Conservation Genetics

, Volume 9, Issue 5, pp 1243–1251 | Cite as

Implications of social dominance and multiple paternity for the genetic diversity of a captive-bred reptile population (tuatara)

  • Jennifer A. Moore
  • Nicola J. Nelson
  • Susan N. Keall
  • Charles H. Daugherty
Research Article

Abstract

Captive breeding is an integral part of many species recovery plans. Knowledge of the genetic mating system is essential for effective management of captive stocks and release groups, and can help to predict patterns of genetic diversity in reintroduced populations. Here we investigate the poorly understood mating system of a threatened, ancient reptile (tuatara) on Little Barrier Island, New Zealand and discuss its impact on the genetic diversity. This biologically significant population was thought to be extinct, due to introduced predators, until 8 adults (4 males, 4 females) were rediscovered in 1991/92. We genotyped these adults and their 121 captively-bred offspring, hatched between 1994 to 2005, at five microsatellite loci. Multiple paternity was found in 18.8% of clutches. Male variance in reproductive success was high with one male dominating mating (77.5% of offspring sired) and one male completely restricted from mating. Little Barrier Island tuatara, although clearly having undergone a demographic bottleneck, are retaining relatively high levels of remnant genetic diversity which may be complemented by the presence of multiple paternity. High variance in reproductive success has decreased the effective size of this population to approximately 4 individuals. Manipulation to equalize founder representation was not successful, and the mating system has thus had a large impact on the genetic diversity of this recovering population. Although population growth has been successful, in the absence of migrants this population is likely at risk of future inbreeding and genetic bottleneck.

Keywords

Sphenodon  Mating system Effective population size Polygyny New Zealand 

References

  1. Aitken N, Hay JM, Sarre SD, Lambert DM, Daugherty CH (2001) Microsatellite DNA markers for tuatara (Sphenodon spp.). Conserv Genet 2:183–185CrossRefGoogle Scholar
  2. Allendorf FW (2001) Genetics and the viability of insular populations of reptiles. NZ J Zool 28:361Google Scholar
  3. Allendorf FW, Luikart G (2007) Conservation and the genetics of populations. Blackwell Publishing, MaldenGoogle Scholar
  4. Anthony LL, Blumstein DT (2000) Integrating behaviour into wildlife conservation: the multiple ways that behaviour can reduce Ne. Biol Conserv 95(3):303–315CrossRefGoogle Scholar
  5. Avise JC, Jones AG, Walker D, DeWoody JA, Collaborators (2002) Genetic mating systems and reproductive natural histories of fishes: Lessons for ecology and evolution. Ann Rev Genet 36:19–45PubMedCrossRefGoogle Scholar
  6. Benton MJ (2000) Vertebrate palaeontology. Blackwell Science, LondonGoogle Scholar
  7. Bretman A, Tregenza T (2005) Measuring polyandry in wild populations: a case study using promiscuous crickets. Mol Ecol 14(7):2169–2179PubMedCrossRefGoogle Scholar
  8. Bull CM (2000) Monogamy in lizards. Behav Proc 51(1–3):7–20CrossRefGoogle Scholar
  9. Calsbeek R, Sinervo B (2004) Within-clutch variation in offspring sex determined by differences in sire body size: cryptic mate choice in the wild. J Evol Biol 17(2):464–470PubMedCrossRefGoogle Scholar
  10. Carmichael CK, Gillingham JC, Keall SN (1989) Feeding ecology of the tuatara (Sphenodon punctatus) on Stephens Island based on niche diversification. NZ J Zool 16:269 (abstract)Google Scholar
  11. Chapple DG, Keogh JS (2005) Complex mating system and dispersal patterns in a social lizard, Egernia whitii. Mol Ecol 14(4):1215–1227PubMedCrossRefGoogle Scholar
  12. Clout MN, Craig JL (1995) The conservation of critically endangered flightless birds in New Zealand. Ibis 1 (supplement 1)Google Scholar
  13. Cree A (1994) Low annual reproductive output in female reptiles from New Zealand. NZ J Zool 21(4):351–372Google Scholar
  14. Cree A, Cockrem JF, Brown MA, Watson PR, Guillette LJ, Newman DG, Chambers GK (1991) Laparoscopy, radiography, and blood analyses as techniques for identifying the reproductive condition of female tuatara. Herpetologica 47(2):238–249Google Scholar
  15. Cree A, Cockrem JF, Guillette Jr. LJ (1992) Reproductive cycles of male and female tuatara (Sphenodon punctatus) on Stephens Island, New Zealand. J Zool 226:199–217CrossRefGoogle Scholar
  16. Cree A, Daugherty CH, Hay JM (1995) Reproduction of a rare New Zealand reptile, the tuatara Sphenodon punctatus, on rat-free and rat-inhabited islands. Conserv Biol 9(2):373–383CrossRefGoogle Scholar
  17. Dakin EE, Avise JC (2004) Microsatellite null alleles in parentage analysis. Heredity 93(5):504–509PubMedCrossRefGoogle Scholar
  18. Daugherty CH, Cree A, Hay JM, Thompson MB (1990) Neglected taxonomy and continuing extinctions of tuatara (Sphenodon). Nature 347(6289):177–179CrossRefGoogle Scholar
  19. Davis LM, Glenn TC, Elsey RM, Dessauer HC, Sawyer RH (2001) Multiple paternity and mating patterns in the American alligator, Alligator mississippiensis. Mol Ecol 10(4):1011–1024PubMedCrossRefGoogle Scholar
  20. Ebenhard T (1995) Conservation breeding as a tool for saving animal species from extinction. Trends Ecol Evol 10(11):438–443CrossRefGoogle Scholar
  21. Eberle M, Kappeler PM (2004) Sex in the dark: determinants and consequences of mixed male mating tactics in Microcebus murinus, a small solitary nocturnal primate. Behav Ecol Sociobiol 57(1):77–90CrossRefGoogle Scholar
  22. Fitze PS, Le Galliard JF, Federici P, Richard M, Clobert J (2005) Conflict over multiple-partner mating between males and females of the polygynandrous common lizards. Evolution 59(11):2451–2459PubMedGoogle Scholar
  23. Fiumera AC, Porter BA, Grossman GD, Avise JC (2002) Intensive genetic assessment of the mating system and reproductive success in a semi-closed population of the mottled sculpin, Cottus bairdi. Mol Ecol 11(11):2367–2377PubMedCrossRefGoogle Scholar
  24. Gibbs HL, Weatherhead PJ, Boag PT, White BN, Tabak LM, Hoysak DJ (1990) Realized reproductive success of polygynous Red-Winged Blackbirds revealed by DNA markers. Science 250(4986):1394–1397PubMedCrossRefGoogle Scholar
  25. Gillingham JC, Carmichael C, Miller T (1995) Social behavior of the tuatara, Sphenodon punctatus. Herpetol Monogr 9:5–16CrossRefGoogle Scholar
  26. Girardet SAB, Veitch CR, Craig JL (2001) Bird and rat numbers on Little Barrier Island, New Zealand, over the period of cat eradication 1976–80. NZ J Zool 28(1):13–29Google Scholar
  27. Gopurenko D, Williams RN, McCormick CR, DeWoody JA (2006) Insights into the mating habits of the tiger salamander (Ambystoma tigrinum tigrinum) as revealed by genetic parentage analyses. Mol Ecol 15:1917–1928PubMedCrossRefGoogle Scholar
  28. Goyache F, Gutierrez JP, Fernandez I, Gomez E, Alvarez I, Diez J, Royo LJ (2003) Using pedigree information to monitor genetic variability of endangered populations: the Xalda sheep breed of Asturias as an example. J Anim Breed Genet 120(2):95–105CrossRefGoogle Scholar
  29. Gutierrez JP, Altarriba J, Diaz C, Quintanilla R, Canon J, Piedrafita J (2003) Pedigree analysis of eight Spanish beef cattle breeds. Genet Sel Evol 35(1):43–63PubMedCrossRefGoogle Scholar
  30. Gutierrez JP, Goyache F (2005) A note on ENDOG: a computer program for analysing pedigree information. J Anim Breed Genet 122(3):172–176PubMedCrossRefGoogle Scholar
  31. 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):1–19PubMedCrossRefGoogle Scholar
  32. Hay JM, Lambert DM (2007) Microsatellite DNA loci identify individuals and provide no evidence for multiple paternity in wild tuatara (Sphenodon: Reptilia). Conserv Genet (in press). doi:10.1007/s10592-007-9445-5 Google Scholar
  33. Hoelzel AR, Le Boeuf BJ, Reiter J, Campagna C (1999) Alpha-male paternity in elephant seals. Behav Ecol Sociobiol 46(5):298–306CrossRefGoogle Scholar
  34. Howard RD, Moorman RS, Whiteman HH (1997) Differential effects of mate competition and mate choice on eastern tiger salamanders. Anim Behav 53:1345–1356PubMedCrossRefGoogle Scholar
  35. Jamieson IG, Quinn JS, Rose PA, White BN (1994) Shared paternity among non-relatives is a result of an egalitarian mating system in a communally breeding bird, the Pukeko. Proc R Soc B 257(1350):271–277CrossRefGoogle Scholar
  36. Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21–64PubMedCrossRefGoogle Scholar
  37. Kimura M, Crow JF (1963) Measurement of effective population number. Evolution 17 (3):279–288Google Scholar
  38. Lee PLM, Hays GC (2004) Polyandry in a marine turtle: females make the best of a bad job. Proc Nat Acad Sci USA 101(17):6530–6535PubMedCrossRefGoogle Scholar
  39. Lenz TL, Jacob A, Wedekind C (2007) Manipulating sex ratio to increase population growth: the example of the Lesser Kestrel. Anim Conserv 10:236–244CrossRefGoogle Scholar
  40. Levitan DR, Petersen C (1995) Sperm limitation in the sea. Trends Ecol Evol 10(6):228–231CrossRefGoogle Scholar
  41. Luikart G, Cornuet JM (1999) Estimating the effective number of breeders from heterozygote excess in progeny. Genetics 151(3):1211–1216PubMedGoogle Scholar
  42. MacAvoy ES, McGibbon LM, Sainsbury JP, Lawrence H, Wilson CA, Daugherty CH, Chambers GK (2007) Genetic variation in island populations of tuatara (Sphenodon spp) inferred from microsatellite markers. Conserv Genet 8(2):305–318CrossRefGoogle Scholar
  43. Madsen T, Shine R, Loman J, Hakansson T (1992) Why do female adders copulate so frequently. Nature 355(6359):440–441CrossRefGoogle Scholar
  44. Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7(5):639–655PubMedCrossRefGoogle Scholar
  45. Miller HC, Andrews-Cookson M, Daugherty CH (2007) Two patterns of variation among MHC class I loci in tuatara (Sphenodon punctatus). J Hered (in press). doi:10.1093/jhered/esm095 PubMedGoogle Scholar
  46. Morrison SF, Keogh JS, Scott IAW (2002) Molecular determination of paternity in a natural population of the multiply mating polygynous lizard Eulamprus heatwolei. Mol Ecol 11(3):535–545PubMedCrossRefGoogle Scholar
  47. Nelson NJ, Cree A, Thompson MB, Keall SN, Daugherty CH (2004) Temperature-dependent sex determination in tuatara. In: Valenzuela N, Lance V (eds) Temperature dependent sex determination in vertebrates, Smithsonian Books, Washington, D.CGoogle Scholar
  48. Nelson NJ, Keall SN, Brown D, Daugherty CH (2002) Establishing a new wild population of tuatara (Sphenodon guntheri). Conserv Biol 16(4):887–894CrossRefGoogle Scholar
  49. Olsson M, Shine R (1997) Advantages of multiple matings to females: A test of the infertility hypothesis using lizards. Evolution 51(5):1684–1688CrossRefGoogle Scholar
  50. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6(1):288–295CrossRefGoogle Scholar
  51. Pearse DE, Avise JC (2001) Turtle mating systems: behavior, sperm storage, and genetic paternity. J Hered 92(2):206–211PubMedCrossRefGoogle Scholar
  52. Penn DJ, Potts WK (1999) The evolution of mating preferences and major histocompatibility complex genes. Am Nat 153(2):145–164CrossRefGoogle Scholar
  53. Pudovkin AI, Zaykin DV, Hedgecock D (1996) On the potential for estimating the effective number of breeders from heterozygote excess in progeny. Genetics 144(1):383–387PubMedGoogle Scholar
  54. Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43(2):258–275CrossRefGoogle Scholar
  55. Ralls K, Ballou J (1986) Captive breeding programs for populations with a small number of founders. Trends Ecol Evol 1(1):19–22CrossRefGoogle Scholar
  56. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  57. Reischek A (1886) Observations on Sphenodon punctatum, fringe-back lizard (tuatara). Trans Proc NZ Inst 18:108–110Google Scholar
  58. Reynolds JD (1996) Animal breeding systems. Trends Ecol Evol 11(2):68–72CrossRefGoogle Scholar
  59. Roberts SC, Gosling LM (2003) Genetic similarity and quality interact in mate choice decisions by female mice. Nature Genet 35(1):103–106PubMedCrossRefGoogle Scholar
  60. Saint Girons H (1983) The tuatara: ecological features and some hypotheses concerning its evolution. Bull Soc Zool Fr 108:631–634Google Scholar
  61. Salvador A, Veiga JP (2001) Male traits and pairing success in the lizard Psammodromus algirus. Herpetologica 57(1):77–86Google Scholar
  62. Sambrook J, Fritsch E, Maniatis T (1989) Molecular cloning. A laboratory manual. Cold spring harbor laboratory press, Cold Springs HarborGoogle Scholar
  63. Sarrazin F, Barbault R (1996) Reintroduction: challenges and lessons for basic ecology. Trends Ecol Evol 11(11):474–478CrossRefGoogle Scholar
  64. 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(2):338–348CrossRefGoogle Scholar
  65. Sugg DW, Chesser RK (1994) Effective population sizes with multiple paternity. Genetics 137(4):1147–1155PubMedGoogle Scholar
  66. Waples RS (1989) A generalized approach for estimating effective population size from temporal changes in allele frequency. Genetics 121(2):379–391PubMedGoogle Scholar
  67. Whitaker AH (1993) Research on the tuatara (Sphenodon punctatus) of Little Barrier Island, 6–20 October 1992. Page 52. Unpublished report, Auckland Conservancy, New Zealand department of conservation, AucklandGoogle Scholar
  68. Whitaker AH, Daugherty CH (1991) Research on the tuatara (Sphenodon punctatus) of Little Barrier Island, 5–12 February 1991. Page 54. Unpublished report, Auckland Conservancy, New Zealand Department of Conservation, AucklandGoogle Scholar
  69. Xu QH, Fang SG, Wang ZP, Wang ZW (2005) Microsatellite analysis of genetic diversity in the Chinese alligator (Alligator sinensis) Changxing captive population. Conserv Genet 6(6):941–951CrossRefGoogle Scholar
  70. Zamudio KR, Sinervo E (2000) Polygyny, mate-guarding, and posthumous fertilization as alternative male mating strategies. Proc Nat Acad Sci USA 97(26):14427–14432PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Jennifer A. Moore
    • 1
  • Nicola J. Nelson
    • 1
  • Susan N. Keall
    • 1
  • Charles H. Daugherty
    • 1
  1. 1.Allan Wilson Centre, School of Biological SciencesVictoria University of WellingtonWellingtonNew Zealand

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