Skip to main content

Coat Color is not an Indicator of Subspecies Identity in Colombian Woolly Monkeys

  • Chapter
  • First Online:
The Woolly Monkey

Part of the book series: Developments in Primatology: Progress and Prospects ((DIPR,volume 39))

Abstract

Woolly monkeys are severely threatened, and disagreement on their taxonomic status complicates conservation strategies. Two subspecies of woolly monkeys inhabit Colombia, but the genetics of their populations have not been studied. Using mitochondrial DNA sequences, we set out to estimate the level of gene flow between populations, and to corroborate their taxonomic position. We found two separate evolving units with limited levels of gene flow. However, their separation does not correlate with the existing subspecies distinction, which is based on pelage color. We, therefore, propose a genetic differentiation of the woolly monkey taxa and emphasize the importance of the detected inconsistency in subspecies differentiation based on coat color.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Bandelt HJ, Foroster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    Article  CAS  PubMed  Google Scholar 

  • Becquet C, Przeworski M, Presgraves D (2009) Learning about modes of speciation by computational approaches. Evolution 63(10):2547–2562

    Article  PubMed  Google Scholar 

  • Botero S, Rengifo LY, Bueno ML et al (2010) How many species of woolly monkeys inhabit Colombian forests? Am J Primatol 72(12):1131–1140

    Article  PubMed  Google Scholar 

  • Boubli JP, Di Fiore A, Rylands AB et al. (2008) Lagothrix cana. In: IUCN. IUCN Red List of Threatened Species. Version 2013.1. www.iucnredlist.org. Downloaded on 31 July 2013

  • Collins AC, Dubach JM (2000) Phylogenetic relationships of spider monkeys (Ateles) based on mitochondrial DNA variation. Int J Primatol 21(3):381–420

    Article  Google Scholar 

  • Defler TR (2004) Woolly monkey. In: Rodriguez-Mahecha JV, Rylands A (eds) Primates of Colombia. Panamericana Formas e Impresos S. A. Conservation International, Bogotá, pp 352–368

    Google Scholar 

  • Di Fiore A, Fleischer R (2005) Social behavior, reproductive strategies, and population genetic structure of Lagothrix poeppigii. Int J Primatol 26(5):1137–1173

    Article  Google Scholar 

  • Di Fiore A, Rodman PS (2001) Time allocation patterns of lowland woolly monkeys (Lagothrix lagothricha poeppigii) in a neotropical terra firma forest. Int J Primatol 22(3):449–480

    Article  Google Scholar 

  • Etter A, McAlpine C, Phinn S et al. (2006) Unplanned land clearing of Colombian rainforests: Spreading like disease? Landsc Urb Plan 77(3):240–254

    Article  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    CAS  PubMed Central  Google Scholar 

  • Fooden J (1963) A revision of the woolly monkeys (genus Lagothrix). J Mammal 44(2):213–247

    Article  Google Scholar 

  • Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147(2):915–925

    CAS  PubMed Central  PubMed  Google Scholar 

  • Groves CP (2001) Primate taxonomy. Smithsonian Institution Press, Washington D.C.

    Google Scholar 

  • Guindon S, Gascuel O (2003) A Simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52(5):696–704

    Article  PubMed  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

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

    Google Scholar 

  • Hernández-Camacho J, Walschburger T, Ortiz R et al. (1992) Origen y distribución de la biota Suramericana y Colombiana. In: Halffter G (ed) La diversidad biológica de Iberoamérica, vol I. Acta Zoológica Mexicana, Xalapa, pp 55–104

    Google Scholar 

  • Hey J (2010) Isolation with migration models for more than two populations. Mol Biol Evol 27(4):905–920

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hey J, Nielsen R (2004) Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 167(2):747–760

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hey J, Nielsen R (2007) Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics. Proc Natl Acad Sci USA 104(8):2785–2790

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Holsinger KE, Weir BS (2009) Genetics in geographically structured populations: defining, estimating and interpreting Fst. Nat Rev Genet 10(9):639–650

    Article  CAS  PubMed  Google Scholar 

  • Kocher TD, Thomas WK, Meyer A et al (1989) Dynamics of mitochondrial DNA evolution in animals: Amplification and sequencing with conserved primers. Proc Natl Acad Sci USA 86:6196–6200

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP et al (2007) ClustalW and ClustalX version 2. Bioinformatics 23(21):2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Maldonado A, Botero S (2009) Possible evidence of male dispersal in common woolly monkeys (Lagothrix lagothricha). Neotrop Primates 16(2):76–78

    Article  Google Scholar 

  • Mantilla-Meluk H (2013) Subspecific variation: An alternative biogeographic hypothesis explaining variation in coat color and cranial morphology in Lagothrix lugens (Primates: Atelidae). Primate Conserv 26:33–48

    Article  Google Scholar 

  • Matthews LJ, Rosenberger AL (2008) Taxon combinations, parsimony analysis (PAUP*), and the taxonomy of the yellow-tailed woolly monkey, Lagothrix flavicauda. Am J Phys Anthropol 137(3):245–255

    Article  PubMed  Google Scholar 

  • Nielsen R, Wakeley J (2001) Distinguishing migration from isolation: a Markov chain Monte Carlo approach. Genetics 158(2):885–896

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nishimura A (1999) Estimation of the retention times and distances of seed dispersed by two monkey species, Alouatta seniculus and Lagothrix lagothricha, in a Colombian forest. Ecol Res 14(2):179–191

    Article  Google Scholar 

  • Nishimura A (2003) Reproductive parameters of wild female Lagothrix lagothricha. Int J Primatol 24(4):707–722

    Article  Google Scholar 

  • Palacios E, Boubli JP, Stevenson P et al. (2008) Lagothrix lagothricha. In: IUCN. IUCN Red List of Threatened Species. Version 2013.1. www.iucnredlist.org. Downloaded on 31 July 2013

  • Peres CA (1996) Use of Space, spatial group structure, and foraging group size of gray woolly monkeys (Lagothrix lagothricha cana) at Urucu, Brazil. In: Norconk MA, Rosenberger AL, Garber PA (eds) Adaptative radiations of neotropical primates. Plenum Press, New York, pp 467–488

    Chapter  Google Scholar 

  • Peres CA, Palacios E (2007) Basin-wide effects of game harvest on vertebrate population densities in Amazonian forests: Implications for animal-mediated seed dispersal. Biotropica 39(3):304–315

    Article  Google Scholar 

  • Pesole G, Gissi C, De Chirico A et al (1999) Nucleotide substitution rate of mammalian mitochondrial genomes. J Mol Evol 48(4):427–434

    Article  CAS  PubMed  Google Scholar 

  • Posada D (2008) jModelTest: Phylogenetic model averaging. Mol Biol Evol 25(7):1253–1256

    Article  CAS  PubMed  Google Scholar 

  • Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19(12):2092–2100

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Rozas J, Sanchez-DelBarrio JC, Messeguer X et al (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19(18):2496–2497

    Article  CAS  PubMed  Google Scholar 

  • Ruiz-Garcia M, Pinedo-Castro MO (2010) Molecular Systematics and Phylogeography of the Genus Lagothrix (Atelidae, Primates) by Means of the Mitochondrial COII Gene. Folia Primatol 81(3):109–128

    Article  PubMed  Google Scholar 

  • Shadel GS, Clayton DA (1997) Mitochondrial DNA maintenance in vertebrates. Annu Rev Biochem 66(1):409–435

    Article  CAS  PubMed  Google Scholar 

  • Shimodaira H, Hasegawa M (1999) Multiple comparisons of log-likelihoods with applications to phylogenetic Inference. Mol Biol Evol 16(8):1114–1116

    Article  CAS  Google Scholar 

  • Stevenson PR (2000) Seed dispersal by woolly monkeys (Lagothrix lagothricha) at Tinigua National Park, Colombia: Dispersal distance, germination rates, and dispersal quantity. Am Primatol 50:275–289

    Article  CAS  Google Scholar 

  • Stevenson PR (2007) Estimates of the number of seeds dispersed by a population of primates in a lowland forest in western Amazonia. In: Dennis AJ, Schupp EW, Green RJ, Westcott DW (eds) Seed dispersal: Theory and its application in a changing world. CAB International, Wallingford, pp 340–368

    Chapter  Google Scholar 

  • Stevenson PR, Link A (2008) Lagothrix lugens. In: IUCN 2013. IUCN Red List of Threatened Species. Version 2013.1. www.iucnredlist.org. Downloaded on 31 July 2013

  • Stevenson PR, Link A, Di Fiore A et al. (2008) Lagothrix poeppigii. In: IUCN. IUCN Red List of Threatened Species. Version 2013.1. www.iucnredlist.org. Downloaded on 31 July 2013

  • Swofford DL (2003) PAUP* Phylogenetic Analysis Using Parsimony (*and Other Methods) Version 4.04beta. Sinauer Associates, Sunderland, Massachusetts

    Google Scholar 

  • Wessel P, Smith WHF (1991) Free software helps map and display data. EOS Trans AGU 72(41):441–446

    Article  Google Scholar 

  • Whittaker DJ, Morales JC, Melnick DJ (2007) Resolution of the Hylobates phylogeny: Congruence of mitochondrial D-loop sequences with molecular, behavioral, and morphological data sets. Mol Phyl Evol 45(2):620–628

    Article  CAS  Google Scholar 

  • Zarate DA, Stevenson PR (2010) Primer estudio de estrategias ecologicas de monos churucos (Lagothrix lagothricha) en bosques fragmentados (Guaviare, Colombia). Universidad de los Andes, Bogotá

    Google Scholar 

Download references

Acknowledgments

The authors express their gratitude to Sebastian Gonzalez for his help with the geographical data processing, to Santiago Herrera for his critical comments on the study and manuscript, and to Diego Zarate for his help sampling the Guaviare population. The research was carried out with permission of the Colombian Ministerio de Ambiente, Vivienda y Desarrollo Territorial, given through Resolución 521 del 1 de abril de 2008, Resolución 751 del 13 de mayo de 2008, Resolución 803 del 16 de mayo de 2008, and Contrato de Acceso a Recursos Genéticos para Investigación Científica sin Interés Comercial No 17. This research was funded by Colciencias, Idea Wild, and Universidad de los Andes.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sergio Botero .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer New York

About this chapter

Cite this chapter

Botero, S., Stevenson, P. (2014). Coat Color is not an Indicator of Subspecies Identity in Colombian Woolly Monkeys. In: Defler, T., Stevenson, P. (eds) The Woolly Monkey. Developments in Primatology: Progress and Prospects, vol 39. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-0697-0_2

Download citation

Publish with us

Policies and ethics