Skip to main content

Advertisement

Log in

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

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  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. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier (France)

  • 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

    Article  PubMed  Google Scholar 

  • 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 

  • Bonin F, Devaux B, Dupre A (2006) Turtles of the world. Johns Hopkins University Press, Baltimore

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Caughley G (1994) Directions in conservation biology. J Anim Ecol 63:215–244. doi:10.2307/5542

    Article  Google Scholar 

  • Ciofi C, Milinkovitch MC, Gibbs JP, Caccone A, Powell JR (2002) Microsatellite analysis of genetic divergence among populations of giant Galápagos tortoises. Mol Ecol 11:2265–2283

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Ernst CH, Barbour RW (1989) Turtles of the world. Smithsonian Institution Press, Washinton DC

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 149–178

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. doi:10.1093/bioinformatics/btn129

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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 63–89

    Chapter  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 111:675–689

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • Murray J (1964) Multiple mating and effective population-size in Cepaea nemoralis. Evolution 18:283–291. doi:10.2307/2406402

    Article  Google Scholar 

  • Narum SR (2006) Beyond Bonferroni: less conservative analyses for conservation genetics. Conserv Genet 7:783–787. doi:10.1007/s10592-005-9056-y

    Article  CAS  Google Scholar 

  • Peakall R, Smouse PE (2006) GenAlEx 6: genetic analysis in excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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 90:502–503

    Article  Google Scholar 

  • Pritchard PCH (1996) The Galápagos tortoises—nomenclatural and survival status. Chelonian Res Monogr 1:1–85

    Google Scholar 

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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pudovkin AI, Zaykin DV, Hedgecock D (1996) On the potential for estimating the effective number of breeders from heterozygote-excess in progeny. Genetics 144:383–387

    CAS  PubMed Central  PubMed  Google Scholar 

  • Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275

    Article  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Rousset F (2008) Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Townsend CH (1931) Giant tortoises. Sci Am 144:42–44

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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, Gland

    Google Scholar 

  • Wahlund S (1928) Composition of populations and correlation appearances viewed in relation to the studies of inheritance. Hereditas 11:65–106

    Article  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating f-statistics for the analysis of population-structure. Evolution 38:1358–1370. doi:10.2307/2408641

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Michael A. Russello.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jensen, E.L., Tapia, W., Caccone, A. et al. Genetics of a head-start program to guide conservation of an endangered Galápagos tortoise (Chelonoidis ephippium). Conserv Genet 16, 823–832 (2015). https://doi.org/10.1007/s10592-015-0703-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-015-0703-7

Keywords

Navigation