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

Persistence of social structuring in an arid zone mammal following reintroduction

Alexander James Cooke A B , Cheryl Lohr https://orcid.org/0000-0002-8925-0983 A * , W. Jason Kennington B and Kym Ottewell A B
+ Author Affiliations
- Author Affiliations

A Biodiversity Conservation Science, Department of Biodiversity Conservation and Attractions, 17 Dick Perry Avenue, Kensington, WA 6151, Australia.

B School of Biological Sciences, Faculty of Science, The University of Western Australia, 35 Stirling Highway, Perth WA 6009, Australia.

* Correspondence to: Cheryl.lohr@dbca.wa.gov.au

Handling Editor: Mark Eldridge

Australian Mammalogy 46, AM23051 https://doi.org/10.1071/AM23051
Submitted: 24 November 2023  Accepted: 17 June 2024  Published: 18 July 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing on behalf of the Australian Mammal Society.

Abstract

Animal social relationships affect animal survival, reproduction, and resource exploitation, and are important to translocation success, but little is known on how they are impacted in reintroduced populations. Here, we investigate the social genetic structure in a reintroduced population of boodies (Bettongia lesueur), one of few social burrowing marsupial species in Australia. Pairwise relatedness of male and female individuals located within seven warrens was determined using 12 microsatellite markers, while mitochondrial DNA was used to identify maternal ancestral lineage. Females were significantly more related within warrens than between warrens, while the difference among males was not significant. We also found evidence of fine-scale genetic structure up to distances of 2 km in females consistent with patterns found in natural populations. Although mean relatedness values were low, our results support the hypothesis that boodies exhibit a female social structure. Multiple maternal lineages were present within all warrens with one exception, suggesting boodies appear to be non-selective when living with individuals from different ancestral backgrounds. We found a significant positive relationship between female sex bias and the number of active entrances in each warren. Together, these results suggest that social structuring should be a key consideration in future reintroductions of boodies.

Keywords: arid zone, Bettongia lesueur, burrowing bettong, hybrid, Indigenous Protected Area, Lorna Glen, social system, warrens.

References

Allendorf, F. W., Luikart, G., and Aitken, S. N. (2013). ‘Conservation and the genetics of populations’, 2nd edn. (Wiley-Blackwell: Great Britain.)

Anstee, S. D., Roberts, J. D., and O’Shea, J. E. (1997). Social structure and patterns of movement of the western pebble-mound mouse, Pseudomys chapmani, at Marandoo, Western Australia. Wildlife Research 24, 295-305.
| Crossref | Google Scholar |

Armstrong, D. P., Moro, D., Hayward, M., and Seddon, P. J. (2015). The development of reintroduction biology in New Zealand and Australia. In ‘Advances in Reintroduction Biology of Australian and New Zealand Fauna’. (Eds D. P. Armstrong, D. Moro, M. Hayward, P. J. Seddon.) pp. 1–6. (CSIRO Publishing: Melbourne.)

Banks, S. C., Skerratt, L. F., and Taylor, A. C. (2002). Female dispersal and relatedness structure in common wombats (Vombatus ursinus). Journal of Zoology 256, 389-399.
| Crossref | Google Scholar |

Berger-Tal, O., Blumstein, D. T., and Swaisgood, R. R. (2020). Conservation translocations: A review of common difficulties and promising directions. Animal Conservation 23, 121-131.
| Crossref | Google Scholar |

Blumstein, D. T., Wey, T. W., and Tang, K. (2009). A test of the social cohesion hypothesis: Interactive female marmots remain at home. Proceedings of the Royal Society B: Biological Sciences 276, 3007-3012.
| Crossref | Google Scholar | PubMed |

Bode, M., Brennan, K. E. C., Morris, K., Burrows, N., and Hague, N. (2012). Choosing cost-effective locations for conservation fences in the local landscape. Wildlife Research 39, 192-201.
| Crossref | Google Scholar |

Burland, T. M., Bennett, N. C., Jarvis, J. U. M., and Faulkes, C. G. (2002). Eusociality in African mole-rats: New insights from patterns of genetic relatedness in the Damaraland mole-rat (Cryptomys damarensis). Proceedings of the Royal Society B: Biological Sciences 269, 1025-1030.
| Crossref | Google Scholar | PubMed |

Cameron, E. Z., Setsaas, T. H., and Linklater, W. L. (2009). Social bonds between unrelated females increase reproductive success in feral horses. Proceedings of the National Academy of Sciences of the United States of America 106, 13850-13853.
| Crossref | Google Scholar | PubMed |

Carter, G. G., and Wilkinson, G. S. (2015). Social benefits of non-kin food sharing by female vampire bats. Proceedings of the Royal Society B: Biological Sciences 282, 20152524.
| Crossref | Google Scholar | PubMed |

Chapman, C. A., and Chapman, L. J. (2000). Constraints on group size in red colobus and red-tailed guenons: Examining the generality of the ecological constraints model. International Journal of Primatology 21, 565-585.
| Crossref | Google Scholar |

Custance, D. M., Whiten, A., and Fredman, T. (2002). Social learning and primate reintroduction. International Journal of Primatology 23, 479-499.
| Crossref | Google Scholar |

Dakin, E. E., and Avise, J. C. (2004). Microsatellite null alleles in parentage analysis. Heredity 93, 504-509.
| Crossref | Google Scholar | PubMed |

Donaldson, F., and Vercoe, P. (2008). Cross-family amplification: Microsatellites isolated from Macropodidae are polymorphic in Potoroidae. Molecular Ecology Resources 8, 452-454.
| Crossref | Google Scholar | PubMed |

Donaldson, F., Bencini, R., Morris, K., Teale, R., Wale, C., How, R., and Schmitt, L. (2017). The burrowing bettongs of Barrow Island: Demographic and genetic insights into a threatened macropod. Australian Journal of Zoology 65, 257-272.
| Crossref | Google Scholar |

Dunlop, J., Smith, A., Burbidge, A., Thomas, N., and Morris, K. (2021). Industry environmental offset funding facilitates a large multi-species fauna translocation program. Pacific Conservation Biology 28, 231-246.
| Crossref | Google Scholar |

Earnhardt, J. M. (1999). Reintroduction programmes: genetic trade‐offs for populations. Animal Conservation 2, 279-286.
| Crossref | Google Scholar |

Ebensperger, L. A., and Bozinovic, F. (2000). Communal Burrowing in the Hystricognath Rodent, Octodon degus: A Benefit of Sociality? Behavioral Ecology and Sociobiology 47, 365-369.
| Crossref | Google Scholar |

Ebensperger, L. A., Correa, L. A., Ly Prieto, Á., De Arce, F. P., Abades, S., and Hayes, L. D. (2019). Multiple mating is linked to social setting and benefits the males in a communally rearing mammal. Behavioral Ecology 30, 675-687.
| Crossref | Google Scholar |

Efford, M. (2022). secr: Spatially Explicit Capture-Recapture. R package version 4.5.8, 20. Available at https://cran.r-project.org/package=secr [accessed 18 January 2023].

Excoffier, L., and Lischer, H. E. L. (2010). Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564-567.
| Crossref | Google Scholar | PubMed |

Firman, R. C., Rubenstein, D. R., Moran, J. M., Rowe, K. C., and Buzatto, B. A. (2020). Extreme and Variable Climatic Conditions Drive the Evolution of Sociality in Australian Rodents. Current Biology 30, 691-697.e3.
| Crossref | Google Scholar | PubMed |

Fischer, J., and Lindenmayer, D. B. (2000). An assessment of the published results of animal relocations. Biological Conservation 96, 1-11.
| Crossref | Google Scholar |

Frankham, R., Ballou, J., and Briscoe, D. (2010). ‘Introduction to conservation genetics’. 2nd Edn. (Cambridge University Press: Cambridge.)

Friend, T., and Beecham, B. (2004). Return to Dryandra: Western Shield review--February 2003. Conservation Science Western Australia 5, 174-193.
| Google Scholar |

Fumagalli, L., Pope, L. C., Taberlet, P., and Moritz, C. (1997). Versatile primers for the amplification of the mitochondrial DNA control region in marsupials. Molecular Ecology 6, 1199-1201.
| Crossref | Google Scholar | PubMed |

Goldenberg, S. Z., Owen, M. A., Brown, J. L., Wittemyer, G., Oo, Z. M., and Leimgruber, P. (2019). Increasing conservation translocation success by building social functionality in released populations. Global Ecology and Conservation 18, e00604.
| Crossref | Google Scholar |

Greggor, A. L., Berger-Tal, O., Blumstein, D. T., Angeloni, L., Bessa-Gomes, C., Blackwell, B. F., St Clair, C. C., Crooks, K., de Silva, S., Fernández-Juricic, E., Goldenberg, S. Z., Mesnick, S. L., Owen, M., Price, C. J., Saltz, D., Schell, C. J., Suarez, A. V., Swaisgood, R. R., Winchell, C. S., and Sutherland, W. J. (2016). Research Priorities from Animal Behaviour for Maximising Conservation Progress. Trends in Ecology and Evolution 31, 953-964.
| Crossref | Google Scholar | PubMed |

Hedrick, P. W., and Fredrickson, R. (2010). Genetic rescue guidelines with examples from Mexican wolves and Florida panthers. Conservation Genetics 11, 615-626.
| Crossref | Google Scholar |

Holekamp, K. E., and Sherman, P. W. (1989). Why male ground squirrels disperse. American Scientist 77, 232-239.
| Google Scholar |

Hoogland, J. L. (1983). Black-Tailed Prairie Dog Coteries are Cooperatively Breeding Units. The American Naturalis 121, 275-280.
| Crossref | Google Scholar |

Houlahan, J. E., Findlay, C. S., Schmidt, B. R., Meyer, A. H., and Kuzmin, S. L. (2000). Quantitative evidence for global amphibian population declines. Nature 404, 752-755.
| Crossref | Google Scholar | PubMed |

IUCN/SSC. (2013). ‘Guidelines for Reintroductions and Other Conservation Translocations’. pp. viiii+57. version 1.0. (IUCN Species Survival Commission: Gland, Switzerland.)

Johnson, C. N., and Payne, A. (2002). Sex-biased dispersal in the rufous bettong Aepyprymnus rufescens. Australian Mammalogy 24, 233-236.
| Crossref | Google Scholar |

Jones, F. W. (1924). ‘The Mammals of South Australia.’ (R.E.E. Rogers, Government Printer: Adelaide.)

Kalinowski, S. T. (2004). Counting alleles with rarefaction: Private alleles and hierarchical sampling designs. Conservation Genetics 5, 539-543.
| Crossref | Google Scholar |

Kalinowski, S. T. (2005). HP-RARE 1.0: A computer program for performing rarefaction on measures of allelic richness. Molecular Ecology Notes 5, 187-189.
| Crossref | Google Scholar |

Kalinowski, S. T., Taper, M. L., and Marshall, T. C. (2007). Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Molecular Ecology 16, 1099-1106.
| Crossref | Google Scholar | PubMed |

Kinlaw, A. (1999). A review of burrowing by semi-fossorial vertebrates in arid environments. Journal of Arid Environments 41, 127-145.
| Crossref | Google Scholar |

Kleiman, D. G. (1989). Reintroduction of Captive Mammals for Conservation. BioScience 39, 152-161.
| Crossref | Google Scholar |

Krause, J., and Ruxton, G. D. (2002). ‘Living in groups.’ (Oxford University Press: Oxford.)

Kumar, S., Stecher, G., Li, M., Knyaz, C., and Tamura, K. (2018). MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35, 1547-1549.
| Crossref | Google Scholar | PubMed |

Lovegrove, A. B. G., and Wissel, C. (1988). Sociality in Molerats. Metabolic Scaling and the Role of Risk Sensitivity. Oecologia 74, 600-606.
| Crossref | Google Scholar | PubMed |

Lukas, D., and Clutton-Brock, T. (2017). Climate and the distribution of cooperative breeding in mammals. Royal Society Open Science 4, 160897.
| Crossref | Google Scholar | PubMed |

Maldonado-Chaparro, A. A., Hubbard, L., and Blumstein, D. T. (2015). Group size affects social relationships in yellow-bellied marmots (Marmota flaviventris). Behavioral Ecology 26, 909-915.
| Crossref | Google Scholar |

McDonald, D. B. (2007). Predicting fate from early connectivity in a social network. Proceedings of the National Academy of Sciences 104, 10910-10914.
| Crossref | Google Scholar | PubMed |

McKenzie, N. L., and Burbidge, A. A. (2002). ‘Australian terrestrial biodiversity assessment 2002.’ (National Land and Water Resources Audit: Canberra, Australia.)

McKenzie, N. L., Burbidge, A. A., Baynes, A., Brereton, R. N., Dickman, C. R., Gordon, G., Gibson, L. A., Menkhorst, P. W., Robinson, A. C., Williams, M. R., et al. (2007). Analysis of factors implicated in the recent decline of Australia’s mammal fauna. Journal of Biogeography 34, 597-611.
| Crossref | Google Scholar |

Moseby, K. E., Read, J. L., Paton, D. C., Copley, P., Hill, B. M., and Crisp, H. A. (2011). Predation determines the outcome of 10 reintroduction attempts in arid South Australia. Biological Conservation 144, 2863-2872.
| Crossref | Google Scholar |

Moseby, K., Carthey, A., and Schroeder, T. (2015). The influence of predators and prey naivety on reintroduction success: current and future directions. In ‘Advances in Reintroduction Biology of Australian and New Zealand Fauna’. (Eds D. P. Armstrong, M. Hayward, D. Moro, P. J. Seddon.) pp. 29–42. (CSIRO Publishing: Melbourne.)

Noble, J. C., Müller, W. J., Detling, J. K., and Pfitzner, G. H. (2007). Landscape ecology of the burrowing bettong: Warren distribution and patch dynamics in semiarid eastern Australia. Austral Ecology 32, 326-337.
| Crossref | Google Scholar |

Oksanen, J., Simpson, G., Blanchet, F., Kindt, R., Legendre, P., Minchin, P., O'Hara, R., Solymos, P., Stevens, M., Szoecs, E., Wagner, H., Barbour, M., Bedward, M., Bolker, B., Borcard, D., Carvalho, G., Chirico, M., De Caceres, M., Durand, S., Evangelista, H., FitzJohn, R., Friendly, M., Furneaux, B., Hannigan, G., Hill, M., Lahti, L., McGlinn, D., Ouellette, M., Ribeiro Cunha, E., Smith, T., Stier, A., Ter Braak, C., Weedon, J. (2024). vegan: Community Ecology Package. R package version 2.6-7. Available at https://github.com/vegandevs/vegan, https://vegandevs.github.io/vegan/

Olson, L. E., Blumstein, D. T., Pollinger, J. R., and Wayne, R. K. (2012). No evidence of inbreeding avoidance despite demonstrated survival costs in a polygynous rodent. Molecular Ecology 21, 562-571.
| Crossref | Google Scholar | PubMed |

Palmer, B., Valentine, L., Lohr, C., Daskalova, G., and Hobbs, R. (2021). Burrowing by translocated boodie (Bettongia lesueur) populations alters soils but has limited effects on vegetation. Ecology and Evolution 11, 2596-2615.
| Crossref | Google Scholar | PubMed |

Ostner, J., and Schülke, O. (2018). Linking Sociality to Fitness in Primates: A Call for Mechanisms. Advances in the Study of Behavior 50, 127-175.
| Crossref | Google Scholar |

Palmer, B., Valentine, L., Page, M., and Hobbs, R. (2020). Translocations of digging mammals and their potential for ecosystem restoration: a review of goals and monitoring programmes. Mammal Review 50, 382-398.
| Crossref | Google Scholar |

Parsons, B. C., Short, J. C., and 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, 219-224.
| Crossref | Google Scholar |

Peakall, R., and Smouse, P. E. (2012). GenALEx 6.5: Genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28, 2537-2539.
| Crossref | Google Scholar | PubMed |

Peakall, R., Ruibal, M., and Lindenmayer, D. B. (2003). Spatial autocorrelation analysis offers new insights into gene flow in the Australian bush rat, Rattus fuscipes. Evolution 57, 1182-1195.
| Crossref | Google Scholar | PubMed |

Pew, J., Muir, P. H., Wang, J., and Frasier, T. R. (2015). related: An R package for analysing pairwise relatedness from codominant molecular markers. Molecular Ecology Resources 15, 557-561.
| Crossref | Google Scholar | PubMed |

Pope, L. C., Blair, D., and Johnson, C. N. (2005). Dispersal and population structure of the rufous bettong, Aepyprymnus rufescens (Marsupialia: Potoroidae). Austral Ecology 30, 572-580.
| Crossref | Google Scholar |

Pope, L. C., Vernes, K., Goldizen, A. W., and Johnson, C. N. (2012). Mating system and local dispersal patterns of an endangered potoroid, the northern bettong (Bettongia tropica). Australian Journal of Zoology 60, 278-287.
| Crossref | Google Scholar |

Pusey, A., and Wolf, M. (1996). Inbreeding avoidance in animals. Trends in Ecology & Evolution 11, 201-206.
| Crossref | Google Scholar | PubMed |

R Core Team. (2018). ‘The R project for statistical computing.’ (R Foundation for Statistical Computing.) Available at https://www.r-project.org/ [accessed 5 August 2020].

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: Perth, Australia.)

Rick, K., Ottewell, K., Lohr, C., Thavornkanlapachai, R., Byrne, M., and Kennington, W. J. (2019). Population genomics of Bettongia lesueur: Admixing increases genetic diversity with no evidence of outbreeding depression. Genes 10, 851.
| Crossref | Google Scholar | PubMed |

Royle, N. J., Pike, T. W., Heeb, P., Richner, H., and Kölliker, M. (2012). Offspring social network structure predicts fitness in families. Proceedings: Biological Sciences 279, 4914-4922.
| Crossref | Google Scholar | PubMed |

Ruykys, L., and Lancaster, M. L. (2015). Population structure and genetic diversity of the black-footed rock-wallaby (Petrogale lateralis MacDonnell Ranges race). Australian Journal of Zoology 63, 91-100.
| Crossref | Google Scholar |

Sander, U., Short, J., and Turner, B. (1997). Social Organisation and Warren Use of the Burrowing Bettong, Bettongia lesueur (Macropodoidea:Potoroidae). Wildlife Research 24, 143-157.
| Crossref | Google Scholar |

Shier, D. (2006). Effect of family support on the success of translocated black-tailed prairie dogs. Conservation Biology 20, 1780-1790.
| Crossref | Google Scholar | PubMed |

Shier, D., and Swaisgood, R. (2012). Fitness costs of neighborhood disruption in translocations of a solitary mammal. Conservation Biology 26, 116-123.
| Crossref | Google Scholar | PubMed |

Shimmin, G. A., Skinner, J., and Baudinette, R. V. (2002). The warren architecture and environment of the southern hairy-nosed wombat (Lasiorhinus latifrons). Journal of Zoology 258, 469-477.
| Crossref | Google Scholar |

Short, J. (1998). The extinction of rat-kangaroos (Marsupialia : Potoroidae) in. Biological Conservation 86, 365-377.
| Crossref | Google Scholar |

Short, J. (2009). ‘The characteristics and success of vertebrate translocations within Australia.’ (Australian Government Department of Agriculture, Fisheries and Forestry: Canberra, Australia.)

Short, J., and Turner, B. (1993). The distribution and abundance of the Burrowing bettong (Marsupialia: Macropodoidea). Wildlife Research 20, 525-534.
| Crossref | Google Scholar |

Short, J., and Turner, B. (1999). Ecology of burrowing bettongs, Bettongia lesueur (Marsupialia : Potoroidae), on Dorre and Bernier Islands, Western Australia. Wildlife Research 26, 651-669.
| Crossref | Google Scholar |

Short, J., and Turner, B. (2000). Reintroduction of the burrowing bettong Bettongia lesueur (Marsupialia: Potoroidae) to mainland Australia. Biological Conservation 96, 185-196.
| Crossref | Google Scholar |

Short, J., Turner, B., Parker, S., and Twiss, J. (1995). Reintroduction of endangered mammals to mainland Shark Bay: a progress report. In ‘Reintroduction biology of Australian and New Zealand fauna’. (Eds M. Doug Armstrong, D. M. Hayward, P. J. Seddon.) pp. 183–188. (CSIRO Publishing: Sydney.)

Silk, J. B. (2007). The adaptive value of sociality in mammalian groups. Philosophical Transactions of the Royal Society B: Biological Sciences 362, 539-559.
| Crossref | Google Scholar | PubMed |

Stodart, E. (1966). Observations of the behaviour of the marsupial Bettongia lesueuri (Quoy & Gaimard) in an enclosure. Wildlife Research 11, 91-99.
| Crossref | Google Scholar |

Sunnucks, P., and 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, 510-524.
| Crossref | Google Scholar | PubMed |

Surridge, A. K., Bell, D. J., and Hewitt, G. M. (1999). From population structure to individual behaviour: genetic analysis of social structure in the European wild rabbit (Oryctolagus cuniculus). Biological Journal of the Linnean Society 68, 57-71.
| Google Scholar |

Thavornkanlapachai, R., Mills, H. R., Ottewell, K., Dunlop, J., Sims, C., Morris, K., Donaldson, F., and 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, 729.
| Crossref | Google Scholar |

Tran, T., and Langford, L. (2015). ‘Negotiating the shared management of Matuwa Kurrara Kurrara’. (Australian Institute of Aboriginal and Torres Strait Islander Studies: Canberra Australia.)

Tyndale-Biscoe, C. H. (1968). Reproduction and post-natal development in the marsupial Bettongia lesueur (Quoy & Gaimard). Australian Journal of Zoology 16, 577-602.
| Google Scholar |

Wang, J. (2002). An estimator for pairwise relatedness using molecular markers. Genetics 160, 1203-1215.
| Crossref | Google Scholar | PubMed |

Whittington-Jones, G. M., Bernard, R. T. F., and Parker, D. M. (2011). Aardvark Burrows: A Potential Resource for Animals in Arid and Semi-Arid Environments. African Zoology 46, 362-370.
| Crossref | Google Scholar |

Woinarski, J. C. Z., Burbidge, A. A., and 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 112, 4531-4540.
| Crossref | Google Scholar | PubMed |