Conservation Genetics

, Volume 7, Issue 3, pp 427–437 | Cite as

Inbreeding and promiscuity in the endangered grand skink

Article

Abstract

The inbreeding avoidance hypothesis predicts that organisms that often encounter relatives as potential mates should evolve behaviours to avoid incestuous matings. Avoidance behaviours have practical importance for small populations because deleterious genetic processes may be less imminent than otherwise expected from genetic models that assume random mating. I used genetic techniques to investigate the extent of inbreeding and inbreeding avoidance behaviours in rare lizards from southern New Zealand. Grand skinks, Oligosoma grande, live in small patchily distributed groups, and have low rates of inter-group dispersal (ca. 3–20% disperse). I used data from 15 microsatellite loci to test the hypothesis that adults are likely to encounter kin as potential mates and will inbreed. These data showed that adult skinks usually inhabited rock outcrops with adult relatives of the opposite sex – up to 35% of potential mates were of equivalent relatedness as half-sibs and 17% were equivalent to full sibs. However, skinks did not preferentially breed with less related mates, and 18.2% of matings were between individuals of equivalent relatedness as full-sibs. Instead, skinks mated with partners of all levels of relatedness, and were promiscuous – almost half of adult females and nearly three quarters of adult males reproduced with multiple partners. In addition, inbreeding had no effect on survival of offspring in their first year. Two other putative mechanisms of inbreeding avoidance, sex-biased and natal dispersal, were not pronounced in this species. This study adds to a growing list of species that inbreed despite the risks.

Keywords

habitat fragmentation inbreeding offspring survival Oligosoma grande skink 

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Notes

Acknowledgements

I thank Jeroen Spitzen, Annemarieke van der Sluijs, and Amanda Smale for assistance with skink catching. Dave Houston and Graeme Loh provided valuable skink-related discussions. Stephen Sarre, Dianne Gleeson, and Tash Lebas provided helpful comments on the manuscript, as did two anonymous referees. Thanks also to Paul Sunnucks for the Mac SE/30, Keith Goodnight for advice on the use of likelihood ratios, and Bill Amos for the IR macro.

References

  1. Amos W, Balmford A (2001) When does conservation genetics matter? Heredity 87: 257–265CrossRefPubMedGoogle Scholar
  2. Amos W, Worthington Wilmer J, Fullard K, et al. (2001) The influence of parental relatedness on reproductive success. Proc. Roy. Soc. Lond. B. 268, 2021–2027.Google Scholar
  3. Berry O, Gleeson DM, Sarre SD (2003) Microsatellite DNA markers for New Zealand skinks. Conservation Genetics 4: 411–414CrossRefGoogle Scholar
  4. Berry O, Tocher M, Gleeson D, Sarre S (2005) Effects of vegetation matrix on animal dispersal: genetic evidence from a study of endangered skinks. Conservation Biology 19: 855–864CrossRefGoogle Scholar
  5. Berry O, Tocher MD, Sarre SD (2004) Can assignment tests measure dispersal? Molecular Ecology 13: 551–561CrossRefPubMedGoogle Scholar
  6. Caughley G (1994) Directions in conservation biology. Journal of Animal Ecology 63: 215–244CrossRefGoogle Scholar
  7. Cockburn A, Scott MP, Scott D (1985) Inbreeding avoidance and male-biased dispersal in Antechinus spp. (Marsupalia: Dasyuridae). Animal Behaviour 33: 908–915CrossRefGoogle Scholar
  8. Cree A (1994) Low annual reproductive output in female reptiles from New Zealand. New Zealand Journal of Zoology 21: 351–372Google Scholar
  9. Duarte LC, Bouteiller C, Fontanillas P, Petit E, Perrin N (2003) Inbreeding in the greater white-toothed shrew, Crocidura russula. Evolution 57: 638–645PubMedGoogle Scholar
  10. Earnhardt JM, Thompson SD, Schad K (2004) Strategic planning for captive populations: projecting changes in genetic diversity. Animal Conservation 7: 9–16CrossRefGoogle Scholar
  11. Elgar MA, Clode D (2001) Inbreeding and extinction in island populations: a cautionary tale. Conservation Biology 15: 284–286CrossRefGoogle Scholar
  12. Falconer DS (1989) Introduction to Quantitative Genetics (3rd. edition) Longman, LondonGoogle Scholar
  13. Favre L, Balloux F, Goudet J, Perrin N (1997) Female biased dispersal in the monogamous mammal Crocidura russula: Evidence from field data and microsatellite patterns. Proceedings of the Royal Society of London B. 264, 127–132Google Scholar
  14. Fisher RA (1930) The Genetical Theory of Natural Selection. Dover Publications, New YorkGoogle Scholar
  15. Frankham R (1995) Conservation genetics. Annual Review of Genetics 29: 305–327CrossRefPubMedGoogle Scholar
  16. Frankham R (2001) Inbreeding and extinction in island populations: reply to Elgar and Clode. Conservation Biology 15: 287–289CrossRefGoogle Scholar
  17. Frankham R, Ballou JD, Briscoe DA (2002) Introduction to Conservation Genetics Cambridge University Press, Cambridge, U.KGoogle Scholar
  18. Frankham R, Ralls K (1998) Inbreeding leads to extinction. Nature, London 392, 441–442CrossRefGoogle Scholar
  19. Franklin IR, Frankham R (1998) How large must populations be to retain evolutionary potential? Animal Conservation 1: 69–73CrossRefGoogle Scholar
  20. Gardner MG, Bull CM, Cooper SJB, Duffield GA (2001) Genetic evidence for a family structure in stable social aggregations of the Australian lizard Egernia stokesii. Molecular Ecology 10: 175–183CrossRefPubMedGoogle Scholar
  21. Gibbs HL, Grant PR (1989) Inbreeding in Darwin’s medium ground finches (Geospiza fortis). Evolution 43: 1273–1284CrossRefGoogle Scholar
  22. Goodnight KF, Queller DC (1999) Computer software for performing likelihood tests of pedigree relationship using genetic markers. Molecular Ecology 8: 1231–1234CrossRefPubMedGoogle Scholar
  23. Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Animal Behaviour 28: 1140–1162CrossRefGoogle Scholar
  24. Haikola S, Singer MC, Pen I (2004) Has inbreeding depression led to avoidance of sib mating in the Glanville fritillary butterfly (Melitaea cinxia). Evolutionary Ecology 18: 113–120CrossRefGoogle Scholar
  25. Harvey PH, Ralls K (1986) Do animals avoid incest? Nature 320: 575–576CrossRefGoogle Scholar
  26. Hedrick PW, Kalinowski ST (2000) Inbreeding depression in conservation biology. Annual Review of Ecology and Systematics 31: 139–162CrossRefGoogle Scholar
  27. Hood G (2002) Poptools 2.5.3Google Scholar
  28. Johnson ML, Gaines MS (1990) Evolution of dispersal: theoretical models and empirical tests using birds and mammals. Annual Review of Ecology and Systematics 21: 449–480CrossRefGoogle Scholar
  29. Keane B, Creel SR, Waser PM (1996) No evidence of inbreeding avoidance or inbreeding depression in a social carnivore. Behavioral Ecology 7: 480–489CrossRefGoogle Scholar
  30. Keller LF, Arcese P (1998) No evidence for Inbreeding avoidance in a natural population of song sparrows (Melospiza melodia). The American Naturalist 152: 380–392CrossRefGoogle Scholar
  31. Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends in Ecology & Evolution 17: 230–241CrossRefGoogle Scholar
  32. Koenig WD, Vuren DV, Hooge PN (1996) Detectability, philopatry, and the distribution of dispersal distances in vertebrates. Trends in Ecology & Evolution 11: 514–517CrossRefGoogle Scholar
  33. Komdeur J, Deerenberg C (1997). The importance of social behavior studies for conservation. In: Clemmons JR, Buchholz R (eds). Behavioral approaches to conservation in the wild. Cambridge University Press, CambridgeU.K, pp. 262–276Google Scholar
  34. Lande R, Shannon S (1996) The role of genetic variation in adaptation and population persistence in a changing environment. Evolution 50: 434–437CrossRefGoogle Scholar
  35. Lehmann L, Perrin N (2003) Inbreeding avoidance through kin recognition: choosy females boost male dispersal. American Naturalist 162: 638–655CrossRefPubMedGoogle Scholar
  36. Léna J, De Fraipont M, Clobert J (2000) Affinity towards maternal odour and offspring dispersal in the common lizard. Ecology Letters 3: 300–308CrossRefGoogle Scholar
  37. Lynch M, Conery J, Bürger R (1995) Mutational meltdowns in sexual populations. Evolution 49: 1067–1080CrossRefGoogle Scholar
  38. Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Molecular Ecology 7: 639–655CrossRefPubMedGoogle Scholar
  39. Middlemiss A (1995) Predation of lizards by feral house cats (Felis catus) and ferrets (Mustela furo) in the tussock grasslands of Otago. M.Sc. thesis, University of OtagoGoogle Scholar
  40. Murphy TJ (1994) Activity rhythms, microhabitat selection, home range and social communication in grand skinks (Leiolopisma grande) at Macraes Flat, Central Otago., Rept No. Department of Conservation, Dunedin. p. 115Google Scholar
  41. Olsson M, Gullberg A, Tegelström H (1996a) Malformed offspring, sibling matings, and selection against inbreeding in the sand lizard (Lacerta agilis). Journal of Evolutionary Biology 9: 229–242CrossRefGoogle Scholar
  42. Olsson M, Madsen T (1998). Sexual selection and sperm competition in reptiles. In: Birkhead TR, Moller AP (eds). Sperm Competition and Sexual Selection. Academic Press, London, pp. 503–564CrossRefGoogle Scholar
  43. Olsson M, Shine R, Madsen T, Gullberg A, Tegelstrom H (1996b) Sperm selection by females. Nature 383: 585CrossRefGoogle Scholar
  44. Parker PG, Waite TA (1997). Mating systems, effective population size, and conservation of natural populations. In: Clemmons JR, Buchholz R (eds). Behavioural approaches to conservation in the wild. Cambridge University Press, CambridgeU.K, pp. 243–261Google Scholar
  45. Pusey A, Wolf M (1996) Inbreeding avoidance in animals. Trends in Ecology & Evolution 11: 201–206CrossRefGoogle Scholar
  46. Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43: 258–275CrossRefGoogle Scholar
  47. Queller DC, Strassmann JE, Hughes CR (1993) Microsatellites and kinship. Trends in Ecology & Evolution 8: 285–288CrossRefGoogle Scholar
  48. Ralls K, Ballou JD, Templeton A (1988) Estimates of lethal equivalents and the cost of inbreeding in mammals. Conservation Biology 2: 185–193CrossRefGoogle Scholar
  49. Ralls K, Harvey PH, Lyles AM (1986) Inbreeding in natural populations of birds and mammals. In: Conservation Biology: The Science of Scarcity and Diversity (ed. Soulé ME), pp. 35–56. Sinauer Associates, Sunderland, MA.Google Scholar
  50. Shields WM (1993) The natural and unnatural history of inbreeding and outbreeding. In: Thornhill NW (ed). The Natural History of Inbreeding and Outbreeding: Theoretical and Empirical Perspectives. The University of Chicago Press, Chicago, pp. 143–169Google Scholar
  51. Stanley MC (1998) Homing in the skink, Oligosoma grande, within a fragmented habitat. Journal of Herpetology 32: 461–464CrossRefGoogle Scholar
  52. Stow AJ, Sunnucks P (2004) Inbreeding avoidance in Cunningham’s skinks (Egernia cunninghami) in natural and fragmented habitat. Mol. Ecol. 13, 443–447Google Scholar
  53. Sunnucks P, Hales DF (1996) Numerous transposed sequences of mitochondrial cytochrome oxidase I-II in aphids of the genus Sitobion (Hemiptera: Aphididae). Molecular Biology and Evolution 13: 510–524PubMedGoogle Scholar
  54. Tainaka K, Itoh Y (1996) Glass effect in inbreeding-avoidance systems - minimum viable population for outbreeders. Journal of the Physical Society of Japan 65: 3379–3385CrossRefGoogle Scholar
  55. Waldman B, McKinnon JS (1993) Inbreeding and outbreeding in fishes, amphibians, and reptiles. In: The Natural History of Inbreeding and Outbreeding: Theoretical and Empirical Perspectives (ed. Thornhill NW), pp. 250–282. University of Chicago Press, ChicagoGoogle Scholar
  56. Waldman B, Rice JE, Honeycutt RL (1992) Kin recognition and incest avoidance in toads. American Zoologist 32: 18–30Google Scholar
  57. Waser PM, Austad SN, Keane B (1986) When should animals tolerate inbreeding? The American Naturalist 128: 529–537CrossRefGoogle Scholar
  58. Wheelwright NT, Mauck RA (1998) Philopatry, natal dispersal, and inbreeding avoidance in an island population of savannah sparrows. Ecology 79: 755–767CrossRefGoogle Scholar
  59. Whitaker AH (1996) Impact of agricultural development on grand skink (Oligosoma grande) (Reptilia : scincidae) populations at Macraes Flat, Otago, New Zealand, Rept No. 33. New Zealand Department of Conservation, Wellington. p. 31.Google Scholar
  60. Zar JH (1996) Biostatistical Analysis, Third edn. Prentice-Hall, LondonGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2005

Authors and Affiliations

  1. 1.School of Animal BiologyUniversity of Western AustraliaPerthAustralia

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