Conservation Genetics

, Volume 11, Issue 3, pp 1063–1081

Genetic diversity and taxonomy: a reassessment of species designation in tuatara (Sphenodon: Reptilia)

  • Jennifer M. Hay
  • Stephen D. Sarre
  • David M. Lambert
  • Fred W. Allendorf
  • Charles H. Daugherty
Research Article

Abstract

The identification of species boundaries for allopatric populations is important for setting conservation priorities and can affect conservation management decisions. Tuatara (Sphenodon) are the only living members of the reptile order Sphenodontia and are restricted to islands around New Zealand that are free of introduced mammals. We present new data of microsatellite DNA diversity and substantially increased mtDNA sequence for all 26 sampled tuatara populations. We also re-evaluate existing allozyme data for those populations, and together use them to examine the taxonomic status of those populations. Although one could interpret the data to indicate different taxonomic designations, we conclude that, contrary to current taxonomy, Sphenodon is best described as a single species that contains distinctive and important geographic variants. We also examine amounts of genetic variation within populations and discuss the implications of these findings for the conservation management of this iconic taxon.

Keywords

Microsatellite DNA Mitochondrial DNA Allozymes Phylogenetics Taxonomy Conservation 

Supplementary material

10592_2009_9952_MOESM1_ESM.pdf (141 kb)
Supplementary material 1 (PDF 140 kb)

References

  1. Aitken N, Hay JM, Sarre SD et al (2001) Microsatellite DNA markers for tuatara (Sphenodon spp.). Conserv Genet 2:183–185CrossRefGoogle Scholar
  2. Allendorf FW (2001) Genetics and viability of insular populations of reptiles. N Z J Zool 28:361Google Scholar
  3. Allendorf FW, Leary RF (1988) Conservation and distribution of genetic variation in a polytypic species, the cutthroat trout. Conserv Biol 2:170–184CrossRefGoogle Scholar
  4. Allendorf FW, Luikart G (2007) Conservation and the genetics of populations. Blackwell, MaldenGoogle Scholar
  5. Anonymous (1987) Tuatara traded for drugs. Oryx 21:125Google Scholar
  6. Apesteguía S, Novas FE (2003) Large Cretaceous sphenodontian from Patagonia provides insight into lepidosaur evolution in Gondwana. Nature 425:609–612CrossRefPubMedGoogle Scholar
  7. Bandelt H-J, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48PubMedGoogle Scholar
  8. Benton MJ (1993) The fossil record 2. Chapman & Hall, LondonGoogle Scholar
  9. Benton MJ (2000) Vertebrate palaeontology, 2nd edn. Blackwell, OxfordGoogle Scholar
  10. Bowcock AM, Ruíz-Linares A, Tomfohrde J et al (1994) High resolution human evolutionary trees with polymorphic microsatellites. Nature 368:455–457CrossRefPubMedGoogle Scholar
  11. Brehm A, Harris DJ, Alves C, Jesus J, Thomarat F, Vicente L (2003) Structure and evolution of the mitochondrial DNA complete control region in the lizard Lacerta dugesii (Lacertidae, Sauria). J Mol Evol 56:46–53CrossRefPubMedGoogle Scholar
  12. Brook FJ, McArdle BH (1999) Morphological variation, biogeography and local extinction of the northern New Zealand landsnail Placostylus hongii (Gastropoda: Bulimulidae). J R Soc N Z 29:407–434Google Scholar
  13. Buller WL (1877) Notes on the tuatara lizard (Sphenodon punctatum), with a description of a supposed new species. Trans Proc N Z Inst 1876(9):317–325Google Scholar
  14. Buller WL (1878) Notice of a new variety of tuatara lizard (Sphenodon) from East Cape Island. Trans Proc N Z Inst 1877(10):220–221Google Scholar
  15. Buller WL (1879) Further notes on the habits of the tuatara lizard. Trans Proc N Z Inst 1878(11):349–351Google Scholar
  16. Cavalli-Sforza LL, Edwards AWF (1967) Phylogenetic analysis: models and estimation procedures. Am J Hum Genet 19:233–257PubMedGoogle Scholar
  17. 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
  18. Cree A, Butler D (1993) Tuatara recovery plan (Sphenodon spp.). Threatened species recovery plan series no. 9. New Zealand Department of Conservation, WellingtonGoogle Scholar
  19. Daugherty CH, Cree A, Hay JM, Thompson MB (1990) Neglected taxonomy and continuing extinctions of tuatara (Sphenodon). Nature 347:177–179CrossRefGoogle Scholar
  20. Daugherty CH, Towns DR, Cree A, Hay JM (1992) The roles of legal protection versus intervention in conserving the New Zealand tuatara, Sphenodon. Dev Landsc Manag Urb Plan 7:247–259Google Scholar
  21. Dawbin WH (1962) The tuatara in its natural habitat. Endeavour 21:16–24CrossRefGoogle Scholar
  22. Dieringer D, Schlötterer C (2003) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 3:167–169CrossRefGoogle Scholar
  23. Duncan RP, Blackburn TM, Worthy TH (2002) Prehistoric bird extinctions and human hunting. Proc R Soc Lond B Biol Sci 269:517–521CrossRefGoogle Scholar
  24. Excoffier L, Smouse P, Quattro J (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedGoogle Scholar
  25. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50PubMedGoogle Scholar
  26. Felsenstein J (2005) PHYLIP (phylogeny inference package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, SeattleGoogle Scholar
  27. Finch MO, Lambert DM (1996) Kinship and genetic divergence among populations of tuatara Sphenodon punctatus as revealed by minisatellite DNA profiling. Mol Ecol 5:651–658CrossRefGoogle Scholar
  28. Frankham R (1996) Relationship of genetic variation to population size in wildlife. Conserv Biol 10:1500–1508CrossRefGoogle Scholar
  29. Fraser WM (1925) The Poor Knights Islands: a brief account of the Maori occupation. N Z J Sci Technol 8:8–14Google Scholar
  30. Gaggiotti OE, Lange O, Rassmann K, Gliddon C (1999) A comparison of two indirect methods for estimating average levels of gene flow using microsatellite data. Mol Ecol 8:1513–1520CrossRefPubMedGoogle Scholar
  31. Gaze P (2001) Tuatara recovery plan 2001–2011. Threatened species recovery plan series no. 47. New Zealand Department of Conservation, WellingtonGoogle Scholar
  32. Goldstein DB, Ruiz Linares A, Cavalli-Sforza LL, Feldman MW (1995) Genetic absolute dating based on microsatellites and the origin of modern humans. Proc Natl Acad Sci USA 92:6723–6727CrossRefPubMedGoogle Scholar
  33. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3.2). Available via http://www.unil.ch/izea/softwares/fstat.html Accessed Feb 2002
  34. Goudet J, Raymond M, Demeeus T, Rousset F (1996) Testing differentiation in diploid populations. Genetics 144:1933–1940PubMedGoogle Scholar
  35. Hanley TC, Caccone A (2005) Development of primers to characterize the mitochondrial control region of Galápagos land and marine iguanas (Conolophus and Amblyrynchus). Mol Ecol Notes 5:599–601CrossRefGoogle Scholar
  36. Hay JM, Daugherty CH, Cree A, Maxson LR (2003) Low genetic divergence obscures phylogeny among populations of Sphenodon, remnant of an ancient reptile lineage. Mol Phylogenet Evol 29:1–19CrossRefPubMedGoogle Scholar
  37. Hay JM, Sarre S, Daugherty CH (2004) Nuclear mitochondrial pseudogenes as molecular outgroups for phylogenetically isolated taxa: a case study in Sphenodon. Heredity 93:468–475CrossRefPubMedGoogle Scholar
  38. Hayward BW (1986) Origin of the offshore islands of northern New Zealand and their landform development. The offshore islands of Northern New Zealand, New Zealand Department of Lands and Survey information series 16, New Zealand Department of Lands and Survey, Wellington, New Zealand, pp 129–138Google Scholar
  39. Hayward BW (1991) Geology and geomorphology of the Poor Knights Islands, northern New Zealand. Tane 33:23–37Google Scholar
  40. Keogh JS, Scott IAW, Hayes C (2005) Rapid and repeated origin of insular gigantism and dwarfism in Australian tiger snakes. Evolution 59:226–233PubMedGoogle Scholar
  41. King M (2003) The penguin history of New Zealand. Penguin Books, AucklandGoogle Scholar
  42. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinformatics 5:150–163CrossRefPubMedGoogle Scholar
  43. Lande R (1999) Extinction risks from anthropogenic, ecological and genetic factors. In: Landweber LF, Dobson AP (eds) Genetics and the extinction of species: DNA and the conservation of biodiversity. Princeton University Press, PrincetonGoogle Scholar
  44. Leberg PL (1992) Effects of population bottlenecks on genetic diversity as measured by allozyme electrophoresis. Evolution 46:477–494CrossRefGoogle Scholar
  45. Luikart G, Cornuet JM (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237CrossRefGoogle Scholar
  46. Luikart G, Allendorf FW, Cornuet JM, Sherwin WB (1998a) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89:238–247CrossRefPubMedGoogle Scholar
  47. Luikart G, Sherwin WB, Steele BM, Allendorf FW (1998b) Usefulness of molecular markers for detecting population bottlenecks via monitoring genetic change. Mol Ecol 7:963–974CrossRefPubMedGoogle Scholar
  48. MacAvoy ES, McGibbon LM, Sainsbury JP et al (2007) Genetic variation in island populations of tuatara (Sphenodon spp.) inferred from microsatellite markers. Conserv Genet 8:305–318CrossRefGoogle Scholar
  49. Mayr E (1963) Animal species and evolution. Belknap Press of Harvard University Press, CambridgeGoogle Scholar
  50. Menozzi P, Piazza A, Cavalli-Sforza L (1978) Synthetic maps of human gene frequencies in Europeans. Science 201:786–792CrossRefPubMedGoogle Scholar
  51. Moore JA, Nelson NJ, Keall SN, Daugherty CH (2008) Implications of social dominance and multiple paternity for the genetic diversity of a captive-bred reptile population (tuatara). Conserv Genet 9:1243–1252CrossRefGoogle Scholar
  52. Nei M (1978) Estimation of average heterozygosity and genetic distance from a number of individuals. Genetics 89:538–590Google Scholar
  53. Nei M, Tajima F, Tateno Y (1983) Accuracy of estimated phylogenetic trees from molecular data. J Mol Evol 19:153–170CrossRefPubMedGoogle Scholar
  54. Nelson NJ, Keall SN, Brown D, Daugherty CH (2002a) Establishing a new wild population of tuatara (Sphenodon guntheri). Conserv Biol 16:887–894CrossRefGoogle Scholar
  55. Nelson NJ, Keall SN, Pledger S, Daugherty CH (2002b) Male-biased sex ratio in a small tuatara population. J Biogeogr 29:633–640CrossRefGoogle Scholar
  56. Newman DG (1986) Can tuatara and mice co-exist? The status of tuatara, Sphenodon punctatus (Reptilia: Rhynchocephalia), on the Whangamata Islands. The offshore islands of New Zealand, New Zealand Department of Lands and Survey information series 16, New Zealand Department of Lands and Survey, Wellington, New Zealand, pp 179–185Google Scholar
  57. Paetkau D, Calvert W, Stirling I, Strobeck C (1995) Microsatellite analysis of population structure in Canadian polar bears. Mol Ecol 4:347–354CrossRefPubMedGoogle Scholar
  58. Paetkau D, Waits LP, Clarkson PL, Craighead L, Strobeck C (1997) An empirical evaluation of genetic distance statistics using microsatellite data from bear (Ursidae) populations. Genetics 147:1943–1957PubMedGoogle Scholar
  59. Parent CE, Caccone A, Petren K (2008) Colonization and diversification of Galápagos terrestrial fauna: a phylogenetic and biogeographical synthesis. Proc R Soc B 363:3347–3361Google Scholar
  60. Paterson H (2005) The competitive Darwin. Paleobiology 31:56–76CrossRefGoogle Scholar
  61. Piry S, Luikart G, Cornuet J-M (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503CrossRefGoogle Scholar
  62. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818CrossRefPubMedGoogle Scholar
  63. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  64. Reich D, Price AL, Patterson N (2008) Principal component analysis of genetic data. Nat Genet 40:491–492CrossRefPubMedGoogle Scholar
  65. Rest JS, Ast JC, Austin CC et al (2003) Molecular systematics of primary reptilian lineages and the tuatara mitochondrial genome. Mol Phylogenet Evol 29:289–297CrossRefPubMedGoogle Scholar
  66. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  67. Ryder OA (1986) Species conservation and systematics: the dilemma of subspecies. Trends Ecol Evol 1:9–10CrossRefGoogle Scholar
  68. Sarre SD, Schwaner T, Georges A (1990) Genetic variation among insular populations of the sleepy lizard, Trachydosaurus rugosus gray (Squamata: Scincidae). Aust J Zool 38:603–616CrossRefGoogle Scholar
  69. Schneider S, Roessli D, Excoffier L (2000) Arlequin ver. 2.000: a software for population genetic data analysis. Genetics and Biometry Laboratory, University of Geneva, SwitzerlandGoogle Scholar
  70. Soulé M, Yang SY (1973) Genetic variation in side-blotched lizards on islands in the Gulf of California. Evolution 27:593–600CrossRefGoogle Scholar
  71. Subramanian S, Hay JM, Mohandesan E, Millar CD, Lambert DM (2008) Molecular and morphological evolution in tuatara are decoupled. Trends in Genetics 25:16–18CrossRefGoogle Scholar
  72. Swofford DL (2003) PAUP* phylogenetic analysis using parsimony (*and other methods) Version 4. Sinauer Associates, SunderlandGoogle Scholar
  73. Terrasa B, Pérez-Mellado V, Brown RP, Picornell A, Castro JA, Ramon MM (2009) Foundations for conservation of intraspecific genetic diversity revealed by analysis of phylogeographical structure in the endangered endemic lizard Podarcis lilfordi. Divers Distrib 15:207–221CrossRefGoogle Scholar
  74. Waples RS (1991) Pacific salmon, Onchorhynchus spp., and the definition of ‘species’ under the endangered species act. Mar Fish Rev 53:11–22Google Scholar
  75. Waser PM, Strobeck C (1998) Genetic signatures of interpopulation dispersal. Trends Ecol Evol 13:43–44CrossRefGoogle Scholar
  76. Whitaker AH (1968) The lizards of the Poor Knights Islands, New Zealand. N Z J Sci 11:623–651Google Scholar
  77. Whittaker RJ, Triantis KA, Ladle RJ (2008) A general dynamic theory of oceanic island biogeography. J Biogeogr 35:977–994CrossRefGoogle Scholar
  78. Wilson AC, Cann RL, Carr SM et al (1985) Mitochondrial DNA and two perspectives on evolutionary genetics. Biol J Linn Soc Lond 26:375–400CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Jennifer M. Hay
    • 1
  • Stephen D. Sarre
    • 2
  • David M. Lambert
    • 3
  • Fred W. Allendorf
    • 4
  • Charles H. Daugherty
    • 5
  1. 1.Allan Wilson Centre for Molecular Ecology and Evolution at Institute of Molecular BioSciencesMassey UniversityAucklandNew Zealand
  2. 2.Institute for Applied EcologyUniversity of CanberraCanberraAustralia
  3. 3.Griffith School of EnvironmentGriffith UniversityNathanAustralia
  4. 4.Division of Biological SciencesUniversity of MontanaMissoulaUSA
  5. 5.School of Biological SciencesVictoria University of WellingtonWellingtonNew Zealand

Personalised recommendations