Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
Shopping Cart: ( empty )
You are here: Home > Journals > RD > RD09061
RESEARCH ARTICLE
Contents Vol 22(3)

Dominance, body size and internal relatedness influence male reproductive success in eastern grey kangaroos (Macropus giganteus)

Emily J. Miller A C D , Mark D. B. Eldridge B , Desmond W. Cooper A and Catherine A. Herbert A C
+ Author Affiliations
- Author Affiliations

A School of Biological, Earth and Environmental Sciences, The University of New South Wales, Kensington, NSW 2052, Australia.

B Molecular Biology, Australian Museum, 6 College Street, Sydney, NSW 2010, Australia.

C Present address: Faculty of Veterinary Science, The University of Sydney, Camperdown, NSW 2006, Australia.

D Corresponding author. Email: emily.miller@sydney.edu.au

Reproduction, Fertility and Development 22(3) 539-549 https://doi.org/10.1071/RD09061
Submitted: 17 March 2009  Accepted: 21 September 2009   Published: 15 February 2010

Abstract

Knowledge of the determinants of reproductive success is essential for understanding the adaptive significance of particular traits. The present study examined whether particular behavioural, morphological, physiological or genetic traits were correlated with male dominance and reproductive success using three semi-free-ranging captive populations (n = 98) of the eastern grey kangaroo (Macropus giganteus). The morphological traits measured included bodyweight, head, forearm, tail, pes and leg length, forearm and bicep circumference, and testis size. Blood samples were collected to determine serum testosterone concentrations. All individuals were typed for 10 microsatellite loci and paternity determined for each pouch young. To determine the influence of relatedness and genetic diversity on male reproductive success, internal relatedness, standardised heterozygosity and mean d2 were calculated. Dominant males sired a significantly higher proportion of offspring than smaller, lower-ranked males and had higher testosterone concentrations. Males that sired offspring were significantly heavier and had larger body size. Sires were significantly more heterozygous and genetically dissimilar to breeding females than non-sires. Despite the wealth of knowledge on the social organisation of kangaroos, this is the first study to assign parentage and male reproductive success using molecular evidence.

Additional keywords: dominance hierarchy, genetic diversity, male–male competition, sire.


Acknowledgements

This research was funded by an ARC Linkage Grant (LP0560344) and forms part of the Koala and Kangaroo Contraception Program. Special thanks to James Cook and Jan Nedved for field assistance, Celine Frère and David Warton for statistical advice, Waratah Park Earth Sanctuary, Australia Walkabout Wildlife Sanctuary, Bill Amos and Karina Acevedo-Whitehouse for the IR macro, Emily Bolitho and Graeme Coulson, and Cameron Wood and Margaret Wilkinson at the Royal North Shore Hospital.


References

Acevedo-Whitehouse, K. , Gulland, F. , Greig, D. , and Amos, W. (2003). Inbreeding: disease susceptibility in California sea lions. Nature 422, 35.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS | Andersson M. (1994). ‘Sexual Selection.’ (Princeton University Press: New Jersey.)

Beacham, J. L. (2003). Models of dominance hierarchy formation: effects of prior experience and intrinsic traits. Behaviour 140, 1275–1303.
| Crossref | GoogleScholarGoogle Scholar | Birkhead T. R., and Møller A. P. (1998). ‘Sperm Competition and Sexual Selection.’ (Academic Press: London.)

Caughley G. (1987). Introduction to the sheep rangelands. In ‘Kangaroos: Their Ecology and Management in the Sheep Rangelands of Australia’. (Eds G. Caughley, N. Shepherd and J. Short.) pp. 1–13. (Cambridge University Press: Cambridge.)

Charmantier, A. , and Sheldon, B. C. (2006). Testing genetic models of mate choice evolution in the wild. Trends Ecol. Evol. 21, 417–419.
| Crossref | GoogleScholarGoogle Scholar | PubMed | Clutton-Brock T. H. (1988). ‘Reproductive Success. Studies of Individual Variation in Constrasting Breeding Systems.’ (University of Chicago Press: Chicago.)

Clutton-Brock, T. H. (1989). Mammalian mating systems. Proc. R. Soc. Lond. B Biol. Sci. 236, 339–372.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS | Clutton-Brock T. H., Guinness F. E., and Albon S. D. (1982). ‘Red Deer: Behaviour and Ecology of Two Sexes.’ (University of Chicago Press: Chicago.)

Clutton-Brock, T. H. , Green, D. , Hiraiwa-Hasegawa, M. , and Albon, S. D. (1988). Passing the buck: resource defence, lek breeding and mate choice in fallow deer. Behav. Ecol. Sociobiol. 23, 281–296.
| Crossref | GoogleScholarGoogle Scholar | Coulson G. (1998). Management of overabundant macropods: are there conservation benefits? In ‘Managing Maruspial Abundance for Conservation Benefits’. (Ed. A. Austin.) pp. 37–48. (Cooperative Research Centre for the Conservation and Management of Marsupials: Sydney.)

Coulson, T. N. , Pemberton, J. M. , Albon, S. D. , Beaumont, M. , Marshall, T. C. , Slate, J. , Guinness, F. E. , and Clutton-Brock, T. H. (1998). Microsatellites reveal heterosis in red deer. Proc. Biol. Sci. 265, 489–495.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS | Department for Environment and Heritage (2007). ‘The Kangaroo Conservation and Management Plan for South Australia 2008–2012.’ (Government of South Australia: Adelaide.)

Dewsbury, D. A. (1982). Dominance rank, copulatory behaviour, and differential reproduction. Q. Rev. Biol. 57, 135–159.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS | Eberhard W. G. (1996). ‘Female Control: Sexual Selection by Female Cryptic Choice.’ (Princeton University Press: NJ.)

Emlen, S. T. , and Oring, L. W. (1977). Ecology, sexual selection, and the evolution of mating systems. Science 197, 215–223.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS | Frankham R., Ballou J. D., and Briscoe D. A. (2002). ‘Introduction to Conservation Genetics.’ (Cambridge University Press: Cambridge.)

Ganslosser U. (1989). Agonistic behaviour in Macropodoids: a review. In ‘Kangaroos, Wallabies and Rat-Kangaroos’. (Eds G. Grigg, P. Jarman and I. Hume.) pp. 475–503. (Surrey Beatty and Sons: Sydney.)

Hamilton, W. D. , and Zuk, M. (1982). Heritable true fitness and bright birds: a role for parasites? Science 218, 384–387.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS | Herbert C. A. (2007). From the urban fringe to the Abrolhos Islands: management challenges of burgeoning marsupial populations. In ‘Pest or Guest: The Zoology of Overabundance’. (Eds D. Lunney, P. Eby, P. Hutchings and S. Burgin.) pp. 129–141. (Royal Zoological Society of New South Wales: Mosman.)

Hill, G. J. E. (1982). Seasonal movement patterns of the eastern grey kangaroo in Southern Queensland. Aust. Wildl. Res. 9, 373–387.
| Crossref | GoogleScholarGoogle Scholar | Hood G. M. (2008). PopTools version 3.0.3. Available at http://www.cse.csiro.au/poptools [Verified 28 January 2010]

Hynes, E. F. , Rudd, C. D. , Temple-Smith, P. D. , Sofronidis, G. , Paris, D. , Shaw, G. , and Renfree, M. B. (2005). Mating sequence, dominance and paternity success in captive male tammar wallabies. Reproduction 130, 123–130.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS | Jarman P. J. (1989). Sexual dimporhism in Macropodoidea. In ‘Kangaroos, Wallabies, and Rat-Kangaroos’. (Eds G. Grigg, P. Jarman and I. Hume.) pp. 433–447. (Surrey Beatty and Sons: Sydney.)

Jarman, P. J. (1991). Social behaviour and organisation in the Macropodoidea. Adv. Stud. Behav. 20, 1–50.
| Crossref | GoogleScholarGoogle Scholar | Jarman P. J. (2000). Males in Macropod society. In ‘Primate Males: Causes and Consequences of Variation in Group Composition. Proceedings of the Gottinger Freilandtage, Deutsches Primatenzentrum, December 1997’. (Ed. P. M. Kappeler.) pp. 21–33. (Cambridge University Press: Cambridge.)

Jarman P. J., and Southwell C. J. (1986). Grouping, associations and reproductive strategies in eastern grey kangaroos. In ‘Ecological Aspects of the Social Evolution’. (Eds P. I. Rubenstein and R. W. Wrangham.) pp. 399–430. (Princeton University Press: London.)

Jarman, P. J. , and Taylor, R. J. (1983). Ranging of eastern grey kangaroos and wallaroos on a New England pastoral property. Aust. Wildl. Res. 10, 33–38.
| Crossref | GoogleScholarGoogle Scholar | Manly B. F. J. (2001). ‘Randomisation, Bootstrap and Monte Carlo Methods in Biology.’ (Chapman & Hall: London.)

Martin P., and Bateson P. (1993). ‘Measuring Behaviour: An Introductory Guide.’ (Cambridge University Press: Cambridge.)

Marvan, R. , Stevens, J. M. G. , Roeder, A. D. , Mazura, I. , Bruford, M. W. , and de Ruiter, J. R. (2006). Male dominance rank, mating and reproductive success in captive bonobos (Pan paniscus). Folia Primatol. 77, 364–376.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS | Miller E. J., Eldridge M. D. B., and Herbert C. A. (2010). Dominance and paternity in the tammar wallaby (Macropus eugenii). In ‘Macropods: The Biology of Kangaroos, Wallabies and Rat-Kangaroos’. (Eds G. Coulson and M. D. B. Eldridge.) pp. 77–86. (CSIRO Publishing: Collingwood.)

Milner-Gulland, E. J. , and Mace, R. H. (1991). The impact of the ivory trade on the elephant population of the trade, as assessed by data from the trade. Biol. Conserv. 55, 215–229.
| Crossref | GoogleScholarGoogle Scholar | Poole W. E., Simms N. G., Wood J. T., and Lubulwa M. (1991). ‘Tables for Age Determination of the Kangaroo Island Wallaby (Tammar), Macropus eugenii, From Body Measurements. CSIRO Division of Wildlife and Ecology, Technical Memorandum No. 32.’ (CSIRO: Canberra.)

Pusey, A. E. (1987). Sex-biased dispersal and inbreeding avoidance in birds and mammals. Trends Ecol. Evol. 2, 295–299.
| Crossref | GoogleScholarGoogle Scholar | Trivers R. L. (1972). Parental investment and sexual selection. In ‘Sexual Selection and the Descent of Man, 1871–1971’. (Ed. B. Campbell.) pp. 136–172. (Aldine-Atherton: Chicago.)

Tyndale-Biscoe C. H., and Renfree M. B. (1987). ‘Reproductive Physiology of Marsupials.’ (Cambridge University Press: Cambridge.)

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. Mol. Ecol. Notes 4, 535–538.
| Crossref | GoogleScholarGoogle Scholar | CAS |

Williamson, P. , Fletcher, T. P. , and Renfree, M. B. (1990). Testicular development and maturation of the hypothalamic–pituitary–testicular axis in the male tammar, Macropus eugenii. J. Reprod. Fertil. 88, 549–557.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Zahavi, A. (1975). Mate selection: a selection for a handicap. J. Theor. Biol. 53, 205–214.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |

Zenger, K. R. , and Cooper, D. W. (2001). Characterisation of 14 macropod microsatellite genetic markers. Anim. Genet. 32, 166–167.
| Crossref | GoogleScholarGoogle Scholar | PubMed | CAS |

Zenger, K. R. , Eldridge, M. D. B. , Pope, L. C. , and Cooper, D. W. (2003). Characterisation and cross-species utility of microsatellite markers within kangaroos, wallabies and rat kangaroos (Macropodoidea: Marsupialia). Aust. J. Zool. 51, 587–596.
| Crossref | GoogleScholarGoogle Scholar | CAS |