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A case for genetic parentage assignment in captive group housing

  • Katherine A. Farquharson
  • Carolyn J. Hogg
  • Catherine E. GrueberEmail author
Short Communication

Abstract

Captive animals are commonly housed in groups to make efficient use of limited resources and allow for natural social behaviour. Captive management relies on accurate pedigrees to estimate various population genetic parameters, such as genetic contributions of breeders, but pedigrees of group-housed offspring can be uncertain. Pedigree analysis software incorporates genetic information from multiple putative parents (“MULT”). Molecular pedigree reconstruction to resolve pedigree uncertainties can be costly. We quantify the need for molecular parentage assignment by comparing predicted offspring contributions (based on uncertain “MULT” pedigrees) to contributions obtained from a molecular genetic pedigree reconstruction. Parentage of 81 insurance population Tasmanian devils (Sarcophilus harrisii) born in free-range enclosures from 2011 to 2017 was resolved using 891 single nucleotide polymorphisms. We observed large discrepancies between the MULT pedigree and molecular pedigree data, revealing both overestimates and underestimates of genetic contributions of individuals, and different pedigree-based effective population sizes (102 vs. 158 respectively). The molecular data revealed that reproductive skew (proportion of adults that failed to breed) was high for both sexes. Over half of the wild-born individuals in our dataset were found to have not bred. If undetected, variation in breeding success undermines the utility of pedigree management and may threaten the success of captive breeding. Molecular techniques are increasingly cost-effective, and our data demonstrate that they are critical to devil management. Where feasible, we recommend molecular management of group-housed species in captivity to avoid inaccurate estimates of genetic diversity and to identify non-breeding individuals, in particular founders, for targeted breeding.

Keywords

Conservation breeding Molecular pedigree analysis PMx Reduced representation sequencing Studbook analysis Zoos 

Notes

Acknowledgements

All the Save the Tasmanian Devil Program keeping staff who have worked with the devils in FREs, in particular Karen Fagg and Olivia Barnard. Thanks also to Carla Srb for her ongoing management of the Tasmanian devil studbook, and the Zoo and Aquarium Association Australasia, and its member zoos, who contribute to the insurance population. We thank two anonymous reviewers for comments that improved the manuscript. This work was funded by ARC LP140100508 and DP170101253.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest. All DNA samples were collected under the STDP Standard Operating Procedures for handling Tasmanian devils as part of the management of the FREs and shared with us.

Supplementary material

10592_2019_1198_MOESM1_ESM.Rmd
Electronic supplementary material 1 (RMD 33 kb)

References

  1. Catchen J, Hohenlohe PA, Bassham S, Amores A, Cresko WA (2013) Stacks: an analysis tool set for population genomics. Mol Ecol 22:3124–3140.  https://doi.org/10.1111/mec.12354 CrossRefGoogle Scholar
  2. Cope HR, Hogg CJ, Fagg K, Barnard O, White PJ, Herbert CA (2018a) Effects of deslorelin implants on reproduction and feeding behavior in Tasmanian devils (Sarcophilus harrisii) housed in free-range enclosures. Theriogenology 107:134–141.  https://doi.org/10.1016/j.theriogenology.2017.10.047 CrossRefGoogle Scholar
  3. Cope HR, Hogg CJ, White PJ, Herbert CA (2018b) A role for selective contraception of individuals in conservation. Conserv Biol 32:546–558.  https://doi.org/10.1111/cobi.13042 CrossRefGoogle Scholar
  4. Frankham R, Ballou JD, Briscoe DA (2010) Introduction to Conservation Genetics, 2nd edn. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  5. Gooley R, Hogg CJ, Belov K, Grueber CE (2017) No evidence of inbreeding depression in a Tasmanian devil insurance population despite significant variation in inbreeding. Sci Rep 7:1830.  https://doi.org/10.1038/s41598-017-02000-y CrossRefGoogle Scholar
  6. Gooley RM, Hogg CJ, Belov K, Grueber CE (2018) The effects of group versus intensive housing on the retention of genetic diversity in insurance populations. BMC Zool 3:2.  https://doi.org/10.1186/s40850-017-0026-x CrossRefGoogle Scholar
  7. Guiler E (1970) Observations on the Tasmanian Devil, Sarcophilus harrisii (Marsupialia : Dasyuridae) II. Reproduction, breeding and growth of pouch young. Aust J Zool 18:63–70.  https://doi.org/10.1071/ZO9700063 CrossRefGoogle Scholar
  8. Hogg CJ, Lee AV, Srb C, Hibbard C (2016) Metapopulation management of an Endangered species with limited genetic diversity in the presence of disease: the Tasmanian devil Sarcophilus harrisii. Int Zoo Yearb 51:137–153.  https://doi.org/10.1111/izy.12144 CrossRefGoogle Scholar
  9. Huisman J (2017) Pedigree reconstruction from SNP data: parentage assignment, sibship clustering and beyond. Mol Ecol Resour 17:1009–1024.  https://doi.org/10.1111/1755-0998.12665 CrossRefGoogle Scholar
  10. Jiménez-Mena B, Schad K, Hanna N, Lacy RC (2016) Pedigree analysis for the genetic management of group-living species. Ecol Evol 6:3067–3078.  https://doi.org/10.1002/ece3.1831 CrossRefGoogle Scholar
  11. Keeley T, O’Brien JK, Fanson BG, Masters K, McGreevy PD (2012) The reproductive cycle of the Tasmanian devil (Sarcophilus harrisii) and factors associated with reproductive success in captivity. Gen Comp Endocrinol 176:182–191.  https://doi.org/10.1016/j.ygcen.2012.01.011 CrossRefGoogle Scholar
  12. Lacy RC (2012) Extending pedigree analysis for uncertain parentage and diverse breeding systems. J Hered 103:197–205.  https://doi.org/10.1093/jhered/esr135 CrossRefGoogle Scholar
  13. Lacy RC, Ballou JD, Pollak JP (2012) PMx: software package for demographic and genetic analysis and management of pedigreed populations. Methods Ecol Evol 3:433–437.  https://doi.org/10.1111/j.2041-210X.2011.00148.x CrossRefGoogle Scholar
  14. Lee L, Tirrell N, Burrell C, Chambers S, Vogel S, Domyan ET (2018) Genetic tests reveal extra-pair paternity among Gentoo penguins (Pyogoscelis papua ellsworthii) at Loveland Living Planet Aquarium: implications for ex situ colony management. Zoo Biol 37:236–244.  https://doi.org/10.1002/zoo.21432 CrossRefGoogle Scholar
  15. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760.  https://doi.org/10.1093/bioinformatics/btp324 CrossRefGoogle Scholar
  16. Li H et al (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079.  https://doi.org/10.1093/bioinformatics/btp352 CrossRefGoogle Scholar
  17. Martin-Wintle MS, Wintle NJP, Díez-León M, Swaisgood RR, Asa CS (2019) Improving the sustainability of ex situ populations with mate choice. Zoo Biol 38:119–132.  https://doi.org/10.1002/zoo.21450 CrossRefGoogle Scholar
  18. McLennan EA, Gooley RM, Wise P, Belov K, Hogg CJ, Grueber CE (2018) Pedigree reconstruction using molecular data reveals an early warning sign of gene diversity loss in an island population of Tasmanian devils (Sarcophilus harrisii). Conserv Genet 19:439–450.  https://doi.org/10.1007/s10592-017-1017-8 CrossRefGoogle Scholar
  19. Murchison Elizabeth P et al (2012) Genome sequencing and analysis of the Tasmanian devil and its transmissible cancer. Cell 148:780–791.  https://doi.org/10.1016/j.cell.2011.11.065 CrossRefGoogle Scholar
  20. Norman AJ, Putnam AS, Ivy JA (2019) Use of molecular data in zoo and aquarium collection management: benefits, challenges, and best practices. Zoo Biol 38:106–118.  https://doi.org/10.1002/zoo.21451 CrossRefGoogle Scholar
  21. Puckett EE (2017) Variability in total project and per sample genotyping costs under varying study designs including with microsatellites or SNPs to answer conservation genetic questions. Conserv Genet Resour 9:289–304.  https://doi.org/10.1007/s12686-016-0643-7 CrossRefGoogle Scholar
  22. R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  23. Russell TC (2017) An investigation into factors affecting breeding success in the Tasmanian devil (Sarcophilus harrisii). PhD Thesis, University of SydneyGoogle Scholar
  24. Srb C (2018) Tasmanian devil studbook. Healesville Sanctuary on behalf of the Zoo and Aquarium Association, HealesvilleGoogle Scholar
  25. Wang J (2004) Monitoring and managing genetic variation in group breeding populations without individual pedigrees. Conserv Genet 5:813–825.  https://doi.org/10.1007/s10592-004-1982-6 CrossRefGoogle Scholar
  26. Wedekind C (2002) Sexual selection and life-history decisions: implications for supportive breeding and the management of captive populations. Conserv Biol 16:1204–1211.  https://doi.org/10.1046/j.1523-1739.2002.01217.x CrossRefGoogle Scholar
  27. Weigel J, Faulkner T, Gabriel L (2019) Devil Ark case study. In: Hogg CJ, Fox S, Pemberton D, Belov K (eds) Save the Tasmanian Devil: recovery through science-based management. CSIRO Publishing, MelbourneGoogle Scholar
  28. Wright B, Farquharson KA, McLennan EA, Belov K, Hogg CJ, Grueber CE (2019) From reference genomes to population genomics: comparing three reference-aligned reduced representation sequencing pipelines in two wildlife species. BMC Genom 20:453.  https://doi.org/10.1186/s12864-019-5806-y CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Faculty of Science, School of Life and Environmental SciencesThe University of SydneySydneyAustralia
  2. 2.San Diego Zoo GlobalSan DiegoUSA

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