Translocation retains genetic diversity of a threatened endemic reptile in Mauritius

Abstract

The island of Mauritius has experienced five reptile extinctions since the 1600s. Approximately half of the remaining herpetofauna has been restricted to offshore islets, resulting in small populations at high risk of extinction. Under the combined pressures of invasive species, habitat loss and fragmentation and climate change, translocations are considered a powerful tool in conservation of threatened and endangered species. The Bojer’s skink, Gongylomorphus bojerii, on the offshore island on Ilot Vacoas represents the remnant population of the species in the southeast of Mauritius. Given the geographic isolation and its genetic distinctiveness, individuals were translocated to the neighbouring island of Ile aux Fouquets in order to re-establish historical range, minimize extinction risk and maintain genetic variation within the species. Using fifteen microsatellite loci, we assessed the genetic structure of the population on Ilot Vacoas in relation to a northern offshore population (on Round Island) and evaluated the genetic consequences of the translocation. Results revealed that the population on Ilot Vacoas exhibits significantly lower levels of genetic variation and strong differentiation (F ST  = 0.16) compared to the northern population. The inbreeding coefficient was low and no recent bottleneck event was detected from its genetic signature. The translocation on Ile aux Fouquets did not provide evidence of negative genetic effects. The newly established population retained much of the source’s genetic material, though the effective population size was found to be relatively small. These findings confirmed the importance of incorporating genetic management and continuous monitoring to detect changes in the long-term survival of translocated populations.

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References

  1. Armstrong DP, Seddon PJ (2008) Directions in reintroduction biology. Trends Ecol Evol 23:20–25

    Article  PubMed  Google Scholar 

  2. Arnold EN (1980) Recently extinct reptile populations from Mauritius and Reunion, Indian-Ocean. J Zool 191:33–47

    Article  Google Scholar 

  3. Arnold EN (2000) Using fossils and phylogenies to understand evolution of reptile communities on islands. In:Rheinwold G (ed) Isolated vertebrate communities in the tropics. Bonner zoologische Monographien, vol 46, pp. 309–323

  4. Austin JJ, Arnold EN (2006) Using ancient and recent DNA to explore relationships of extinct and endangered Leiolopisma skinks (Reptilia: Scincidae) in the Mascarene islands. Mol Phylogenet Evol 39:503–511

    Article  CAS  PubMed  Google Scholar 

  5. Austin JJ, Arnold EN, Jones CG (2004) Reconstructing an island radiation using ancient and recent DNA: the extinct and living day geckos (Phelsuma) of the Mascarene islands. Mol Phylogenet Evol 31:109–122

    Article  CAS  PubMed  Google Scholar 

  6. Austin JJ, Arnold EN, Jones CG (2009) Interrelationships and history of the slit-eared skinks (Gongylomorphus, Scincidae) of the Mascarene islands, based on mitochondrial DNA and nuclear gene sequences. Zootaxa 2153:55–68

    Google Scholar 

  7. Beaumont MA, Zhang WY, Balding DJ (2002) Approximate Bayesian computation in population genetics. Genetics 162:2025–2035

    PubMed Central  PubMed  Google Scholar 

  8. Bonin A, Nicole F, Pompanon F, Miaud C, Taberlet P (2007) Population adaptive index: a new method to help measure intraspecific genetic diversity and prioritize populations for conservation. Conserv Biol 21:697–708

    Article  PubMed  Google Scholar 

  9. Bouzat JL, Johnson JA, Toepfer JE, Simpson SA, Esker TL, Westemeier RL (2009) Beyond the beneficial effects of translocations as an effective tool for the genetic restoration of isolated populations. Conserv Genet 10:191–201

    Article  Google Scholar 

  10. Breitenmoser U, Breitenmoser-Wursten C, Carbyn LN, Funk SM (2001) Assessment of carnivore reintroductions. In: Gittleman JL, Funk SM, Macdonald DW, Wayne RK (eds) Carnivore conservation. Cambridge University Press, Cambridge, pp 241–281

    Google Scholar 

  11. Cardoso M, Eldridge M, Oakwood M, Rankmore B, Sherwin W, Firestone K (2009) Effects of founder events on the genetic variation of translocated island populations: implications for conservation management of the northern quoll. Conserv Genet 10(6):1719–1733

    Article  Google Scholar 

  12. Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631

    Article  CAS  PubMed  Google Scholar 

  13. Cheke AS, Hume JP (2008) Lost land of the Dodo: an ecological history of Mauritius, Reunion and Rodrigues. A&C Black, London

    Google Scholar 

  14. Cole N, Goetz M (2013) Mauritius Reptile Recovery Programme. Conservation status of the orange-tailed skink. A technical report submitted to the National Parks and Conservation Service. Ministry of Agro-Industry, Government of Mauritius

  15. Cole N, Jones C, Buckland S, Jhumka Z, Mootoocurpen R, Tatayah V, Bachraz V, Nundlaul V, Roopa P, Seewajee P (2009) The reintroduction of endangered Mauritian reptiles Mauritian Wildlife Foundation. Vacoas, Mauritius

    Google Scholar 

  16. Cole N, Goder M, Vencatasamy D, Mootoocurpen R, Havery S, Gamble F, Nundlaul V (2013) Restoration of Island Ecosystems in Mauritius: The Mauritius Reptile Recovery Programme Annual Report 2013. Durrell Wildlife Conservation Trust, Jersey

    Google Scholar 

  17. Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295

    Article  PubMed  Google Scholar 

  18. Dempster AP, Laird NM, Rubin DB (1977) Maximum likelihood from incomplete data via the EM algorithm. J Roy Stat Soc Ser B 39:1–38

    Google Scholar 

  19. Desjardins J (1831) Sur trois espèces de lézard du genre Scinque qui habitent l’Île Maurice (Île de France). Ann Sci Nat 22:292–299

    Google Scholar 

  20. Dodd CK, Seigel RA (1991) Relocation, repatriation and translocation of amphibians and reptiles—are they conservation strategies that work? Herpetologica 47:336–350

    Google Scholar 

  21. Earl Da, vonHoldt BM (2011) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

  22. 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

    Article  CAS  PubMed  Google Scholar 

  23. Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    PubMed Central  CAS  Google Scholar 

  24. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    PubMed Central  CAS  PubMed  Google Scholar 

  25. Fischer J, Lindenmayer DB (2000) An assessment of the published results of animal relocations. Biol Conserv 96:1–11

    Article  Google Scholar 

  26. Frankham R (1995) Effective population size—adult population size ratios in wildlife—a review. Genet Res 66:95–107

    Article  Google Scholar 

  27. Frankham R (1996) Relationship of genetic variation to population size in wildlife. Conserv Biol 10:1500–1508

    Article  Google Scholar 

  28. Frankham R (1997) Do island populations have less genetic variation than mainland populations? Heredity 78:311–327

    Article  PubMed  Google Scholar 

  29. Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge

    Google Scholar 

  30. Freeman KLM (2003) Ecology and conservation genetics of the Gongylomorphus genus in Mauritius. PhD. Queen Mary University, London

    Google Scholar 

  31. Germano JM, Bishop PJ (2009) Suitability of amphibians and reptiles for translocation. Conserv Biol 23:7–15

    Article  PubMed  Google Scholar 

  32. Goossens B, Funk SM, Vidal C, Latour S, Jamart A, Ancrenaz M, Wickings EJ, Tutin CEG, Bruford MW (2002) Measuring genetic diversity in translocation programmes: principles and application to a chimpanzee release project. Anim Conserv 5:225–236

    Article  Google Scholar 

  33. Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  34. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available from http://www.unil.ch/izea/softwares/fstat.html. Updated from Goudet (1995)

  35. Griffith B, Scott JM, Carpenter JW, Reed C (1989) Translocation as a species conservation tool—status and strategy. Science 245:477–480

    Article  CAS  PubMed  Google Scholar 

  36. Hartl DL, Clark AG (2007) Principles of population genetics, 4th edn. Sinauer Associateas Inc, Sunderland

    Google Scholar 

  37. Hill WG (1981) Estimating effective population size from data on linkage disequilibrium. Genet Res 38:209–216

    Article  Google Scholar 

  38. Hoegh-Guldberg O, Hughes L, McIntyre S, Lindenmayer DB, Parmesan C, Possingham HP, Thomas CD (2008) Assisted colonization and rapid climate change. Science 321:345–346

    Article  CAS  PubMed  Google Scholar 

  39. Houlden BA, England PR, Taylor AC, Greville WD, Sherwin WB (1996) Low genetic variability of the koala Phascolarctos cinereus in south-eastern Australia following a severe population bottleneck. Mol Ecol 5:269–281

    Article  CAS  PubMed  Google Scholar 

  40. IUCN (1998) Guidelines for Re-introductions. IUCN/SSC Re-introduction specialist group, Cambridge

    Google Scholar 

  41. 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 23:1801–1806

    Article  CAS  PubMed  Google Scholar 

  42. Jones CG (1988) A note on the Macchabée skink with a record of predation by the lesser Indian Mongoose. Proc Roy Soc Arts Sci Maurit 5:131–134

    Google Scholar 

  43. Jones CG (1993) The ecology and conservation of Mauritian skinks. Proc Roy Soc Arts Sci Maurit 5:71–95

    Google Scholar 

  44. Kalinowski ST, Waples RS (2002) Relationship of effective to census size in fluctuating populations. Conserv Biol 16:129–136

    Article  Google Scholar 

  45. Kimura M, Ohta T (1978) Stepwise mutation model and distribution of allelic frequencies in a finite population. Proc Natl Acad Sci USA 75:2868–2872

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  46. Leberg P (2005) Genetic approaches for estimating the effective size of populations. J Wildl Manag 69:1385–1399

    Article  Google Scholar 

  47. Lindenmayer DB, Likens GE (2009) Adaptive monitoring: a new paradigm for long-term research and monitoring. Trends Ecol Evol 24:482–486

    Article  PubMed  Google Scholar 

  48. Luikart G, Allendorf FW, Cornuet JM, Sherwin WB (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89:238–247

    Article  CAS  PubMed  Google Scholar 

  49. Mackay TFC (2007) Wild populations are smaller than we think: a commentary on ‘Effective population size/adult population size ratios in wildlife: a review’ by Richard Frankham. Genet Res 89:489

    Article  PubMed  Google Scholar 

  50. Madsen T, Shine R, Olsson M, Wittzell H (1999) Conservation biology—restoration of an inbred adder population. Nature 402:34–35

    Article  CAS  Google Scholar 

  51. Maudet C, Miller C, Bassano B, Breitenmoser-Wursten C, Gauthier D, Obexer-Ruff G, Michallet J, Taberlet P, Luikart G (2002) Microsatellite DNA and recent statistical methods in wildlife conservation management: applications in Alpine ibex [Capra ibex (ibex)]. Mol Ecol 11:421–436

    Article  CAS  Google Scholar 

  52. Moritz C (1994) Defining evolutionarily significant units for conservation. Trends Ecol Evol 9:373–375

    Article  CAS  PubMed  Google Scholar 

  53. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  54. Nei M, Tajima F (1981) Genetic drift and estimation of effective population size. Genetics 98:625–640

    PubMed Central  CAS  PubMed  Google Scholar 

  55. Palstra FP, Ruzzante DE (2008) Genetic estimates of contemporary effective population size: what can they tell us about the importance of genetic stochasticity for wild population persistence? Mol Ecol 17:3428–3447

    Article  PubMed  Google Scholar 

  56. Peel D, Ovenden JR, Peel SL (2004) NeEstimator: software for estimating effective population size, Version 1.3. Queensland Government. Department of Primary Industries and Fisheries, St. Lucia

    Google Scholar 

  57. 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 90:502–503

    Article  Google Scholar 

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

    PubMed Central  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  60. R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  61. Ricciardi A, Simberloff D (2009) Assisted colonization is not a viable conservation strategy. Trends Ecol Evol 24:248–253

    Article  PubMed  Google Scholar 

  62. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

  63. Rosenberg NA (2004) Distruct: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138

    Article  Google Scholar 

  64. Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  PubMed  Google Scholar 

  65. Sarre SD, Georges A (2009) Genetics in conservation and wildlife management: A revolution since Caughley. Wildl Res 36:70–80

  66. Schlaepfer MA, Helenbrook WD, Searing KB, Shoemaker KT (2009) Assisted colonization: evaluating contrasting management actions (and values) in the face of uncertainty. Trends Ecol Evol 24:471–472

    Article  PubMed  Google Scholar 

  67. Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234

    Article  CAS  PubMed  Google Scholar 

  68. Schwartz MK, Luikart G, Waples RS (2007) Genetic monitoring as a promising tool for conservation and management. Trends Ecol Evol 22:25–33

    Article  PubMed  Google Scholar 

  69. Seddon PJ (1999) Persistence without intervention: assessing success in wildlife reintroductions. Trends Ecol Evol 14:503

    Article  PubMed  Google Scholar 

  70. Seddon PJ, Armstrong DP, Soorae PS, Launay F, Walker S, Ruiz-Miranda CR, Molur S, Koldewey H, Kleiman DG (2009) The risks of assisted colonization. Conserv Biol 23:788–789

    Article  PubMed  Google Scholar 

  71. Sigg DP (2006) Reduced genetic diversity and significant genetic differentiation after translocation: comparison of the remnant and translocated populations of bridled nailtail wallabies (Onychogalea fraenata). Conserv Genet 7:577–589

    Article  Google Scholar 

  72. Slatkin M (1987) Gene flow and the geographic structure of natural populations. Science 236:787–792

    Article  CAS  PubMed  Google Scholar 

  73. Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462

    PubMed Central  CAS  PubMed  Google Scholar 

  74. Stephens PA, Sutherland WJ (1999) Consequences of the Allee effect for behaviour, ecology and conservation. Trends Ecol Evol 14:401–405

    Article  PubMed  Google Scholar 

  75. Tonge S (1990) The past, present and future of the herpetofauna of Mauritius. Bull Chic Herpetol Soc 25:220–226

    Google Scholar 

  76. 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

    Article  Google Scholar 

  77. Vernesi C, Crestanello B, Pecchioli E, Tartari D, Caramelli D, Hauffe H, Bertorelle G (2003) The genetic impact of demographic decline and reintroduction in the wild boar (Sus scrofa): a microsatellite analysis. Mol Ecol 12:585–595

    Article  CAS  PubMed  Google Scholar 

  78. Vinson J, Vinson JM (1969) The saurian fauna of the Mascarene Islands. Maurit Inst Bull 6:203–320

    Google Scholar 

  79. Wandeler P, Hoeck PEA, Keller LF (2007) Back to the future: museum specimens in population genetics. Trends Ecol Evol 22:634–642

    Article  PubMed  Google Scholar 

  80. Waples RS (1989) A generalized approach for estimating effective population size from temporal changes in allele frequency. Genetics 121:379–391

    PubMed Central  CAS  PubMed  Google Scholar 

  81. Waples RS (2006) A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci. Conserv Genet 7:167–184

    Article  Google Scholar 

  82. Waples RS, Do C (2008) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Resour 8:753–756

    Article  PubMed  Google Scholar 

  83. Weeks AR, Sgro CM, Young AG, Frankham R, Mitchell NJ, Miller KA, Byrne M, Coates DJ, Eldridge MD, Sunnucks P, Breed MF, James EA, Hoffmann AA (2011) Assessing the benefits and risks of translocations in changing environments: a genetic perspective. Evol Appl 4:709–725

    Article  PubMed Central  PubMed  Google Scholar 

  84. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  85. Wolf MC, Garland T, Griffith B (1998) Predictors of avian and mammalian translocation success: reanalysis with phylogenetically independent contrasts. Biol Conserv 86:243–255

    Article  Google Scholar 

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Acknowledgments

Permission to export the Bojer’s skink samples was given by the National Parks and Conservation Service of Mauritius. The collection of the samples and need for this project was supported by Defra’s Darwin Initiative (project reference 15–038), the Mauritian Wildlife Foundation and National Parks and Conservation Service. We would like to thank Steeves Buckland, Rouben Mootoocurpen, Zayd Jhumka and Mauritian Wildlife Foundation for support in the field and Dr Tim Wright and Ann Thomasson for assistance in the lab at the Durrell Wildlife Conservation Trust. Finally we thank Dr Vikash Tatayah and two anonymous reviewers for comments and suggestions on this article.

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Michaelides, S., Cole, N. & Funk, S.M. Translocation retains genetic diversity of a threatened endemic reptile in Mauritius. Conserv Genet 16, 661–672 (2015). https://doi.org/10.1007/s10592-014-0691-z

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Keywords

  • Translocations
  • Conservation genetics
  • Microsatellites
  • Reptiles
  • Skinks
  • Mauritius