Mating system and local dispersal patterns of an endangered potoroid, the northern bettong (Bettongia tropica)
L. C. Pope A D , K. Vernes B C , A. W. Goldizen A and C. N. Johnson B
+ Author Affiliations
- Author Affiliations
A School of Biological Science, University of Queensland, St Lucia, Qld 4072, Australia.
B School of Tropical Biology, James Cook University, Townsville, Qld 4811, Australia.
C Department of Ecosystem Management, University of New England, Armidale, NSW 2351, Australia.
D Corresponding author. Email: l.pope@uq.edu.au
Australian Journal of Zoology 60(4) 278-287 https://doi.org/10.1071/ZO12071
Submitted: 26 July 2012 Accepted: 27 November 2012 Published: 7 January 2013
Abstract
The northern bettong (Bettongia tropica) (Potoroidae), is an endangered macropod with a restricted distribution. We combined radio-tracking and trapping data with microsatellite genotypes to infer the mating system and local dispersal patterns of this species, and discuss their relevance to translocations. We defined the mating system as ‘overlap promiscuity’ (sensu Wittenberger 1979), though we cannot rule out serial monogamy. We found significant effects of proximity (average distance between parents = 190 m) and male weight, but not size, on the likelihood of paternity, suggesting that closer, heavier males have greater mating success. The average distance between putative pairs of relatives suggested that most dispersal occurred over short distances, with the distance between ‘related’ females significantly lower than that between related males (0.9 km versus 1.3 km). A spatial autocorrelation analysis showed high female relatedness across distances of up to 435 m, equivalent to half an average home range width. Conversely, male pairs had low relatedness across 0 to 870 m. These results suggested that female young often settle next to their mother, while males avoid nesting within their father’s home range. Both limited natal and ‘mating’ dispersal may have contributed to the strong genetic structure previously reported for this species.
Additional keywords: homomorphic, marsupial, overlap promiscuity, paternity, sex-biased dispersal.
References
Bateman, B. L., VanDerWal, J., and Johnson, C. N. (2012). Nice weather for bettongs: using weather events, not climate means, in species distribution models. Ecography 35, 306–314.| Nice weather for bettongs: using weather events, not climate means, in species distribution models.Crossref | GoogleScholarGoogle Scholar |
Blouin, M. S., Parsons, M., Lacaille, V., and Lotz, S. (1996). Use of microsatellite loci to classify individuals by relatedness. Molecular Ecology 5, 393–401.
| 1:STN:280:DyaK283ms1Kquw%3D%3D&md5=66bc5e18d7797f70a633d5c78630f308CAS |
Breslow, N. E., and Clayton, D. G. (1993). Approximate inference in generalized linear mixed models. Journal of the American Statistical Association 88, 9–25.
| Approximate inference in generalized linear mixed models.Crossref | GoogleScholarGoogle Scholar |
Burbidge, A. A., and McKenzie, N. L. (1989). Patterns in the modern decline of Western Australia’s vertebrate fauna: causes and conservation implications. Biological Conservation 50, 143–198.
| Patterns in the modern decline of Western Australia’s vertebrate fauna: causes and conservation implications.Crossref | GoogleScholarGoogle Scholar |
Carpenter, G., Gillison, A. N., and Winter, J. (1993). DOMAIN: a flexible modeling procedure for mapping potential distributions of plants and animals. Biodiversity and Conservation 2, 667–680.
| DOMAIN: a flexible modeling procedure for mapping potential distributions of plants and animals.Crossref | GoogleScholarGoogle Scholar |
Carpenter, P., Pope, L. C., Greig, C., Dawson, D., Erven, K., Rogers, L. M., Wilson, G., Delahay, R., Cheeseman, C. L., and Burke, T. (2005). Mating system of the Eurasian badger, Meles meles, in a high density population. Molecular Ecology 14, 273–284.
| Mating system of the Eurasian badger, Meles meles, in a high density population.Crossref | GoogleScholarGoogle Scholar |
Christensen, P. E. S. (1980). The biology of Bettongia penicillata (Gray 1837), and Macropus eugenii (Desmarest 1817) in relation to fire. Forests Department of Western Australia, Bulletin No. 91.
Christensen, P., and Maisey, K. G. (1987). The use of fire as a management tool in fauna conservation reserves. In ‘Nature Conservation: the Role of Remnants of Native Vegetation’. (Eds D. A. Saunders, G. W. Arnold, A. A. Burbidge and A. J. M. Hopkins.) pp. 323–329. (Surrey Beatty: Sydney.)
Clinchy, M., Taylor, A. C., Zanette, L. Y., Krebs, C. J., and Jarman, P. J. (2004). Body size, age and paternity in common brushtail possums (Trichosurus vulpecula). Molecular Ecology 13, 195–202.
| Body size, age and paternity in common brushtail possums (Trichosurus vulpecula).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhs1Wksbc%3D&md5=922ead69c2930999190efbd4456cfb6dCAS |
Delaney, R., and Marsh, H. (1995). Estimating the age of wild rock-wallabies by dental radiography – a basis for quantifying the age structure of a discrete colony of Petrogale assimilis. Wildlife Research 22, 547–559.
| Estimating the age of wild rock-wallabies by dental radiography – a basis for quantifying the age structure of a discrete colony of Petrogale assimilis.Crossref | GoogleScholarGoogle Scholar |
Department of Sustainability, Environment, Water, Population and Communities (DSEWPC) (2012). Bettongia tropica in Species Profile and Threats Database. Department of Sustainability, Environment, Water, Population and Communities, Canberra
Eldridge, M. D. B., Piggott, M. P., and Hazlitt, S. L. (2010). Population genetic studies of the Macropodoidea: a review. In ‘Macropods: The Biology of Kangaroos, Wallabies and Rat-kangaroos’. (Eds G. Coulson and M. D. B. Eldridge.) pp. 35–51.
Emlen, S. T., and Oring, L. W. (1977). Ecology, sexual selection, and evolution of mating systems. Science 197, 215–223.
| Ecology, sexual selection, and evolution of mating systems.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2s3hsFyrtQ%3D%3D&md5=1d06483d35f8fb79b8db49de4e7ddd6eCAS |
Favre, L., Balloux, F., Goudet, J., and Perrin, N. (1997). Female-biased dispersal in the monogamous mammal Crocidura russula: evidence from field data and microsatellite patterns. Proceedings of the Royal Society of London. Series B, Biological Sciences 264, 127–132.
| Female-biased dispersal in the monogamous mammal Crocidura russula: evidence from field data and microsatellite patterns.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s3hsFKiuw%3D%3D&md5=fb205d17db9bc1cd8548f85b3a549345CAS |
Finlayson, G. R., Finlayson, S. T., and Dickman, C. R. (2010). Returning the rat-kangaroos: translocation attempts in the family Potoroidae (superfamily Macropodoidea) and recommendations for conservation. In ‘Macropods: The Biology of Kangaroos, Wallabies and Rat-kangaroos.’ (Eds G. Coulson and M. D. B. Eldridge.) pp. 245–262.
Fisher, D. O., and Lara, M. C. (1999). Effects of body size and home range on access to mates and paternity in male bridled nailtail wallabies. Animal Behaviour 58, 121–130.
| Effects of body size and home range on access to mates and paternity in male bridled nailtail wallabies.Crossref | GoogleScholarGoogle Scholar |
Frederick, H., and Johnson, C. N. (1996). Social organisation in the rufous bettong, Aepyprymnus rufescens. Australian Journal of Zoology 44, 9–17.
| Social organisation in the rufous bettong, Aepyprymnus rufescens.Crossref | GoogleScholarGoogle Scholar |
Gaston, K. J. (2009). Geographic range limits: achieving synthesis. Proceedings of the Royal Society B. Biological Sciences 276, 1395–406.
| Geographic range limits: achieving synthesis.Crossref | GoogleScholarGoogle Scholar |
Goodnight, K. F., and Queller, D. C. (1999). Computer software for performing likelihood tests of pedigree relationship using genetic markers. Molecular Ecology 8, 1231–1234.
| Computer software for performing likelihood tests of pedigree relationship using genetic markers.Crossref | GoogleScholarGoogle Scholar |
Goudet, J. (1995). FSTAT (Version 1.2): a computer program to calculate F-statistics. The Journal of Heredity 86, 485–486.
Goudet, J., Perrin, N., and Waser, P. (2002). Tests for sex-biased dispersal using bi-parentally inherited genetic markers. Molecular Ecology 11, 1103–1114.
| Tests for sex-biased dispersal using bi-parentally inherited genetic markers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xls1arsrc%3D&md5=7cf7a959512a344d84ca7ce520d063a1CAS |
Green, K., Mitchell, A., and Tennant, P. (1998). Home range and microhabitat use by the long-footed potoroo, Potorous longipes. Wildlife Research 25, 357–372.
| Home range and microhabitat use by the long-footed potoroo, Potorous longipes.Crossref | GoogleScholarGoogle Scholar |
Greenwood, P. J. (1980). Mating systems, philopatry and dispersal in birds and mammals. Animal Behaviour 28, 1140–1162.
| Mating systems, philopatry and dispersal in birds and mammals.Crossref | GoogleScholarGoogle Scholar |
Hardy, O. J., and Vekemans, X. (2002). SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Molecular Ecology Notes 2, 618–620.
| SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels.Crossref | GoogleScholarGoogle Scholar |
Hardy, O. J., Maggia, L., Bandou, E., Breyne, P., Caron, H., Chevallier, M. H., Doligez, A., Dutech, C., Kremer, A., Latouche-Halle, C., Troispoux, V., Veron, V., and Degen, B. (2006). Fine-scale genetic structure and gene dispersal inferences in 10 Neotropical tree species. Molecular Ecology 15, 559–571.
| Fine-scale genetic structure and gene dispersal inferences in 10 Neotropical tree species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xktlelt7Y%3D&md5=e8f24834c08a1893476fba035c51e5f9CAS |
Harville, D. A. (1977). Maximum likelihood approaches to variance component estimation and to related problems. Journal of the American Statistical Association 72, 320–338.
| Maximum likelihood approaches to variance component estimation and to related problems.Crossref | GoogleScholarGoogle Scholar |
Hayne, D. W. (1949). Calculation of size of home range. Journal of Mammalogy 30, 1–18.
| Calculation of size of home range.Crossref | GoogleScholarGoogle Scholar |
Jarman, P. J. (1991). Social behaviour and organisation in the Macropodoidea. Advances in the Study of Behavior 20, 1–50.
| Social behaviour and organisation in the Macropodoidea.Crossref | GoogleScholarGoogle Scholar |
Johnson, C. (1989). Dispersal and philopatry in the macropods. In ‘Kangaroos, Wallabies and Rat-kangaroos. Vol. 2’. (Eds G. Grigg, P. Jarman and I. Hume.) pp. 593–601. (Surrey Beatty: Sydney.)
Johnson, C., and McIlwee, A. (1997). Ecology of the northern bettong, Bettongia tropica, a tropical mycophagist. Wildlife Research 24, 549–559.
| Ecology of the northern bettong, Bettongia tropica, a tropical mycophagist.Crossref | GoogleScholarGoogle Scholar |
Johnson, C, and Payne, A (2002). Sex-biased dispersal in the rufous bettong. Australian Mammalogy 24, 233–235.
Johnson, P. M., and Delean, S. (2001). Reproduction in the northern bettong, Bettongia tropica Wakefield (Marsupialia: Potoroidae), in captivity, with age estimation and development of the pouch young. Wildlife Research 28, 79–85.
| Reproduction in the northern bettong, Bettongia tropica Wakefield (Marsupialia: Potoroidae), in captivity, with age estimation and development of the pouch young.Crossref | GoogleScholarGoogle 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.
| Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment.Crossref | GoogleScholarGoogle Scholar |
Kingsley, L., Goldizen, A., and Fisher, D. O. (2012). Establishment of an endangered species on a private nature refuge: what can we learn from reintroductions of the bridled nailtail wallaby Onychogalea fraenata? Oryx 46, 240–248.
| Establishment of an endangered species on a private nature refuge: what can we learn from reintroductions of the bridled nailtail wallaby Onychogalea fraenata?Crossref | GoogleScholarGoogle Scholar |
Koenig, W. D., Van Vuren, D., and Hooge, P. N. (1996). Detectability, philopatry, and the distribution of dispersal distances in vertebrates. Trends in Ecology & Evolution 11, 514–517.
| Detectability, philopatry, and the distribution of dispersal distances in vertebrates.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itFGksw%3D%3D&md5=2a2657bf536336f78414aace2b65ad97CAS |
Lobert, B. (1990). Home range and activity period of the southern brown bandicoot (Isoodon obesulus) in a Victorian Heathland. In ‘Bandicoots and Bilbies’. (Eds J. H. Seebeck, R. L. Brown, R. L. Wallis and C. M. Kemper.) pp. 319–325. (Surrey Beatty: Sydney.)
Maxwell, S., Burbidge, A., and Morris, K. (1996). The 1996 action plan of Australian marsupials and monotremes. Environment Australia, Canberra.
Maynard Smith, J. (1982). ‘Evolution and the Theory of Games.’ (Cambridge University Press: Cambridge.)
Miller, E. J., Eldridge, M. D. B., Cooper, D. W., and Herbert, C. A. (2010). Dominance, body size and internal relatedness influence male reproductive success in eastern grey kangaroos (Macropus giganteus). Reproduction, Fertility and Development 22, 539–549.
| Dominance, body size and internal relatedness influence male reproductive success in eastern grey kangaroos (Macropus giganteus).Crossref | GoogleScholarGoogle Scholar |
Nelson, L. S., Storr, R. F., and Robinson, A. C. (1992). Plan of the management for the brush-tailed bettong, Bettongia penicillata Gray, 1837 (Marsupalia, Potoroidae) in South Australia. National Parks and Wildlife Service, Department of Environment and Planning, South Australia, Adelaide.
Paetkau, D., Calvert, W., Stirling, I., and Strobeck, C. (1995). Microsatellite analysis of population structure in Canadian polar bears. Molecular Ecology 4, 347–354.
| Microsatellite analysis of population structure in Canadian polar bears.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXntValu78%3D&md5=6c6c80871b7ccced7d5f06e10f52f432CAS |
Pope, L., Sharp, A., and Moritz, C. (1996). Population structure of the yellow-footed rock-wallaby Petrogale xanthopus (Gray, 1854) inferred from mtDNA sequences and microsatellite loci. Molecular Ecology 5, 629–640.
| Population structure of the yellow-footed rock-wallaby Petrogale xanthopus (Gray, 1854) inferred from mtDNA sequences and microsatellite loci.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmsValsb4%3D&md5=9dd0edfaa17bff20ebf5a64a44c3df97CAS |
Pope, L. C., Estoup, A., and Moritz, C. (2000). Phylogeography and population structure of an ecotonal marsupial, Bettongia tropica, determined using mtDNA and microsatellites. Molecular Ecology 9, 2041–2053.
| Phylogeography and population structure of an ecotonal marsupial, Bettongia tropica, determined using mtDNA and microsatellites.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXot1Oksg%3D%3D&md5=59a976ed509458afa25de31972c39714CAS |
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.
| Dispersal and population structure of the rufous bettong, Aepyprymnus rufescens (Marsupialia: Potoroidae).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 |
R Development Core Team (2011). ‘R: A Language and Environment for Statistical Computing.’ (R Foundation for Statistical Computing: Vienna.)
Rousset, F. (2000). Genetic differentiation between individuals. Journal of Evolutionary Biology 13, 58–62.
| Genetic differentiation between individuals.Crossref | GoogleScholarGoogle Scholar |
Rousset, F. (2001). Genetic approaches to the estimation of dispersal rates. In ‘Dispersal.’ (Eds J. Clobert, E. Danchin, A. A. Dhondt and J. D. Nichols.) pp. 18–28. (Oxford University Press: Oxford.)
Seebeck, J. H., and Rose, R. W. (1988). Potoroidae. In ‘Fauna of Australia. Mammalia. Vol. 1B’. (Eds D. W. Walton and B. J. Richardson.) pp. 716–39. (Australian Government Publishing Service: Canberra.)
Seebeck, J. H., Bennett, A. F., and Scotts, D. J. (1989). Ecology of the Potoroidae – a review. In ‘Kangaroos, Wallabies and Rat-kangaroos. Vol. 1’. (Eds G. Grigg, P. Jarman and I. Hume.) pp. 67–88. (Surrey Beatty: Sydney.)
Sheean, V. A., Manning, A. D., and Lindenmayer, D. B. (2012). An assessment of scientific approaches towards species relocations in Australia. Austral Ecology 37, 204–215.
| An assessment of scientific approaches towards species relocations in Australia.Crossref | GoogleScholarGoogle Scholar |
Short, J. (1998). The extinction of rat-kangaroos (Marsupialia: Potoroidae) in New South Wales, Australia. Biological Conservation 86, 365–377.
| The extinction of rat-kangaroos (Marsupialia: Potoroidae) in New South Wales, Australia.Crossref | GoogleScholarGoogle Scholar |
Sigg, D. P., Goldizen, A. W., and Pople, A. R. (2005). The importance of mating system in translocation programs: reproductive success of released male bridled nailtail wallabies. Biological Conservation 123, 289–300.
| The importance of mating system in translocation programs: reproductive success of released male bridled nailtail wallabies.Crossref | GoogleScholarGoogle Scholar |
Smith, M. J. (1998). Establishment of a captive colony of Bettongia tropica (Marsupialia: Potoroidae) by cross-fostering; and observations on reproduction. Journal of Zoology 244, 43–50.
| Establishment of a captive colony of Bettongia tropica (Marsupialia: Potoroidae) by cross-fostering; and observations on reproduction.Crossref | GoogleScholarGoogle Scholar |
Taylor, R. J. (1993). Home range, nest use and activity of the Tasmanian bettong, Bettongia gaimardi. Wildlife Research 20, 87–95.
| Home range, nest use and activity of the Tasmanian bettong, Bettongia gaimardi.Crossref | GoogleScholarGoogle Scholar |
Todd, I. (1992). Wildtrak: Non parametric home range analysis. In ‘.’ 1.17 edn. (Isis Innovation Ltd.)
van Dyck, S., and Strahan, R. (Eds) (2008). ‘The Mammals of Australia.’ 3rd edn. (New Holland: Sydney.)
Venables, W. N., and Ripley, B. D. (2002). ‘Modern Applied Statistics with S.’ 4th edn. (Springer: New York.)
Vernes, K, Castellano, M, and Johnson, C. N. (2001). Effects of season and fire on the diversity of hypogeous fungi consumed by a tropical mycophagous marsupial. Journal of Animal Ecology 70, 945–954.
| Effects of season and fire on the diversity of hypogeous fungi consumed by a tropical mycophagous marsupial.Crossref | GoogleScholarGoogle Scholar |
Vernes, K., and Pope, L. (2001a). Stability of nest range, home range and movement of the northern bettong (Bettongia tropica) following moderate-intensity fire in a tropical woodland, north-eastern Queensland. Wildlife Research 28, 141–150.
| Stability of nest range, home range and movement of the northern bettong (Bettongia tropica) following moderate-intensity fire in a tropical woodland, north-eastern Queensland.Crossref | GoogleScholarGoogle Scholar |
Vernes, K., and Pope, L. C. (2001b). Fecundity, pouch young survivorship and breeding season of the northern bettong (Bettongia tropica) in the wild. Australian Mammalogy 23, 95–100.
| Fecundity, pouch young survivorship and breeding season of the northern bettong (Bettongia tropica) in the wild.Crossref | GoogleScholarGoogle Scholar |
Vernes, K., and Pope, L. (2006). Population density of the northern bettong Bettongia tropica in northeastern Queensland. Australian Mammalogy 28, 87–92.
| Population density of the northern bettong Bettongia tropica in northeastern Queensland.Crossref | GoogleScholarGoogle Scholar |
Wallis, I. R., Jarman, P. J., Johnson, B. E., and Liddle, R. W. (1989). Nest site and use of nests by rufous bettongs Aepyprymnus rufescens. In ‘Kangaroos, Wallabies and Rat-kangaroos. Vol. 2’. (Eds G. Grigg, P. Jarman and I. Hume.) pp. 619–623. (Surrey Beatty: Sydney.)
Weir, B. S., and Cockerham, C. C. (1984). Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370.
| Estimating F-statistics for the analysis of population structure.Crossref | GoogleScholarGoogle Scholar |
Winter, J.W. (1990). A study of the brush-tailed bettong (Bettongia penicillata) in north-east Australia. Third progress report to World Wide Fund for Nature, Sydney.
Winters, J. B., and Waser, P. M. (2003). Gene dispersal and outbreeding in a philopatric mammal. Molecular Ecology 12, 2251–2259.
| Gene dispersal and outbreeding in a philopatric mammal.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmvFShtbc%3D&md5=81969ef8da55c81ff475f5bf02c3cbd4CAS |
Wittenberger, J. F. (1979). The evolution of mating systems in birds and mammals. In ‘Handbook of Behavioural Neurobiology, Vol. 3: Social Behaviour and Communication’. (Eds P. Marler and J. Vandenbergh.) pp. 271–349. (Plenum Press: New York.)
