Multi-generational evaluation of genetic diversity and parentage in captive southern pygmy perch (Nannoperca australis)

Abstract

Maintaining genetic diversity within captive breeding populations is a key challenge for conservation managers. We applied a multi-generational genetic approach to the captive breeding program of an endangered Australian freshwater fish, the southern pygmy perch (Nannoperca australis). During previous work, fish from the lower Murray-Darling Basin were rescued before drought exacerbated by irrigation resulted in local extinction. This endemic lineage of the species was captive-bred in genetically designed groups, and equal numbers of F1 individuals were reintroduced to the wild with the return of favourable habitat. Here, we implemented a contingency plan by continuing the genetic-based captive breeding in the event that a self-sustaining wild population was not established. F1 individuals were available as putative breeders from the subset of groups that produced an excess of fish in the original restoration program. We used microsatellite-based parentage analyses of these F1 fish to form breeding groups that minimized inbreeding. We assessed their subsequent parental contribution to F2 individuals and the maintenance of genetic diversity. We found skewed parental contribution to F2 individuals, yet minimal loss of genetic diversity from their parents. However, the diversity was substantially less than that of the original rescued population. We attribute this to the unavoidable use of F1 individuals from a limited number of the original breeding groups. Alternative genetic sources for supplementation or reintroduction should be assessed to determine their suitability. The genetic fate of the captive-bred population highlights the strong need to integrate DNA-based tools for monitoring and adaptive management of captive breeding programs.

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References

  1. Attard CRM, Möller LM, Sasaki M, Hammer MP, Bice CM, Brauer CJ, Carvalho DC, Harris JO, Beheregaray LB (2016) A novel holistic framework for genetic-based captive breeding and reintroduction programs. Conserv Biol. doi:10.1111/cobi.12699

    PubMed  Google Scholar 

  2. Brauer CJ, Unmack PJ, Hammer MP, Adams M, Beheregaray LB (2013) Catchment-scale conservation units identified for the threatened Yarra pygmy perch (Nannoperca obscura) in highly modified river systems. PLoS One 8:e82953

    Article  PubMed  PubMed Central  Google Scholar 

  3. Brown RC, Woolliams JA, McAndrew BJ (2005) Factors influencing effective population size in commercial populations of gilthead seabream, Sparus aurata. Aquaculture 247:219–225

    Article  Google Scholar 

  4. Carvalho DC, Hammer MP, Beheregaray LB (2012) Isolation and PCR-multiplex genotyping of 18 novel microsatellite markers for the threatened southern pygmy perch (Nannoperca australis). Conserv Genet Resour 4:15–17

    Article  Google Scholar 

  5. Cole T, Hammer M, Unmack P, Teske P, Brauer C, Adams M, Beheregaray L (2016) Range-wide fragmentation in a threatened fish associated with post-European settlement modification in the Murray-Darling Basin, Australia. Conserv Genet. doi:10.1007/s10592-016-0868-8

    Google Scholar 

  6. Duchesne P, Godbout M-H, Bernatchez L (2002) PAPA (package for the analysis of parental allocation): a computer program for simulated and real parental allocation. Mol Ecol Notes 2:191–193

    CAS  Article  Google Scholar 

  7. Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140

    Article  Google Scholar 

  8. Frankham R (2008) Genetic adaptation to captivity in species conservation programs. Mol Ecol 17:325–333

    Article  PubMed  Google Scholar 

  9. Frankham R, Ballou JD, Briscoe DA (2009) Introduction to conservation genetics, 2nd edn. Cambridge University Press, Cambridge

    Google Scholar 

  10. Fraser DJ (2008) How well can captive breeding programs conserve biodiversity? a review of salmonids. Evol Appl 1:535–586

    Article  PubMed  PubMed Central  Google Scholar 

  11. Hammer MP, Bice CM, Hall A, Frears A, Watt A, Whiterod NS, Beheregaray LB, Harris JO, Zampatti BP (2013) Freshwater fish conservation in the face of critical water shortages in the southern Murray-Darling Basin, Australia. Mar Freshw Res 64:807–821

    Article  Google Scholar 

  12. Hammerly SC, de la Cerda DA, Bailey H, Johnson JA (2016) A pedigree gone bad: increased offspring survival after using DNA-based relatedness to minimize inbreeding in a captive population. Anim Conserv 19:296–303

    Article  Google Scholar 

  13. Hobbs RJ, Higgs E, Harris JA (2009) Novel ecosystems: implications for conservation and restoration. Trends Ecol Evol 24:599–605

    Article  PubMed  Google Scholar 

  14. Kingsford R, Walker K, Lester R, Young W, Fairweather P, Sammut J, Geddes MC (2011) A ramsar wetland in crisis—the coorong, lower lakes and murray mouth, Australia. Mar Freshw Res 62:255–265

    CAS  Article  Google Scholar 

  15. Knief U, Hemmrich-Stanisak G, Wittig M, Franke A, Griffith SC, Kempenaers B, Forstmeier W (2015) Quantifying realized inbreeding in wild and captive animal populations. Heredity 114:397–403

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  16. Lacy RC (2013) Achieving true sustainability of zoo populations. Zoo Biol 32:19–26

    Article  PubMed  Google Scholar 

  17. Lintermans M (2007) Fishes of the murray-darling basin: an introductory guide. Murray-Darling Basins Commission, Canberra

    Google Scholar 

  18. Liu P, Xia JH, Lin G, Sun F, Liu F, Lim HS, Pang HY, Yue GH (2012) Molecular parentage analysis is essential in breeding Asian seabass. PLoS One 7:e51142

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  19. Loughnan SR, Domingos JA, Smith-Keune C, Forrester JP, Jerry DR, Beheregaray LB, Robinson NA (2013) Broodstock contribution after mass spawning and size grading in barramundi (Lates calcarifer, Bloch). Aquaculture 404–405:139–149

    Article  Google Scholar 

  20. Mitchell P (1976) A study of the behaviour and breeding biology of the Southern pigmy perch Nannoperca australis australis (Günther) (Teleosteri, Nannopercidae). B.Sc. (Honors) thesis, University of Melbourne

  21. Mitchell AA, Lau J, Chemnick LG, Thompson EA, Alberts AC, Ryder OA, Gerber GP (2011) Using microsatellite diversity in wild Anegada iguanas (Cyclura pinguis) to establish relatedness in a captive breeding group of this critically endangered species. Conserv Genet 12:771–781

    Article  Google Scholar 

  22. Morrongiello JR, Bond NR, Crook DA, Wong BBM (2010) Nuptial coloration varies with ambient light environment in a freshwater fish. J Evol Biol 23:2718–2725

    CAS  Article  PubMed  Google Scholar 

  23. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in excel. population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  24. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in excel. population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria www.R-project.org

  26. Saddlier S, Koehn JD, Hammer MP (2013) Let’s not forget the small fishes—conservation of two threatened species of pygmy perch in south-eastern Australia. Mar Freshw Res 64:874–886

    Article  Google Scholar 

  27. Wedderburn SD, Hammer MP, Bice CM (2012) Shifts in small-bodied fish assemblages resulting from drought-induced water level recession in terminating lakes of the Murray-Darling Basin, Australia. Hydrobiologia 691:35–46

    CAS  Article  Google Scholar 

  28. Weeks AR, Sgro CM, Young AG, Frankham R, Mitchell NJ, Miller KA, Byrne M, Coates DJ, Eldridge MDB, Sunnucks P, Breed MF, James EA, Hoffmann AA (2011) Assessing the benefits and risks of translocations in changing environments: a genetic perspective. Evol Appl 4:709–725

    Article  PubMed  PubMed Central  Google Scholar 

  29. Williams SE, Hoffman EA (2009) Minimizing genetic adaptation in captive breeding programs: a review. Biol Conserv 142:2388–2400

    Article  Google Scholar 

  30. Witzenberger K, Hochkirch A (2011) Ex situ conservation genetics: a review of molecular studies on the genetic consequences of captive breeding programmes for endangered animal species. Biodivers Conserv 20:1843–1861

    Article  Google Scholar 

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Acknowledgments

We thank the many people who helped with or supported the genetic captive breeding program, especially S. Westergaard, H. Mahon, A. Hall, N. Whiterod, A. Watt, C. Bice, B. Zampatti, and A. Frears. Financial support was provided by the Australian Research Council (LP100200409 to L.B.B., J.O.H. and M Adams; FT130101068 to L.B.B.). We thank the Flinders University component of FT130101068 for providing the salary for C.R.M.A. Additional support was received by Department of Environment, Water and Natural Resources SA, SA Museum, SA Murray Darling NRMB, PIRSA Fisheries, and Native Fish Australia SA. This work was conducted under approval from the Flinders University Animal Welfare Committee (approval E313).

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Correspondence to Luciano B. Beheregaray.

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Attard, C.R.M., Brauer, C.J., Van Zoelen, J.D. et al. Multi-generational evaluation of genetic diversity and parentage in captive southern pygmy perch (Nannoperca australis). Conserv Genet 17, 1469–1473 (2016). https://doi.org/10.1007/s10592-016-0873-y

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Keywords

  • Restoration genetics
  • Pedigree
  • Kinship
  • Relatedness
  • Fish
  • Biodiversity extinction