Conservation Genetics

, Volume 12, Issue 1, pp 119–128 | Cite as

Past bottlenecks and current population fragmentation of endangered huemul deer (Hippocamelus bisulcus): implications for preservation of genetic diversity

  • Paulo Corti
  • Aaron B. A. Shafer
  • David W. Coltman
  • Marco Festa-Bianchet
Research Article

Abstract

Small populations in fragmented habitats can lose genetic variation through drift and inbreeding. The huemul (Hippocamelus bisulcus) is an endangered deer endemic to the southern Andes of Chile and Argentina. Huemul numbers have declined by 99% and its distribution by 50% since European settlement. The total population is estimated at less than 2,000 individuals and is highly fragmented. At one isolated population in Chilean Patagonia we sampled 56 individuals between 2005 and 2007 and genotyped them at 14 microsatellite loci. Despite low genetic variability (average 2.071 alleles/locus and average HO of 0.341), a low inbreeding coefficient (FIS) of 0.009 suggests nearly random mating. Population genetic bottleneck tests suggest both historical and contemporary reductions in population size. Simulations indicated that the population must be maintained at 75% of the current size of 120 individuals to maintain 90% of its current genetic diversity over the next 100 years. Potential management strategies to maintain genetic variability and limit future inbreeding include the conservation and establishment of habitat corridors to facilitate gene flow and the enlargement of protected areas to increase effective population size.

Keywords

Huemul deer Hippocamelus bisulcus Genetic variability Inbreeding Endangered Ungulate 

References

  1. Anderson JD, Honeycutt RL, Gonzales RA, Gee KL, Skow LC, Gallagher RL, Honeycutt DA, DeYoung RW (2002) Development of microsatellite DNA markers for the automated genetic characterization of white-tailed deer populations. J Wildl Manag 66:67–74CrossRefGoogle Scholar
  2. Banks SC, Piggott MP, Stow AJ, Taylor AC (2007) Sex and sociality in a disconnected world: a review of the impacts of habitat fragmentation on animal social interactions. Can J Zool 85:1065–1079CrossRefGoogle Scholar
  3. Barendse W, Armitage SM, Kossarek LM et al (1994) A genetic-linkage map of the bovine genome. Nat Genet 6:227–235CrossRefPubMedGoogle Scholar
  4. Bishop MD, Kappes SM, Keele JW, Stone RT, Sunden SLF, Hawkins GA, Toldo SS, Fries R, Grosz MD, Yoo JY, Beattie CW (1994) A genetic-linkage map for cattle. Genetics 136:619–639PubMedGoogle Scholar
  5. Brashares JS, Arcese P, Sam MK (2001) Human demography and reserve size predict wildlife extinction in West Africa. Proc R Soc Lond B Biol Sci 268:2473–2478CrossRefGoogle Scholar
  6. Brezinsky L, Kemp SJ, Teale AJ (1993) 5 Polymorphic bovine microsatellites (Ilsts010-014). Anim Genet 24:75–76CrossRefPubMedGoogle Scholar
  7. Buchanan FC, Crawford AM (1993) Ovine microsatellites at the OarFCB11, OarFCB128, OarFCB193, OarFCB266 and OarFCB304 loci. Anim Genet 24:145CrossRefPubMedGoogle Scholar
  8. Cabrera A, Yepes J (1960) Mamíferos sudamericanos, 2nd edn. Edian, Buenos AiresGoogle Scholar
  9. Caro TM, Laurenson MK (1994) Ecological and genetic factors in conservation: a cautionary tale. Science 263:485–486CrossRefPubMedGoogle Scholar
  10. Caughley G (1994) Directions in conservation biology. J Anim Ecol 63:215–244CrossRefGoogle Scholar
  11. Caughley G, Gunn A (1996) Conservation biology in theory and practice. Blackwell Science, CambridgeGoogle Scholar
  12. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedGoogle Scholar
  13. Corti P (2008) Organisation sociale, dynamique de population, et conservation du cerf huemul (Hippocamelus bisulcus) dans la Patagonie du Chili. Département de biologie, Université de Sherbrooke, Sherbrooke, p xv+143Google Scholar
  14. Corti P, Wittmer HU, Festa-Bianchet M (in press) Dynamics of a small population of endangered huemul deer (Hippocamelus bisulcus) in Chilean Patagonia. J MammGoogle Scholar
  15. Cosse M, Gonzalez S, Maldonado JE (2007) Cross amplification tests of ungulate primers in the endangered neotropical pampas deer (Ozotoceros bezoarticus). Genet Mol Res 6:1118–1122PubMedGoogle Scholar
  16. Couvet D (2002) Deleterious effects of restricted gene flow in fragmented populations. Conserv Biol 16:276–369CrossRefGoogle Scholar
  17. Crawford AM, Dodds KG, Ede AJ et al (1995) An autosomal genetic-linkage map of the sheep genome. Genetics 140:703–724PubMedGoogle Scholar
  18. Dewoody JA, Honeycutt RL, Skow LC (1995) Microsatellite markers in white-tailed deer. J Hered 86:317–319PubMedGoogle Scholar
  19. Diaz NI, Smith-Flueck JAM (2000) El huemul patagónico: un misterioso cérvido al borde de la extinción. L.O.L.A. (Literature of Latin America), Buenos AiresGoogle Scholar
  20. Donoso PJ, Otero LA (2005) Towards a definition of a forest country: where is Chile located? Bosque 26:5–18Google Scholar
  21. Dudash M, Fenster C (2000) Inbreeding and outbreeding depression in fragmented populations. In: Young AG, Clarke GM (eds) Genetics, demography and viability of fragmented populations. Cambridge University Press, New York, pp 35–53CrossRefGoogle Scholar
  22. Estoup A, Angers B (1998) Microsatellites and minisatellites for molecular ecology: theoretical and empirical considerations. In: Carvalho G (ed) Advances in molecular ecology. IOS Press, Amsterdam, pp 55–86Google Scholar
  23. Fahrig L (2002) Effect of habitat fragmentation on the extinction threshold: a synthesis. Ecol Appl 12:346–353Google Scholar
  24. Flueck WT, Smith-Flueck JM (2006) Predicaments of endangered huemul deer, Hippocamelus bisulcus, in Argentina: a review. Eur J Wildl Res 52:69–80CrossRefGoogle Scholar
  25. Forbes SH, Hogg JT (1999) Assessing population structure at high levels of differentiation: microsatellite comparisons of bighorn sheep and large carnivores. Anim Conserv 2:223–233CrossRefGoogle Scholar
  26. Frankham R, Briscoe DA, Ballou JD (2002) Introduction to conservation genetics. Cambridge University Press, CambridgeGoogle Scholar
  27. Frid A (1994) Observations on habitat use and social organization of a huemul Hippocamelus bisulcus coastal population in Chile. Biol Conserv 67:13–19CrossRefGoogle Scholar
  28. Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318CrossRefPubMedGoogle Scholar
  29. Gilbert C, Ropiquet A, Hassanin A (2006) Mitochondrial and nuclear phylogenies of Cervidae (Mammalia, Ruminantia): systematics, morphology, and biogeography. Mol Phylogenet Evol 40:101–117CrossRefPubMedGoogle Scholar
  30. Gill R, Saucedo C, Aldridge D, Morgan G (2008) Ranging behaviour of huemul in relation to habitat and landscape. J Zool 274:254–260CrossRefGoogle Scholar
  31. Goñi R, Barrientos G, Figuerero MJ, Mengoni GL, Mena F, Lucero V, Reyes O (2004) Distribución espacial de entierros en la cordillera de Patagonia centro-meridional (Lago salitroso-Paso Roballos Arg/Entrada Baker-Río Chacabuco Ch). Chungará 36:1101–1107Google Scholar
  32. Goudet J (2000) FSTAT, a program to estimate and test gene diversities and fixation indices, version 2.9.1. Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland. http://www.unil.ch/izea/softwares/fstat.html
  33. Grosz MD, Solinas Toldo S, Stone RT et al (1997) Chromosomal localization of six bovine microsatellite markers. Anim Genet 28:39–40CrossRefPubMedGoogle Scholar
  34. Guo SW, Thompson EA (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48:361–372CrossRefPubMedGoogle Scholar
  35. Hailer F, Helander B, Folkestad AO, Ganusevich SA, Garstad S, Hauff P, Koren C, Nygård T, Volke V, Vilà C, Ellegren H (2006) Bottlenecked but long-lived: high genetic diversity retained in white-tailed eagles upon recovery from population decline. Biol Lett 2:316–319CrossRefPubMedGoogle Scholar
  36. Hanski I, Gilpin ME (eds) (1997) Metapopulation biology: ecology, genetics, and evolution. Academic Press, San DiegoGoogle Scholar
  37. Hedrick PW (1994) Purging inbreeding depression and the probability of extinction: full-sib mating. Heredity 73:363–372CrossRefPubMedGoogle Scholar
  38. Hewitt G (2000) The genetic legacy of the quaternary ice ages. Nature 405:907–913CrossRefPubMedGoogle Scholar
  39. IUCN (2009) IUCN red list of threatened species. Version 2009.1. http://www.iucnredlist.org. Accessed 12 Oct 2009
  40. Johansson M, Primmer CR, Merilä J (2007) Does habitat fragmentation reduce fitness and adaptability? A case study of the common frog (Rana temporaria). Mol Ecol 16:2693–2700CrossRefPubMedGoogle Scholar
  41. Jones KC, Levine KF, Banks JD (2000) DNA-based genetic markers in black-tailed and mule deer for forensic applications. Calif Fish Game 86:115–126Google Scholar
  42. Kaeuffer R, Coltman DW, Chapuis JL, Pontier D, Réale D (2007) Unexpected heterozygosity in an island mouflon population founded by a single pair of individuals. Proc R Soc Lond B Biol Sci 274:527–533CrossRefGoogle Scholar
  43. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106CrossRefPubMedGoogle Scholar
  44. Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241CrossRefGoogle Scholar
  45. Kirkpatrick M, Jarne P (2000) The effects of a bottleneck on inbreeding depression and the genetic load. Am Nat 155:154–167CrossRefPubMedGoogle Scholar
  46. Kuo CH, Janzen FJ (2003) BOTTLESIM: a bottleneck simulation program for long-lived species with overlapping generations. Mol Ecol Notes 3:669–673CrossRefGoogle Scholar
  47. Lande R (1988) Genetics and demography in biological conservation. Science 241:1455–1460CrossRefPubMedGoogle Scholar
  48. Leite KCE, Collevatti RG, Menegasso TR, Tomas WM, Duarte JMB (2007) Transferability of microsatellite loci from Cervidae species to the endangered Brazilian marsh deer, Blastocerus dichotomus. Genet Mol Res 6:325–330PubMedGoogle Scholar
  49. Lippé C, Dumont P, Bernatchez L (2006) High genetic diversity and no inbreeding in the endangered copper redhorse, Moxostoma hubbsi (Catostomidae, Pisces): the positive sides of a long generation time. Mol Ecol 15:1769–1780CrossRefPubMedGoogle Scholar
  50. Luikart G, Cornuet JM (1999) Estimating the effective number of breeders from heterozygote excess in progeny. Genetics 151:1211–1216PubMedGoogle Scholar
  51. Mainguy J, Llewellyn AS, Worsley K, Côté SD, Coltman DW (2005) Characterization of 29 polymorphic artiodactyl microsatellite markers for the mountain goat (Oreamnos americanus). Mol Ecol Notes 5:809–811CrossRefGoogle Scholar
  52. Moore SS, Byrne K, Berger KT et al (1994) Characterization of 65 bovine microsatellites. Mamm Genome 5:84–90CrossRefPubMedGoogle Scholar
  53. Newman D, Tallmon DA (2001) Experimental evidence for beneficial fitness effects of gene flow in recently isolated populations. Conserv Biol 15:1054–1063CrossRefGoogle Scholar
  54. Nunney L (1999) The effective size of a hierarchically structured population. Evolution 53:1–10CrossRefGoogle Scholar
  55. Pérez T, Albornoz J, Domínguez A (2002) Phylogeography of chamois (Rupicapra spp.) inferred from microsatellites. Mol Phylogenet Evol 25:524–534CrossRefPubMedGoogle Scholar
  56. Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503CrossRefGoogle Scholar
  57. Poissant J, Shafer ABA, Mainguy J, Davis CS, Côté SD, Hogg JT, Coltman DW (2009) Genome-wide cross-amplification of domestic sheep microsatellite loci in bighorn sheep and mountain goats. Mol Ecol Resour 9:1121–1126CrossRefGoogle Scholar
  58. Povilitis A (1998) Characteristics and conservation of a fragmented population of huemul Hippocamelus bisulcus in central Chile. Biol Conserv 86:97–104CrossRefGoogle Scholar
  59. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  60. Redford KH, Eisenberg JF (1992) Mammals of the neotropics. Vol. 2. The southern cone: Chile, Argentina, Uruguay, Paraguay. University of Chicago Press, ChicagoGoogle Scholar
  61. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  62. Rinehart TA (2004) AFLP analysis using GENEMAPPER® software and an EXCEL® macro that aligns and converts output to binary. Biotechniques 37:186–188PubMedGoogle Scholar
  63. Sarre SD, Georges A (2009) Genetics in conservation and wildlife management: a revolution since Caughley. Wildl Res 36:70–80CrossRefGoogle Scholar
  64. Sinclair ARE, Fryxell JM, Caughley G (2006) Wildlife ecology, conservation, and management, 2nd edn. Blackwell Pub, MaldenGoogle Scholar
  65. Spielman D, Brook BW, Frankham R (2004) Most species are not driven to extinction before genetic factors impact them. Proc Natl Acad Sci USA 101:15261–15264CrossRefPubMedGoogle Scholar
  66. Steffen P, Eggen A, Dietz AB et al (1993) Isolation and mapping of polymorphic microsatellites in cattle. Anim Genet 24:121–124CrossRefPubMedGoogle Scholar
  67. Vaiman D, Osta R, Mercier D, Grohs C, Leveziel H (1992) Characterization of 5 new bovine dinucleotide repeats. Anim Genet 23:537–541CrossRefPubMedGoogle Scholar
  68. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  69. Velásquez H, Mena F, Trejo V, Reyes O (2005) Historical and archaeological overview of XIX–XX centuries, transition at Aisen’s mountain range. Werken 7:5–20Google Scholar
  70. Vila AR, López R, Pastore H, Faúndez R, Serret A (2006) Current distribution and conservation of the huemul (Hippocamelus bisulcus) in Argentina and Chile. Mastozool Neotrop 13:263–269Google Scholar
  71. Wang J, Hill WG, Charlesworth D, Charlesworth B (1999) Dynamics of inbreeding depression due to deleterious mutations in small populations: mutation parameters and inbreeding rate. Genet Res 74:165–178CrossRefPubMedGoogle Scholar
  72. Weir BS, Cockerman CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  73. Wilson GA, Strobeck C (1999) The isolation and characterization of microsatellite loci in bison, and their usefulness in other artiodactyls. Anim Genet 30:226–227CrossRefPubMedGoogle Scholar
  74. Wilson GA, Strobeck C, Wu L, Coffin JW (1997) Characterization of microsatellite loci in caribou Rangifer tarandus, and their use in other artiodactyls. Mol Ecol 6:697–699CrossRefPubMedGoogle Scholar
  75. Wilson GA, Nishi JS, Elkin BT, Strobeck C (2005) Effects of a recent founding event and intrinsic population dynamics on genetic diversity in an ungulate population. Conserv Genet 6:905–916CrossRefGoogle Scholar
  76. Woodroffe R, Ginsberg JR (1998) Edge effects and the extinction of populations inside protected areas. Science 280:2126–2128CrossRefPubMedGoogle Scholar
  77. Worley K, Strobeck C, Arthur S, Carey J, Schwantje H, Veitch A, Coltman DW (2004) Population genetic structure of North American thinhorn sheep (Ovis dalli). Mol Ecol 13:2545–2556CrossRefPubMedGoogle Scholar
  78. Young AG, Clarke GM (2000) Genetics, demography, and viability of fragmented populations. Cambridge University Press, New YorkCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Paulo Corti
    • 1
    • 3
  • Aaron B. A. Shafer
    • 2
  • David W. Coltman
    • 2
  • Marco Festa-Bianchet
    • 1
  1. 1.Département de biologieUniversité de SherbrookeSherbrookeCanada
  2. 2.Department of Biological SciencesUniversity of AlbertaEdmontonCanada
  3. 3.Instituto de Zoología, Universidad Austral de ChileValdiviaChile

Personalised recommendations