Genetic mixing in conservation translocations increases diversity of a keystone threatened species, Bettongia lesueur.

Barrow Island Shark Bay Islands burrowing bettong conservation ddRADseq historical DNA target capture translocation

Journal

Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478

Informations de publication

Date de publication:
16 Sep 2023
Historique:
revised: 11 07 2023
received: 10 04 2023
accepted: 17 08 2023
medline: 16 9 2023
pubmed: 16 9 2023
entrez: 16 9 2023
Statut: aheadofprint

Résumé

Translocation programmes are increasingly being informed by genetic data to monitor and enhance conservation outcomes for both natural and established populations. These data provide a window into contemporary patterns of genetic diversity, structure and relatedness that can guide managers in how to best source animals for their translocation programmes. The inclusion of historical samples, where possible, strengthens monitoring by allowing assessment of changes in genetic diversity over time and by providing a benchmark for future improvements in diversity via management practices. Here, we used reduced representation sequencing (ddRADseq) data to report on the current genetic health of three remnant and seven translocated boodie (Bettongia lesueur) populations, now extinct on the Australian mainland. In addition, we used exon capture data from seven historical mainland specimens and a subset of contemporary samples to compare pre-decline and current diversity. Both data sets showed the significant impact of population founder source (whether multiple or single) on the genetic diversity of translocated populations. Populations founded by animals from multiple sources showed significantly higher genetic diversity than the natural remnant and single-source translocation populations, and we show that by mixing the most divergent populations, exon capture heterozygosity was restored to levels close to that observed in pre-decline mainland samples. Relatedness estimates were surprisingly low across all contemporary populations and there was limited evidence of inbreeding. Our results show that a strategy of genetic mixing has led to successful conservation outcomes for the species in terms of increasing genetic diversity and provides strong rationale for mixing as a management strategy.

Identifiants

pubmed: 37715549
doi: 10.1111/mec.17119
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Informations de copyright

© 2023 Commonwealth of Australia. Arid Recovery. Australian Wildlife Conservancy and The Authors. Molecular Ecology published by John Wiley & Sons Ltd.

Références

Amos, W., Worthington Wilmer, J., Fullard, K., Burg, T. M., Croxall, J. P., Bloch, D., & Coulson, T. (2001). The influence of parental relatedness on reproductive success. Proceedings of the Royal Society B: Biological Sciences, 268(1480), 2021-2027.
Andrews, S. (2010). FastQC: A quality control tool for high throughput sequence data. https://www.bioinformatics.babraham.ac.uk/projects/download.html#fastqc.
Bannister, H. L., Letnic, M., Blumstein, D. T., & Moseby, K. E. (2021). Individual traits influence survival of a reintroduced marsupial only at low predator densities. Animal Conservation, 24(5), 904-913.
Bannister, H. L., Lynch, C. E., & Moseby, K. E. (2016). Predator swamping and supplementary feeding do not improve reintroduction success for a threatened Australian mammal, Bettongia lesueur. Australian Mammalogy, 38(2), 177-187.
Bi, K., Linderoth, T., Singhal, S., Vanderpool, D., Patton, J. L., Nielsen, R., Moritz, C., & Good, J. M. (2019). Temporal genomic contrasts reveal rapid evolutionary responses in an alpine mammal during recent climate change. PLoS Genetics, 15(5), e1008119.
Bice, J., & Moseby, K. (2008). Diets of the re-introduced greater bilby (Macrotis lagotis) and burrowing bettong (Bettongia lesueur) in the Arid Recovery Reserve, Northern South Australia. Australian Mammalogy, 30(1), 1-12.
Bieback, I., & Keller, L. F. (2009). A strong genetic footprint of the re-introduction history of alpine ibex (Capra ibex ibex). Molecular Ecology, 18, 5046-5058.
Bragg, J. G., Potter, S., Bi, K., Catullo, R., Donnellan, S. C., Eldridge, M. D. B., Joseph, L., Keogh, J. S., Oliver, P., Rowe, K. C., & Moritz, C. (2017). Resources for phylogenomic analyses of Australian terrestrial vertebrates. Molecular Ecology Resources, 17(5), 869-876.
Burbidge, A. A., McKenzie, N. L., Brennan, K. E. C., Woinarski, J. C. Z., Dickman, C. R., Baynes, A., Gordon, G., Menkhorst, P. W., & Robinson, A. C. (2008). Conservation status and biogeography of Australia's terrestrial mammals. Australian Journal of Zoology, 56(6), 411.
Burbidge, A. A., & Short, J. C. (2008). In S. Van Dyck & R. Strahan (Eds.), The mammals of Australia. New Holland Publishers.
Byrne, A. Q., Richards-Zawacki, C. L., Voyles, J., Bi, K., Ibáñez, R., & Rosenblum, E. B. (2021). Whole exome sequencing identifies the potential for genetic rescue in iconic and critically endangered Panamanian harlequin frogs. Global Change Biology, 27(1), 50-70.
Capel, S. L. R., Bouzat, J. L., Catchen, J. M., Johnson, J. A., Dunn, P. O., & Paige, K. N. (2022). Evaluating the genome-wide impacts of species translocations: The greater prairie-chicken as a case study. Conservation Genetics, 23(1), 179-191.
Cardoso, M. J., Eldridge, M. D. B., Oakwood, M., Rankmore, B., Sherwin, W. B., & Firestone, K. B. (2009). Effects of founder events on the genetic variation of translocated island populations: Implications for conservation management of the northern quoll. Conservation Genetics, 10(6), 1719-1733.
Catchen, J., Hohenlohe, P. A., Bassham, S., Amores, A., & Cresko, W. A. (2013). Stacks: An analysis tool set for population genomics. Molecular Ecology, 22(11), 3124-3140.
Chapman, T. F., Sims, C., Thomas, N. D., & Reinhold, L. (2015). Assessment of mammal populations on Bernier and Dorre Island 2006-2013. Department of Parks and Wildlife.
Coulon, A. (2010). GENHET: An easy-to-use R function to estimate individual heterozygosity. Molecular Ecology Resources, 10(1), 167-169.
Criscuolo, A., & Gribaldo, S. (2010). BMGE (block mapping and gathering with entropy): A new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evolutionary Biology, 10, 210.
Dalziel, A. E., Sainsbury, A. W., McInnes, K., Jakob-Hoff, R., & Ewen, J. G. (2017). A comparison of disease risk analysis tools for conservation translocations. EcoHealth, 14, 30-41.
Danecek, P., Auton, A., Abecasis, G., Albers, C. A., Banks, E., DePristo, M. A., Handsaker, R. E., Lunter, G., Marth, G. T., Sherry, S. T., McVean, G., & Durbin, R. (2011). The variant call format and VCFtools. Bioinformatics, 27(15), 2156-2158.
Do, C., Waples, R. S., Peel, D., Macbeth, G. M., Tillett, B. J., & Ovenden, J. R. (2014). NeEstimator V2: Re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Molecular Ecology Resources, 14, 209-214.
Doherty, T. S., Dickman, C. R., Nimmo, D. G., & Ritchie, E. G. (2015). Multiple threats, or multiplying the threats? Interactions between invasive predators and other ecological disturbances. Biological Conservation, 190, 60-68.
Doherty, T. S., Glen, A. S., Nimmo, D. G., Ritchie, E. G., & Dickman, C. R. (2016). Invasive predators and global biodiversity loss. Proceedings of the National Academy of Sciences of the United States of America, 113(40), 11261-11265.
Duchene, D. A., Bragg, J. G., Duchene, S., Neaves, L. E., Potter, S., Moritz, C., Johnson, R. N., Ho, S. Y. W., & Eldridge, M. D. B. (2018). Analysis of phylogenomic tree space resolves relationships among marsupial families. Systematic Biology, 67(3), 400-412.
Duncan, R. P., Dexter, N., Wayne, A., & Hone, J. (2020). Eruptive dynamics are common in managed mammal populations. Ecology, 101, e03175.
Eldridge, M. D. B., Kinnear, J. E., Zenger, K. R., McKenzie, L. M., & Spencer, P. B. S. (2004). Genetic diversity in remnant mainland and “pristine” Island populations of three endemic Australian macropodids (Marsupialia): Macropus eugenii, Lagorchestes hirsutus and Petrogale lateralis. Conservation Genetics, 5(3), 325-338.
Eldridge, M. D. B., Neaves, L. E., & Spencer, P. B. S. (2019). Genetic analysis of three remnant populations of the rufous hare-wallaby (Lagorchestes hirsutus) in arid Australia. Australian Mammalogy, 41(1), 123-131.
Farquharson, K. A., McLennan, E. A., Wayne, A., Smith, M., Peel, E., Belov, K., & Hogg, C. J. (2021). Metapopulation management of a critically endangered marsupial in the age of genomics. Global Ecology and Conservation, 31(August), e01869.
Fitzpatrick, S. W., Gerberich, J. C., Kronenberger, J. A., Angeloni, L. M., & Funk, W. C. (2015). Locally adapted traits maintained in the face of high gene flow. Ecology Letters, 18(1), 37-47.
Frankham, R. (1997). Do Island populations have less genetic variation than mainland populations? Heredity, 78, 311-327.
Frankham, R. (2007). Genetic adaptation to captivity in species conservation programs. Molecular Ecology, 17, 325-333.
Frankham, R. (2015). Genetic rescue of small inbred populations: Meta-analysis reveals large and consistent benefits of gene flow. Molecular Ecology, 24, 2610-2618.
Frankham, R., Ballou, J. D., & Briscoe, D. A. (2010). Introduction to conservation genetics. Cambridge University Press.
Frankham, R., Ballou, J. D., Eldridge, M. D. B., Lacy, R. C., Ralls, K., Dudash, M. R., & Fenster, C. B. (2011). Predicting the probability of outbreeding depression: Predicting outbreeding depression. Conservation Biology, 25(3), 465-475.
Frankham, R., Bradshaw, C. J. A., & Brook, B. W. (2014). Genetics in conservation management: Revised recommendations for the 50/500 rules, red list criteria and population viability analyses. Biological Conservation, 170, 56-63.
Franklin, I. R. (1980). Evolutionary change in small populations. In M. E. Soulé & B. A. Wilcox (Eds.), Conservation biology: An evolutionary-ecological perspective (pp. 135-149). Sinauer Associates.
Gonzalez, A., Ronce, O., Ferriere, R., & Hochberg, M. E. (2013). Evolutionary rescue: An emerging focus at the intersection between ecology and evolution. Philosophical Transactions of the Royal Society B: Biological Sciences, 368(1610), 20120404. https://doi.org/10.1098/rstb.2012.0404
Gosselin, T., Lamothe, M., Devloo-Delva, F., & Grewe, P. (2020). Radiator: RADseq data exploration, manipulation and visualization using R. R package version 1.1.5.
Gruber, B., Unmack, P. J., Berry, O. F., & Georges, A. (2018). DARTR: An R package to facilitate analysis of SNP data generated from reduced representation genome sequencing. Molecular Ecology Resources, 18(3), 691-699.
Gustafson, K. D., Winston Vickers, T., Boyce, W. M., & Ernest, H. B. (2017). A single migrant enhances the genetic diversity of an inbred puma population. Royal Society Open Science, 4, 170115.
Hedrick, P. W., Gutierrez-Espeleta, G. A., & Lee, R. N. (2001). Founder effect in an Island population of bighorn sheep. Molecular Ecology, 10(4), 851-857.
Hoban, S., Archer, F. I., Bertola, L. D., Bragg, J. G., Breed, M. F., Bruford, M. W., Coleman, M. A., Ekblom, R., Funk, W. C., Grueber, C. E., Hand, B. K., Jaffé, R., Jensen, E., Johnson, J. S., Kershaw, F., Liggins, L., MacDonald, A. J., Mergeay, J., Miller, J. M., … Hunter, M. E. (2022). Global genetic diversity status and trends: Towards a suite of essential biodiversity variables (EBVs) for genetic composition. Biological Reviews, 97(4), 1511-1538.
Hoffmann, A. A., Miller, A. D., & Weeks, A. R. (2021). Genetic mixing for population management: From genetic rescue to provenancing. Evolutionary Applications, 14(3), 634-652.
Hofman, C. A., Rick, T. C., Fleischer, R. C., & Maldonado, J. E. (2015). Conservation archaeogenomics: Ancient DNA and biodiversity in the Anthropocene. Trends in Ecology & Evolution, 30(9), 540-549.
Holderegger, R., Kamm, U., & Gugerli, F. (2006). Adaptive vs. neutral genetic diversity: Implications for landscape genetics. Landscape Ecology, 21, 797-807.
Hone, J., Duncan, R. P., & Forsyth, D. M. (2010). Estimates of maximum annual population growth rates (rm) of mammals and their application in wildlife management. Journal of Applied Ecology, 47(3), 507-514.
Hufford, K. M., & Mazer, S. J. (2003). Plant ecotypes: Genetic differentiation in the age of ecological restoration. Trends in Ecology and Evolution, 18(3), 147-155.
IUCN/SSC. (2013). Guidelines for reintroductions and other conservation translocations. Version 1.0. (p. viiii + 57 pp.). IUCN Species Survival Commission.
Jamieson, I. G., & Allendorf, F. W. (2012). How does the 50/500 rule apply to MVPs? Trends in Ecology & Evolution, 27(10), 578-584.
Jombart, T., & Ahmed, I. (2011). adegenet 1.3-1: New tools for the analysis of genome-wide SNP data. Bioinformatics, 21, 3070-3071.
Joseph, L., Boussès, P., Wilke, T., & Austin, J. J. (2016). Ancient DNA resolves the subspecific identity of the holotype of the Galah Eolophus roseicapilla, a widespread Australian cockatoo. Emu - Austral Ornithology, 116(4), 472-475.
Kimura, M. (1983). The neutral theory of molecular evolution. Cambridge University Press.
Kolde, R. (2018). Pheatmap: Pretty heatmaps. R package version 1.0.10.
Kopatz, A., Eiken, H. G., Schregel, J., Aspi, J., Kojola, I., & Hagen, S. B. (2017). Genetic substructure and admixture as important factors in linkage disequilibrium-based estimation of effective number of breeders in recovering wildlife populations. Ecology and Evolution, 7(24), 10721-10732.
Lambert, D. M., King, T., Shepherd, L. D., Livingston, A., Anderson, S., & Craig, J. L. (2005). Serial population bottlenecks and genetic variation: Translocated populations of the New Zealand Saddleback (Philesturnus carunculatus rufusater). Conservation Genetics, 6(1), 1-14.
Legge, S., Woinarski, J. C. Z., Burbidge, A. A., Palmer, R., Ringma, J., Radford, J. Q., Mitchell, N., Bode, M., Wintle, B., Baseler, M., Bentley, J., Copley, P., Dexter, N., Dickman, C. R., Gillespie, G. R., Hill, B., Johnson, C. N., Latch, P., Letnic, M., … Tuft, K. (2018). Havens for threatened Australian mammals: The contributions of fenced areas and offshore islands to the protection of mammal species susceptible to introduced predators. Wildlife Research, 45(7), 627-644.
Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., Marth, G., Abecasis, G., & Durbin, R. (2009). The sequence alignment/map format and SAMtools. Bioinformatics, 25(16), 2078-2079.
Li, H., & Durbin, R. (2009). Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25(14), 1754-1760.
Liddell, E., Sunnucks, P., & Cook, C. N. (2021). To mix or not to mix gene pools for threatened species management? Few studies use genetic data to examine the risks of both actions, but failing to do so leads disproportionately to recommendations for separate management. Biological Conservation, 256, 109072.
Lomolino, M. V., & Channell, R. (1995). Splendid isolation: Patterns of geographic range collapse in endangered mammals. Journal of Mammalogy, 76(2), 335-347.
Lott, M. J., Wright, B. R., Neaves, L. E., Frankham, G. J., Dennison, S., Eldridge, M. D. B., Potter, S., Alquezar-Planas, D. E., Hogg, C. J., Belov, K., & Johnson, R. N. (2022). Future-proofing the koala: Synergising genomic and environmental data for effective species management. Molecular Ecology, 31(11), 3035-3055.
Manichaikul, A., Mychaleckyj, J. C., Rich, S. S., Daly, K., Sale, M., & Chen, W. M. (2010). Robust relationship inference in genome-wide association studies. Bioinformatics, 26(22), 2867-2873.
Meyer, M., & Kircher, M. (2010). Illumina sequencing library preparation for highly multiplexed target capture and sequencing. Cold Spring Harbor Protocols, 5(6), pdb.prot5448.
Mills, H. R., Moro, D., & Spencer, P. B. S. (2004). Conservation significance of island versus mainland populations: A case study of dibblers (Parantechinus apicalis) in Western Australia. Animal Conservation, 7(4), 387-395.
Mills, L. S., & Smouse, P. E. (1994). Demographic consequences of inbreeding in remnant populations. The American Naturalist, 144(3), 412-431.
Mock, K. E., Latch, E. K., & Rhodes, O. E. (2004). Assessing losses of genetic diversity due to translocation: Long-term case histories in Merriam's turkey (Meleagris gallopavo merriami). Conservation Genetics, 5, 631-645.
Morris, K. D., Page, M., Kay, R., Renwick, J., Desmond, A., Comer, S., Burbidge, A., Kuchling, G., & Sims, C. (2015). Forty years of fauna translocations in Western Australia: Lessons learned. In Advances in reintroduction biology of Australian and New Zealand Fauna (pp. 217-236). CSIRO Publishing.
Nei, M., Maruyama, T., & Chakraborty, R. (1975). The bottleneck effect and genetic variability in populations. Evolution, 29, 1-10.
Ottewell, K., Dunlop, J., Thomas, N., Morris, K., Coates, D., & Byrne, M. (2014). Evaluating success of translocations in maintaining genetic diversity in a threatened mammal. Biological Conservation, 171, 209-219.
Pacifici, M., Santini, L., Di Marco, M., Baisero, D., Francucci, L., Marasini, G. G., Visconti, P., & Rondinini, C. (2013). Generation length for mammals. Nature Conservation, 5, 87-94.
Palmer, B. J., Valentine, L. E., Lohr, C. A., Daskalova, G. N., & Hobbs, R. J. (2021). Burrowing by translocated boodie (Bettongia lesueur) populations alters soils but has limited effects on vegetation. Ecology and Evolution, 11(6), 2596-2615.
Parsons, B. C., Short, J. C., & Calver, M. C. (2002). Evidence for male-biased dispersal in a reintroduced population of burrowing Bettongs Bettongia lesueur at Heirisson Prong, Western Australia. Australian Mammalogy, 24(2), 219-224.
Peel, E., Silver, L., Brandies, P., Hogg, C. J., & Belov, K. (2021). A reference genome for the critically endangered woylie, Bettongia penicillata ogilbyi. Gigabyte, 2021, 1-15.
Pembleton, L. W., Cogan, N. O. I., & Forster, J. W. (2013). StAMPP: An R package for calculation of genetic differentiation and structure of mixed-ploidy level populations. Molecular Ecology Resources, 13(5), 946-952.
Poirier, M., Coltman, D. W., Pelletier, F., Jorgenson, J., & Festa-Bianchet, M. (2019). Genetic decline, restoration and rescue of an isolated ungulate population. Evolutionary Applications, 12(7), 1318-1328. https://doi.org/10.1111/eva.12706
Potter, S., Eldridge, M. D. B., Cooper, S. J. B., Paplinska, J., & Taggart, D. A. (2012). Habitat connectivity, more than species' biology influences genetic differentiation in a habitat specialist, the short-eared rock-wallaby (Petrogale brachyotis). Conservation Genetics, 13, 937-952.
Puckett, E. E., Kristensen, T. V., Wilton, C. M., Lyda, S. B., Noyce, K. V., Holahan, P. M., Leslie, D. M., Beringer, J., Belant, J. L., White, D., & Eggert, L. S. (2014). Influence of drift and admixture on population structure of American black bears (Ursus americanus) in the Central Interior Highlands, USA, 50 years after translocation. Molecular Ecology, 23(10), 2414-2427. https://doi.org/10.1111/mec.12748
R Core Team. (2021). R: A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.r-project.org/
Raj, A., Stephens, M., & Pritchard, J. K. (2014). FastSTRUCTURE: Variational inference of population structure in large SNP data sets. Genetics, 197(2), 573-589.
Ralls, K., Ballou, J. D., Dudash, M. R., Eldridge, M. D. B., Fenster, C. B., Lacy, R. C., Sunnucks, P., & Frankham, R. (2018). Call for a paradigm shift in the genetic management of fragmented populations. Conservation Letters, 11(2), 1-6.
Ralls, K., Sunnucks, P., Lacy, R. C., & Frankham, R. (2020). Genetic rescue: A critique of the evidence supports maximizing genetic diversity rather than minimizing the introduction of putatively harmful genetic variation. Biological Conservation, 251(April), 108784.
Richards, J. D. (2012). Western barred bandicoot Perameles bougainville, burrowing Bettong Bettongia lesueur and banded hare-wallaby Lagostrophus fasciatus National Recovery Plan. Department of Environment and Conservation.
Rick, K., Ottewell, K., Lohr, C., Thavornkanlapachai, R., Byrne, M., & Kennington, W. J. (2019). Population genomics of Bettongia lesueur: Admixing increases genetic diversity with no evidence of outbreeding depression. Genes, 10(11), 851.
Ride, W. D. L., Mees, G. F., Douglas, A. M., Royce, R. D., & Tyndale-Biscoe, C. H. (1962). The results of an expedition to Bernier and Dorre Islands, Shark Bay, Western Australia in July 1959. Fauna Bulletin 2. Perth Government Printer.
Ringma, J., Legge, S., Woinarski, J., Radford, J., Wintle, B., & Bode, M. (2018). Australia's mammal fauna requires a strategic and enhanced network of predator-free havens. Nature Ecology and Evolution, 2(3), 410-411.
Roycroft, E., Macdonald, A. J., Moritz, C., Moussalli, A., Portela Miguez, R., & Rowe, K. C. (2021). Museum genomics reveals the rapid decline and extinction of Australian rodents since European settlement. Proceedings of the National Academy of Sciences of the United States of America, 118, e2021390118.
Roycroft, E., Moritz, C., Rowe, K. C., Moussalli, A., Eldridge, M. D. B., Portela Miguez, R., Piggott, M. P., & Potter, S. (2022). Sequence capture from historical museum specimens: Maximizing value for population and phylogenomic studies. Frontiers in Ecology and Evolution, 10, 931644.
Roycroft, E. J., Moussalli, A., & Rowe, K. C. (2020). Phylogenomics uncovers confidence and conflict in the rapid radiation of Australo-Papuan rodents. Systematic Biology, 69(3), 431-444.
Russell, J. C., & Fewster, R. M. (2009). Evaluation of the linkage disequilibrium method for estimating effective population size. In D. L. Thomson, E. G. Cooch, & M. J. Conroy (Eds.), Modeling demographic processes in marked populations (Vol. 3, pp. 291-320). Environmental and Ecological Statistics Series). Springer.
Sander, U., Short, J., & Turner, B. (1997). Social organisation and warren use of the burrowing bettong, Bettongia lesueur (Macropodoidea: Potoroidae). Wildlife Research, 24(2), 143-157.
Schmidt, T. L., Jasper, M., Weeks, A. R., & Hoffmann, A. A. (2021). Unbiased population heterozygosity estimates from genome-wide sequence data. Methods in Ecology and Evolution, 12(10), 1888-1898.
Seaborn, T., Andrews, K. R., Applestein, C. V., Breech, T. M., Garrett, M. J., Zaiats, A., & Caughlin, T. T. (2021). Integrating genomics in population models to forecast translocation success. Restoration Ecology, 29(4), 1-12.
Short, J. (2009). The characteristics and success of vertebrate translocations within Australia: A progress report to Department of Agriculture, Fisheries and Forestry. June 2009.
Short, J., & Smith, A. (1994). Mammal decline and recovery in Australia. Journal of Mammalogy, 75(2), 288-297.
Short, J., & Turner, B. (1999). Ecology of burrowing bettongs, Bettongia lesueur (Marsupialia: Potoroidae), on Dorre and Bernier Islands, Western Australia. Wildlife Research, 26, 651-669.
Short, J., & Turner, B. (2000). Reintroduction of the burrowing bettong Bettongia lesueur (Marsupialia: Potoroidae) to mainland Australia. Biological Conservation, 96, 185-196.
Short, J., Turner, B., Majors, C., & Leone, J. (1998). The fluctuating abundance of endangered mammals on Bernier and Dorre Islands, Western Australia-Conservation implications. Australian Mammalogy, 20(1), 53.
Smith, S., & Hughes, J. (2008). Microsatellite and mitochondrial DNA variation defines island genetic reservoirs for reintroductions of an endangered Australian marsupial, Perameles Bougainville. Conservation Genetics, 9(3), 547-557.
Spencer, P. B. S., Adams, M., Marsh, H., Miller, D. J., & Eldridge, M. D. B. (1997). High levels of genetic variability in an isolated colony of Rock-wallabies (Petrogale assimilis): Evidence from three classes of molecular markers. Australian Journal of Zoology, 45(2), 199-210.
Sunnucks, P., & Hales, D. F. (1996). Numerous transposed sequences of mitochondrial cytochrome oxidase I-II in aphids of the genus Sitobion (Hemiptera: Aphididae). Molecular Biology and Evolution, 13(3), 510-524.
Tay, N. E., Fleming, P. A., Warburton, N. M., & Moseby, K. E. (2021). Predator exposure enhances the escape behaviour of a small marsupial, the burrowing bettong. Animal Behaviour, 175, 45-56.
Taylor, S. S., & Jamieson, I. G. (2008). No evidence for loss of genetic variation following sequential translocations in extant populations of a genetically depauperate species. Molecular Ecology, 17, 545-556.
Teixeira, J. C., & Huber, C. D. (2021). The inflated significance of neutral genetic diversity in conservation genetics. Proceedings of the National Academy of Sciences of the United States of America, 118(10), 1-10.
Thavornkanlapachai, R., Mills, H. R., Ottewell, K., Dunlop, J., Sims, C., Morris, K., Donaldson, F., & Kennington, W. J. (2019). Mixing genetically and morphologically distinct populations in translocations: Asymmetrical introgression in a newly established population of the Boodie (Bettongia lesueur). Genes, 10(9), 1-18.
Thomas, N., Friend, T., & Marlow, N. (2003). Translocation proposal. Reintroduction of the Boodie (Bettongia lesueur) to Dryandra woodland from the return to Dryandra field breeding facility June 2003. Department of Environment and Conservation, Perth.
Treloar, S., Lohr, C., Hopkins, A. J. M., & Davis, R. A. (2021). Rapid population expansion of Boodie (Burrowing Bettong, Bettongia lesueur) creates potential for resource competition with Mala (Rufous Hare-wallaby, Lagorchestes hirsutus). Ecological Management & Restoration, 22(S1), 54-57.
Watterson, I., Abbs, D., Bhend, J., Chiew, F., Church, J., Ekstrom, M., Kirono, D., Lenton, A., Lucas, C., McInnes, K., Moise, A., Monselesan, D., Mpelasoka, F., Webb, L., & Whetton, P. (2015). Rangelands cluster report, climate change in Australia projections for Australia's natural resource management regions: Cluster reports. CSIRO and Bureau of Meteorology.
Weeks, A. R., Sgro, C. M., Young, A. G., Frankham, R., Mitchell, N. J., Miller, K. A., Byrne, M., Coates, D. J., Eldridge, M. D. B., Sunnucks, P., Breed, M. F., James, E. A., & Hoffmann, A. A. (2011). Assessing the benefits and risks of translocations in changing environments: A genetic perspective. Evolutionary Applications, 4(6), 709-725.
Weeks, A. R., Stoklosa, J., & Hoffmann, A. A. (2016). Conservation of genetic uniqueness of populations may increase extinction likelihood of endangered species: The case of Australian mammals. Frontiers in Zoology, 13(1), 1-9.
White, L. C., Moseby, K. E., Thomson, V. A., Donnellan, S. C., & Austin, J. J. (2018). Long-term genetic consequences of mammal reintroductions into an Australian conservation reserve. Biological Conservation, 219, 1-11.
White, L. C., Thomson, V. A., West, R., Ruykys, L., Ottewell, K., Kanowski, J., Moseby, K. E., Byrne, M., Donnellan, S. C., Copley, P., & Austin, J. J. (2020). Genetic monitoring of the greater stick-nest rat meta-population for strategic supplementation planning. Conservation Genetics, 21(5), 941-956.
Wickham, H. (2016). ggplot2: Elegant graphics for data analysis. Springer-Verlag.
Willi, Y., Kristensen, T. N., Sgro, C. M., Weeks, A. R., Orsted, M., & Hoffmann, A. A. (2022). Conservation genetics as a management tool: The five best-supported paradigms to assist the management of threatened species. Proceedings of the National Academy of Sciences of the United States of America, 119, e2105076119.
Wisely, S. M., Santymire, R. M., Livieri, T. M., Mueting, S. A., & Howard, J. (2008). Genotypic and phenotypic consequences of reintroduction history in the black-footed ferret (Mustela nigripes). Conservation Genetics, 9(2), 389-399. https://doi.org/10.1007/s10592-007-9351-x
Woinarski, J. C. Z., Burbidge, A. A., & Harrison, P. L. (2015). Ongoing unraveling of a continental fauna: Decline and extinction of Australian mammals since European settlement. Proceedings of the National Academy of Sciences of the United States of America, 112(15), 4531-4540.
Wright, D. J., Spurgin, L. G., Collar, N. J., Komdeur, J., Burke, T., & Richardson, D. S. (2014). The impact of translocations on neutral and functional genetic diversity within and among populations of the Seychelles warbler. Molecular Ecology, 23(9), 2165-2177.
Zecherle, L. J., Nichols, H. J., Bar-David, S., Brown, R. P., Hipperson, H., Horsburgh, G. J., & Templeton, A. R. (2021). Subspecies hybridization as a potential conservation tool in species reintroductions. Evolutionary Applications, 14(5), 1216-1224.

Auteurs

Heidi M Nistelberger (HM)

Biodiversity and Conservation Science, Department of Biodiversity, Conservation and Attractions, Kensington, Western Australia, Australia.

Emily Roycroft (E)

Division of Ecology & Evolution, Research School of Biology, ANU College of Science, The Australian National University, Canberra, Australian Capital Territory, Australia.

Anna J Macdonald (AJ)

Division of Ecology & Evolution, Research School of Biology, ANU College of Science, The Australian National University, Canberra, Australian Capital Territory, Australia.

Shelley McArthur (S)

Biodiversity and Conservation Science, Department of Biodiversity, Conservation and Attractions, Kensington, Western Australia, Australia.

Lauren C White (LC)

Department of Environment, Land, Water and Planning, Arthur Rylah Institute for Environmental Research, Heidelberg, Victoria, Australia.

Patrick G S Grady (PGS)

Department of Molecular and Cell Biology, University of Connecticut, Storrs, Connecticut, USA.

Jennifer Pierson (J)

Australian Wildlife Conservancy, Subiaco, Western Australia, Australia.

Colleen Sims (C)

Biodiversity and Conservation Science, Department of Biodiversity, Conservation and Attractions, Kensington, Western Australia, Australia.

Saul Cowen (S)

Biodiversity and Conservation Science, Department of Biodiversity, Conservation and Attractions, Kensington, Western Australia, Australia.

Katherine Moseby (K)

Centre for Ecosystem Science, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, New South Wales, Australia.

Katherine Tuft (K)

Arid Recovery, Roxby Downs, South Australia, Australia.

Craig Moritz (C)

Division of Ecology & Evolution, Research School of Biology, ANU College of Science, The Australian National University, Canberra, Australian Capital Territory, Australia.

Mark D B Eldridge (MDB)

Terrestrial Vertebrates, Australian Museum Research Institute, Sydney, New South Wales, Australia.

Margaret Byrne (M)

Biodiversity and Conservation Science, Department of Biodiversity, Conservation and Attractions, Kensington, Western Australia, Australia.

Kym Ottewell (K)

Biodiversity and Conservation Science, Department of Biodiversity, Conservation and Attractions, Kensington, Western Australia, Australia.

Classifications MeSH