Article | Published:

Comparing genetic diversity and demographic history in co-distributed wild South American camelids

Heredityvolume 121pages387400 (2018) | Download Citation


Vicuñas and guanacos are two species of wild South American camelids that are key ruminants in the ecosystems where they occur. Although closely related, these species feature differing ecologies and life history characters, which are expected to influence both their genetic diversity and population differentiation at different spatial scales. Here, using mitochondrial and microsatellite genetic markers, we show that vicuña display lower genetic diversity within populations than guanaco but exhibit more structure across their Peruvian range, which may reflect a combination of natural genetic differentiation linked to geographic isolation and recent anthropogenic population declines. Coalescent-based demographic analyses indicate that both species have passed through a strong bottleneck, reducing their effective population sizes from over 20,000 to less than 1000 individuals. For vicuña, this bottleneck is inferred to have taken place ~3300 years ago, but to have occurred more recently for guanaco at ~2000 years ago. These inferred dates are considerably later than the onset of domestication (when the alpaca was domesticated from the vicuña while the llama was domesticated from the guanaco), coinciding instead with a major human population expansion following the mid-Holocene cold period. As importantly, they imply earlier declines than the well-documented Spanish conquest, where major mass mortality events were recorded for Andean human and camelid populations. We argue that underlying species’ differences and recent demographic perturbations have influenced genetic diversity in modern vicuña and guanaco populations, and these processes should be carefully evaluated in the development and implementation of management strategies for these important genetic resources.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.


  1. Aldenderfer M (1999) The Pleistocene/Holocene transition in Peru and its effects upon human use of the landscape. Quat Int 53–54:11–19

  2. Ammann C, Jenny B, Kammer K, Messerli B (2001) Late quaternary glacier response to humidity changes in the arid Andes of Chile (18–29°S). Palaeogeogr Palaeoclimatol Palaeoecol 172:313–326

  3. Anello M, Daverio MS, Romero SR, Rigalt F, Silbestro MB, Vidal-Rioja L et al (2016) Genetic diversity and conservation status of managed vicuna (Vicugna vicugna) populations in Argentina. Genetica 144(1):85–97

  4. Baldi R, Acebedes P, Cuéllar E, Funes M, Hoces D, Puig S et al (2016) Lama guanicoe. The IUCN Red List of Threatened Species. e.T11186A18540211.ISSN 2307-8235

  5. Barnosky A, Lindsey E (2010) Timing of Quaternary megafaunal extinction in South America in relation to human arrival and climate change. Quat Int 217:10–29

  6. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (1996) Laboratoire génome, populations, interactions, CNRS UMR 5000. Université de Montpellier II, Montpellier, 2004

  7. Benjamin Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29:1165–1188

  8. Brack A (1980) Conservación de la vicuña en el Peru. Fondo Editorial del Ministerio de Agricultura y Alimentacion, Lima, (Peru), 33pp.

  9. Bruford M, Hanotte O, Burke T (1998) Multi- and single locus DNA fingerprinting. IRL Press, Oxford

  10. Bustamante A, Zambelli A, De Lamo D, von Thungen J, Vidal-Rioja A (2002) Genetic variability of guanaco and llama populations in Argentina. Small Rumin Res 47:97–101

  11. Chikhi L, Sousa VC, Luisi P, Goossens B, Beaumont MA (2010) The confounding effects of population structure, genetic diversity and the sampling scheme on the detection and quantification of population size changes. Genetics 186(3):983–995

  12. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9(10):1657–1659

  13. Dieringer D, Schlötterer C (2003) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 3:167–169

  14. Dillehay TD (2009) Probing deeper into first American studies. Proc Natl Acad Sci USA 106(4):971–978

  15. Dodd C, Rodriguez J, Hoces D, Rosadio R, Wheeler J, Bruford M (2006) Genetic diversity and management implications for vicuña populations in Peru. In: Gerkin M, Renieri C (eds) South American Camelid Research, Vol 1. Wageningen Academic Publishers, Wageningen, p 87–96

  16. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14(8):2611–2620

  17. 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

  18. Frankin W (1983) Contrasting socioecologies of South America’s wild camelids: the vicuña and the guanaco. In: Eisenberg J, Kleiman D (eds) Advances in the study of animal behaviour, American Society of Mammalogists, Allen Press, Lawrence, Kansas, USA. pp 573–629.

  19. Goldberg A, Mychajliw AM, Hadly EA (2016) Post-invasion demography of prehistoric humans in South America. Nature 532(7598):232–235

  20. Gonzalez BA, Orozco-Terwengel P, von Borries R, Johnson WE, Franklin WL, Marín JC (2014) Maintenance of genetic diversity in an introduced island population of guanacos after seven decades and two severe demographic bottlenecks: implications for camelid conservation. PLoS ONE 9(3):e91714

  21. Goossens B, Chikhi L, Jalil MF, Ancrenaz M, Lackman-Ancrenaz I, Mohamed M et al. (2005) Patterns of genetic diversity and migration in increasingly fragmented and declining orang-utan (Pongo pygmaeus) populations from Sabah, Malaysia. Mol Ecol 14(2):441–456

  22. Grimwood I (1969) Notes on the distribution and status of some Peruvian mammals. American Committee for Wildlife Protection. Zoological Society Special Publication, New York, Vol 21

  23. Hamilton G, Stoneking M, Excoffier L (2005) Molecular analysis reveals tighter social regulation of immigration in patrilocal populations than in matrilocal populations. Proc Natl Acad Sci USA 102(21):7476–7480

  24. Hoces D (2005) Guanaco: el camélido injustamente olvidado. Rev Agric 300:140–143

  25. Hutter CM, Schug MD, Aquadro CF (1998) Microsatellite variation in Drosophila melanogaster and Drosophila simulans: a reciprocal test of the ascertainment bias hypothesis. Mol Biol Evol 15(12):1620–1636

  26. INEI (2013) Resultados difinitivos: IV censo nacional agropecuario 2012.

  27. IUCN (2010) The IUCN red list of threatened species.

  28. Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23(14):1801–1806

  29. Kadwell M, Fernandez M, Stanley HF, Baldi R, Wheeler JC, Rosadio R et al. (2001) Genetic analysis reveals the wild ancestors of the llama and the alpaca. Proc Biol Sci 268(1485):2575–2584

  30. Kuentz A, Ledlru M, Thouret J (2011) Environmental changes in the highlands of the western Andean Cordillera, southern Peru, during the Holocene. Holocene 22(11):1215–1226

  31. Kuhner MK, Yamato J, Felsenstein J (1998) Maximum likelihood estimation of population growth rates based on the coalescent. Genetics 149(1):429–434

  32. Kunkel K, Atwood T, Ruth T, Pletscher D, Hornocker M (2013) Assessing wolves and cougars as conservation surrogates. Anim Conserv 16:32–40

  33. Lang K, Wang Y, Plante Y (1996) Fifteen polymorphic dinucleotide microsatellites in llamas and alpacas. Anim Genet 27:293

  34. Lessa EP, Cook JA, Patton JL (2003) Genetic footprints of demographic expansion in North America, but not Amazonia, during the Late Quaternary. Proc Natl Acad Sci USA 100(18):10331–10334

  35. Lichtenstein G, Baldi R, Villalba L, Hoces D, Baigún R, Laker J (2008) Vicugna vicugna. The IUCN Red List of Threatened Species. e.T22956A9402796.ISSN 2307-8235

  36. Marín JC (2004) Filogenia molecular, filogeografía y domesticación de camelidos sudamericanos (ARTIODACTYLA: CAMELIDAE). PhD thesis, Universidad de Chile, Santiago.

  37. Marín JC, Casey CS, Kadwell M, Yaya K, Hoces D, Olazabal J et al. (2007) Mitochondrial phylogeography and demographic history of the vicuna: implications for conservation. Hered (Edinb) 99(1):70–80

  38. Marín JC, Gonzalez BA, Poulin E, Casey CS, Johnson WE (2013) The influence of the arid Andean high plateau on the phylogeography and population genetics of guanaco (Lama guanicoe) in South America. Mol Ecol 22(2):463–482

  39. Marín JC, Spotorno A, Gonzalez B, Bonacic C, Wheeler J, Casey C et al. (2008) Mitochondrial DNA variation and systematics of the guanaco (Lama guanicoe: Artiodactyla: Camelidae). J Mammal 89:269–281

  40. Metcalf JL, Turney C, Barnett R, Martin F, Bray SC, Vilstrup JT et al. (2016) Synergistic roles of climate warming and human occupation in Patagonian megafaunal extinctions during the Last Deglaciation. Sci Adv 2(6):e1501682

  41. Narum S (2006) Beyond Bonferroni: Less conservative analyses for conservation genetics. Conserv Genet 7:783–787

  42. Nichols R, Beaumont M (1996) Is it ancient or modern history that we can read in the genes? In: Hochberg M, Clobert J, Barbault R (eds) Apects of the genesis and maintenance of biological diversity. Oxford University Press, Oxford

  43. Park S (2001) Trypanotolerance in West African cattle and the population genetic effects of selection. PhD thesis, University of Dublin

  44. Penedo M, Caetano A, Cordova K (1998) Microsatellite markers for South American camelids. Anim Genet 29:411–412

  45. Peter BM, Wegmann D, Excoffier L (2010) Distinguishing between population bottleneck and population subdivision by a Bayesian model choice procedure. Mol Ecol 19(21):4648–4660

  46. Plummer M, Best N, Cowles K, Vines K (2006) Coda: output analysis and diagnostic for MCMC. R News 6:7–11

  47. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959

  48. R Development Core Team (2009) R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria

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

  50. Romiguier J, Gayral P, Ballenghien M, Bernard A, Cahais V, Chenuil A et al. (2014) Comparative population genomics in animals uncovers the determinants of genetic diversity. Nature 515(7526):261–263

  51. Rosenberg N (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138

  52. Ross KG (2001) Molecular ecology of social behaviour: analyses of breeding systems and genetic structure. Mol Ecol 10(2):265–284

  53. Rousset F (2008) genepop'007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8(1):103–106

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

  55. Sarno R, Franklin W, O’Brien S, Johnson W (2001) Patterns of mtDNA and microsatellite variation in an island and mainland population of guanacos in southern Chile. Anim Conserv 4:93–101

  56. Sarno RJ, David VA, Franklin WL, O’Brien SJ, Johnson WE (2000) Development of microsatellite markers in the guanaco, Lama guanicoe: utility for South American camelids. Mol Ecol 9(11):1922–1924

  57. Shockey B, Salas-Gismondi R, Baby P, Guyot J, Baltazar M, Huaman L et al. (2009) New Pleistocene Cave Faunas of the Andes of Central Peru: radiocarbon ages and the survival of low latitude, Pleistocene DNA. Palaeontol Electron 12:15A

  58. Storz JF, Beaumont MA (2002) Testing for genetic evidence of population expansion and contraction: an empirical analysis of microsatellite DNA variation using a hierarchical Bayesian model. Evolution 56(1):154–166

  59. Taberlet P, Griffin S, Goossens B, Questiau S, Manceau V, Escaravage N et al. (1996) Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acid Res 24:3189–3194

  60. Thompson LG, Mosley-Thompson E, Brecher H, Davis M, Leon B, Les D et al. (2006) Abrupt tropical climate change: past and present. Proc Natl Acad Sci USA 103(28):10536–10543

  61. van Oosterhout C, Hutchinson W, Willis D, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

  62. Watterson G (1975) On the number of segregating sites. Theor Popul Biol 7:256–276

  63. Weeks AR, Stoklosa J, Hoffmann AA (2016) Conservation of genetic uniqueness of populations may increase extinction likelihood of endangered species: the case of Australian mammals. Front Zool 13:31

  64. Wheeler J (1995) Evolution and present situation of the South American camelidae. Biol J Linn Soc 54:271–295

  65. Wheeler J (2012a) South American camelids – past, present and future. J Camelid Sci 5:1–24

  66. Wheeler J, Hoces D, Bruford M (2006) Actas IV Congreso Mundial sobre Camélidos. In: Miragaya M, Olivera D, Puig S (eds). Fundación biodiversidad, FIDA, CFI, Fundación Biodiversidad. Catamarca (Argentina), pp 76

  67. Wheeler J, Pires-Ferreira E, Kaulicke P (1976) Preceramic animal utilization in the Central Peruvian Andes. Science 194:483–490

  68. Wheeler JC (2012b) South American camelids - past, present and future. J Camelid Sci 5:1–24

  69. Wheeler JC, Russel AJF, Redden H (1995) Llamas and Alpacas: pre-conquest breeds and post-conquest hybrids. J Archaelogical Sci 22:833–840

  70. Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163(3):1177–1191

Download references


Darwin Initiative for the Survival of Species (UK) grants 162/06/126 and 162/12/022; Asociación Ancash (Peru); European Commission INCO-DC ICA4-2000-10229—MACS; FINCyT (Peru) grant 006-FINCyT-PIBAP-2007; COLP (Peru) grants PLNG-EV-9832, PLNG-EV-09012; CONICYT PhD studentship, and FONDECYT (Chile) grants 1140785 and 3050046. Peruvian samples were collected under permits from CONACS (28 Sept. 1994, 15 June 1997), INRENA (011-c/c-2004-INRENA-IANP; 012-c/c-2004-INRENA-IANP; 016-c/c-2004-INRENA-IFFS-DCB; 016-c/c-2004-INRENA-IFFS-DCB; 021-c/c-2004-INRENA-IFFS-DCB; 026-c/c-2005-INRENA-IANP) and DGFFS (109-2009-AG-DGFFS-DGEFFS). Chilean samples were collected under the permit 447 of the Servicio Agricola y Ganadero SAG, and permit 6/02/2002 of the Corporación Nacional Forestal (CONAF). Peruvian samples were exported to the UK under CITES permit numbers 00658, 6282, 4222, 6007, 5971, 0005177, 0005178, 023355, 022967 and 022920 and import permit numbers 269602/01 and 262547/02. Chilean samples were exported to the UK under CITES permit numbers 0007 and 0005176 and import permit numbers 269658/01 and 262547/02. The authors would like to thank the anonymous reviewers that contributed to improve our manuscript.

Author contributions

Authors contributed the following to this manuscript: project leaders (M.W.B., J.C.W. and R.R.), fieldwork (M.K., M.F., J.C.M. and D.H.), laboratory work (C.S.C., M.K., M.F., J.C.M. and L.M.), data analysis (P.O-.T.W., C.S.C., Y.H., J.C.M. and M.W.B.), produced the manuscript (P.O.T.W., C.S.C., J.C.W., and M.W.B.).

Author information

Author notes

  1. These authors contributed equally: C.S. Casey, P. Orozco-terWengel


  1. School of Biosciences, Cardiff University, Cathays Park, Cardiff, CF10 3AX, UK

    • C. S. Casey
    • , P. Orozco-terWengel
    •  & M. W. Bruford
  2. School of Life Sciences, University of Lincoln, Riseholme Park, Lincoln, LN2 2LG, UK

    • C. S. Casey
  3. CONOPA, Instituto de Investigación y Desarrollo de Camélidos Sudamericanos, Avenida Reusche Mz. M Lt. 4, Pachacamac, Lima 19, Peru

    • K. Yaya
    • , M. Fernández
    • , R. Rosadio
    • , L. Maturrano
    • , D. Hoces
    • , J. C. Wheeler
    •  & M. W. Bruford
  4. Institute of Zoology, Zoological Society of London, Regent’s Park, London, NW1 4RY, UK

    • M. Kadwell
  5. Departamento de Ciencias Básicas, Facultad de Ciencias, Universidad del Bío - Bío, Casilla 447, Chillan, Chile

    • J. C. Marín
  6. Facultad de Medicina Veterinaria, Universidad Nacional Mayor de San Marcos, Lima, Peru

    • R. Rosadio
    •  & L. Maturrano
  7. Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, 1-5 Beichen West Road, 100101, Beijing, China

    • Y. Hu


  1. Search for C. S. Casey in:

  2. Search for P. Orozco-terWengel in:

  3. Search for K. Yaya in:

  4. Search for M. Kadwell in:

  5. Search for M. Fernández in:

  6. Search for J. C. Marín in:

  7. Search for R. Rosadio in:

  8. Search for L. Maturrano in:

  9. Search for D. Hoces in:

  10. Search for Y. Hu in:

  11. Search for J. C. Wheeler in:

  12. Search for M. W. Bruford in:

Conflict of interest

The authors declare that they have no conflict of interest.

Corresponding authors

Correspondence to J. C. Wheeler or M. W. Bruford.

Electronic supplementary material

About this article

Publication history





Issue Date


Further reading