Advertisement

Conservation Genetics

, Volume 16, Issue 4, pp 823–832 | Cite as

Genetics of a head-start program to guide conservation of an endangered Galápagos tortoise (Chelonoidis ephippium)

  • Evelyn L. Jensen
  • Washington Tapia
  • Adalgisa Caccone
  • Michael A. Russello
Research Article

Abstract

Critically endangered wildlife species typically require intensive management using a variety of in situ and ex situ approaches. Yet, despite broad application of ex situ conservation strategies, comparatively few programs incorporate genetic tools into management decisions and monitoring efforts. This is the case with the giant Galápagos tortoise endemic to Pinzón Island (Chelonoidis ephippium); a head-start program has been in place for 50 years without an evaluation of whether this conservation intervention has captured the breadth of diversity present in the wild population. Here we used microsatellite genotypic data to reconstruct patterns of within- and among-population genetic variation in the wild and captivity, and to assess the degree to which head-start cohorts and adult captive founders are representative of the gene pool in situ. We found that Pinzón giant tortoises maintain high levels of variation in situ despite their well-documented decline and that the founders of the captive population are a reasonably diverse and representative group. However, we also found that the head-start cohorts are not representative of the wild population, as evidenced by significant genetic differentiation between the in situ and ex situ samples and by the private alleles detected in both. Future head-start activities should broaden the source locations of eggs and hatchlings to more comprehensively capture the extent and distribution of genetic variation in this critically endangered keystone herbivore. More broadly, this study further highlights the utility of integrating genetic information within ex situ conservation programs.

Keywords

Captive breeding Ex situ conservation Giant Galápagos tortoise Pinzón Island Microsatellite 

Notes

Acknowledgments

We gratefully acknowledge the Parque Nacional de Galápagos for support, logistics and assistance with sampling, particularly Fausto Llerena and Galo Quezada. Claudia Hollatz also assisted with sample collection and Linda Cayot provided valuable feedback on an earlier version of this manuscript. This work was funded by the Mohamed bin Zayed Species Conservation Fund (project # 62R63567; MR, GC, WT). EJ was supported by a National Science and Engineering Research Council Postgraduate Scholarship. GC was supported by the Yale Institute for Biospheric Studies.

References

  1. Beheregaray LB, Ciofi C, Caccone A, Gibbs JP, Powell JR (2003a) Genetic divergence, phylogeography and conservation units of giant tortoises from Santa Cruz and Pinzón, Galápagos Islands. Conserv Genet 4:31–46. doi: 10.1023/a:1021864214375 CrossRefGoogle Scholar
  2. Beheregaray LB, Ciofi C, Geist D, Gibbs JP, Caccone A, Powell JR (2003b) Genes record a prehistoric volcano eruption in the Galapagos. Science 302:75. doi: 10.1126/science.1087486 PubMedCrossRefGoogle Scholar
  3. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2004) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier (France)Google Scholar
  4. Benavides E, Russello MA, Boyer D, Wiese RJ, Kajdacsi B, Marquez L, Garrick R, Caccone A (2012) Lineage identification and genealogical relationships among captive Galápagos tortoises. Zoo Biol 31:107–120. doi: 10.1002/zoo.20397 PubMedCrossRefGoogle Scholar
  5. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc Ser B Stat Methodol 57:289–300. doi: 10.2307/2346101 Google Scholar
  6. Bonin F, Devaux B, Dupre A (2006) Turtles of the world. Johns Hopkins University Press, BaltimoreGoogle Scholar
  7. Castric V, Bernatchez L, Belkhir K, Bonhomme F (2002) Heterozygote deficiencies in small lacustrine populations of brook charr Salvelinus fontinalis Mitchill (Pisces, Salmonidae): a test of alternative hypotheses. Heredity 89:27–35. doi: 10.1038/sj.hdy.6800089 PubMedCrossRefGoogle Scholar
  8. Caughley G (1994) Directions in conservation biology. J Anim Ecol 63:215–244. doi: 10.2307/5542 CrossRefGoogle Scholar
  9. Ciofi C, Milinkovitch MC, Gibbs JP, Caccone A, Powell JR (2002) Microsatellite analysis of genetic divergence among populations of giant Galápagos tortoises. Mol Ecol 11:2265–2283PubMedCrossRefGoogle Scholar
  10. Ciofi C, Wilson GA, Beheregaray LB, Marquez C, Gibbs JP, Tapia W, Snell HL, Caccone A, Powell JR (2006) Phylogeographic history and gene flow among giant Galapagos tortoises on southern Isabela Island. Genetics 172:1727–1744. doi: 10.1534/genetics.105.047860 PubMedCentralPubMedCrossRefGoogle Scholar
  11. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedCentralPubMedGoogle Scholar
  12. Earl DA, vonHoldt BM (2011) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Res 4:359–361. doi: 10.1007/s12686-011-9548-7 CrossRefGoogle Scholar
  13. Edwards DL, Benavides E, Garrick RC, Gibbs JP, Russello MA, Dion KB, Hyseni C, Flanagan JP, Tapia W, Caccone A (2013) The genetic legacy of Lonesome George survives: giant tortoises with Pinta Island ancestry identified in Galápagos. Biol Conserv 157:225–228. doi: 10.1016/j.biocon.2012.10.014 CrossRefGoogle Scholar
  14. Ernst CH, Barbour RW (1989) Turtles of the world. Smithsonian Institution Press, Washinton DCGoogle Scholar
  15. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620. doi: 10.1111/j.1365-294X.2005.02553.x PubMedCrossRefGoogle Scholar
  16. Foose TJ (1993) Riders of the last ark: the role of captive breeding in conservation strategies. In: Kaufman L, Mallory K (eds) The last extinction. MIT Press and New England Aquarium, Cambridge, pp 149–178Google Scholar
  17. Garrick RC, Benavides E, Russello MA, Gibbs JP, Poulakakis N, Dion KB, Hyseni C, Kajdacsi B, Marquez L, Bahan S, Ciofi C, Tapia W, Caccone A (2012) Genetic rediscovery of an ‘extinct’ Galapagos giant tortoise species. Curr Biol 22:R10–R11. doi: 10.1016/j.cub.2011.12.004 PubMedCrossRefGoogle Scholar
  18. Garrick RC, Kajdacsi B, Russello MA, Benavides E, Hyseni C, Gibbs JP, Tapia W, Caccone A (2015) Naturally rare versus newly rare: demographic inferences on two timescales inform conservation of Galápagos giant tortoises. Ecol Evol. doi: 10.1002/ece3.1388 PubMedCentralPubMedGoogle Scholar
  19. Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318PubMedCrossRefGoogle Scholar
  20. Gonçalves da Silva A, Russello MA (2011) iREL: software for implementing pairwise relatedness estimators and evaluating their performance. Conserv Genet Resour 3:69–71. doi: 10.1007/s12686-010-9292-4 CrossRefGoogle Scholar
  21. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). http://www.unil.ch/izea/softwares/fstat.html. Accessed 4 July 2014
  22. Iyengar A, Gilbert T, Woodfine T, Knowles JM, Diniz FM, Brenneman RA, Louis EE Jr, MaClean N (2007) Remnants of ancient genetic diversity preserved within captive groups of scimitar-horned oryx (Oryx dammah). Mol Ecol 16:2436–2449. doi: 10.1111/j.1365-294X.2007.03291.x PubMedCrossRefGoogle Scholar
  23. Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. doi: 10.1093/bioinformatics/btn129 PubMedCrossRefGoogle Scholar
  24. Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94. doi: 10.1186/1471-2156-11-94 PubMedCentralPubMedCrossRefGoogle Scholar
  25. Jones OR, Wang J (2010) COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Resour 10:551–555. doi: 10.1111/j.1755-0998.2009.02787.x PubMedCrossRefGoogle Scholar
  26. Kalinowski ST (2005) Hp-rare 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189. doi: 10.1111/j.1471-8286.2004.00845.x CrossRefGoogle Scholar
  27. Karl SA (2008) The effect of multiple paternity on the genetically effective size of a population. Mol Ecol 17:3973–3977. doi: 10.1111/j.1365-294X.2008.03902.x PubMedCrossRefGoogle Scholar
  28. Lacy RC (1994) Managing genetic diversity in captive populations of animals. In: Bowles ML, Whelan CJ (eds) Restoration of endangered species: conceptual issues, planning and implementation. Cambridge University Press, Cambridge, pp 63–89CrossRefGoogle Scholar
  29. MacFarland CG, Villa J, Toro B (1974) The Galápagos giant tortoises (Geochelone elephantopus) Part I: status of the surviving populations. Biol Conserv 6:118–133. doi: 10.1016/0006-3207(74)90024-X CrossRefGoogle Scholar
  30. Maruyama T, Fuerst PA (1985) Population bottlenecks and non equilibrium models in population genetics. II. Number of alleles in a small population that was formed by a recent bottleneck. Genetics 111:675–689PubMedCentralPubMedGoogle Scholar
  31. Milinkovitch MC, Monteyne D, Gibbs JP, Fritts TH, Tapia W, Snell HL, Tiedemann R, Caccone A, Powell JR (2004) Genetic analysis of a successful repatriation programme: giant Galápagos tortoises. Proc R Soc Lond B Biol Sci 271:341–345. doi: 10.1098/rspb.2003.2607 CrossRefGoogle Scholar
  32. Milinkovitch MC, Monteyne D, Russello M, Gibbs JP, Snell HL, Tapia W, Marquez C, Caccone A, Powell JR (2007) Giant Galápagos tortoises: molecular genetic analyses identify a trans- island hybrid in a repatriation program of an endangered taxon. BMC Ecol 7:2. doi: 10.1186/1472-6785-7-2 PubMedCentralPubMedCrossRefGoogle Scholar
  33. Milinkovitch MC, Kanitz R, Tiedemann R, Tapia W, Llerena F, Caccone A, Gibbs JP, Powell JR (2013) Recovery of a nearly extinct Galapagos tortoise despite minimal genetic variation. Evol Appl 6:377–383. doi: 10.1111/eva.12014 PubMedCentralPubMedCrossRefGoogle Scholar
  34. Murray J (1964) Multiple mating and effective population-size in Cepaea nemoralis. Evolution 18:283–291. doi: 10.2307/2406402 CrossRefGoogle Scholar
  35. Narum SR (2006) Beyond Bonferroni: less conservative analyses for conservation genetics. Conserv Genet 7:783–787. doi: 10.1007/s10592-005-9056-y CrossRefGoogle Scholar
  36. Peakall R, Smouse PE (2006) GenAlEx 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  37. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539. doi: 10.1093/bioinformatics/bts460 PubMedCentralPubMedCrossRefGoogle Scholar
  38. Pearse DE, Avise JC (2001) Turtle mating systems: behavior, sperm storage, and genetic paternity. J Hered 92:206–211. doi: 10.1093/jhered/92.2.206 PubMedCrossRefGoogle Scholar
  39. Peery MZ, Kirby R, Reid BN, Stoelting R, Doucet-Beer E, Robinson S, Vasquez-Carrillo C, Pauli JN, Palsboll PJ (2012) Reliability of genetic bottleneck tests for detecting recent population declines. Mol Ecol 21:3403–3418. doi: 10.1111/j.1365-294X.2012.05635.x PubMedCrossRefGoogle Scholar
  40. Piry S, Luikart G, Cornuet J-M (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele freqency data. J Hered 90:502–503CrossRefGoogle Scholar
  41. Pritchard PCH (1996) The Galápagos tortoises—nomenclatural and survival status. Chelonian Res Monogr 1:1–85Google Scholar
  42. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedCentralPubMedGoogle Scholar
  43. Pudovkin AI, Zaykin DV, Hedgecock D (1996) On the potential for estimating the effective number of breeders from heterozygote-excess in progeny. Genetics 144:383–387PubMedCentralPubMedGoogle Scholar
  44. Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275CrossRefGoogle Scholar
  45. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  46. Rousset F (2008) Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Resour 8:103–106PubMedCrossRefGoogle Scholar
  47. Russello MA, Amato G (2007) On the horns of a dilemma: molecular approaches refine ex situ conservation in crisis. Mol Ecol 16:2405–2406. doi: 10.1111/j.1365-294X.2007.03376.x PubMedCrossRefGoogle Scholar
  48. Russello MA, Glaberman S, Gibbs JP, Marquez C, Powell JR, Caccone A (2005) A cryptic taxon of Galápagos tortoise in conservation peril. Biol Lett 1:287–290. doi: 10.1098/rsbl.2005.0317 PubMedCentralPubMedCrossRefGoogle Scholar
  49. Russello MA, Beheregaray LB, Gibbs JP, Fritts T, Havill N, Powell JR, Caccone A (2007a) Lonesome George is not alone among Galapagos tortoises. Curr Biol 17:R317–R318. doi: 10.1016/j.cub.2007.03.002 PubMedCrossRefGoogle Scholar
  50. Russello MA, Hyseni C, Gibbs JP, Cruz S, Marquez C, Tapia W, Velensky P, Powell JR, Caccone A (2007b) Lineage identification of Galapagos tortoises in captivity worldwide. Anim Conserv 10:304–311. doi: 10.1111/j.1469-1795.2007.00113.x CrossRefGoogle Scholar
  51. Russello MA, Poulakakis N, Gibbs JP, Tapia W, Benavides E, Powell JR, Caccone A (2010) DNA from the past informs ex situ conservation for the future: an “extinct” species of Galapagos tortoise identified in captivity. PLoS ONE 5:e8683. doi: 10.1371/journal.pone.0008683 PubMedCentralPubMedCrossRefGoogle Scholar
  52. Saltzgiver M, Heist E, Hedrick P (2012) Genetic evaluation of the initiation of a captive population: the general approach and a case study in the endangered pallid sturgeon (Scaphirhynchus albus). Conserv Genet 13:1381–1391. doi: 10.1007/s10592-012-0381-7 CrossRefGoogle Scholar
  53. Snyder NFR, Derrickson SR, Beissinger SR, Wiley JW, Smith TB, Toone WD, Miller B (1996) Limitations of captive breeding in endangered species recovery. Conserv Biol 10:338–348. doi: 10.1046/j.1523-1739.1996.10020338.x CrossRefGoogle Scholar
  54. Townsend CH (1931) Giant tortoises. Sci Am 144:42–44CrossRefGoogle Scholar
  55. 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 4:535–538. doi: 10.1111/j.1471-8286.2004.00684.x CrossRefGoogle Scholar
  56. Vié JC, Hilton-Taylor C, Stuart SN (2009) Wildlife in a changing world—an analysis of the 2008 IUCN Red List of Threatened Species™. IUCN, GlandGoogle Scholar
  57. Wahlund S (1928) Composition of populations and correlation appearances viewed in relation to the studies of inheritance. Hereditas 11:65–106CrossRefGoogle Scholar
  58. Weir BS, Cockerham CC (1984) Estimating f-statistics for the analysis of population-structure. Evolution 38:1358–1370. doi: 10.2307/2408641 CrossRefGoogle Scholar
  59. Williamson-Natesan EG (2005) Comparison of methods for detecting bottlenecks from microsatellite loci. Conserv Genet 6:551–562. doi: 10.1007/s10592-005-9009-5 CrossRefGoogle Scholar
  60. Witzenberger KA, Hochkirch A (2011) Ex situ conservation genetics: a review of molecular studies on the genetic consequences of captive breeding programmes for endangered animal species. Biodivers Conserv 20:1843–1861. doi: 10.1007/S10531-011-0074-4 CrossRefGoogle Scholar
  61. Zhang D-X, Hewitt GM (2003) Nuclear DNA analyses in genetic studies of populations: practice, problems and prospects. Mol Ecol 12:563–584. doi: 10.1046/j.1365-294X.2003.01773.x PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  • Evelyn L. Jensen
    • 1
  • Washington Tapia
    • 2
  • Adalgisa Caccone
    • 3
  • Michael A. Russello
    • 1
  1. 1.Department of BiologyUniversity of British ColumbiaKelownaCanada
  2. 2.Giant Tortoise Restoration InitiativeGalápagos ConservancyPuerto AyoraEcuador
  3. 3.Department of Ecology & Evolutionary BiologyYale UniversityNew HavenUSA

Personalised recommendations