Abstract
Conservation breeding programs, such as fenced reserves, conserve species by removing populations from key threatening processes and providing supplementary resources to support species preservation. This form of management often has the eventual aim to reintroduce individuals back to their native habitat. A key issue with captive management is the small breeding pool, due to generally small population sizes and limited migration, which may lead to inbreeding and consequent inbreeding depression. We investigated inbreeding and its potential fitness consequences in a large, free-ranging, captive population of an Australian marsupial, the long-nosed potoroo (Potorous tridactylus), a species that has been recently impacted by severe bushfire. We used reduced-representation sequencing to genotype single nucleotide polymorphisms and reconstruct a pedigree for the population. We detected low levels of inbreeding in our partial pedigree that incorporated 50.7% (34/67) of sampled individuals. Inbreeding depression was investigated using heterozygosity–fitness correlations of six fitness measurements, but we found no evidence of inbreeding depression in the population despite strong molecular evidence for inter-individual variation in inbreeding coefficient. Our findings suggest that the potoroo population at Tidbinbilla Nature Reserve (TNR) maintains a high level of diversity. As the population is descendant of animals from divergent sources, the TNR population also helps conservationists to learn more about potential consequences of admixture, and plan recovery strategies for the species. For TNR potoroos, we suggest that current management protocols have been effective at maintaining diversity to date. More generally, our results show how modern molecular techniques can efficiently characterise the genetic profile of a free-ranging, captive population to help inform management guidelines for wild recovery.
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References
Alho JS, Välimäki K, Merilä J (2010) Rhh: an R extension for estimating multilocus heterozygosity and heterozygosity–heterozygosity correlation. Mol Ecol Resour 10:720–722
Amos W, Worthington Wilmer J, Fullard K, Burg T, Croxall J, Bloch D, Coulson T (2001) The influence of parental relatedness on reproductive success. Proc R Soc B 268:2021–2027
Aparicio J, Ortego J, Cordero P (2006) What should we weigh to estimate heterozygosity, alleles or loci? Mol Ecol 15:4659–4665
Armbruster P, Reed D (2005) Inbreeding depression in benign and stressful environments. Heredity 95:235
Ballou JD, Lees C, Faust LJ, Long S, Lynch C, Bingaman Lackey L, Foose TJ (2010) Demographic and genetic management of captive populations. In: Kleiman DG, Thompson KV, Kirk Baer C (eds) Wild mammals in captivity: principles and techniques for zoo management. University of Chicago Press, Chicago, pp 291–252
Blyton MDJ, Shaw RE, Peakall R, Lindenmayer DB, Banks SC (2016) The role of relatedness in mate choice by an arboreal marsupial in the presence of fine-scale genetic structure. Behav Ecol 70:313–321
Calaby J, Taylor JM (1981) Reproduction in two marsupial-mice, Antechinus bellus and A. bilarni (Dasyuridae), of tropical Australia. J Mamm 62:329–341
Charlesworth D, Willis JH (2009) The genetics of inbreeding depression. Nat Rev Genet 10:783
Cockburn A, Scott MP, Scotts DJ (1985) Inbreeding avoidance and male-biased natal dispersal in Antechinus spp. (Marsupialia: Dasyuridae). Anim Behav 33:908–915
Conde DA, Flesness N, Colchero F, Jones OR, Scheuerlein A (2011) An emerging role of zoos to conserve biodiversity. Science 331:1390–1391
David P (1998) Heterozygosity–fitness correlations: new perspectives on old problems. Heredity 80:531
David P, Pujol B, Viard F, Castella V, Goudet J (2007) Reliable selfing rate estimates from imperfect population genetic data. Mol Ecol 16:2474–2487
Eldridge MDB, Frankham GJ (2015) Family Potoroidae (bettongs and potoroos). In: Wilson DE, Mittermeier RA (eds) Handbook of the mammals of the world. Monotremes and marsupials, vol 5. Lynx Edicions, Barcelona, pp 600–628
Farquharson KA, Hogg CJ, Grueber CE (2019) A case for genetic parentage assignment in captive group housing. Conserv Genet 20:1187–1193
Frankham GJ, Handasyde KA, Norton M, Murray A, Eldridge MD (2014) Molecular detection of intra-population structure in a threatened potoroid, Potorous tridactylus: conservation management and sampling implications. Conserv Genet 15:547–560
Frankham GJ, Reed RL, Eldridge MD, Handasyde KA (2013) The genetic mating system of the long-nosed potoroo (Potorous tridactylus) with notes on male strategies for securing paternity. Aus J Zool 60:225–234
Frankham R (2015) Genetic rescue of small inbred populations: meta-analysis reveals large and consistent benefits of gene flow. Mol Ecol 24:2610–2618
Frankham GJ, Reed RL, Fletcher TP, Handasyde KA (2011a) Population ecology of the long-nosed potoroo (Potorous tridactylus) on French Island, Victoria. Aus Mamm 33:73–81
Frankham R, Ballou JD, Eldridge MDB, Lacy RC, Ralls K, Dudash MR, Fenster CB (2011b) Predicting the probability of outbreeding depression. Conserv Biol 25:465–475
Frankham R, Ballou JD, Ralls K, Eldridge MDB, Dudash MR, Fenster CB, Lacy RC, Sunnocks P (2017) Genetic management of fragmented animal and plant populations. Oxford University Press, Oxford
Frankham R, Ballou JD, Ralls K, Eldridge MDB, Dudash MR, Fenster CB, Lacy RC, Sunnocks P (2019) A practical guide for genetic management of fragmented animal and plant populations. Oxford University Press, Oxford
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
Gruber B, Unmack PJ, Berry OF, Georges A (2018) dartr: An R package to facilitate analysis of SNP data generated from reduced representation genome sequencing. Mol Ecol Resour 18:691–699
Grueber CE, Peel E, Wright B, Hogg CJ, Belov K (2019) A Tasmanian devil breeding program to support wild recovery. Reprod Fertil Dev 31:1296–1304
Hammerly SC, Morrow ME, Johnson JA (2013) A comparison of pedigree-and DNA-based measures for identifying inbreeding depression in the critically endangered Attwater's Prairie-chicken. Mol Ecol 22:5313–5328
Hedrick PW, Garcia-Dorado A (2016) Understanding inbreeding depression, purging, and genetic rescue. Trends Ecol Evol 31:940–952
Hoffman JI, Simpson F, David P, Rijks JM, Kuiken T, Thorne MA, Lacy RC, Dasmahapatra KK (2014) High-throughput sequencing reveals inbreeding depression in a natural population. Proc Nat Acad Sci USA 111:3775–3780
Hogg CJ, McLennan EA, Wise P, Lee AV, Pemberton D, Fox S, Belov K, Grueber CE (2020) Preserving the demographic and genetic integrity of a single source population during multiple translocations. Biol Conserv 241:108318
Huisman J (2017) Pedigree reconstruction from SNP data: parentage assignment, sibship clustering and beyond. Mol Ecol Resour 17:1009–1024
Isaac JL (2005) Potential causes and life-history consequences of sexual size dimorphism in mammals. Mammal Rev 35:101–115
Johnson SD, Buchmann OLKA (1993) First record of the concurrent presence of sibling pouch young in free-living potoroo (Potorous tridactylus). Mammalia 57:441–441
Kean EF, Bruford MW, Russo I-RM, Müller CT, Chadwick EA (2017) Odour dialects among wild mammals. Sci Rep 7:13593
Keulartz J (2015) Captivity for conservation? Zoos at a crossroads. J Agric Environ Ethics 28:335–351
Lacy RC (1987) Loss of genetic diversity from managed populations: interacting effects of drift, mutation, immigration, selection, and population subdivision. Conserv Biol 1:143–158
Lacy RC, Petric A, Warneke M (1993) Inbreeding and outbreeding in captive populations of wild animal species. In: Thornhill NW (ed) The natural history of inbreeding and outbreeding: theoretical and empirical perspectives. The University of Chicago Press, Chicago, pp 352–374
Legge S, Woinarski J, Garnett S, Scheele B, Lintermans M, Mitchell N, Whiterod N, Ferris J (2020) Rapid analysis of impacts of the 2019-20 fires on animal species, and prioritisation of species for management response. Department of Agriculture, Water and the Environment
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
McLennan EA, Grueber CE, Wise P, Belov K, Hogg CJ (2020) Mixing genetic lineages successfully boosts diversity of an endangered carnivore. Anim Conserv. https://doi.org/10.1111/acv.12589
McLennan EA, Wright BR, Belov K, Hogg CJ, Grueber CE (2019) Too much of a good thing? Finding the most informative genetic dataset to answer conservation questions. Mol Ecol Res 19:659–671
Menkhorst P (1996) Mammals of Victoria. Oxford University Press in association with the Dept. of Conservation and Environment, Oxford
Miller J, Malenfant R, David P, Davis C, Poissant J, Hogg J, Festa-Bianchet M, Coltman D (2014) Estimating genome-wide heterozygosity: effects of demographic history and marker type. Heredity 112:240
Nichols HJ (2017) The causes and consequences of inbreeding avoidance and tolerance in cooperatively breeding vertebrates. J Zool 303:1–14
Norman AJ, Putnam AS, Ivy JA (2019) Use of molecular data in zoo and aquarium collection management: benefits, challenges, and best practices. Zool Biol 38:106–118
Pickrell J (2019) As fires rage across Australia, fears grow for rare species. Science. https://doi.org/10.1126/science.aba6144
R Core Team (2019) R: A language and environment for statistical computing. Vienna. https://www.R-project.org/.
Ralls K, Ballou JD, Dudash MR, Eldridge MDB, Fenster CB, Lacy RC, Sunnucks P, Frankham R (2018) Call for a paradigm shift in the genetic management of fragmented populations. Conserv Lett 11:e12412
Ruiz-López MJ, Gañan N, Godoy JA, Del Olmo A, Garde J, Espeso G, Vargas A, Martinez F, Roldán ER, Gomendio M (2012) Heterozygosity-fitness correlations and inbreeding depression in two critically endangered mammals. Conserv Biol 26:1121–1129
Sargent HJ, Pierson JC, Frankham GJ, Banks SC (in review) Quantifying abundance and genetic diversity of the long-nosed potoroo (Pororous tridactylus) population at Tidbinbilla Nature Reserve to inform population management and potential utility for reintroduction. Conserv Genet.
Schulte-Hostedde AI, Mastromonaco GF (2015) Integrating evolution in the management of captive zoo populations. Evol Appl 8:413–422
Sinnwell JP, Therneau TM, Schaid DJ (2014) The kinship2 R package for pedigree data. J Hered 78:91–93
Stevens EL, Heckenberg G, Roberson ED, Baugher JD, Downey TJ, Pevsner J (2011) Inference of relationships in population data using identity-by-descent and identity-by-state. PLoS Genet 7:e1002287
Stoffel MA, Esser M, Kardos M, Humble E, Nichols H, David P, Hoffman JI (2016) inbreedR: an R package for the analysis of inbreeding based on genetic markers. Meth Ecol Evol 7:1331–1339
Verhoeven KJ, Macel M, Wolfe LM, Biere A (2010) Population admixture, biological invasions and the balance between local adaptation and inbreeding depression. Proc R Soc B 278:2–8
Von Mark VC, Kilian A, Dierig DA (2013) Development of DArT marker platforms and genetic diversity assessment of the US collection of the new oilseed crop lesquerella and related species. PLoS ONE 8:e64062
Weeks AR, Moro D, Thavornkanlapachai R, Taylor HR, White NE, Weiser EL, Heinze D (2015) Conserving and enhancing genetic diversity in translocation programs. In: Armstrong D, Hayward M, Moro D, Seddon PJ (eds) Advances in reintroduction biology of Australian and New Zealand Fauna. CSIRO Publishing, Clayton, pp 127–140
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
Werner J, Lyons S (2020) The size of Australia's bushfire crisis captured in five big numbers. ABC News, Accessed 24 April 2020. https://www.abc.net.au/news/science/2020-03-05/bushfire-crisis-five-big-numbers/12007716, Last updated 5 March 2020.
Witzenberger KA, Hochkirch A (2011) Ex situ conservation genetics: a review of molecular studies on the genetic consequences of captive breeding programmes for endangered animal species. Biodiv Conserv 20:1843–1861
Woinarski J, Burbidge AA. 2016. Potorous tridactylus. The IUCN Red List of Threatened Species 2016: e.T41511A21960633.
Woinarski JC, Burbidge AA, Harrison PL (2015) Ongoing unraveling of a continental fauna: decline and extinction of Australian mammals since European settlement. Proc Nat Acad Sci USA 112:4531–4540
Wright S (1931) Evolution in Mendelian populations. Genetics 16:97
Acknowledgements
We thank the staff at Tidbinbilla Nature Reserve, especially Lisa Steindler and Nicole Hill, for their support during fieldwork, and Holly Sergent for potoroo samples. We acknowledge the members of the University of Sydney Applied and Evolutionary Zoology Group and Australasian Wildlife Genomics Group for fruitful conversations and advice during this project. This study was funded by a University of Sydney Robinson Fellowship to CEG.
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Mulvena, S.R., Pierson, J.C., Farquharson, K.A. et al. Investigating inbreeding in a free-ranging, captive population of an Australian marsupial. Conserv Genet 21, 665–675 (2020). https://doi.org/10.1007/s10592-020-01278-2
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DOI: https://doi.org/10.1007/s10592-020-01278-2