Australian Journal of Zoology Australian Journal of Zoology Society
Evolutionary, molecular and comparative zoology
RESEARCH ARTICLE

Limited sex bias in the fine-scale spatial genetic structure of the eastern grey kangaroo and its relationship to habitat

Linda E. Neaves A B F , Michael W. Roberts C D , Catherine A. Herbert E and Mark D. B. Eldridge A
+ Author Affiliations
- Author Affiliations

A Australian Museum Research Institute, Australian Museum, 1 William Street, Sydney, NSW 2010, Australia.

B Royal Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh EH3 5LR, UK.

C Endeavour Energy, PO Box 811, Seven Hills, NSW 1730, Australia.

D Department of Biological Science, Macquarie University, Sydney, NSW 2109, Australia.

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

F Corresponding author. Email: lneaves@gmail.com

Australian Journal of Zoology 65(1) 33-44 https://doi.org/10.1071/ZO16051
Submitted: 27 July 2016  Accepted: 2 May 2017   Published: 6 June 2017

Abstract

Animals exhibit a range of dispersal strategies that impact on the organisation of individuals and can be influenced by both the environment and population demography. We examined the fine-scale spatial genetic structure and patterns of relatedness in 139 adult eastern grey kangaroos (Macropus giganteus) to test predictions of male-biased dispersal and female philopatry in comparison with previous studies in different environments in the species’ distributions. We found evidence of limited differences between the sexes, with little spatial genetic structure in both males and females. The levels of relatedness among females in close proximity were not indicative of close relatives (e.g. mother–daughter) and there was no evidence of matrilineal structure. Among males, there was little evidence of genetic structure. Although our results are, in general, consistent with those of previous studies, we found study-specific differences in the extent of genetic structure that appear to be related to differences in environmental and demographic conditions across the distribution. This highlights the need for additional research focussing on populations from a range of environmental conditions.

Additional keywords: female philopatry, gene flow, group formation, marsupial, sex-biased dispersal.


References

Albon, S. D., Staines, H. J., Guinness, F. E., and Clutton-Brock, T. H. (1992). Density-dependent changes in the spacing behaviour of female kin in red deer. Journal of Animal Ecology 61, 131–137.
Density-dependent changes in the spacing behaviour of female kin in red deer.CrossRef |

Banks, S. C., and Peakall, R. (2012). Genetic spatial autocorrelation can readily detect sex-biased dispersal. Molecular Ecology 21, 2092–2105.
Genetic spatial autocorrelation can readily detect sex-biased dispersal.CrossRef |

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.
Female dispersal and relatedness structure in common wombats (Vombatus ursinus).CrossRef |

Best, E. C., Seddon, J. M., Dwyer, R. G., and Goldizen, A. W. (2013). Social preference influences female community structure in a population of wild eastern grey kangaroos. Animal Behaviour 86, 1031–1040.
Social preference influences female community structure in a population of wild eastern grey kangaroos.CrossRef |

Best, E. C., Dwyer, R. G., Seddon, J. M., and Goldizen, A. W. (2014). Associations are more strongly correlated with space use than kinship in female eastern grey kangaroos. Animal Behaviour 89, 1–10.
Associations are more strongly correlated with space use than kinship in female eastern grey kangaroos.CrossRef |

Bonnot, N., Gaillard, J., Coulon, A., Galan, M., Cosson, J.-F., Delorme, D., Klein, F., and Hewison, A. J. M. (2010). No difference between the sexes in fine-scale spatial genetic structure of roe deer. PLoS One 5, e14436.
No difference between the sexes in fine-scale spatial genetic structure of roe deer.CrossRef | 1:CAS:528:DC%2BC3MXlslyltQ%3D%3D&md5=de4794b44c2ffa4ef55ddf9f52b86facCAS |

Börger, L., Franconi, N., De Michele, G., Gantz, A., Meschi, F., Manica, A., Lovari, S., and Coulson, T. (2006). Effects of sampling regime on the mean and variance of home range size estimates. Journal of Animal Ecology 75, 1393–1405.
Effects of sampling regime on the mean and variance of home range size estimates.CrossRef |

Calenge, C. (2006). The package ‘adehabitat’ for the R software: a tool for the analysis of space and habitat use by animals. Ecological Modelling 197, 516–519.
The package ‘adehabitat’ for the R software: a tool for the analysis of space and habitat use by animals.CrossRef |

Carter, A., Pays, O., and Goldizen, A. W. (2009). Individual variation in the relationship between vigilance and group size in eastern grey kangaroos. Behavioral Ecology and Sociobiology 64, 237–245.
Individual variation in the relationship between vigilance and group size in eastern grey kangaroos.CrossRef |

Carter, K. D., Seddon, J. M., Frère, C. H., Carter, J. K., and Goldizen, A. W. (2013). Fission–fusion dynamics in wild giraffes may be driven by kinship, spatial overlap and individual social preferences. Animal Behaviour 85, 385–394.
Fission–fusion dynamics in wild giraffes may be driven by kinship, spatial overlap and individual social preferences.CrossRef |

Clement, M., Snell, Q., Walker, P., Posada, D., and Crandall, K. (2002). TCS: estimating gene genealogies. In ‘Parallel and Distributed Processing Symposium, International Proceedings. 2002’. p. 184. Available at: http://www.computer.org/csdl/proceedings/ipdps/2002/1573/02/15730184.pdf

Clutton-Brock, T. H., and Lukas, D. (2012). The evolution of social philopatry and dispersal in female mammals. Molecular Ecology 21, 472–492.
The evolution of social philopatry and dispersal in female mammals.CrossRef | 1:STN:280:DC%2BC387jvFWqsw%3D%3D&md5=c714988321cd6f65ca45762b4e9b2506CAS |

Coltman, D. W., Pilkington, J. G., and Pemberton, J. M. (2003). Fine-scale genetic structure in a free-living ungulate population. Molecular Ecology 12, 733–742.
Fine-scale genetic structure in a free-living ungulate population.CrossRef | 1:STN:280:DC%2BD3s7mtVWntQ%3D%3D&md5=d08329981b841fbc80d330b63777d689CAS |

Coulson, G. (2008). Eastern grey kangaroo Macropus giganteus. In ‘The Mammals of Australia’. (Eds S. Van Dyck and R. Strahan.) pp. 335–338. (CSIRO Publishing: Melbourne.)

Coulson, G., Alviano, P., Ramp, D., Way, S., McLean, N., and Yazgin, V. (2000). The kangaroos of Yan Yean: issues for a forested water catchment in a semi-rural matrix. In ‘Conservation in Production Environments: Managing the Matrix’. (Eds J. L. Craig, N. Mitchell, and D. A. Saunders.) pp. 146–156. (Surrey Beatty: Sydney.)

Dawson, T. (2012). ‘Kangaroos.’ 2nd edn. (CSIRO Publishing: Melbourne.)

Dobson, F. S. (1982). Competition for mates and predominant juvenile male dispersal in mammals. Animal Behaviour 30, 1183–1192.
Competition for mates and predominant juvenile male dispersal in mammals.CrossRef |

Dobson, F. S. (2013). The enduring question of sex-biased dispersal: Paul J. Greenwood’s (1980) seminal contribution. Animal Behaviour 85, 299–304.
The enduring question of sex-biased dispersal: Paul J. Greenwood’s (1980) seminal contribution.CrossRef |

Eldridge, M. D. B., and Coulson, G. M. (2015). Family Macropodidae (kangaroos and wallabies). In ‘Handbook of the Mammals of the World. Volume 5. Monotremes and Marsupials’. (Eds D. E. Wilson and R. A. Mittermeier.) pp. 630–735. (Lynx Edicions: Barcelona, Spain.)

Evanno, G., Regnaut, S., and Goudet, J. (2005). Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14, 2611–2620.
Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study.CrossRef | 1:CAS:528:DC%2BD2MXmvF2qtrg%3D&md5=ea63a9f32dd3db49f95c38a12f824430CAS |

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.
Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows.CrossRef |

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 B: Biological Sciences 264, 127–132.
Female-biased dispersal in the monogamous mammal Crocidura russula: evidence from field data and microsatellite patterns.CrossRef | 1:STN:280:DyaK2s3hsFKiuw%3D%3D&md5=baf2ea903d4eab86b11d7db452a1837eCAS |

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.
Versatile primers for the amplification of the mitochondrial DNA control region in marsupials.CrossRef | 1:CAS:528:DyaK1cXisVWntA%3D%3D&md5=39217c7c6d5a90d2faeb420342092dc0CAS |

Goudet, J. (1995). FSTAT (Version 1.2): a computer program to calculate F-statistics. The Journal of Heredity 86, 485–486.
FSTAT (Version 1.2): a computer program to calculate F-statistics.CrossRef |

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 |

Hazlitt, S. L., Eldridge, M. D. B., and Goldizen, A. W. (2004). Fine-scale spatial genetic correlation analyses reveal strong female philopatry within a brush-tailed rock-wallaby colony in southeast Queensland. Molecular Ecology 13, 3621–3632.
Fine-scale spatial genetic correlation analyses reveal strong female philopatry within a brush-tailed rock-wallaby colony in southeast Queensland.CrossRef | 1:STN:280:DC%2BD2crnvFyrsg%3D%3D&md5=379d754e96482af123e36be725b263baCAS |

Jaremovic, R. V., and Croft, D. B. (1987). Comparison of techniques to determine eastern grey kangaroo home range. Journal of Wildlife Management 51, 921–930.
Comparison of techniques to determine eastern grey kangaroo home range.CrossRef |

Jarman, P. J. (1994). Individual behaviour and social organisation of kangaroos. In ‘Animal Societies – Individuals, Interactions and Organisation’. (Eds A. Rossiter and P. J. Jarman.) pp. 70–85. (Kyoto University Press: Japan.)

Jarman, P. J., and Taylor, R. J. (1983). Ranging of eastern grey kangaroos and wallaroos on a New England pastoral property. Australian Wildlife Research 10, 33–38.
Ranging of eastern grey kangaroos and wallaroos on a New England pastoral property.CrossRef |

Johnson, C. N. (1983). Variations in group size and composition in red and western grey kangaroos, Macropus rufus (Desmarest) and M. fuliginosus (Desmarest). Australian Wildlife Research 10, 25–31.
Variations in group size and composition in red and western grey kangaroos, Macropus rufus (Desmarest) and M. fuliginosus (Desmarest).CrossRef |

Johnson, C. N. (1989). Dispersal and philopatry in the macropodoids. In ‘Kangaroos, Wallabies and Rat-kangaroos’. (Eds G. C. Grigg, P. J. Jarman, and I. Hume.) pp. 593–601. (Surrey Beatty: Sydney.)

Johnson, C. N., and Jarman, P. J. (1987). Macropod studies at Wallaby Creek, New South Wales, Australia. VI. A validation of the use of dung-pellet counts for measuring absolute densities of populations of macropodids. Australian Wildlife Research 14, 139–146.
Macropod studies at Wallaby Creek, New South Wales, Australia. VI. A validation of the use of dung-pellet counts for measuring absolute densities of populations of macropodids.CrossRef |

Kaufmann, J. H. (1975). Field observations of the social behaviour of the eastern grey kangaroo, Macropus giganteus. Animal Behaviour 23, 214–221.
Field observations of the social behaviour of the eastern grey kangaroo, Macropus giganteus.CrossRef |

King, W. J., Garant, D., and Festa-Bianchet, M. (2015). Mother–offspring distances reflect sex differences in fine-scale genetic structure of eastern grey kangaroos. Ecology and Evolution 5, 2084–2094.
Mother–offspring distances reflect sex differences in fine-scale genetic structure of eastern grey kangaroos.CrossRef |

Laver, P. N., and Kelly, M. J. (2008). A critical review of home range studies. Journal of Wildlife Management 72, 290–298.
A critical review of home range studies.CrossRef |

Mabry, K. E., Shelley, E. L., Davis, K. E., Blumstein, D. T., and Van Vuren, D. H. (2013). Social mating system and sex-biased dispersal in mammals and birds: a phylogenetic analysis. PLoS One 8, e57980.
Social mating system and sex-biased dispersal in mammals and birds: a phylogenetic analysis.CrossRef | 1:CAS:528:DC%2BC3sXktlSqtbo%3D&md5=e5e0f7b37141e8bbe83d9fd5e77e2ffcCAS |

Mathews, N. E., and Porter, W. F. (1993). Effect of social structure on genetic structure of free-ranging white-tailed deer in the Adirondack Mountains. Journal of Mammalogy 74, 33–43.
Effect of social structure on genetic structure of free-ranging white-tailed deer in the Adirondack Mountains.CrossRef |

McCullough, D. R., and McCullough, Y. (2000). ‘Kangaroos in Outback Australia: Comparative Ecology and Behaviour of Three Coexisting Species.’ (Columbia University Press: New York.)

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 |

Moyer, M. A., McCown, J. W., Eason, T. H., and Oli, M. K. (2006). Does genetic relatedness influence space use pattern? A test on Florida black bears. Journal of Mammalogy 87, 255–261.
Does genetic relatedness influence space use pattern? A test on Florida black bears.CrossRef |

Neaves, L. E., Zenger, K. R., Prince, R. I. T., Eldridge, M. D. B., and Cooper, D. W. (2009). Landscape discontinuities influence gene flow and genetic structure in a large, vagile Australian mammal, Macropus fuliginosus. Molecular Ecology 18, 3363–3378.
Landscape discontinuities influence gene flow and genetic structure in a large, vagile Australian mammal, Macropus fuliginosus.CrossRef | 1:CAS:528:DC%2BD1MXhtFKmsr%2FN&md5=2d64f288870dedceca6be214e9d14784CAS |

Neaves, L. E., Zenger, K. R., Prince, R. I. T., and Eldridge, M. D. B. (2012). Impact of Pleistocene aridity oscillations on the population history of a widespread, vagile Australian mammal, Macropus fuliginosus. Journal of Biogeography 39, 1545–1563.
Impact of Pleistocene aridity oscillations on the population history of a widespread, vagile Australian mammal, Macropus fuliginosus.CrossRef |

Nei, M. (1978). Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89, 538–590.

Peakall, R., and Smouse, P. (2006). Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6, 288–295.
Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research.CrossRef |

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.
Spatial autocorrelation analysis offers new insights into gene flow in the Australian bush rat, Rattus fuscipes.CrossRef |

Pérez-Espona, S., Pérez-Barbería, F. J., Jiggins, C. D., Gordon, I. J., and Pemberton, J. M. (2010). Variable extent of sex-biased dispersal in a strongly polygynous mammal. Molecular Ecology 19, 3101–3113.
Variable extent of sex-biased dispersal in a strongly polygynous mammal.CrossRef |

Pritchard, J. K., Stephens, M., and Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics 155, 945–959.
| 1:STN:280:DC%2BD3cvislKrtA%3D%3D&md5=ebd32f6e3060730a6655a20992d2ddc6CAS |

Queller, D. C., and Goodnight, K. F. (1989). Estimating relatedness using genetic markers. Evolution 43, 258–275.
Estimating relatedness using genetic markers.CrossRef |

R Development Core Team (2014). R: A language and environment for statistical computing. Available at: http://www.r-project.org/

Rioux-Paquette, E., Garant, D., Martin, A. M., Coulson, G., and Festa-Bianchet, M. (2015). Paternity in eastern grey kangaroos: moderate skew despite strong sexual dimorphism. Behavioral Ecology 26, 1147–1155.
Paternity in eastern grey kangaroos: moderate skew despite strong sexual dimorphism.CrossRef |

Roberts, M. W. (2011). The ecology of eastern grey kangaroos, Macropus giganteus, and their potential source of human pathogens in Sydney’s water supply catchment. Ph.D. Thesis, Macquarie University, Sydney.

Roberts, M. W., Neaves, L. E., Claassens, R., and Herbert, C. A. (2010). Darting eastern grey kangaroos: a protocol for free-ranging populations. In ‘Macropods: The Biology of Kangaroos, Wallabies and Rat-kangaroos’. (Eds G. Coulson and M. D. B. Eldridge.) p. 325. (Surrey Beatty: Sydney.)

Southwell, C. J., Cairns, S. C., Palmer, R., Delaney, R., and Broers, R. (1997). Abundance of large macropods in the eastern highlands of Australia. Wildlife Society Bulletin 25, 125–132.

Stuart-Dick, R. I., and Higginbottom, K. B. (1989). Strategies of parental investment in macropodoids. In ‘Kangaroos, Wallabies and Rat-kangaroos’. (Eds G. C. Grigg, P. J. Jarman, and I. Hume.) pp. 571–592. (Surrey Beatty: Sydney.)

Sunnucks, P., and Hales, P. (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.
Numerous transposed sequences of mitochondrial cytochrome oxidase I–II in aphids of the genus Sitobion (Hemiptera: Aphididae).CrossRef | 1:CAS:528:DyaK28Xht1Kgurk%3D&md5=2976eed10845feab92ab0c010c27fc05CAS |

Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution 30, 2725–2729.
MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0.CrossRef | 1:CAS:528:DC%2BC3sXhvVKhurzP&md5=8da55d066d73877ea73394f77444cc5bCAS |

Taylor, A. C., and Cooper, D. W. (1998). A set of tammar wallaby (Macropus eugenii) microsatellites tested for genetic linkage. Molecular Ecology 7, 925–926.
| 1:CAS:528:DyaK1cXlsFKlur4%3D&md5=ef74127eb20c1bf3fced6f2ddd47cb22CAS |

Van Oosterhout, C., Hutchinson, W. F., Wills, D. P. M., and Shipley, P. (2004). Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4, 535–538.
Micro-checker: software for identifying and correcting genotyping errors in microsatellite data.CrossRef | 1:CAS:528:DC%2BD2cXnvFOktb8%3D&md5=9cd3b93c23d1169be30f5281343cfa4eCAS |

Viggers, K. L., and Hearn, J. P. (2005). The kangaroo conundrum: home range studies and implications for land management. Journal of Applied Ecology 42, 99–107.
The kangaroo conundrum: home range studies and implications for land management.CrossRef |

Worton, B. J. (1989). Kernel methods for estimating the utilization distribution in home-range studies. Ecology 70, 164–168.
Kernel methods for estimating the utilization distribution in home-range studies.CrossRef |

Zenger, K. R., and Cooper, D. W. (2001a). A set of highly polymorphic microsatellite markers developed for the eastern grey kangaroo (Macropus giganteus). Molecular Ecology Notes 1, 98–100.
A set of highly polymorphic microsatellite markers developed for the eastern grey kangaroo (Macropus giganteus).CrossRef | 1:CAS:528:DC%2BD3MXlslaksbc%3D&md5=f747d8f05161381736054634e903e534CAS |

Zenger, K. R., and Cooper, D. W. (2001b). Characterisation of 14 macropod microsatellite genetic markers. Animal Genetics 32, 166–167.
Characterisation of 14 macropod microsatellite genetic markers.CrossRef | 1:CAS:528:DC%2BD3MXms1egtbw%3D&md5=185ad175488124bda353f44148a7f10aCAS |

Zenger, K. R., Eldridge, M. D. B., and Cooper, D. W. (2003). Intraspecific variation, sex-biased dispersal and phylogeography of the eastern grey kangaroo (Macropus giganteus). Heredity 91, 153–162.
Intraspecific variation, sex-biased dispersal and phylogeography of the eastern grey kangaroo (Macropus giganteus).CrossRef | 1:CAS:528:DC%2BD3sXlslKju74%3D&md5=8c06a745d9774d7b8cff60f036a41434CAS |



Rent Article (via Deepdyve) Supplementary MaterialSupplementary Material (214 KB) Export Citation

View Altmetrics