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

Heredityvolume 121pages387400 (2018) | Download Citation

Abstract

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.

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Acknowledgements

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.).

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Author notes

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

Affiliations

  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

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The authors declare that they have no conflict of interest.

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

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https://doi.org/10.1038/s41437-018-0120-z