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Conservation Genetics

, Volume 15, Issue 5, pp 1013–1020 | Cite as

Combining genetic data to identify relatedness among founders in a genetically depauperate parrot, the Kakapo (Strigops habroptilus)

  • Laura M. Bergner
  • Ian G. Jamieson
  • Bruce C. Robertson
Research Article

Abstract

Small populations that have experienced a bottleneck often suffer from low genetic diversity and inbreeding, the effects of which may further threaten persistence over time. The iconic Kakapo (Strigops habroptilus) is an endemic parrot of New Zealand, which was nearly driven to extinction by introduced predators and has subsequently experienced a severe bottleneck of 60 individuals. The population has since recovered to 125 individuals, but exhibits high hatching failure and other signs of inbreeding depression. Previous studies have indicated that contemporary Kakapo possess low genetic diversity, thus maintaining existing genetic diversity is high priority in Kakapo management. The future plans are to manage Kakapo using a pedigree-based system. An assumption common to most pedigrees is that founding individuals are unrelated. However, this is unlikely to be the case for Kakapo, as most founders originate from a small area of Stewart Island. Therefore the goal of this study was to examine the current Kakapo founders for potential relationships using several molecular techniques. Founders were genotyped at 25 microsatellites, which were used to generate relatedness estimates and assign relationships. 94 pedigree relationships were identified among founders comprising full sibling and half sibling pairs, as well as 110 with high pairwise relatedness values indicating likely close relationships. These relationships, along with mtDNA control region haplotypes, were combined to inform the pedigree. The improved pedigree will be used to manage the Kakapo population genetically through artificial insemination and planned matings.

Keywords

Inbreeding Microsatellites mtDNA control region Pedigree Relatedness Sibship inference 

Notes

Acknowledgements

We are grateful to the New Zealand Department of Conservation for collecting samples and assisting with pedigree information, particularly R. Moorhouse and D. Eason. Microsatellite genotyping was done by BCR, F. Robertson and K. Ludwig. T. King also provided assistance with laboratory work. Funding for this research was provided by the Allan Wilson Centre (IGJ) and the Department of Conservation Kakapo Recovery Group (BCR). LMB was supported by a US Fulbright Graduate Student Award.

Supplementary material

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Supplementary material 1 (PDF 92 kb)
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Supplementary material 2 (PDF 38 kb)
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Supplementary material 3 (PDF 70 kb)
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Supplementary material 4 (PDF 41 kb)
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Supplementary material 5 (PDF 29 kb)

References

  1. Ballard JWO, Whitlock MC (2004) The incomplete natural history of mitochondria. Mol Ecol 13:729–744PubMedCrossRefGoogle Scholar
  2. Ballou JD, Lacy RC (1995) Identifying genetically important individuals for management of genetic variation in pedigreed populations. In: Ballou JD, Gilpin M, Foose TJ (eds) Population management for survival and recovery. Columbia University Press, New York, pp 76–111Google Scholar
  3. Blouin MS (2003) DNA-based methods for pedigree reconstruction and kinship analysis in natural populations. Trends Ecol Evol 18:503–511CrossRefGoogle Scholar
  4. Csillery K, Johnson T, Beraldi D et al (2006) Performance of marker-based relatedness estimators in natural populations of outbred vertebrates. Genetics 173:2091–2101PubMedCrossRefPubMedCentralGoogle Scholar
  5. Eason DK, Elliott GP, Merton DV, Jansen PW, Harper GA, Moorhouse RJ (2006) Breeding biology of kakapo (Strigops habroptilus) on offshore island sanctuaries, 1990–2002. Notornis 53:27–36Google Scholar
  6. Elliott GP, Merton DV, Jansen PW (2001) Intensive management of a critically endangered species: the kakapo. Biol Conserv 99:121–133CrossRefGoogle Scholar
  7. Ewing SR, Nager RG, Nicoll MAC, Aumjaud A, Jones CG, Keller LF (2008) Inbreeding and loss of genetic variation in a reintroduced population of Mauritius kestrel. Conserv Biol 22:395–404PubMedCrossRefGoogle Scholar
  8. Frankham R, Ballou JD, Briscoe DA (2010) Introduction to conservation genetics, 2nd edn. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  9. Gautschi B, Jacob G, Negro JJ, Godoy JA, Mullar JP, Schmid B (2003) Analysis of relatedness and determination of the source of founders in the captive bearded vulture, Gypaetus barbatus, population. Conserv Genet 4:479–490CrossRefGoogle Scholar
  10. Goncalves da Silva A, Lalonde DR, Quse V, Shoemaker A, Russello MA (2010) Genetic approaches refine ex situ Lowland Tapir (Tapirus terrestris) conservation. J Hered 101:581–590PubMedCrossRefGoogle Scholar
  11. Grueber CE, Jamieson IG (2008) Quantifying and managing the loss of genetic variation in a free-ranging population of takahe through the use of pedigrees. Conserv Genet 9:645–651CrossRefGoogle Scholar
  12. Guerier AS, Bishop JM, Crawford SJ, Schmidt-Küntzel A, Stratford KJ (2012) Parentage analysis in a managed free ranging population of southern white rhinoceros: genetic diversity, pedigrees and management. Conserv Genet 13:811–822CrossRefGoogle Scholar
  13. Henkel JR, Jones KL, Hereford SG, Savoie ML, Leibo SP, Howard JJ (2012) Integrating microsatellite and pedigree analyses to facilitate the captive management of the endangered Mississippi sandhill crane (Grus canadensis pulla). Zoo Biol 31:322–335PubMedCrossRefGoogle Scholar
  14. Herbinger CM, O’Reilly PT, Verspoor E (2006) Unravelling first-generation pedigrees in wild endangered salmon populations using molecular genetic markers. Mol Ecol 15:2261–2275PubMedCrossRefGoogle Scholar
  15. IUCN 2011. IUCN red list of threatened species. Version 2011.2. www.iucnredlist.org. Downloaded on 20 February 2012
  16. Ivy JA, Miller A, Lacy RC, DeWoody JA (2009) Methods and prospects for using molecular data in captive breeding programs: an empirical example using Parma Wallabies (Macropus parma). J Hered 100:441–454PubMedCrossRefGoogle Scholar
  17. Jamieson IG (2010) Founder effects, inbreeding, and loss of genetic diversity in four avian reintroduction programs. Conserv Biol 25:115–123PubMedCrossRefGoogle Scholar
  18. Jones OR, Wang J (2010) COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Resour 10:551–555PubMedCrossRefGoogle Scholar
  19. Jones KL, Glenn TC, Lacy RC, Pierce JR, Unruh N, Mirande CM, Chavez-Ramirez F (2002) Refining the whooping crane studbook by incorporating microsatellite DNA and leg-banding analyses. Conserv Biol 16:789–799CrossRefGoogle Scholar
  20. Karaket T, Poompuang S (2012) CERVUS vs. COLONY for successful parentage and sibship determinations in freshwater prawn Macrobrachium rosenbergii de Man. Aquaculture 324–325:307–311CrossRefGoogle Scholar
  21. Kvist L, Martens J, Nazarenko AA, Orell M (2003) Paternal leakage of mitochondrial DNA in the great tit (Parus major). Mol Biol Evol 20:243–247PubMedCrossRefGoogle Scholar
  22. Lacy RC (1989) Analysis of founder representation in pedigrees: founder equivalents and founder genome equivalents. Zoo Biol 8:111–123CrossRefGoogle Scholar
  23. Lloyd B, Powlesland R (1994) The decline of Kakapo and attempts at conservation by translocation. Biol Conserv 69:75–85CrossRefGoogle Scholar
  24. Lynch M, Ritland K (1999) Estimation of pairwise relatedness with molecular markers. Genetics 152:1753–1766PubMedPubMedCentralGoogle Scholar
  25. Miller HC, Lambert DM, Millar CD, Robertson BC, Minot EO (2003) Minisatellite DNA profiling detects lineages and parentage in the endangered kakapo. Conserv Genet 4:265–274CrossRefGoogle Scholar
  26. Neill E (2008) Kakapo recovery plan, 2006–2016. Department of Conservation New Zealand, WellingtonGoogle Scholar
  27. Pemberton JM (2008) Wild pedigrees: the way forward. Proc R Soc B 275:613–621PubMedCrossRefPubMedCentralGoogle Scholar
  28. Powlesland RG, Roberts A, Lloyd BD, Merton DV (1995) Number, fate, and distribution of kakapo (Strigops habroptilus) found on Stewart Island, New Zealand, 1979–92. N Z J Zool 22:239–248CrossRefGoogle Scholar
  29. Powlesland RG, Merton DV, Cockrem JF (2006) A parrot apart: the natural history of the kakapo (Strigops habroptilus), and the context of its conservation management. Notornis 53:3–26Google Scholar
  30. Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275CrossRefGoogle Scholar
  31. R Development Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/. Accessed 25 June 2012
  32. Ralls K, Ballou JD (2004) Genetic status and management of California condors. Condor 106:215–228CrossRefGoogle Scholar
  33. Read KD, Lemay MA, Acheson S, Boulding EG (2012) Using molecular pedigree reconstruction to evaluate the long-term survival of outplanted hatchery-reared larval and juvenile northern abalone (Haliotis kamtschatkana). Conserv Genet 13:801–810CrossRefGoogle Scholar
  34. Riehl C (2012) Mating system and reproductive skew in a communally breeding cuckoo: hard-working males do not sire more young. Anim Behav 84:707–714CrossRefGoogle Scholar
  35. Robertson BC (2006) The role of genetics in kakapo recovery. Notornis 53:173–183Google Scholar
  36. Robertson BC, Minot EO, Lambert DM (2000) Microsatellite primers for the kakapo (Strigops habroptilus) and their utility in other parrots. Conserv Genet 1:93–95CrossRefGoogle Scholar
  37. Robertson BC, Frauenfelder N, Eason DK, Elliot G, Moorhouse R (2009) Thirty polymorphic microsatellite loci from the critically endangered kakapo (Strigops habroptilus). Mol Ecol Resour 9:664–666PubMedCrossRefGoogle Scholar
  38. Robertson BC, Blanco JM, Adams SL, Eason DK, Vercoe DA, Moorhouse RJ (2011) Artificial insemination allows genetic management of the kakapo Strigops habroptilus. Conference abstract, presented at the 25th International Congress for Conservation Biology, Auckland, NZ. 5–9 December 2011Google Scholar
  39. Rudnick JA, Lacy RC (2008) The impact of assumptions about founder relationships on the effectiveness of captive breeding strategies. Conserv Genet 9:1439–1450CrossRefGoogle Scholar
  40. Russello MA, Amato G (2004) Ex situ population management in the absence of pedigree information. Mol Ecol 13:2829–2840PubMedCrossRefGoogle Scholar
  41. Swinnerton KJ, Groombridge JJ, Jones CG, Burn RW, Mungroo Y (2004) Inbreeding depression and founder diversity among captive and free-living populations of the endangered pink pigeon Columba mayeri. Anim Conserv 7:353–364CrossRefGoogle Scholar
  42. Tzika AC, Remy C, Gibson R, Milinkovitch MC (2008) Molecular genetic analysis of a captive-breeding program: the vulnerable endemic Jamaican yellow boa. Conserv Genet 10:69–77CrossRefGoogle Scholar
  43. van de Casteele T, Galbusera P, Matthysen E (2001) A comparison of microsatellite-based pairwise relatedness estimators. Mol Ecol 10:1539–1549PubMedCrossRefGoogle Scholar
  44. Walling CA, Pemberton JM, Hadfield JD, Kruuk LEB (2010) Comparing parentage inference software: reanalysis of a red deer pedigree. Mol Ecol 19:1914–1928PubMedCrossRefGoogle Scholar
  45. Walsh PS, Metzger DA, Higuchi R (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506–513PubMedGoogle Scholar
  46. Wang J (2007) Triadic IBD coefficients and applications to estimating pairwise relatedness. Genet Res 89:135–153PubMedCrossRefGoogle Scholar
  47. Wang J (2011) COANCESTRY: a program for simulating, estimating and analysing relatedness and inbreeding coefficients. Mol Ecol Resour 11:141–145PubMedCrossRefGoogle Scholar
  48. Wang J, Santure AW (2009) Parentage and sibship inference from multilocus genotype data under polygamy. Genetics 181:1579–1594PubMedCrossRefPubMedCentralGoogle Scholar
  49. Weir BS, Anderson AD, Hepler AB (2006) Genetic relatedness analysis: modern data and new challenges. Nat Rev Genet 7:771–780PubMedCrossRefGoogle Scholar
  50. White K (2012) The role of inbreeding in the reproductive fitness of kakapo (Strigops habroptilus). Masters Thesis, University of OtagoGoogle Scholar
  51. Willis K (2001) Unpedigreed populations and worst-case scenarios. Zoo Biol 20:305–314CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Laura M. Bergner
    • 1
  • Ian G. Jamieson
    • 1
  • Bruce C. Robertson
    • 1
  1. 1.Department of Zoology, Allan Wilson Centre for Molecular Ecology and EvolutionUniversity of OtagoDunedinNew Zealand

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