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Genetic differentiation and diversity of the Bolivian endemic titi monkeys, Plecturocebus modestus and Plecturocebus olallae

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Abstract

The genetic variability of New World primates is still poorly documented. We present the first genetic study on two threatened endemic titi monkey species in northern Bolivia (Plecturocebus modestus and Plecturocebus olallae) using six microsatellite markers to investigate genetic structure and variability of 54 individuals from two wild populations. A low level of genetic diversity was found (34 alleles in the total sampled population). Locus 1118 presented the greatest number of alleles. The mean number of alleles per locus in the total population was 5.6 and the average heterozygosity was 0.38 (range 0.12–0.88). The FIS value for the total population using all microsatellite loci shows a statistically significant heterozygote deficit. The inbreeding coefficients (FIS) were positive and significantly different from zero (0.064 for P. olallae and 0.213 for P. modestus). The genetic differentiation between populations (FST) was moderate with a pair-wise FST estimate of 0.14. Population structure analyses assigned the two populations to two differentiated clusters (K = 2). These results suggest that these two species with very close distributional ranges arose from a single population, and that they remain in a process of genetic differentiation and speciation. This study further underlines the urgent need for conservation actions for both endemic primate species.

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References

  • Alcantarino ML, Costa GE, Silva A, Ferrari FF, Cruz Schneider MP (2009) Genetic diversity of red-bellied titis (Callicebus moloch) from Eastern Amazonia based on microsatellite markers. Biochem Genet 47:235–240

    Article  Google Scholar 

  • Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge

    Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2004) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Montpellier, France: Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II

  • Bicca-Marques JC, Heymann EW (2013) Ecology and behavior of titi monkeys (genus Callicebus). In: Veiga LM, Barnett AA, Ferrari SF, Norconk MA (eds) Evolutionary Biology and Conservation of Titis, Sakis and Uacaris. Cambridge University Press, Cambridge, pp 196–207

  • Byrne H, Rylands AB, Carneiro JC, Lynch-Alfaro JW, Bertuol F, Da Silva MNF, Messias M, Groves CP, Mittermeier RA, Farias I, Hrbek T, Schneider H, Sampaio I, Boubli JP (2016) Phylogenetic relationships of the New World titi monkeys (Callicebus): first appraisal of taxonomy based on molecular evidence. Front Zool. https://doi.org/10.1186/s12983-016-0142-4

    Article  PubMed  PubMed Central  Google Scholar 

  • Byrne H, Lynch Alfaro JW, Sampaio I, Farias I, Schneider H, Hrbek T, Boubli JP (2018) Titi monkey biogeography: parallel Pleistocene spread by Plecturocebus and Cheracebus into a post- Pebas Western Amazon. Zool Scr 2018:1–19

    Google Scholar 

  • Chikhi L, Goznes B, Treanor A, Bruford MW (2004) Population genetic, structure and inbreeding in an insular cattle breed, the jersey, and its implications for genetic resource management. Heredity 92:396–401

    Article  CAS  PubMed  Google Scholar 

  • Daltoé A (2006) Caracterização genética de Alouatta caraya (Primates, Atelidae) utilizando marcadores heterólogos do tipo microssatélites. Programas de Pósgraduação em Biología Animal. Universidade de Brasilia, Brazil

  • Di Fiore A, Fleischer RC (2004) Microsatellite markers for woolly monkeys (Lagothrix lagotricha) and their amplification in other New World primates (Primates: Platyrrhini). Mol Ecol Notes 4:246–249

    Article  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Eguiarte LE (1990) Genética de poblaciones de Astrocaryum mexicanum Liebm. en Los Tuxtlas, Veracruz. Tesis de doctorado, Centro de Ecología, Universidad Nacional Autónoma de México

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

    Article  CAS  PubMed  Google Scholar 

  • Felton A, Felton AM, Wallace RB, Gomez H (2006) Identification, distribution and behavioural observations of the titi monkeys Callicebus modestus Lönnberg 1939, and Callicebus olallae Lönnberg 1939. Primate Conserv 20:41–46

    Article  Google Scholar 

  • García del Valle Y, Estrada, A, Espinoza E, Lorenzo C, Naranjo E (2005) Genética de poblaciones de monos aulladores (Alouatta pigra) en hábitat continuo y fragmentado en la selva lacandona, México: Un estudio preliminar. Universidad y Ciencia, Num Esp II, pp 55–60. ISSN: 0186-2979. http://www.redalyc.org/articulo.oa?id=15421206

  • Gilpin ME, Soulé ME (1986) Minimum viable populations: processes of species extinction. In: Soulé ME (ed) Conservation biology: the science of scarcity and diversity. Sinauer, Sunderland, pp 19–34

    Google Scholar 

  • Groom MJ (2006) Threats to biodiversity. In: Groom MJ, Meffe GK, Carroll CR (eds) Principles of conservation biology. Sinauer Associates inc., Sunderland, pp 63–109

    Google Scholar 

  • Hershkovitz P (1990) Titis, New World monkeys of the genus Callicebus (Cebidae, Platyrrhini): a preliminary taxonomic review. Fieldiana Zool NS 55:1–109

    Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kinzey WG (1981) The titi monkeys, genus Callicebus. In: Coimbra-Filho AF, Mittermeier RA (eds) Ecology and Behavior of Neotropical Primates, Vol 1. Academia Brasileira de Ciencias, Rio de Janeiro, pp 240–276

  • Kobayashi S (1995) A phylogenetic study of titi monkeys, genus Callicebus, based on cranial measurements: i. Phyletic groups of Callicebus. Primates 36:101–120

    Article  Google Scholar 

  • Lacy RC (1987) Loss of genetic diversity from managed populations: interacting effects of drift, mutation, immigration, selection, and population subdivision. Conserv Biol 1:143–158

    Article  Google Scholar 

  • Lönnberg E (1939) Notes on some members of the genus Callicebus. Arkiv Für Zoologi 31(13):1–18

    Google Scholar 

  • López-Strauss H, Wallace RB (2015) Density estimates of two Bolivian primate endemics, Callicebus olallae and C. modestus. Mastozool Neotrop 22:23–34

    Google Scholar 

  • Martinez J, Wallace RB (2007) Further notes on the distribution of the Bolivian endemic titi monkeys, Callicebus modestus and Callicebus olallae. Neotrop Primates 14:47–54

    Article  Google Scholar 

  • Martinez J, Wallace RB (2013) New information about the distribution of Callicebus in Bolivia. Ecología en Bolivia 48:57–62

    Google Scholar 

  • Martinez J, Wallace RB (2016) Plecturocebus olallae. In: Rowe N, Myers M (eds) All the World’s Primates. Pogonias Press Inc, Charlestown, p 201

    Google Scholar 

  • Martinez J, Wallace RB, Lopez-Strauss H, De La Torre P, Aranibar H (2013) Two new specimens for the Bolivian endemic titi monkeys, Callicebus olallae and Callicebus modestus. Neotrop Primates 20:39–44

    Article  Google Scholar 

  • Martínez J, Wallace RB (2010) Pitheciidae. In: Wallace RB, Gómez H, Porcel ZR, Rumiz DI (eds) Distribución, Ecología y Conservación de los Mamíferos Medianos y Grandes de Bolivia. Editorial: Centro de Ecología Difusión Simón I. Patiño, Santa Cruz de la Sierra, pp 305–330

    Google Scholar 

  • Muniz L, Vigilant L (2008) Isolation and characterization of microsatellite markers in the white-faced capuchin monkey (Cebus capucinus) and cross species amplification in other New World monkeys. Mol Ecol Resour 8:402–405

    Article  CAS  PubMed  Google Scholar 

  • Nei M (1972) Genetic distance between populations. Am Nat 106(949):283–292

    Article  Google Scholar 

  • Onderdonk DA, Chapman CA (2000) Copying with forest fragmentation: the primates of Kibale National Park, Uganda. Int J Primatol 21:587–611

    Article  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Raymond ML, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283

    Article  PubMed  Google Scholar 

  • Ruíz-García M, Castillo MI, Álvarez D, Gardeazabal J, Borrero LM, Ramírez DM, Carrillo L, Nassar F, Gálvez H (2007) Estudio de 14 especies de primates platirrinos (Cebus, Saimiri, Aotus, Saguinus, Lagothrix, Alouatta y Ateles), utilizando 10 loci microsatélites: análisis de la diversidad génica y de la detección de cuellos de botella con propósitos conservacionistas. Orinoquia 11(2):19–37

    Google Scholar 

  • Van Roosmalen MGM, Van Roosmalen T, Mittermeier RA (2002) A taxonomic review of the titi monkeys, genus Callicebus Thomas, 1903, with the descriptions of two new species, Callicebus bernhardi and Callicebus stephennashi, from Brazilian Amazonia. Neotrop Primates 10:1–52

    Google Scholar 

  • Veiga LM, Wallace RB, Martinez J (2008) Callicebus modestus. The IUCN Red list of threatened species, p e.T41550A10498144. http://dx.doi.org/10.2305/IUCN.UK.2008.RLTS.T41550A10498144.en. Downloaded on 28 September 2016

  • Veiga LM, Wallace RB, Martinez J (2008) Callicebus olallae. The IUCN Red list of threatened species, p e.T3554A9939925. http://dx.doi.org/10.2305/IUCN.UK.2008.RLTS.T3554A9939925.en. Downloaded on 28 September 2016

  • Wallace RB, Martinez J, Lopez-Strauss H, Barreta J, Reinaga A, Lopez L (2013) Conservation challenges facing two threatened endemic titi monkeys (Callicebus modestus & C. olallae) in a naturally fragmented Bolivian forest. In: Marsh LK (ed) Primate in fragments: complexity and resilience. Developments in primatology: progress and prospects. Springer Science + Business Media, New York, pp 493–501

    Google Scholar 

  • Weir BS, Cockerham C (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    CAS  PubMed  Google Scholar 

  • Woodward SR, King MJ, Chiu NM, Kuchar MJ, Griggs CW (1994) Amplification ancient nuclear DNA from teeth and soft tissues. PCR Methods Appl 13:224–244

    Google Scholar 

Download references

Acknowledgements

We thank the Wildlife Conservation Society, Gordon and Betty Moore Foundation, Primate Conservation Inc., Margot Marsh Biodiversity Foundation, BP Conservation Leadership Program, and Conservation International Primate Action Fund for financial support for conservation research efforts on the Bolivian Plecturocebus endemics. We thank our field assistant Hector Cáceres, and also Lesly Lopez who helped in data collection. We thank the National Directorate for the Protection of Biodiversity for help in acquiring necessary research permits, as well as the collaboration of the Municipalities of Reyes, San Borja, and Santa Rosa del Yacuma, and the Nogales cattle ranches for access to the study sites. We acknowledge the support of the Institute of Biology Molecular and Biotechnology (Universidad Mayor de San Andres) in La Paz.

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  1. Instituto de Biología Molecular y Biotecnología, Universidad Mayor de San Andrés, UMSA, Cota Cota Calle 27 s/n, La Paz, Bolivia

    Julia Barreta Pinto, Yahaira Bernal & Rolando Sánchez

  2. Wildlife Conservation Society (WCS), Greater Madidi-Tambopata Landscape Conservation Program, Casilla 3-35181, San Miguel, La Paz, Bolivia

    Jesús Martinez & Robert Wallace

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  1. Julia Barreta Pinto
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Correspondence to Julia Barreta Pinto.

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Barreta Pinto, J., Martinez, J., Bernal, Y. et al. Genetic differentiation and diversity of the Bolivian endemic titi monkeys, Plecturocebus modestus and Plecturocebus olallae. Primates 60, 565–573 (2019). https://doi.org/10.1007/s10329-019-00750-z

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