al (2020) Atlas de la biodiversidad de Colombia: Primates. Instituto de Investigación de Recursos Biológicos Alexander von Humboldt, Bogota
Huck M, Löttker P, Böhle UR et al (2005) Paternity and kinship patterns in polyandrous moustached tamarins (Saguinus mystax). Am J Phys Anthropol 127:449–464. https://doi.org/10.1002/ajpa.20136
Huck M, Roos C, Heymann EW (2007) Spatio-genetic population structure in mustached tamarins, Saguinus mystax. Am J Phys Anthropol 132:576–583. https://doi.org/10.1002/ajpa.20559
Jombart T (2008) ADEGENET: an R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. https://doi.org/10.1093/bioinformatics/btn129
Kattan GH, Franco P, Rojas V et al (2004) Biological diversification in a complex region: a spatial analysis of faunistic diversity and biogeography of the Andes of Colombia. J Biogeogr 31:1829–1839. https://doi.org/10.1111/j.1365-2699.2004.01109.x
Kopelman NM, Mayzel J, Jakobsson M et al (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Resour 15:1179–1191. https://doi.org/10.1111/1755-0998.12387
Kumar A, Mhatre S, Godbole S et al (2019) Optimization of extraction of genomic DNA from archived dried blood spot (DBS): potential application in epidemiological research & bio banking. Gates Open Res 2:57. https://doi.org/10.12688/gatesopenres.12855.2
Leal A, Granados JL, Zerda E et al (2010) Liberación y seguimiento de dos grupos de tití gris (Saguinus leucopus) en el departamento de Tolima. Rev Med Vet Zoot 57:132–143. http://www.bdigital.unal.edu.co/21069/
Leigh JW, Bryant D (2015) PopART: full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116. https://doi.org/10.1111/2041-210X.12410
Li MH, Merilä J (2010) Extensive linkage disequilibrium in a wild bird population. Heredity 104(6):600–610. https://doi.org/10.1038/hdy.2009.150
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. https://doi.org/10.1093/bioinformatics/btp187
MADS (2012) Ministerio de Ambiente y Desarrollo Sostenible Estrategia Nacional para la prevención y control al Tráfico Ilegal de Especies Silvestres: Diagnóstico y Plan de Acción ajustado; Colombia. Ministerio de Ambiente y Desarrollo Sostenible, Bogota
Marshall AJ, Wich SA (2016) Why conserve primates. In: Wich SA, Marshall A (eds) An introduction to primate conservation. Oxford University Press, Oxford, pp 13–30
Matauschek C, Roos C, Heymann EW (2011) Mitochondrial phylogeny of tamarins (Saguinus, Hoffmannsegg 1807) with taxonomic and biogeographic implications for the S. nigricollis species group. Am J Phys Anthropol 144(4):564–574. https://doi.org/10.1002/ajpa.21445
Mello B, Vilela JF, Schrago CG (2018) Conservation phylogenetics and computational species delimitation of Neotropical primates. Biol Conserv 217:397–406. https://doi.org/10.1016/j.biocon.2017.11.017
Morales-Jiménez AL, Link A, Stevenson P (2008a) Saguinus leucopus. The IUCN red list of threatened species 2008: e.T19819A9019454. https://doi.org/10.2305/IUCN.UK.2008.RLTS.T19819A9019454.en. Accessed 14 Oct 2020
Morales-Jiménez AL, Vejarano S, Rodríguez CL et al (2008b) Programa Nacional para la Conservación de la Especie Endémica de Colombia tití gris (Saguinus leucopus). Ministerio de Ambiente. Vivienda y Desarrollo Territorial, Bogota
Mundy NI, Pissinatti A, Woodruff DS (2000) Multiple nuclear insertions of mitochondrial cytochrome b sequences in callitrichine primates. Mol Biol Evol 17:1075–1080. https://doi.org/10.1093/oxfordjournals.molbev.a026388
Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York
Nievergelt CM (1998) Microsatellite primers for genotyping common marmosets (Callithrix jacchus) and other callitrichids. Mol Ecol 7(10):1341–1349
Nikolic N, Chevalet C (2014) Detecting past changes of effective population size. Evol Appl 7(6):663–681. https://doi.org/10.1111/eva.12170
Nores M (2020) Avian diversity in humid tropical and subtropical south American forests, with a discussion about their related climatic and geological underpinnings. In: Rull V, Carnaval AC (eds) Neotropical diversification: patterns and processes. Springer, Cham, pp 145–188
Oklander LI, Caputo M, Solari A et al (2020) Genetic assignment of illegally trafficked neotropical primates and implications for reintroduction programs. Sci Rep 10(1):1–9. https://doi.org/10.1038/s41598-020-60569-3
Pacifici M, Santini L, Di Marco M et al (2013) Generation length for mammals. Nat Conserv 5:89–94. https://doi.org/10.3897/natureconservation.5.5734
Peakall ROD, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Resour 6:288–295. https://doi.org/10.1111/j.1471-8286.2005.01155.x
Perez-Sweeney BM, Valladares-Padua C, Martins CS et al (2008) Examination of the taxonomy and diversification of Leontopithecus using the mitochondrial control region. Int J Primatol 29:245–263. https://doi.org/10.1007/s10764-007-9224-7
Piry S, Luikart G, Cornuet JM (1999) Computer note. BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503. https://doi.org/10.1093/jhered/90.4.502
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Rambaut A, Drummond AJ (2009) Tracer v1. 5. http://beast.bio.ed.ac.uk.Tracer. Accessed Dec 2016
Rand DM (1996) Neutrality tests of molecular markers and the connection between DNA polymorphism, demography, and conservation biology. Biol Conserv 10:665–671
Rioux Paquette S (2011) PopGenKit: useful functions for (batch) file conversion and data resampling in microsatellite datasets. R package version 1.0
Rodríguez-Ramilo ST, Wang J (2012) The effect of close relatives on unsupervised Bayesian clustering algorithms in population genetic structure analysis. Ecol Res 12(5):873–884. https://doi.org/10.1111/j.1755-0998.2012.03156.x
Roncancio N, Acosta Castañeda A, García Loaiza LM et al (2013) Distribución potencial y disponibilidad de hábitat actual del tití gris (Saguinus leucopus): un primate endémico de Colombia y en peligro de extinción. In: Defler TR, Stevenson PR, Bueno ML et al (eds) Primates Colombianos en peligro de extinción. Asociación Primatológica Colombiana, Bogota, pp 213–230
Ross CN, French JA, Ortí G (2007) Germ-line chimerism and paternal care in marmosets (Callithrix kuhlii). Proc Natl Acad Sci U S A 104:6278–6282. https://doi.org/10.1073/pnas.0607426104
Ruiz-García M, Escobar-Armel P, Leguizamon N et al (2014) Genetic characterization and structure of the endemic Colombian silvery brown bare-face tamarin, Saguinus leucopus (Callitrichinae, Cebidae, Primates). Primates 55:415–435. https://doi.org/10.1007/s10329-014-0418-2
Rutkowski R, Zawadzka D, Suchecka E et al (2017) Conservation genetics of the capercaillie in Poland-delineation of conservation units. PLoS One 12(4):e0174901. https://doi.org/10.1371/journal.pone.0174901
Rylands AB, Mittermeier RA, Silva JS Jr (2012) Neotropical primates: taxonomy and recently described species and subspecies. Int Zoo Yearb 46(1):11–24. https://doi.org/10.1111/j.1748-1090.2011.00152.x
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, New York
Savage A, Causado J (2014) Saguinus oedipus. The IUCN red list of threatened species 2014:e.T19823A17930260. https://doi.org/10.2305/IUCN.UK.2014-3.RLTS.T19823A17930260.en. Accessed 8 Apr 2019
Savage A, Giraldo LH, Sblumer E et al (1993) Field techniques for monitoring cotton-top tamarins (Saguinus oedipus oedipus) in Colombia. Am J Primatol 31:189–196. https://doi.org/10.1002/ajp.1350310304
Silva MO, Armada JLA, Verona CES et al (2017) Cytogenetics and molecular genetic analysis of chimerism in marmosets (Callithrix: Primates). An Acad Bras Ciênc 89:2793–2804. https://doi.org/10.1590/0001-3765201720170484
Soares P, Ermini L, Thomson N et al (2009) Correcting for purifying selection: an improved human mitochondrial molecular clock. Am J Hum Genet 84(6):740–759. https://doi.org/10.1016/j.ajhg.2009.05.001
Soto-Calderón ID, Acevedo-Garcés YA, Álvarez-Cardona J et al (2016) Physiological and parasitological implications of living in a city: the case of the white-footed tamarin (Saguinus leucopus). Am J Primatol 78:1272–1281. https://doi.org/10.1002/ajp.22581
Soto-Calderón ID, Acevedo-Garcés YA, Restrepo-Agudelo T et al (2018) Phenotypic, genetic, and cytogenetic evidence of hybridization between species of trans-Andean tamarins (genus Saguinus). Int J Primatol 39:1022–1038. https://doi.org/10.1007/s10764-018-0044-8
Sun JX, Helgason A, Masson G et al (2012) A direct characterization of human mutation based on microsatellites. Nate Genet 44(10):1161–1165. https://doi.org/10.1038/ng.2398.
Sweeney CG, Curran E, Westmoreland SV et al (2012) Quantitative molecular assessment of chimerism across tissues in marmosets and tamarins. BMC Genomics 13(1):98
Tamura K, Stecher G, Peterson D et al (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729. https://doi.org/10.1093/molbev/mst197
Valencia Rodríguez LM (2018) Effects of anthropogenic habitat fragmentation on silvery brown tamarin (Saguinus leucopus) dispersal and movement patterns: landscape genetics, habitat connectivity and conservation implications. Dissertation, University of Texas, Austin. https://repositories.lib.utexas.edu/handle/2152/82284
Van Oosterhout C, Hutchinson WF, Wills DP et al (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538. https://doi.org/10.1111/j.1471-8286.2004.00684.x
Wang J (2011) COANCESTRY: a program for simulating, estimating and analysing relatedness and inbreeding coefficients. Mol Ecol Resour 11:141–145. https://doi.org/10.1111/j.1755-0998.2010.02885.x
Wang J (2017) Estimating pairwise relatedness in a small sample of individuals. Heredity 119(5):302–313. https://doi.org/10.1038/hdy.2017.52
Watsa M, Erkenswick G, Halloran D et al (2015) A field protocol for the capture and release of callitrichids. Neotrop Primates 22(2):59–68
Watterson GA (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7:256–276. https://doi.org/10.1016/0040-5809(75)90020-9
White T, van der Ende J, Nichols TE (2019) Beyond Bonferroni revisited: concerns over inflated false positive research findings in the fields of conservation genetics, biology, and medicine. Conserv Genet 20:927–937. https://doi.org/10.1007/s10592-019-01178-0
Yannic G, St-Laurent MH, Ortego J et al (2016) Integrating ecological and genetic structure to define management units for caribou in eastern Canada. Conserv Genet 17:437–453. https://doi.org/10.1007/s10592-015-0795-0
Acknowledgments
This research was funded by ISAGEN (grant No. 46/4208, 2012), CORPOCALDAS (agreement No. 241, 2015), Universidad CES—Área Metropolitana del Valle de Aburrá—Corantioquia alliance (agreements No. CV-1611-215 and No. CV-1612-217), Colciencias (doctoral scholarship 617-2, 2013), Wildlife Conservation Society, Ministerio de Ambiente y Desarrollo Sostenible (agreement 039, 2012), Cortolima (agreement 588, 2014), Empresas Públicas de Medellín (EPM) (agreement CT2017-001448), European Association of Zoos and Aquaria (EAZA), Fundación Santo Domingo, Fundación Proyecto Primates, the National Science Foundation of the US (Award No. BSC-1540270), the Margot Marsh Biodiversity Foundation, Primate Conservation, Inc., the Rufford Foundation, the Primate Society of Great Britain, the Conservation Leadership Program and the Schlumberger Faculty for the Future. We thank the Corporación Autónoma Regional de las Cuencas de los Ríos Negro y Nare (CORNARE) for access to the samples from San Luis and some samples from San Carlos. We would like to acknowledge Drs. Claudia Ceballos y Victor Hugo Merchan for their comments on earlier versions of this manuscript.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
1 Electronic Supplementary Material
Supplementary File 8.1
(PDF 923 kb)
Rights and permissions
Copyright information
© 2021 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Acevedo-Garcés, Y.A. et al. (2021). Current and Historical Genetic Structure of the White-Footed Tamarin (Saguinus leucopus). In: Nardelli, M., Túnez, J.I. (eds) Molecular Ecology and Conservation Genetics of Neotropical Mammals. Springer, Cham. https://doi.org/10.1007/978-3-030-65606-5_8
Download citation
DOI: https://doi.org/10.1007/978-3-030-65606-5_8
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-65605-8
Online ISBN: 978-3-030-65606-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)