Skip to main content

Advertisement

SpringerLink
Log in

Inbreeding and promiscuity in the endangered grand skink

  • Published:
Conservation Genetics Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Amos W, Balmford A (2001) When does conservation genetics matter? Heredity 87: 257–265

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Berry O, Gleeson DM, Sarre SD (2003) Microsatellite DNA markers for New Zealand skinks. Conservation Genetics 4: 411–414

    Article  CAS  Google Scholar 

  • 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: 855–864

    Article  Google Scholar 

  • Berry O, Tocher MD, Sarre SD (2004) Can assignment tests measure dispersal? Molecular Ecology 13: 551–561

    Article  PubMed  Google Scholar 

  • Caughley G (1994) Directions in conservation biology. Journal of Animal Ecology 63: 215–244

    Article  Google Scholar 

  • Cockburn A, Scott MP, Scott D (1985) Inbreeding avoidance and male-biased dispersal in Antechinus spp. (Marsupalia: Dasyuridae). Animal Behaviour 33: 908–915

    Article  Google Scholar 

  • Cree A (1994) Low annual reproductive output in female reptiles from New Zealand. New Zealand Journal of Zoology 21: 351–372

    Google Scholar 

  • Duarte LC, Bouteiller C, Fontanillas P, Petit E, Perrin N (2003) Inbreeding in the greater white-toothed shrew, Crocidura russula. Evolution 57: 638–645

    PubMed  CAS  Google Scholar 

  • Earnhardt JM, Thompson SD, Schad K (2004) Strategic planning for captive populations: projecting changes in genetic diversity. Animal Conservation 7: 9–16

    Article  Google Scholar 

  • Elgar MA, Clode D (2001) Inbreeding and extinction in island populations: a cautionary tale. Conservation Biology 15: 284–286

    Article  Google Scholar 

  • Falconer DS (1989) Introduction to Quantitative Genetics (3rd. edition) Longman, London

    Google Scholar 

  • 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, 127–132

    Google Scholar 

  • Fisher RA (1930) The Genetical Theory of Natural Selection. Dover Publications, New York

    Google Scholar 

  • Frankham R (1995) Conservation genetics. Annual Review of Genetics 29: 305–327

    Article  PubMed  CAS  Google Scholar 

  • Frankham R (2001) Inbreeding and extinction in island populations: reply to Elgar and Clode. Conservation Biology 15: 287–289

    Article  Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2002) Introduction to Conservation Genetics Cambridge University Press, Cambridge, U.K

    Google Scholar 

  • Frankham R, Ralls K (1998) Inbreeding leads to extinction. Nature, London 392, 441–442

    Article  CAS  Google Scholar 

  • Franklin IR, Frankham R (1998) How large must populations be to retain evolutionary potential? Animal Conservation 1: 69–73

    Article  Google Scholar 

  • 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: 175–183

    Article  PubMed  CAS  Google Scholar 

  • Gibbs HL, Grant PR (1989) Inbreeding in Darwin’s medium ground finches (Geospiza fortis). Evolution 43: 1273–1284

    Article  Google Scholar 

  • Goodnight KF, Queller DC (1999) Computer software for performing likelihood tests of pedigree relationship using genetic markers. Molecular Ecology 8: 1231–1234

    Article  PubMed  Google Scholar 

  • Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Animal Behaviour 28: 1140–1162

    Article  Google Scholar 

  • 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: 113–120

    Article  Google Scholar 

  • Harvey PH, Ralls K (1986) Do animals avoid incest? Nature 320: 575–576

    Article  Google Scholar 

  • Hedrick PW, Kalinowski ST (2000) Inbreeding depression in conservation biology. Annual Review of Ecology and Systematics 31: 139–162

    Article  Google Scholar 

  • Hood G (2002) Poptools 2.5.3

  • Johnson ML, Gaines MS (1990) Evolution of dispersal: theoretical models and empirical tests using birds and mammals. Annual Review of Ecology and Systematics 21: 449–480

    Article  Google Scholar 

  • Keane B, Creel SR, Waser PM (1996) No evidence of inbreeding avoidance or inbreeding depression in a social carnivore. Behavioral Ecology 7: 480–489

    Article  CAS  Google Scholar 

  • Keller LF, Arcese P (1998) No evidence for Inbreeding avoidance in a natural population of song sparrows (Melospiza melodia). The American Naturalist 152: 380–392

    Article  Google Scholar 

  • Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends in Ecology & Evolution 17: 230–241

    Article  Google Scholar 

  • Koenig WD, Vuren DV, Hooge PN (1996) Detectability, philopatry, and the distribution of dispersal distances in vertebrates. Trends in Ecology & Evolution 11: 514–517

    Article  Google Scholar 

  • 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. 262–276

    Google Scholar 

  • Lande R, Shannon S (1996) The role of genetic variation in adaptation and population persistence in a changing environment. Evolution 50: 434–437

    Article  Google Scholar 

  • Lehmann L, Perrin N (2003) Inbreeding avoidance through kin recognition: choosy females boost male dispersal. American Naturalist 162: 638–655

    Article  PubMed  Google Scholar 

  • Léna J, De Fraipont M, Clobert J (2000) Affinity towards maternal odour and offspring dispersal in the common lizard. Ecology Letters 3: 300–308

    Article  Google Scholar 

  • Lynch M, Conery J, Bürger R (1995) Mutational meltdowns in sexual populations. Evolution 49: 1067–1080

    Article  Google Scholar 

  • Marshall TC, Slate J, Kruuk LEB, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Molecular Ecology 7: 639–655

    Article  PubMed  CAS  Google Scholar 

  • 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 Otago

  • 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. 115

  • 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: 229–242

    Article  Google Scholar 

  • 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. 503–564

    Chapter  Google Scholar 

  • Olsson M, Shine R, Madsen T, Gullberg A, Tegelstrom H (1996b) Sperm selection by females. Nature 383: 585

    Article  CAS  Google Scholar 

  • 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. 243–261

    Google Scholar 

  • Pusey A, Wolf M (1996) Inbreeding avoidance in animals. Trends in Ecology & Evolution 11: 201–206

    Article  Google Scholar 

  • Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43: 258–275

    Article  Google Scholar 

  • Queller DC, Strassmann JE, Hughes CR (1993) Microsatellites and kinship. Trends in Ecology & Evolution 8: 285–288

    Article  Google Scholar 

  • Ralls K, Ballou JD, Templeton A (1988) Estimates of lethal equivalents and the cost of inbreeding in mammals. Conservation Biology 2: 185–193

    Article  Google Scholar 

  • 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.

  • 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. 143–169

    Google Scholar 

  • Stanley MC (1998) Homing in the skink, Oligosoma grande, within a fragmented habitat. Journal of Herpetology 32: 461–464

    Article  Google Scholar 

  • Stow AJ, Sunnucks P (2004) Inbreeding avoidance in Cunningham’s skinks (Egernia cunninghami) in natural and fragmented habitat. Mol. Ecol. 13, 443–447

    Google Scholar 

  • 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: 510–524

    PubMed  CAS  Google Scholar 

  • Tainaka K, Itoh Y (1996) Glass effect in inbreeding-avoidance systems - minimum viable population for outbreeders. Journal of the Physical Society of Japan 65: 3379–3385

    Article  CAS  Google Scholar 

  • 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, Chicago

    Google Scholar 

  • Waldman B, Rice JE, Honeycutt RL (1992) Kin recognition and incest avoidance in toads. American Zoologist 32: 18–30

    Google Scholar 

  • Waser PM, Austad SN, Keane B (1986) When should animals tolerate inbreeding? The American Naturalist 128: 529–537

    Article  Google Scholar 

  • Wheelwright NT, Mauck RA (1998) Philopatry, natal dispersal, and inbreeding avoidance in an island population of savannah sparrows. Ecology 79: 755–767

    Article  Google Scholar 

  • 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.

  • Zar JH (1996) Biostatistical Analysis, Third edn. Prentice-Hall, London

    Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. School of Animal Biology, University of Western Australia, 35 Stirling Highway, Crawley, Perth, 6009, WA, Australia

    Oliver Fleetwood Berry

Authors
  1. Oliver Fleetwood Berry
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Oliver Fleetwood Berry.

Appendix

Appendix

Appendix 1. Parameters used in the simulation for parentage analysis using CERVUS 2.0.
Full size table

Rights and permissions

Reprints and permissions

About this article

Cite this article

Berry, O.F. Inbreeding and promiscuity in the endangered grand skink. Conserv Genet 7, 427–437 (2006). https://doi.org/10.1007/s10592-005-9054-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-005-9054-0

Keywords

Search

Navigation