Body size and sexual selection in the koala

Abstract

Sexual selection is often characterized by polygynous breeding systems, size dimorphism, and skewed operational sex ratios. Koalas are sexually dimorphic in multiple domains, yet are absent from the literature on sexual selection and the structure of their mating system is unclear. We provide the first documentation of the strength of sexual selection in koalas by using microsatellite markers to identify sires. We combine the genetic data with morphological data in order to assess the role of body size in regulating reproductive output. During our 4-year study, 37% of males were identified as possible sires. Males were significantly larger than females, with sires heavier than non-sires. Male body mass correlated with annual reproductive output, with Crow’s Index of Opportunity for Selection revealing that variation in male reproductive success was threefold higher than that of females. Since it appears that male koalas rarely engage in physical confrontations over access to females, size dimorphism could be based upon non-agonistic competition and/or female mate choice. We propose that size dimorphism in koalas evolved as a consequence of endurance rivalry promoting vocal sexual advertisements that attract females. We suggest that female choice is a key mediator of male reproductive output.

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References

  1. Andersson M (1994) Sexual selection. Princeton University Press, Princeton

    Google Scholar 

  2. Bercovitch FB (1997) Reproductive strategies of rhesus macaques. Primates 38:247–263

    Article  Google Scholar 

  3. Bercovitch FB (2007) Connecting conservation biology with evolutionary ecology: the case of the koala. Biodiversity 8:33–37

    Google Scholar 

  4. Bercovitch FB, Bashaw MJ, del Castillo SM (2006a) Sociosexual behavior, male mating tactics, and the reproductive cycle of giraffe, Giraffa camelopardalis. Horm Behav 50:314–321

    PubMed  Article  Google Scholar 

  5. Bercovitch FB, Tobey JR, Andrus CH, Doyle L (2006b) Mating patterns and reproductive success in captive koalas (Phascolarctos cinereus). J Zool 270:512–516

    Article  Google Scholar 

  6. Breuer T, Robbins AM, Polejniczac C, Parnell RJ, Stokes EJ, Robbins MM (2010) Variance in the male reproductive success of western gorillas: acquiring females is just the beginning. Behav Ecol Sociobiol 64:515–528

    Article  Google Scholar 

  7. Clutton-Brock TH (2004) What is sexual selection? In: Kappeler PM, van Schaik C (eds) Sexual selection in primates: new and comparative perspectives. Cambridge University Press, Cambridge, pp 24–36

    Google Scholar 

  8. Cornwallis CK, Uller T (2010) Towards and evolutionary ecology of sexual traits. TREE 25:145–152

    PubMed  Google Scholar 

  9. Crow JF (1962) Population genetics. Am J Hum Genet 13:137–150

    Google Scholar 

  10. Darwin CR (1871) The descent of man and selection in relation to sex. John Murray, London

    Google Scholar 

  11. Derocher AE, Andersen M, Wiig O, Aars J (2010) Sexual dimorphism and the mating ecology of polar bears (Ursus maritimus) at Svalbard. Behav Ecol Sociobiol 64:939–946

    Article  Google Scholar 

  12. Dique DS, Thompson J, Preece HJ, de Villiers DL, Carrick FN (2003) Dispersal patterns in a regional koala population in south-east Queensland. Wildl Res 30:281–290

    Article  Google Scholar 

  13. Eberhard W (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, Princeton

    Google Scholar 

  14. Ellefson JO (1968) Territorial behavior in the common white-handed gibbon, Hylobates lar Linn. In: Jay PC (ed) Primates: studies in adaptation and variability. Holt, Rinehart, & Winston, New York, pp 180–199

    Google Scholar 

  15. Ellis W, Carrick FN (1992) Total-body water and the estimation of fat in the koala (Phascolarctos cinereus). Aust Vet J 69:229–231

    PubMed  Article  CAS  Google Scholar 

  16. Ellis WAH, Melzer A, Green B, Newgrain K, Hindell MA, Carrick FN (1995) Seasonal variation in water flux, field metabolic rate and food consumption of free-ranging koalas (Phascolarctos cinereus). Aust J Zool 43:59–68

    Article  Google Scholar 

  17. Ellis WA, Hale PT, Carrick F (2002) Breeding dynamics of koalas in open woodlands. Wildl Res 29:19–25

    Article  Google Scholar 

  18. Ellis WAH, Melzer A, Bercovitch FB (2009) Spatiotemporal dynamics of habitat use by koalas: the checkerboard model. Behav Ecol Sociobiol 63:1181–1188

    Article  Google Scholar 

  19. Ellis W, Bercovitch FB, FitzGibbon S, Melzer A, de Villiers D, Dique D (2010) Koala birth seasonality and sex ratios across multiple sites in Queensland, Australia. J Mammal 90:177–182

    Article  Google Scholar 

  20. Ellis W, Bercovitch F, FitzGibbon S, Roe P, Wimmer J, Melzer A, Wilson RJ (2011) Koala bellows and their impact on the spatial dynamics of free ranging koalas. Behav Ecol (in press)

  21. Gordon G, McGreevy DG, Lawrie BC (1990) Koala population turnover and male social organization. In: Lee AK, Handasyde KA, Sanson GD (eds) Biology of the koala. Surrey Beatty, Chipping Northon, pp 189–192

    Google Scholar 

  22. Haldane JBS (1932) The causes of evolution. Longman, London

    Google Scholar 

  23. Johnston SD, McGowan MR, Phillips NJ, O'Callaghan P (2000) Optimal physicochemical conditions for the manipulation and short-term preservation of koala (Phascolarctos cinereus) spermatozoa. J Reprod Fertil 118:273–281

    PubMed  Article  CAS  Google Scholar 

  24. Jones AG (2009) On the opportunity for sexual selection, the Bateman gradient and the maximum intensity of sexual selection. Evolution 63:1673–1684

    PubMed  Article  Google Scholar 

  25. Kamilar JM, Pokempner AA (2008) Does body mass dimorphism increase male–female dietary niche separation? A comparative study of primates. Behaviour 145:1211–1234

    Article  Google Scholar 

  26. Krockenberger A (2003) Meeting the energy demands of reproduction in female koalas, Phascolarctos cinereus: evidence for energetic compensation. J Comp Physiol B Biochem Syst Environ Physiol 173:531–540

    Article  CAS  Google Scholar 

  27. Le Boeuf BJ, Reiter J (1988) Lifetime reproductive success in northern elephant seals. In: Clutton-Brock TH (ed) Reproductive success. University of Chicago Press, Chicago, pp 344–362

    Google Scholar 

  28. Lee A, Martin R (1988) The koala, a natural history. University of New South Wales Press, Sydney

    Google Scholar 

  29. Lee KE, Seddon JM, Ellis WAH, Johnston SD, de Villiers DL, Preece HJ, Carrick FN (2010) Genetic variation and structuring in the threatened koala populations of Southeast Queensland. Conservat Genet 11:2091–2103

    Article  Google Scholar 

  30. Martin R, Handasyde KA (1999) The Koala: natural history, conservation and management. University of New South Wales Press, Sydney

    Google Scholar 

  31. Mitchell P (1990a) The home ranges and social activity of koalas—a quantitative analysis. In: Lee AK, Handasyde KA, Sanson GD (eds) Biology of the Koala. Surrey Beatty and Sons, Sydney, pp 171–187

    Google Scholar 

  32. Mitchell P (1990b) Social behaviour and communication of koalas. In: Lee AK, Handasyde KA, Sanson GD (eds) Biology of the koala. Surrey Beatty and Sons, Sydney, pp 151–170

    Google Scholar 

  33. Mitchell P, Martin R (1990) The structure and dynamics of koala populations—French Island in perspective. In: Lee AK, Handasyde KA, Sanson GD (eds) Biology of the koala. Surrey Beatty, Chipping Norton, pp 97–108

    Google Scholar 

  34. Moore BD, Foley WJ (2005) Tree use by koalas in a chemically complex landscape. Nature 435:488–490

    PubMed  Article  CAS  Google Scholar 

  35. Pontzer H, Raichlen DA, Shumaker RW, Ocobock C, Wich SA (2010) Metabolic adaptation for low energy throuhput in orangutans. PNAS. doi:10.1073/pnas.1001031107

    PubMed  Google Scholar 

  36. Ruckstuhl K, Neuhaus P (2006) Sexual segregation in vertebrates. Cambridge University Press, Cambridge

    Google Scholar 

  37. Schultz AH (1969) The life of primates. Weidenfeld and Nicolson, London

    Google Scholar 

  38. Selander R (1972) Sexual selection and sexual dimorphism in birds. In: Campbell B (ed) Sexual selection and the descent of man, 1871–1971. Aldine, Chicago, pp 180–230

    Google Scholar 

  39. Smith M (1980a) Behaviour of the koala, Phascolarctos cinereus (Goldfuss), in captivity. 3. Vocalizations. Wildl Res 7:13–24

    Article  Google Scholar 

  40. Smith M (1980b) Behaviour of the koala, Phascolarctos cinereus (Goldfuss), in captivity. 5. Sexual behaviour. Wildl Res 7:41–51

    Article  Google Scholar 

  41. Tobey JR, Andrus CH, Doyle L, Thompson VD, Bercovitch FB (2006) Maternal effort and joey growth in koalas (Phascolarctos cinereus). J Zool 268:423–431

    Article  Google Scholar 

  42. Tobey JR, Nute TR, Bercovitch FB (2009) Age and seasonal changes in the semiochemicals of the sternal gland secretions of male koalas (Phascolarctos cinereus). Aust J Zool 57:111–118

    Article  Google Scholar 

  43. Tucker GM (2009) Ecology, behaviour and growth of sub-adult koalas (Phascolarctos cinereus) on St Bees Island, Central Queensland. In: Centre for Environmental Management. Central Queensland University, Rockhampton, pp 285

  44. Tucker GM, Melzer A, Ellis W (2007) The development of habitat selection by subadult koalas. Aust J Zool 55:285–289

    Article  Google Scholar 

  45. Utami SA, van Hooff JARAM (2004) Alternative male reproductive strategies: male bimaturism in orangutans. In: Kappeler P, van Schaik C (eds) Sexual selection in primates. Cambridge University Press, Cambridge, pp 196–207

    Google Scholar 

  46. Vannoni E, McElligott AG (2009) Fallow bucks get hoarse: vocal fatigue as a possible signal to conspecifics. Anim Behav 78:3–10

    Article  Google Scholar 

  47. Wade MJ, Arnold SJ (1980) The intensity of sexual selection in relation to male sexual behaviour, female choice, and sperm precedence. Anim Behav 28:446–461

    Article  Google Scholar 

  48. Wade MJ (1987) Measuring sexual selection. In: Bradbury JW, Andersson MB (eds) Sexual selection: testing the alternatives. Chichester, New York, pp 197–207

    Google Scholar 

  49. Wade MJ, Shuster SM (2004) Sexual selection: harem size and the variance in male reproductive success. Am Nat 164:E83–E89

    PubMed  Article  Google Scholar 

  50. Wells KD (2001) The energetic cost of calling in tree frogs. In: Ryan MJ (ed) Anuran communication. Smithsonian Institution Press, Washington, DC, pp 45–60

    Google Scholar 

  51. Wells KD, Schwartz JJ (2006) The behavioural ecology of anuran communication. In: Narins PM, Feng AS, Fay RR, Popper AK (eds) Hearing and sound communication in amphibians. Springer, New York, pp 44–86

    Google Scholar 

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Acknowledgments

This study could not have been completed without the valuable input of Sean FitzGibbon and Alistair Melzer, both of whom contributed data and ideas to this report. The project was funded by The Earthwatch Organization and The San Diego Zoo Institute for Conservation Research. Field work was supported by Queensland Marine Parks Mackay. Kristen Lee oversaw all genetic analyses. Delma Clifton, Gail Tucker, Steve Burke, and Steve Fisher assisted with fieldwork. Queensland Department of Environmental and Resource Management provided the permits to work with koalas (WISP00491302), and the project was carried out under The University of Queensland animal ethics permit (ZOO/ENT/115/04/RT) and approved by the Institutional Animal Care and Use Committee of the Zoological Society of San Diego.

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Correspondence to William A. H. Ellis.

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Communicated by F. Trillmich

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Ellis, W.A.H., Bercovitch, F.B. Body size and sexual selection in the koala. Behav Ecol Sociobiol 65, 1229–1235 (2011). https://doi.org/10.1007/s00265-010-1136-4

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Keywords

  • Koalas
  • Sexual selection
  • Size dimorphism
  • Reproductive success
  • Mate choice
  • Microsatellite DNA