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Australian Mammalogy Australian Mammalogy Society
Journal of the Australian Mammal Society
RESEARCH ARTICLE

Skewed paternity impacts genetic diversity in a small reintroduced population of western quolls (Dasyurus geoffroii)

Tessa P. Manning https://orcid.org/0000-0002-7038-6418 A * , Jeremy J. Austin https://orcid.org/0000-0003-4244-2942 A B , Katherine E. Moseby https://orcid.org/0000-0003-0691-1625 C D and Melissa A. Jensen https://orcid.org/0000-0002-0817-1758 A C
+ Author Affiliations
- Author Affiliations

A School of Biological Sciences, University of Adelaide, SA 5005, Australia.

B Australian Centre for Ancient DNA, School of Biological Sciences, University of Adelaide, SA 5005, Australia.

C Arid Recovery, Roxby Downs, SA 5725, Australia.

D Centre for Ecosystem Science, University of New South Wales, NSW 2052, Australia.

* Correspondence to: tessa.manning@adelaide.edu.au

Handling Editor: Mark Eldridge

Australian Mammalogy 45(2) 199-209 https://doi.org/10.1071/AM22012
Submitted: 29 March 2022  Accepted: 8 November 2022   Published: 28 November 2022

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing on behalf of the Australian Mammal Society.

Abstract

Reintroduction programs can face issues maintaining genetic diversity due to founder effects, and subsequent bottlenecks related to mortality and reproductive skews in the first generations after release. We assessed genetic diversity and undertook a pedigree analysis of 12 founders and 23 first-generation western quolls (Dasyurus geoffroii) at a reintroduced population at Arid Recovery, South Australia, in 2018. Genetic pedigrees showed that five of the eight females and three of the four males produced offspring. We also identified multiple paternity in this species. However, skewed paternity was evident with one male siring 65% of the sampled offspring. The reason for the paternity skew is unclear. The most successful male was smaller in body mass but had the largest home range compared to the other males, was released 4 days prior to two of the other males and spent more time inside the reserve. Failure of 33% of founders to breed in the first year combined with the strong paternity skew indicate that genetic drift and inbreeding pose a risk to the long-term success of this reintroduction. Genetic management, including the release of additional males, has already been undertaken, but may be required longer-term. Future quoll reintroductions should test if releasing all males simultaneously reduces paternity skew, and paternity should be measured through several generations to determine if paternity skew is a reintroduction protocol issue or one that is common in small populations more generally.

Keywords: chuditch, Dasyuridae, genetic management, marsupial, multiple paternity, pedigree assessment, quoll, reintroduction.


References

Abbott, I. (2006). Mammalian faunal collapse in Western Australia, 1875-1925: the hypothesised role of epizootic disease and a conceptual model of its origin, introduction, transmission, and spread. Australian Zoologist 33, 530–561.
Mammalian faunal collapse in Western Australia, 1875-1925: the hypothesised role of epizootic disease and a conceptual model of its origin, introduction, transmission, and spread.Crossref | GoogleScholarGoogle Scholar |

Allendorf, F. W., and Luikart, G. (2007). ‘Conservation and the Genetics of Populations.’ (Wiley-Blackwell: Malden, MA.)

Anthony, L. L., and Blumstein, D. T. (2000). Integrating behaviour into wildlife conservation: the multiple ways that behaviour can reduce Ne. Biological Conservation 95, 303–315.
Integrating behaviour into wildlife conservation: the multiple ways that behaviour can reduce Ne.Crossref | GoogleScholarGoogle Scholar |

Berger-Tal, O., Blumstein, D. T., and Swaisgood, R. R. (2019). Conservation translocations: a review of common difficulties and promising directions. Animal Conservation 23, 121–131.
Conservation translocations: a review of common difficulties and promising directions.Crossref | GoogleScholarGoogle Scholar |

Biebach, I., and Keller, L. F. (2009). Inbreeding in reintroduced populations: the effects of early reintroduction history and contemporary processes. Conservation Genetics 11, 527–538.
Inbreeding in reintroduced populations: the effects of early reintroduction history and contemporary processes.Crossref | GoogleScholarGoogle Scholar |

Biebach, I., and Keller, L. F. (2012). Genetic variation depends more on admixture than number of founders in reintroduced Alpine ibex populations. Biological Conservation 147, 197–203.
Genetic variation depends more on admixture than number of founders in reintroduced Alpine ibex populations.Crossref | GoogleScholarGoogle Scholar |

Birkhead, T. R. (2000). ‘Promiscuity: an Evolutionary History of Sperm Competition and Sexual Conflict.’ (Faber & Faber: London.)

Calsbeek, R., Bonneaud, C., Prabhu, S., Manoukis, N., and Smith, T. B. (2007). Multiple paternity and sperm storage lead to increased genetic diversity in Anolis lizards. Evolutionary Ecology Research 9, 495–503.

Chan, R., Dunlop, J., and Spencer, P. B. S. (2019). Highly promiscuous paternity in mainland and island populations of the endangered Northern Quoll. Journal of Zoology 310, 210–220.
Highly promiscuous paternity in mainland and island populations of the endangered Northern Quoll.Crossref | GoogleScholarGoogle Scholar |

Cohas, A., Yoccoz, N. G., and Allainé, D. (2007). Extra-pair paternity in alpine marmots, Marmota marmota: genetic quality and genetic diversity effects. Behavioral Ecology and Sociobiology 61, 1081–1092.
Extra-pair paternity in alpine marmots, Marmota marmota: genetic quality and genetic diversity effects.Crossref | GoogleScholarGoogle Scholar |

Department of Environment and Conservation (2012). ‘Chuditch (Dasyurus geoffroii) National Recovery Plan’. Wildlife Management Program No. 54. Government of Western Australia, Perth, WA. Available at https://www.dcceew.gov.au/sites/default/files/documents/dasyurus-geoffroii-2012.pdf

DeWoody, J. A., Harder, A. M., Mathur, S., and Willoughby, J. R. (2021). The long‐standing significance of genetic diversity in conservation Molecular Ecology 30, 4147–4154.
The long‐standing significance of genetic diversity in conservationCrossref | GoogleScholarGoogle Scholar |

Dunbar, R. (1982). Intraspecific Variations in Mating Strategy. In ‘Ontogeny: Perspectives in Ethology’. (Eds P. P. G. Bateson, P. H. Klopfer.) pp. 385–420. (Springer: Boston.)

Finlayson, H. H. (1961). On central Australian mammals, Part IV. The distribution and status of central Australian species. Records of the South Australian Museum 41, 141–191.

Firestone, K. B., Houlden, B. A., Sherwin, W. B., and Geffen, E. (2000). Variability and differentiation of microsatellites in the genus Dasyurus and conservation implications for the large Australian carnivorous marsupials. Conservation Genetics 1, 115–133.
Variability and differentiation of microsatellites in the genus Dasyurus and conservation implications for the large Australian carnivorous marsupials.Crossref | GoogleScholarGoogle Scholar |

Frankham, R. (2010). Challenges and opportunities of genetic approaches to biological conservation. Biological Conservation 143, 1919–1927.
Challenges and opportunities of genetic approaches to biological conservation.Crossref | GoogleScholarGoogle Scholar |

Frankham, R., Ballou, J. D., and Briscoe, D. A. (2010). ‘Introduction to Conservation Genetics’, 2 edn. (Cambridge University Press: Cambridge.)

Glen, A. S., Cardoso, M. J., Dickman, C. R., and Firestone, K. B. (2009a). Who’s your daddy? Paternity testing reveals promiscuity and multiple paternity in the carnivorous marsupial Dasyurus maculatus (Marsupialia: Dasyuridae). Biological Journal of the Linnean Society 96, 1–7.
Who’s your daddy? Paternity testing reveals promiscuity and multiple paternity in the carnivorous marsupial Dasyurus maculatus (Marsupialia: Dasyuridae).Crossref | GoogleScholarGoogle Scholar |

Glen, A. S., de Tores, P. J., Sutherland, D. R., and Morris, K. D. (2009b). Interactions between chuditch (Dasyurus geoffroii) and introduced predators: a review. Australian Journal of Zoology 57, 347–356.
Interactions between chuditch (Dasyurus geoffroii) and introduced predators: a review.Crossref | GoogleScholarGoogle Scholar |

Holleley, C. E., Dickman, C. R., Crowther, M. S., and Oldroyd, B. P. (2006). Size breeds success: multiple paternity, multivariate selection and male semelparity in a small marsupial, Antechinus stuartii. Molecular Ecology 15, 3439–3448.
Size breeds success: multiple paternity, multivariate selection and male semelparity in a small marsupial, Antechinus stuartii.Crossref | GoogleScholarGoogle Scholar |

Illumina (2021). Illumina Adapter Sequences. 2021. Available at https://support-docs.illumina.com/SHARE/AdapterSeq/Content/SHARE/AdapterSeq/AdapterSequencesIntro.htm [viewed 25 November 2021].

Jamieson, I. G. (2009). ‘Loss of genetic diversity and inbreeding in New Zealand’s threatened bird species’. Science for Conservation 293 pp. 5–58. (Department of Conservation, Wellington, New Zealand.)

Jamieson, I. G. (2011). Founder Effects, Inbreeding, and Loss of Genetic Diversity in Four Avian Reintroduction Programs. Conservation Biology 25, 115–123.
Founder Effects, Inbreeding, and Loss of Genetic Diversity in Four Avian Reintroduction Programs.Crossref | GoogleScholarGoogle Scholar |

Jennions, M. D., and Petrie, M. (2000). Why do females mate multiply? A review of the genetic benefits. Biological Reviews 75, 21–64.
Why do females mate multiply? A review of the genetic benefits.Crossref | GoogleScholarGoogle Scholar |

Keller, L. F., and Waller, D. M. (2002). Inbreeding effects in wild populations. Trends in Ecology and Evolution 17, 230–241.
Inbreeding effects in wild populations.Crossref | GoogleScholarGoogle Scholar |

Keller, L. F., Biebach, I., Ewing, S. R., and Hoeck, P. E. A. (2012). The genetics of reintroductions: inbreeding and genetic drift. In ‘Reintroduction Biology: Integrating Science and Management’. (Eds J. G. Ewen, D. P. Armstrong, K. A. Parker, P. J. Seddon.), pp. 362–395. (Blackwell Publishing.)

Kraaijeveld-Smit, F., Ward, S., and Temple-Smith, P. (2002a). Multiple paternity in a field population of a small carnivorous marsupial, the agile antechinus, Antechinus agilis. Behavioral Ecology and Sociobiology 52, 84–91.
Multiple paternity in a field population of a small carnivorous marsupial, the agile antechinus, Antechinus agilis.Crossref | GoogleScholarGoogle Scholar |

Kraaijeveld-Smit, F., Ward, S. J, Temple-Smith, P. D., and Paetkau, S. (2002b). Factors influencing paternity success in Antechinus agilis: last-male sperm precedence, timing of mating and genetic compatibility. Journal of Evolutionary Biology 15, 100–107.
Factors influencing paternity success in Antechinus agilis: last-male sperm precedence, timing of mating and genetic compatibility.Crossref | GoogleScholarGoogle Scholar |

Marshall, T. C., Slate, J., Kruuk, L. E. B., and Pemberton, J. M. (1998). Statistical confidence for likelihood-based paternity inference in natural populations. Molecular Ecology 7, 639–655.
Statistical confidence for likelihood-based paternity inference in natural populations.Crossref | GoogleScholarGoogle Scholar |

Lacy, R. C., Ballou, J. D., and Pollak, J. P. (2011). PMx: software package for demographic and genetic analysis and management of pedigreed populations Methods in Ecology and Evolution 3, 433–437.
PMx: software package for demographic and genetic analysis and management of pedigreed populationsCrossref | GoogleScholarGoogle Scholar |

Miller, K. A., Nelson, N. J., Smith, H. G., and Moore, J. A. (2009). How do reproductive skew and founder group size affect genetic diversity in reintroduced populations? Molecular Ecology 18, 3792–3802.
How do reproductive skew and founder group size affect genetic diversity in reintroduced populations?Crossref | GoogleScholarGoogle Scholar |

Morris, K., Page, M., Kay, R., Renwick, J., Desmond, A., Comer, S., Burbidge, A., Kuchling, G., and Sims, C. (2015) Forty years of fauna translocations in Western Australia: lessons learned. In ‘Advances in Reintroduction Biology of Australian and New Zealand Fauna’. (Eds D. Armstrong, M. Hayward, D. Moro, P. Sesson.). pp. 217–236. (CSIRO Publishing: Clayton South.)

Moseby, K. E., and Read, J. L. (2006). The efficacy of feral cat, fox and rabbit exclusion fence designs for threatened species protection. Biological Conservation 127, 429–437.
The efficacy of feral cat, fox and rabbit exclusion fence designs for threatened species protection.Crossref | GoogleScholarGoogle Scholar |

Moseby, K. E., Hodgens, P., Peacock, D., Mooney, P., Brandle, R., Lynch, C., West, R., Young, C. M., Bannister, H., Copley, P., and Jensen, M. A. (2021). Intensive monitoring, the key to identifying cat predation as a major threat to native carnivore (Dasyurus geoffroii) reintroduction. Biodiversity and Conservation 30, 1547–1571.
Intensive monitoring, the key to identifying cat predation as a major threat to native carnivore (Dasyurus geoffroii) reintroduction.Crossref | GoogleScholarGoogle Scholar |

Pacioni, C., Wayne, A. F., and Page, M. (2019). Guidelines for genetic management in mammal translocation programs. Biological Conservation 237, 105–113.
Guidelines for genetic management in mammal translocation programs.Crossref | GoogleScholarGoogle Scholar |

Parker, P. G., and Waite, T. A. (1997). Mating systems, effective population size, and conservation of natural populations. In ‘Behavioral Approaches to Conservation in the Wild’. (Eds J. R. Clemmons, R. Buchholtz.), pp. 243–261. (Cambridge University Press: Cambridge.)

Parrott, M. L., Ward, S. J., and Temple-Smith, P. D. (2006). Genetic similarity, not male size, influences female mate choice in the agile antechinus (Antechinus agilis). Australian Journal of Zoology 54, 319–323.
Genetic similarity, not male size, influences female mate choice in the agile antechinus (Antechinus agilis).Crossref | GoogleScholarGoogle Scholar |

Peakall, R., and Smouse, P. E. (2006). genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6, 288–295.
genalex 6: genetic analysis in Excel. Population genetic software for teaching and research.Crossref | GoogleScholarGoogle Scholar |

Queller, D. C., and Goodnight, K. F. (1989). Estimating Relatedness Using Genetic Markers. Evolution 43, 258–275.
Estimating Relatedness Using Genetic Markers.Crossref | GoogleScholarGoogle Scholar |

Rayner, K., Chambers, B., Johnson, B., Morris, K. D., and Mills, H. R. (2012). Spatial and dietary requirements of the chuditch (Dasyurus geoffroii) in a semiarid climatic zone. Australian Mammalogy 34, 59–67.
Spatial and dietary requirements of the chuditch (Dasyurus geoffroii) in a semiarid climatic zone.Crossref | GoogleScholarGoogle Scholar |

Rohland, N., and Reich, D. (2012). Cost-effective, high-throughput DNA sequencing libraries for multiplexed target capture. Genome Research 22, 939–946.
Cost-effective, high-throughput DNA sequencing libraries for multiplexed target capture.Crossref | GoogleScholarGoogle Scholar |

Russell, T., Lane, A., Clarke, J., Hogg, C., Morris, K., Keeley, T., Madsen, T., and Ujvari, B. (2019). Multiple paternity and precocial breeding in wild Tasmanian devils, Sarcophilus harrisii (Marsupialia: Dasyuridae). Biological Journal of the Linnean Society 128, 201–210.
Multiple paternity and precocial breeding in wild Tasmanian devils, Sarcophilus harrisii (Marsupialia: Dasyuridae).Crossref | GoogleScholarGoogle Scholar |

Sale, M. G., Kraaijeveld-Smit, F. J. L., and Arnould, J. P. Y. (2013). Multiple paternity in the swamp antechinus (Antechinus minimus). Australian Mammalogy 35, 227–230.
Multiple paternity in the swamp antechinus (Antechinus minimus).Crossref | GoogleScholarGoogle Scholar |

Serena, M., and Soderquist, T. R. (1988). Growth and development of pouch young of wild and captive Dasyurus geoffroii (Marsupialia, Dasyuridae). Australian Journal of Zoology 36, 533–543.
Growth and development of pouch young of wild and captive Dasyurus geoffroii (Marsupialia, Dasyuridae).Crossref | GoogleScholarGoogle Scholar |

Spencer, P. B. S., Cardoso, M., How, R. A., Williams, J., Bunce, M., and Schmitt, L. H. (2007). Cross-species amplification at microsatellite loci in Australian quolls including the description of five new markers from the Chuditch (Dasyurus geoffroii). Molecular Ecology Notes 7, 1100–1103.
Cross-species amplification at microsatellite loci in Australian quolls including the description of five new markers from the Chuditch (Dasyurus geoffroii).Crossref | GoogleScholarGoogle Scholar |

Stephen, C. L., Whittaker, D. G., Gillis, D., Cox, L. L., and Rhodes, O. E. (2005). Genetic consequences of reintroductions: an example from Oregon pronghorn antelope (Antilocapra americana). The Journal of Wildlife Management 69, 1463–1474.
Genetic consequences of reintroductions: an example from Oregon pronghorn antelope (Antilocapra americana).Crossref | GoogleScholarGoogle Scholar |

Wacker, S., Larsen, B. M., Jakobsen, P., and Karlsson, S. (2019). Multiple paternity promotes genetic diversity in captive breeding of a freshwater mussel. Global Ecology and Conservation 17, e00564.
Multiple paternity promotes genetic diversity in captive breeding of a freshwater mussel.Crossref | GoogleScholarGoogle Scholar |

Wattier, R., Engel, C. R., Saumitou-Laprade, P., and Valero, M. (1998). Short allele dominance as a source of heterozygote deficiency at microsatellite loci: experimental evidence at the dinucleotide locus Gv1CT in Gracilaria gracilis (Rhodophyta). Molecular Ecology 7, 1569–1573.
Short allele dominance as a source of heterozygote deficiency at microsatellite loci: experimental evidence at the dinucleotide locus Gv1CT in Gracilaria gracilis (Rhodophyta).Crossref | GoogleScholarGoogle Scholar |

Weeks, A. R., Moro, D., Thavornkanlapachai, R., Taylor, H. R., White, N. E., Weiser, E. L., and Heinze, D. (2015). Conserving and enhancing genetic diversity in translocation programs. In ‘Advances in Reintroduction Biology’. (Eds D. P. Armstrong, M. Hayward, D. Moro, P. J. Seddon.) (CSIRO Publishing.)

West, R. S., Tilley, L., and Moseby, K. E. (2020). A trial reintroduction of the western quoll to a fenced conservation reserve: implications of returning native predators. Australian Mammalogy 42, 257–265.
A trial reintroduction of the western quoll to a fenced conservation reserve: implications of returning native predators.Crossref | GoogleScholarGoogle Scholar |

White, L. C., Moseby, K. E., Thomson, V. A., Donnellan, S. C., and Austin, J. J. (2018). Long-term genetic consequences of mammal reintroductions into an Australian conservation reserve’. Biological Conservation 219, 1–11.
Long-term genetic consequences of mammal reintroductions into an Australian conservation reserve’.Crossref | GoogleScholarGoogle Scholar |

Wolff, J. O., and Macdonald, D. W. (2004). Promiscuous females protect their offspring. Trends in Ecology & Evolution 19, 127–134.
Promiscuous females protect their offspring.Crossref | GoogleScholarGoogle Scholar |

Woolley, P. A., Krajewski, C., and Westerman, M. (2015). Phylogenetic relationships within Dasyurus (Dasyuromorphia: Dasyuridae): quoll systematics based on molecular evidence and male characteristics. Journal of Mammalogy 96, 37–46.
Phylogenetic relationships within Dasyurus (Dasyuromorphia: Dasyuridae): quoll systematics based on molecular evidence and male characteristics.Crossref | GoogleScholarGoogle Scholar |

Yasui, Y. (2001). Female multiple mating as a genetic bet-hedging strategy when mate choice criteria are unreliable. Ecological Research 16, 605–616.
Female multiple mating as a genetic bet-hedging strategy when mate choice criteria are unreliable.Crossref | GoogleScholarGoogle Scholar |