Conservation Genetics

, Volume 15, Issue 6, pp 1357–1369 | Cite as

Cryptic structure and niche divergence within threatened Galápagos giant tortoises from southern Isabela Island

  • D. L. EdwardsEmail author
  • R. C. Garrick
  • W. Tapia
  • A. Caccone
Research Article


Although Galápagos giant tortoises are an icon for both human-mediated biodiversity losses and conservation management successes, populations of two species on southern Isabela Island (Chelonoidis guntheri, and C. vicina) remain threatened by hunting and persistence of feral animals. Conservation management of these tortoises has been hampered by lack of clarity regarding their taxonomy, ecological and morphological diversity, and the spatial distribution of evolutionarily significant units that may exist. Analyses of 16 microsatellite loci did not group samples according to current taxonomy. Instead, three (rather than two) genetic clusters were revealed. We show that the three regions of southern Isabela associated with these genetic clusters are significantly different in their ecological niches, which could suggest that ecological divergence may have shaped patterns of genetic differentiation in these tortoises. Furthermore, results suggest limited recent gene flow among sampled localities and between each of the three regions associated with genetic clusters. We discuss the need for further research on the ecological factors shaping the genetic and morphological diversity of southern Isabela tortoises. We suggest that current strategies whereby populations are managed separately are warranted pending further study, but due to mixed ancestry we recommend that Cerro Paloma tortoises be excluded from management programs.


Chelonoidis Conservation Management Ecological divergence Evolutionarily significant unit Galápagos tortoise Genetic divergence 



We thank the PNG for instrumental support for this project and the collection of tortoise distribution data, Alizon Llerena for distribution data curation and Linda Cayot (Galápagos Conservancy) for discussion of ideas and invaluable comments on this manuscript. We thank two anonymous reviewers for improving the manuscript. Permits for sample collection were granted by the PNG, and CITES permits (12US209142) were issued by the US Fish & Wildlife Service. Financial support came from the PNG, CDF and Yale Institute for Biospheric Studies.

Supplementary material

10592_2014_622_MOESM1_ESM.docx (415 kb)
Supplementary material 1 (DOCX 416 kb)


  1. Allendorf FW, Hohenlohe PA, Luikart G (2010) Genomics and the future of conservation genetics. Nat Rev Genet 11:697–709PubMedCrossRefGoogle Scholar
  2. Beck R (1903) In the home of the giant tortoise. 7th Annual Report of the New York Zoological Society, vol 7, pp 160–174Google Scholar
  3. Beheregaray LB, Ciofi C, Geist D, Gibbs JP, Caccone A, Powell JR (2003) Genes record a prehistoric volcano eruption in the Galápagos. Science 302:75PubMedCrossRefGoogle Scholar
  4. Beheregaray LB, Gibbs JP, Havill N, Fritts TH, Powell JR, Caccone A (2004) Giant tortoises are not so slow: rapid diversification and biogeographic consensus in the Galápagos. Proc Natl Acad Sci USA 101:6514–6519PubMedCentralPubMedCrossRefGoogle Scholar
  5. Benavides E, Russello MA, Boyer D, Wiese RJ, Kajdacsi B, Márquez L, Garrick RC, Caccone A (2012) Lineage identification and genealogical relationships among captive Galápagos tortoises. Zoo Biol 31:101–120CrossRefGoogle Scholar
  6. Blake S, Wikelski M, Cabrera F, Guezou A, Silva M, Sadeghayobi E, Yackulic CB, Jaramillo P (2012a) Seed dispersal by Galápagos tortoises. J Biogeogr 39:1961–1972CrossRefGoogle Scholar
  7. Blake S, Yackulia CB, Cabrera F, Tapia W, Gibbs JP, Kümmeth F, Wikelski M (2012b) Vegetation dynamics drive segregation by body size in Galápagos tortoises migrating across altitudinal gradients. J Anim Ecol 82:310–321PubMedCrossRefGoogle Scholar
  8. Burns CE, Ciofi C, Beheregaray LB, Fritts TH, Gibbs JP, Márquez C, Milinkovitch MC, Powell JR, Caccone A (2003) the origin of captive Galápagos tortoises based on DNA analysis: implications for the management of natural populations. Anim Conserv 6:329–337CrossRefGoogle Scholar
  9. Caccone A, Gentile G, Gibbs JP, Fritts TH, Snell HL, Betts J, Powell JR (2002) Phylogeography and history of giant Galápagos tortoises. Evolution 56:2052–2066PubMedGoogle Scholar
  10. Causton CE, Peck SB, Sinclair BJ, Roque-Albelo L, Hodgson CJ, Landry B (2006) Alien insects: threats and implications for conservation of Galápagos Islands. Ann Entomol Soc Am 99:121–143CrossRefGoogle Scholar
  11. Cayot LJ (2008) The restoration of giant tortoise and land iguana populations in Galápagos. Notícias de Galápagos 43:39–43Google Scholar
  12. Cayot LJ, Lewis E (1994) Recent increase in killing of giant tortoises on Isabela Island. Notícias de Galápagos 54:2–7Google Scholar
  13. Cayot LJ, Snell HM (1996) Tortoises from Cerro Paloma, Isabela threatened. Notícias de Galápagos 56:2Google Scholar
  14. Cayot LJ, Snell HL, Llerena W, Snell HM (1994) Conservation biology of Galápagos reptiles: twenty-five years of successful research and management. In: Murphy JB, Adler K, Collins JT (eds) Captive management and conservation of amphibians and reptiles. Contributions to herpetology, vol 11. Society for the Study of Amphibians and Reptiles, Ithaca, pp 297–305Google Scholar
  15. 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
  16. 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 Galápagos tortoises on southern Isabela island. Genetics 172:1727–1744PubMedCentralPubMedCrossRefGoogle Scholar
  17. Colinvaux PA (1972) Climate and the Galápagos Islands. Nature 240:17–20CrossRefGoogle Scholar
  18. Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295PubMedCrossRefGoogle Scholar
  19. Darwin C (1839) Journal of Researches into the geology and natural history of the various countries visited by H.M.S. Beagle, under command of Captain Fitz Roy, R.N. from 1832–1836. Henry Colburn, LondonGoogle Scholar
  20. Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20Google Scholar
  21. Earl D, von Holdt B (2011) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4(2):359–361CrossRefGoogle Scholar
  22. 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 157:225–228CrossRefGoogle Scholar
  23. England PR, Cornuet JM, Berthier P, Tallmon DA, Luikart G (2006) Estimating effective population size from linkage disequilibrium: severe bias in small samples. Conserv Genet 7:303–308CrossRefGoogle Scholar
  24. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620PubMedCrossRefGoogle Scholar
  25. Excoffier L, Lischer HEL (2010) Arlequin suite ver. 3.5: a new series of programs to perform population genetics analysis under Linus and Windows. Mol Ecol Resour 10:564–567PubMedCrossRefGoogle Scholar
  26. Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol Ecol 10:2741–2752PubMedCrossRefGoogle Scholar
  27. Fritts TH (1984) Evolutionary divergence of giant tortoises in Galápagos. Biol J Linn Soc 21:165–176CrossRefGoogle Scholar
  28. Garrick RC, Benavides E, Russello MA, Gibbs JP, Poulakakis N, Dion KB, Hyseni C, Kajdacsi B, Márquez L, Bahan S, Ciofi C, Tapia W, Caccone A (2012) Genetic rediscovery of an ‘extinct’ Galápagos giant tortoise species. Curr Biol 22:R10–R11PubMedCrossRefGoogle Scholar
  29. Geist D, Snell HL, Snell H, Goddard C, Kurz M (2014) A paleaogeographic model of the Galápagos Islands and biogeographical and evolutionary implications. In Harpp K, d’Ozouville N, Mittelstaedt E, Graham D (eds) The Galápagos: a natural laboratory for the earth sciences. American Geophysical Union Monograph, Washington Google Scholar
  30. Gibbs JP, Márquez C, Sterling EJ (2008) The role of endangered species reintroduction in ecosystem restoration: tortoise-cactus interactions on Española Island. Galápagos Rest Ecol 16:88–93CrossRefGoogle Scholar
  31. Gibbs JP, Sterilng EJ, Zabala FJ (2010) Giant tortoises as ecosystem engineers: a long-term quasi-experiment in the Galápagos Islands. Biotropica 42:208–214CrossRefGoogle Scholar
  32. Goudet J (2013) hierfstat: estimation and tests of hierarchical F-statistics. R package version 0.04-10.
  33. Goward SN, Markham B, Dye DG, Dulaney W, Yang J (1991) Normalized difference vegetation index measurements from the advanced very high resolution radiometer. Remote Sens Environ 35:257–277CrossRefGoogle Scholar
  34. Hennessy E (2013) Producing “prehistoric” life: conservation breeding and the remaking of wildlife genealogies. Geoforum 49:71–80CrossRefGoogle Scholar
  35. Hijmans RJ, van Etten J (2013) raster: geographic data analysis and modeling. R package version 2.1-25.
  36. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Clim 25:1965–1978CrossRefGoogle Scholar
  37. Idury RM, Cardon LR (1997) A simple method for automated allele binning in microsatellite markers. Genome Res 7:1104–1109PubMedCentralPubMedGoogle Scholar
  38. 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 23:1801–1806PubMedCrossRefGoogle Scholar
  39. Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405PubMedCrossRefGoogle Scholar
  40. Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026PubMedCrossRefGoogle Scholar
  41. Keenan K, McGinnity P, Cross TF, Crozier WW, Prodöhl PA (2013) diveRsity: an R package for the estimation of population genetics parameters and their associated errors. Methods Ecol Evol 4:782–788CrossRefGoogle Scholar
  42. Lande R (1988) Genetics and demography in biological conservation. Science 241:1455–1460PubMedCrossRefGoogle Scholar
  43. Le Corre V, Kremer A (1998) Cumulative effects of founding events during colonization on genetic diversity and differentiation in an island and stepping-stone model. J Evol Biol 11:495–512CrossRefGoogle Scholar
  44. MacFarland CG, Villa J, Toro B (1974) The Galápagos tortoises (Geochelone elephantopus). Part 1: status of surviving populations. Biol Conserv 6:118–133CrossRefGoogle Scholar
  45. Márquez C, Wiedenfeld DA, Landázuri S, Chávez J (2007) Human-caused and natural mortality of giant tortoises in the Galápagos Islands during 1995–2004. Oryx 41:337–342CrossRefGoogle Scholar
  46. Matschiner M, Salzburger W (2009) TANDEM: integrating automated allele binning into genetics and genomics workflows. Bioinformatics 25:1982–1983PubMedCrossRefGoogle Scholar
  47. McCormack JE, Zellmer AJ, Knowles LL (2010) Does niche divergence accompany allopatric divergence in Aphelocoma jays as predicted under ecological speciation?: insights from tests with niche models. Evolution 64:1231–1244PubMedGoogle Scholar
  48. 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 program: giant Galápagos tortoises. Proc R Soc Lond B 271:341–345CrossRefGoogle Scholar
  49. Milinkovitch MC, Kanitz R, Tiedmann R, Tapia W, Llerena F, Caccone A, Gibbs JP, Powell JR (2013) Recovery of a nearly extinct Galápagos tortoise despite minimal genetic variation. Evol Appl 6:377–383PubMedCentralPubMedCrossRefGoogle Scholar
  50. Mills LS (2012) Conservation of wildlife populations: demography, genetics, and management, 2nd edn. Wiley, OxfordGoogle Scholar
  51. Moritz C (2002) Strategies to protect biological diversity and the evolutionary processes that sustain it. Syst Biol 51:238–254PubMedCrossRefGoogle Scholar
  52. Myneni RB, Ramakrishna R, Nemani R, Running SW (1997) Estimation of global leaf area index and absorbed par using radiative transfer models. Geosci Remote Sens 35:1380–1393CrossRefGoogle Scholar
  53. Narum SR (2006) Beyond Bonferroni: less conservative analyses for conservation genetics. Conserv Genet 7:787–793Google Scholar
  54. Naumann T, Geist D (2000) Physical volcanology and structural development of Cerro Azul volcano, Isabela Island, Galápagos: implications for the development of Galápagos-type shield volcanoes. Bull Volcanol 61:497–514Google Scholar
  55. Nicholls H (2006) Lonesome George: the life and loves of a conservation icon. MacMillan, LondonGoogle Scholar
  56. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2013) vegan: Community Ecology Package. R package version 2.0-6Google Scholar
  57. Paetkau D, Calvert W, Stirling I, Strobeck C (1995) Microsatellite analysis of population structure in Canadian polar bears. Mol Ecol 4:347–354PubMedCrossRefGoogle Scholar
  58. Paetkau D, Slade R, Burden M, Estoup A (2004) Direct, real-time estimation of migration rate using assignment methods: a simulation-based exploration of accuracy and power. Mol Ecol 13:55–65PubMedCrossRefGoogle Scholar
  59. Phillips RB, Widenfeld DA, Snell HL (2012) Current status of alien vertebrates in the Galápagos Islands: invasion history, distribution, and potential impacts. Biol Invasions 14:461–480CrossRefGoogle Scholar
  60. Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, Estoup A (2004) GeneClas: a software for genetic assignment and first-generation migrant detection. J Heredity 95:536–539CrossRefGoogle Scholar
  61. Porter DM (1976) Geography and dispersal of Galápagos Islands vascular plants. Nature 264:745–746CrossRefGoogle Scholar
  62. Poulakakis N, Glaberman S, Russello MA, Beheregaray LB, Ciofi C, Powell JR, Caccone A (2008) Historical DNA analysis reveals living descendants of an extinct species of Galápagos tortoise. Proc Natl Acad Sci USA 105:15464–15469PubMedCentralPubMedCrossRefGoogle Scholar
  63. Poulakakis N, Russello MA, Geist D, Caccone A (2012) Unravelling the peculiarities of island life: vicariance, dispersal and the diversification of the extinct species of Galápagos tortoises. Mol Ecol 21:160–173PubMedCrossRefGoogle Scholar
  64. Pritchard PCH (1996) The Galápagos tortoises nomenclatural and survival status: Chelonian Research Monographs 1. Chelonian Research Foundation, LunenburgGoogle Scholar
  65. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedCentralPubMedGoogle Scholar
  66. Raymond M, Rousset F (1995) Genepop (version 1.2): population genetics software for exact tests and ecumenicism. J Heredity 86:248–249Google Scholar
  67. Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237CrossRefGoogle Scholar
  68. Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138CrossRefGoogle Scholar
  69. Russello MA, Glaberman S, Gibbs JP, Márquez C, Powell JR, Caccone A (2005) A cryptic taxon of Galápagos tortoise in conservation peril. Biol Lett 1:287–290PubMedCentralPubMedCrossRefGoogle Scholar
  70. Russello MA, Beheregaray LB, Gibbs JP, Fritts TH, Havill N, Powell JR, Caccone A (2007) Lonesome George is not alone among Galápagos tortoises. Curr Biol 17:R317–R318PubMedCrossRefGoogle Scholar
  71. 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 Galápagos tortoise identified in captivity. PLoS ONE 5:e8683PubMedCentralPubMedCrossRefGoogle Scholar
  72. Ryder OA (1986) Species conservation and systematics: the dilemma of the subspecies. Trends Ecol Evol 1:9–10CrossRefGoogle Scholar
  73. Schoville SD, Bonin A, François O, Lobreaux A, Melodelima C, Manel S (2012) Adaptive genetic variation on the landscape: methods and cases. Annu Rev Ecol Evol Syst 43:23–43CrossRefGoogle Scholar
  74. Schwartz MK, Luikart G, Waples RS (2007) Genetic monitoring as a promising tool for conservation and management. Trends Ecol Evol 22:25–33PubMedCrossRefGoogle Scholar
  75. Tapia W (1997) Estado actual y distribución estacional de las tortugas gigantes (Geochelone elephantopus spp.) de CincoCerros, volcán Cerro Azul, islaIsabela, Galápagos, Ecuador. Tesis de grado, Universidad Técnica del Norte, Ibarra, EcuadorGoogle Scholar
  76. Townsend CH (1925) The Galápagos tortoises in relation to the whaling industry. Zoological Society, New YorkGoogle Scholar
  77. Van Denburgh J (1914) The gigantic land tortoises of the Galápagos Archipelago. Proc Calif Acad Sci USA 4:203–374Google Scholar
  78. 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
  79. Vavrek MJ (2011) Fossil: palaeoecological and palaeogeographical analysis tools. Palaeontol Electron 14:1TGoogle Scholar
  80. Waples RS (2006) A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci. Conserv Genet 7:167–184CrossRefGoogle Scholar
  81. Waples RS, Do CHI (2008) LDNe: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Resour 8:753–756PubMedCrossRefGoogle Scholar
  82. Warren DL, Glor RE, Turelli M (2008) Environmental niche equivalency versus conservatism: quantitative approaches to niche evolution. Evolution 62:2868–2883PubMedCrossRefGoogle Scholar
  83. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  84. Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191PubMedCentralPubMedGoogle Scholar
  85. Wright S (1943) Isolation by distance. Genetics 28:114–138PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • D. L. Edwards
    • 1
    Email author
  • R. C. Garrick
    • 2
  • W. Tapia
    • 3
  • A. Caccone
    • 1
  1. 1.Department of Ecology and Evolutionary BiologyYale UniversityNew HavenUSA
  2. 2.Department of BiologyUniversity of MississippiUniversityUSA
  3. 3.Parque Nacional de GalápagosPuerto AyoraEcuador

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