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RESEARCH ARTICLE
Contents Vol 36(4)

Inbreeding and testicular abnormalities in a bottlenecked population of koalas (Phascolarctos cinereus)

Romane Cristescu A H , Valma Cahill B , William B. Sherwin A , Kathrine Handasyde C , Kris Carlyon A , Desley Whisson D , Catherine A. Herbert A E , Britt Louise J. Carlsson F , Alan N. Wilton F G and Des W. Cooper A
+ Author Affiliations
- Author Affiliations

A School of Biological, Earth and Environmental Sciences, University of New South Wales, NSW 2052, Australia.

B Creek Street, Oakey, Qld 4401, Australia.

C Department of Zoology, University of Melbourne, Vic. 3010, Australia.

D School of Life and Environmental Sciences, Deakin University, 221 Burwood Highway, Burwood, Vic. 3125, Australia.

E Faculty of Veterinary Science, University of Sydney, Sydney, NSW 2006, Australia.

F School of Biotechnology and Biomolecular Sciences, University of New South Wales, NSW 2052, Australia.

G Ramaciotti Centre for Gene Function Analysis, University of New South Wales, NSW 2052, Australia.

H Corresponding author. Email: romane@student.unsw.edu.au

Wildlife Research 36(4) 299-308 https://doi.org/10.1071/WR08010
Submitted: 23 January 2008  Accepted: 23 March 2009   Published: 1 June 2009

Abstract

Habitat destruction and fragmentation, interactions with introduced species or the relocation of animals to form new populations for conservation purposes may result in a multiplication of population bottlenecks. Examples are the translocations of koalas to French Island and its derivative Kangaroo Island population, with both populations established as insurance policies against koala extinction. In terms of population size, these conservation programs were success stories. However, the genetic story could be different. We conducted a genetic investigation of French and Kangaroo Island koalas by using 15 microsatellite markers, 11 of which are described here for the first time. The results confirm very low genetic diversity. French Island koalas have 3.8 alleles per locus and Kangaroo Island koalas 2.4. The present study found a 19% incidence of testicular abnormality in Kangaroo Island animals. Internal relatedness, an individual inbreeding coefficient, was not significantly different in koalas with testicular abnormalities from that in other males, suggesting the condition is not related to recent inbreeding. It could instead result from an unfortunate selection of founder individuals carrying alleles for testicular abnormalities, followed by a subsequent increase in these alleles’ frequencies through genetic drift and small population-related inefficiency of selection. Given the low diversity and possible high prevalence of deleterious alleles, the genetic viability of the population remains uncertain, despite its exponential growth so far. This stands as a warning to other introductions for conservation reasons.


Acknowledgements

This work was funded by ARC linkage grant (LPO560344). We thank the Department for Environment and Heritage (DEH), South Australia, for providing access to unpublished data from the Koala Management Program. We also thank the Rangers from French Island National Park (Parks Victoria) and the members of the Koala Management Program (DEH) for their support and assistance in the field and Bill Amos for providing the program to estimate IR. We also thank Andrea Taylor and three anonymous reviewers for their most helpful comments. All the work and particularly manipulations of koalas were approved by relevant ethic committees and accredited with relevant licences and permits. Authorisations were obtained under the Prevention of Cruelty to Animals Act 1985 (SA), Licence #46, dated 14 October 1997, the Macquarie University ACEC Permit #97041, the University of Melbourne Science Animal Experimentation Ethics Committee Project #03147, the Victorian Department of Sustainability & Environment Wildlife Research Permit #10003860, the Department for Environment and Heritage, South Australia, Wildlife Ethics Committee Approval #45/2005, Scientific Research Permit #E25038-2 and Licence #169.


References

Acevedo-Whitehouse, K. , Gulland, F. , Greig, D. , and Amos, W. (2003). Inbreeding: disease susceptibility in California sea lions. Nature 422, 35.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | Belkhir K. , Borsa P. , Chikhi L. , Raufaste N. , and Bonhomme F. (1996–2004). ‘GENETIX 4.05, Logiciel sous Windows TM pour la Génétique des Populations.’ (Laboratoire Génome, Populations, Interactions, CNRS UMR 5171, Université de Montpellier II: Montpellier, France.)

Bijlsma, R. , Bundgaard, J. , and Van Putten, W. F. (1999). Environmental dependence of inbreeding depression and purging in Drosophila melanogaster. Journal of Evolutionary Biology 12, 1125–1137.
| Crossref | GoogleScholarGoogle Scholar | Brook B. W. , Tonkyn D. W. , O’Grady J. J. , and Frankham R. (2002). Contribution of inbreeding to extinction risk in threatened species. Conservation Ecology 6, 16. Available at www.consecol.org/vol6/iss1/art16 [Verified April 2009]

Brown, A. S. , Carrick, F. N. , Gordon, G. , and Reynolds, K. (1984). The diagnosis and epidemiology of an infertility disease in the female koala, Phascolarctos cinereus (Marsupialia). Veterinary Radiology & Ultrasound 25, 242–248.
| Crossref | GoogleScholarGoogle Scholar | Crow J. , and Kimura M. (Eds) (1970). ‘An Introduction to Population Genetics Theory.’ (Harper & Row Publishers Inc.: New York.)

Cunningham, A. A. (1996). Disease risks of wildlife translocations. Conservation Biology 10, 349–353.
| Crossref | GoogleScholarGoogle Scholar | Falconer D. (1960). Small populations: I. Changes of gene frequency under simplified conditions. In ‘Introduction to Quantitative Genetics’. (Ed. R. Clay.) pp. 47–67. (The Chaucer Press Ltd: Bungay, Suffolk, UK.)

Ferlin, A. , Simonato, M. , Bartoloni, L. , Rizzo, G. , Bettella, A. , Dottorini, T. , Dallapiccola, B. , and Foresta, C. (2003). The INSL3–LGR8/GREAT ligand-receptor pair in human cryptorchidism. Journal of Clinical Endocrinology and Metabolism 88, 4273–4279.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | Frankham R. , Ballou J. , and Briscoe D. (Eds) (2002). ‘Introduction to Conservation Genetics.’ (Cambridge University Press: Cambridge, UK.)

Gharrett, A. J. , Smoker, W. W. , Reisenbichler, R. R. , and Taylor, S. G. (1999). Outbreeding depression in hybrids between odd- and even-broodyear pink salmon. Aquaculture 173, 117–129.
| Crossref | GoogleScholarGoogle Scholar | Hedrick P. (2004). Conservation biology: the impact of population biology and a current perspective. In ‘Evolution of Population Biology’. (Eds R. C. Lewontin, R. S. Singh and M. K. Uyenoyama.) pp. 347–365. (Cambridge University Press: Cambridge, UK.)

Houlden, B. A. , England, P. , and Sherwin, W. B. (1996a). Paternity exclusion in koalas using hypervariable microsatellites. Journal of Heredity 87, 149–152.
|  CAS | PubMed | Lee A. K. , Martin R. W. , and Ward S. (Eds) (1988). ‘The Koala: Natural History.’ (New South Wales University: Sydney.)

Le Page, S. L. , Livermore, R. A. , Cooper, D. W. , and Taylor, A. C. (2000). Genetic analysis of a documented population bottleneck: introduced Bennett’s wallabies (Macropus rufogriseus rufogriseus) in New Zealand. Molecular Ecology 9, 753–763.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed | Martin R. , and Handasyde K. (Eds) (1999). ‘The Koala: Natural History, Conservation and Management, Australian Natural History Series.’ (University of New South Wales Press Ltd: Hong Kong.)

Masters, P. , Duka, T. , Berris, S. , and Moss, G. (2004). Koalas on Kangaroo Island: from introduction to pest status in less than a century. Wildlife Research 31, 267–272.
| Crossref | GoogleScholarGoogle Scholar | Pahl L. , Wylie F. , and Fisher R. (1990). Koala population decline associated with loss of habitat, and suggested remedial strategies. In ‘Koala Summit: Managing Koalas in New South Wales’. (Ed. P. Reed.) pp. 39–47. (NSW National Parks and Wildlife Service: Sydney.)

Park, W.-H. , and Hutson, J. M. (1991). A new inbred rat strain (TS) with suprainguinal ectopic testes: a model for human cryptorchidism. Pediatric Surgery International 6, 172–175.
| Crossref | GoogleScholarGoogle Scholar | Rozen S. , and Skaletsky H. J. (2000). Primer3 on the WWW for general users and for biologist programmers. In ‘Bioinformatics methods and protocols: methods in molecular biology’. (Eds S. Krawetz and S. Misener.) pp. 365–386. (Humana Press: Totowa, NJ.)

Seymour, A. M. , Montgomery, M. E. , Costello, B. H. , Ihle, S. , Johnsson, G. , St John, B. , Taggart, D. , and Houlden, B. A. (2001). High effective inbreeding coefficients correlate with morphological abnormalities in populations of South Australian koalas (Phascolarctos cinereus). Animal Conservation 4, 211–219.
| Crossref | GoogleScholarGoogle Scholar | Strahan R. , and Martin R. (1982). The Koala: little fact, much emotion. In ‘Species at risk, research in Australia’. (Eds R. Groves and W. Ride.) pp. 147–155. (Australian Academy of Science: Canberra.)

Tallmon, D. A. , Luikart, G. , and Waples, R. S. (2004). The alluring simplicity and complex reality of genetic rescue. Trends in Ecology & Evolution 19, 489–496.
| Crossref | GoogleScholarGoogle Scholar |

Tarlinton, R. E. , Meers, J. , and Young, P. R. (2006). Retroviral invasion of the koala genome. Nature 442, 79–81.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Taylor, A. C. , Graves, J. A. , Murray, N. D. , and Sherwin, W. B. (1991). Conservation genetics of the koala (Phascolarctos cinereus). II. Limited variability in minisatellite DNA sequences. Biochemical Genetics 29, 355–363.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Taylor, A. , Sherwin, W. , and Wayne, R. (1994). Genetic variation of microsatellite loci in a bottleneck species: the northern hairy nosed wombat Lasiorhinus krefftii. Molecular Ecology 3, 277–290.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Taylor, A. C. , Graves, J. M. , Murray, N. D. , O’Brien, S. J. , Yuhki, N. , and Sherwin, B. (1997). Conservation genetics of the koala (Phascolarctos cinereus): low mitochondrial DNA variation amongst southern Australian populations. Genetical Research 69, 25–33.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Tsitrone, A. , Rousset, F. , and David, P. (2001). Heterosis, marker mutational processes and population inbreeding history. Genetics 159, 1845–1859.
|  CAS | PubMed |

Vilà, C. , Sundqvist, A.-K. , Flagstad, Ø. , Seddon, J. , Bjornerfeldt, S. , Kojola, I. , Casulli, A. , Sand, H. , Wabakken, P. , and Ellegren, H. (2003). Rescue of a severely bottlenecked wolf (Canis lupus) population by a single immigrant. Proceedings of the Royal Society of London. Series B. Biological Sciences 270, 91–97.
| Crossref | GoogleScholarGoogle Scholar |

Vucetich, J. A. , and Waite, T. A. (1999). Erosion of heterozygosity in fluctuating populations. Conservation Biology 13, 860–868.
| Crossref | GoogleScholarGoogle Scholar |

Weir, B. S. , and Cockerham, C. C. (1984). Estimating F-statistics for the analysis of population-structure. Evolution 38, 1358–1370.
| Crossref | GoogleScholarGoogle Scholar |

Worthington, J. M. W. , Melzer, A. , Carrick, F. , and Moritz, C. (1993). Low genetic diversity and inbreeding depression in Queensland koalas. Wildlife Research 20, 177–188.
| Crossref | GoogleScholarGoogle Scholar |