Olfactory cues, genetic relatedness and female mate choice in the agile antechinus (Antechinus agilis)

Abstract

Females show mate preferences for males that are genetically dissimilar to themselves in a variety of taxa, but how females choose these males is not clearly understood. In this study, we examined the effects of olfactory stimuli and genetic relatedness on female mate choice in a small carnivorous marsupial, the agile antechinus (Antechinus agilis), during two breeding seasons. Captive female antechinus in oestrus were provided with a combination of male urine and body scent from two novel males, one more genetically similar and one more dissimilar to the females, in a Y-maze olfactometer. Genetic relatedness between females and pairs of males was determined using highly polymorphic, species-specific, microsatellite markers. Females consistently chose to visit the scents of males that were genetically dissimilar to themselves first, spent significantly more time near the source of those scents and showed more sexual and non-exploratory behaviours near those scents. These data demonstrate that chemosensory cues are important in mate choice in the agile antechinus and that females prefer males that are genetically dissimilar to themselves.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3

References

  1. Aeschlimann PB, Haberli MA, Reusch TBH, Boehm T, Milinski M (2003) Female sticklebacks Gasterosteus aculeatus use self-reference to optimise MHC allele number during mate selection. Behav Ecol Sociobiol 54:119–126

    Google Scholar 

  2. Andersson M (1994) Sexual selection. Princeton University Press, Princeton, New Jersey

    Google Scholar 

  3. Banks SC, Finlayson GR, Lawson SJ, Lindenmayer DB, Paetkau D, Ward SJ, Taylor AC (2005) The effects of habitat fragmentation due to forestry plantation establishment on the demography and genetic variation of a marsupial carnivore, Antechinus agilis. Biol Conserv 122:581–597, DOI 10.1016/j.biocon.2004.09.013

    Article  Google Scholar 

  4. Bateson PPG (1983) Mate choice. Cambridge University Press, Cambridge, UK

    Google Scholar 

  5. Bradley AJ, McDonald IR, Lee AK (1980) Stress and mortality in a small marsupial (Antechinus stuartii, Macleay). Gen Comp Endocrinol 40:188–200

    PubMed  Article  CAS  Google Scholar 

  6. Braithwaite RW (1974) Behavioural changes associated with the population cycle of Antechinus stuartii (Marsupialia). Aust J Zool 22:45–62

    Article  Google Scholar 

  7. Braithwaite RW, Lee AK (1979) A mammalian example of semelparity. Am Nat 113:151–155

    Article  Google Scholar 

  8. Cockburn A, Scott MP, Scotts DJ (1985) Inbreeding avoidance and male-biased natal dispersion in Antechinus spp. (Marsupialia: Dasyuridae). Anim Behav 33:908–915

    Article  Google Scholar 

  9. Darwin C (1871) The descent of man, and selection in relation to sex. J. Murray, London, UK

    Google Scholar 

  10. Dickman CR, Parnaby HE, Crowther MS, King DH (1998) Antechinus agilis (Marsupialia: Dasyuridae), a new species from the A. stuartii complex in south eastern Australia. Aust J Zool 46:1–26

    Article  Google Scholar 

  11. Drickamer LC, Gowaty PA, Holmes CM (2000) Free female mate choice in house mice affects reproductive success and offspring viability and performance. Anim Behav 59:371–378

    PubMed  Article  Google Scholar 

  12. Kraaijeveld-Smit FJL, Ward SJ, Temple-Smith PD (2002a) Multiple paternity in a field population of a small carnivorous marsupial, the agile antechinus, Antechinus agilis. Behav Ecol Sociobiol 52:84–91, DOI 10.1007/s00265-002-0485-z

    Article  Google Scholar 

  13. Kraaijeveld-Smit FJL, Ward SJ, Temple-Smith PD, Paetkau D (2002b) Factors influencing paternity success in Antechinus agilis: last-male sperm precedence, timing of mating and genetic compatibility. J Evol Biol 15:100–107

    Article  Google Scholar 

  14. Landry C, Garant D, Duchesne P, Bernatchez L (2001) ‘Good genes as heterozygosity’: the major histocompatibility complex and mate choice in Atlantic salmon (Salmo salar). Proc R Soc Lond B 268:1279–1285

    Article  CAS  Google Scholar 

  15. Lazenby-Cohen KA, Cockburn A (1988) Lek promiscuity in a semelparous mammal, Antechinus stuartii (Marsupialia, Dasyuridae)? Behav Ecol Sociobiol 22:195–202

    Article  Google Scholar 

  16. Mays HL, Hill GE (2004) Choosing mates: good genes versus genes that are a good fit. TREE 19:554–559, DOI 10.1016/j.tree.2004.07.018

    PubMed  Google Scholar 

  17. Neff BD, Pitcher TE (2005) Genetic quality and sexual selection: an integrated framework for good genes and compatible genes. Molec Ecol 14:19–38, DOI 10.1111/j.1365-294X.2004.02395.x

    Article  CAS  Google Scholar 

  18. Olsson M, Madsen T, Nordby J, Wapstra E, Ujvari B, Wittsell H (2003) Major histocompatibility complex and mate choice in sand lizards. Proc R Soc Lond B 270:S254–S256

    CAS  Google Scholar 

  19. Potts WK, Manning CJ, Wakeland EK (1991) Mating patterns in seminatural populations of mice influenced by MHC genotype. Nature 352:619–621

    PubMed  Article  CAS  Google Scholar 

  20. Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275

    Article  Google Scholar 

  21. Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283

    Article  Google Scholar 

  22. Salamon M (1994) Seasonal, sexual and dietary induced variations in the sternal scent secretion in the brushtail possum (Trichosurus vulpecula). Adv Biosc 93:211–222

    Google Scholar 

  23. Salamon M, Davies NW (1998) Identification and variation of volatile compounds in sternal gland secretions of male koalas (Phascolarctos cinereus). J Chem Ecol 24:1659–1676

    Article  CAS  Google Scholar 

  24. Selwood L (1982) Brown antechinus Antechinus stuartii: management of breeding colonies to obtain embryonic material and pouch young. In: Evans DD (ed) The management of Australian mammals in captivity. Zoological Board of Victoria, Melbourne, pp 31–36

    Google Scholar 

  25. Shimmin GA, Taggart DA, Temple-Smith PD (2000) Sperm competition and genetic diversity in the agile antechinus (Dasyuridae: Antechinus agilis). J Zool 252:343–350

    Article  Google Scholar 

  26. SYSTAT (2004) SYSTAT for Windows, statistics, version 11 edn. SYSTAT, Illinois

  27. Toftegaard CL, Bradley AJ (2003) Chemical communication in dasyurid marsupials. In: Jones M, Dickman C, Archer M (eds) Predators with pouches. CSIRO Publishing, Melbourne, pp 347–357

    Google Scholar 

  28. Toftegaard CL, McMahon KL, Galloway GL, Bradley AJ (2002) Processing of urinary pheromones in Antechinus stuartii (Marsupialia: Dasyuridae): functional magnetic resonance imaging of the brain. J Mammal 83:71–80

    Article  Google Scholar 

  29. Tregenza T, Wedell N (2000) Genetic compatibility, mate choice and patterns of parentage: Invited Review. Molec Ecol 9:1013–1027

    Article  CAS  Google Scholar 

  30. Wedekind C, Füri S (1997) Body odour preferences in men and women: do they aim for specific MHC combinations or simple heterozygosity? Proc R Soc Lond B 264:1471–1479

    Article  CAS  Google Scholar 

  31. Wegner KM, Reusch TBH, Kalbe M (2003) Multiple parasites are driving major histocompatibility complex polymorphism in the wild. J Evol Biol 16:224–232

    PubMed  Article  CAS  Google Scholar 

  32. Westneat DF, Stewart IRK (2003) Extra-pair paternity in birds: causes, correlates and conflict. Annu Rev Ecol Evol 34:365–396

    Article  Google Scholar 

  33. Yamazaki K, Boyse EA, Mike V, Thaler HT, Mathieson BJ, Abbott J, Boyse J, Zayas ZA, Thomas L (1976) Control of mating preferences in mice by genes in the major histocompatibility complex. J Exp Med 144:1324–1335

    PubMed  Article  CAS  Google Scholar 

  34. Zabaras R, Richardson BJ, Wyllie SG (2005) Evolution in the suit of semiochemicals secreted by the sternal gland of Australian marsupials. Aust J Zool 53:257–263, DOI 10.1071/ZO04070

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was funded by a Melbourne Research PhD Scholarship, grants from the Holsworth Wildlife Research Endowment and Winifred Violet Scott Estate, a Loftus–Hills Memorial Fund Award and David Hay Postgraduate Writing-up Award to M. Parrott. We thank Lynne Selwood and Mark Elgar for their valuable advice and comments on the manuscript. This research adhered to the Animal Behaviour Society Guidelines for the use of animals and was carried out with ethics approval from the Animal Ethics Sub-Committee at the University of Melbourne and under the Department of Sustainability and Environment Wildlife permits.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Marissa L. Parrott.

Additional information

Communicated by P. Banks

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Parrott, M.L., Ward, S.J. & Temple-Smith, P.D. Olfactory cues, genetic relatedness and female mate choice in the agile antechinus (Antechinus agilis). Behav Ecol Sociobiol 61, 1075–1079 (2007). https://doi.org/10.1007/s00265-006-0340-8

Download citation

Keywords

  • Mate choice
  • Olfactory cues
  • Genetic relatedness
  • Antechinus agilis