Behavioral Ecology and Sociobiology

, Volume 68, Issue 7, pp 1085–1096 | Cite as

Proximate and ultimate explanations of mammalian sex allocation in a marsupial model

  • Lisa E. Schwanz
  • Kylie A. Robert
Original Paper


Offspring sex ratios in mammals vary in potentially adaptive yet unpredictable ways. An integrative approach that simultaneously examines proximate and ultimate explanations of mammalian sex ratios would greatly advance the field. We examined the importance of maternal glucose and stress hormones for offspring sex (male or female) as mechanisms associated with the Trivers–Willard and the local resource competition hypotheses of sex allocation. We tested this framework in a marsupial mammal, the tammar wallaby (Macropus eugenii). Mothers that were better able to maintain body condition over the driest part of the year, a presumptive proxy for local resource availability, were more likely to produce daughters (the philopatric sex), consistent with local resource competition. Maternal glucose was correlated with offspring sex, but in the opposite direction than we predicted—higher maternal glucose was associated with female pouch young. These patterns, however, were not consistent across the 2 years of our study. Maternal stress hormone metabolites measured from fecal samples did not predict glucose or offspring sex. A causative glucose mechanism may underlie an adaptive strategy for mothers with high local resources (high glucose) to produce philopatric daughters that will benefit from inheriting resource access. Examining species-specific relationships between glucose and offspring sex across mammals could provide crucial insight into the disparate ecological and selective pressures faced by mammals with respect to offspring sex ratio.


Sex allocation Glucocorticoids Corticosteroids Maternal condition Resource competition Sex ratio Glucose 



This research was conducted with the permission of the Australian Department of Defence. We thank J. Wann and T. Smith for assistance in accessing the animals and research facilities, and B. Chambers and R. Bencini for advice on research design, logistics, loaned traps, and lodging. Numerous field assistants helped with the trapping. Comments from C. Johnson, M. Jennions, and D. Reznick improved the manuscript. We thank E. Berkeley, F. Krikowa, B. Maher, R. McCuaig, S. Thomas, and the University of Canberra Faculty of Applied Science Molecular Lab for equipment, space, advice, and assistance with the hormonal analyses. The research was funded by a U.S. National Science Foundation International Research Fellowship (LES), a University of Western Australia Postdoctoral Research Fellowship (KAR), University of Western Australia Research Grants Scheme (KAR), and the Australian Department of Defence (KAR and LES).

Ethical standards

This research was conducted in compliance with ethical standards in Australia, under the ethical approval of the University of Western Australia’s Animal Ethics Committee (approval: RA/3/100/897) and Department of Environment and Conservation Research approval (permits: SF007185 and SF007651).

Conflict of interest

The authors have no conflict of interest regarding the publication of this paper.

Supplementary material

265_2014_1720_MOESM1_ESM.docx (35 kb)
ESM 1 (DOCX 35 kb)


  1. Banks SC, Knight EJ, Dubach JE, Lindenmayer DB (2008) Microhabitat heterogeneity influences offspring sex allocation and spatial kin structure in possums. J Animal Ecol 77:1250–1256CrossRefGoogle Scholar
  2. Barker JM (1961) Metabolism of carbohydrate and volatile fatty acids in marsupial, Setonix brachyurus. Q J Exp Physiol CMS 46:54–68Google Scholar
  3. Bermejo-Alvarez P, Rizos D, Rath D, Lonergan P, Gutierrez-Adan A (2010) Sex determines the expression level of one third of the actively expressed genes in bovine blastocysts. Proc Natl Acad Sci U S A 107:3394–3399PubMedCentralPubMedCrossRefGoogle Scholar
  4. Blumstein D, Evans CS, Daniel JC (1999) An experimental study of behavioural group size effects in tammar wallabies, Macropus eugenii. Anim Behav 58:351–360PubMedCrossRefGoogle Scholar
  5. Blumstein DT, Ardron JG, Evans CS (2002a) Kin discrimination in a macropod marsupial. Ethology 108:815–823CrossRefGoogle Scholar
  6. Blumstein DT, Daniel JC, Ardron JG, Evans CS (2002b) Does feeding competition influence tammar wallaby time allocation? Ethology 108:937–945CrossRefGoogle Scholar
  7. Blumstein DT, Daniel JC, Springett BP (2004) A test of the multi-predator hypothesis: rapid loss of antipredator behavior after 130 years of isolation. Ethology 110:919–934CrossRefGoogle Scholar
  8. Bonier F, Martin PR, Wingfield JC (2007) Maternal corticosteroids influence primary offspring sex ratio in a free-ranging passerine bird. Behav Ecol 18:1045–1050CrossRefGoogle Scholar
  9. Cameron EZ (2004) Facultative adjustment of mammalian sex ratios in support of the Trivers-Willard hypothesis: evidence for a mechanism. Proc R Soc Lond B 271:1723–1728CrossRefGoogle Scholar
  10. Cameron EZ, Lemons PR, Bateman PW, Bennett NC (2008) Experimental alteration of litter sex ratios in a mammal. Proc R Soc Lond B 275:323–327CrossRefGoogle Scholar
  11. Catling PC, Vinson GP (1976) Adrenocortical hormones in the neonate and pouch young of the tammar wallaby, Macropus eugenii. J Endocrinol 69:447–448PubMedCrossRefGoogle Scholar
  12. Chambers BK (2009) Human disturbance affects the ecology and population dynamics of the tammar wallaby, Macropus eugenii, on Garden Island. Dissertation, University of Western Australia, Western AustraliaGoogle Scholar
  13. Chambers BK, Bencini R (2010) Impact of human disturbance on the population dynamics and ecology of tammar wallabies on Garden Island, Western Australia. In: Coulson G, Eldridge M (eds) Macropods: the biology of kangaroos, wallabies and rat-kangaroos. CSIRO, Collingwood, pp 211–218Google Scholar
  14. Charnov EL (1982) The theory of sex allocation. Princeton University Press, PrincetonGoogle Scholar
  15. Clark AB (1978) Sex ratio and local resource competition in a prosimian primate. Science 201:163–165PubMedCrossRefGoogle Scholar
  16. Cockburn A (1994) Adaptive sex allocation by brood reduction in Antechinus. Behav Ecol Sociobiol 35:53–62CrossRefGoogle Scholar
  17. Cockburn A, Scott MP, Dickman CR (1985) Sex ratio and intrasexual kin competition in mammals. Oecologia 66:427–429CrossRefGoogle Scholar
  18. Cooley H, Janssens PA (1977) Metabolic effects of infusion of cortisol and adrenocorticotrophin in the tammar wallaby (Macropus eugenii Desmarest). Gen Comp Endocrinol 33:352–358PubMedCrossRefGoogle Scholar
  19. Cork SJ, Dove H (1989) Lactation in the tammar wallaby (Macropus eugenii). 2. Intake of milk components and maternal allocation of energy. J Zool 219:399–409CrossRefGoogle Scholar
  20. Creel S, Dantzer B, Goymann W, Rubenstein DR (2013) The ecology of stress: effects of the social environment. Funct Ecol 27:66–80CrossRefGoogle Scholar
  21. Croft DB (1989) Social organization of the Macropodoidea. In: Grigg G, Jarman P, Hume I (eds) Kangaroos, wallabies and rat-kangaroos. Surrey Beatty & Sons Pty Limited, Chipping Norton, pp 505–525Google Scholar
  22. Davison MJ, Ward SJ (1998) Prenatal bias in sex ratios in a marsupial, Antechinus agilis. Proc R Soc Lond B 265:2095–2099CrossRefGoogle Scholar
  23. Ewen KR, Templesmith PD, Bowden DL, Marinopoulos J, Renfree MB, Yan H (1993) DNA-fingerprinting in relation to male-dominance and paternity in a captive colony of tammar wallabies (Macropus eugenii). J Reprod Fert 99:33–37CrossRefGoogle Scholar
  24. Gam AE, Mendonça MT, Navara KJ (2011) Acute corticosterone treatment prior to ovulation biases offspring sex ratios towards males in zebra finches Taeniopygia guttata. J Avian Biol 42:253–258CrossRefGoogle Scholar
  25. Gardner DK, Larman MG, Thouas GA (2010) Sex-related physiology of the preimplantation embryo. Mol Hum Reprod 16:539–547PubMedCrossRefGoogle Scholar
  26. Goltsman M, Kruchenkova EP, Sergeev S, Johnson PJ, Macdonald DW (2005) Effects of food availability on dispersal and cub sex ratio in the Mednyi Arctic fox. Behav Ecol Sociobiol 59:198–206CrossRefGoogle Scholar
  27. Green B, Merchant JC, Newgrain K (1988) Milk consumption and energetics of growth in pouch young of the tammar wallaby, Macropus eugenii. Aust J Zool 36:217–227CrossRefGoogle Scholar
  28. Gutierrez-Adan A, Granados J, Pintado B, de la Fuente J (2001) Influence of glucose on the sex ratio of bovine IVM/IVF embryos cultured in vitro. Reprod Fert Develop 13:361–365CrossRefGoogle Scholar
  29. Helle S, Laaksonen T, Adamsson A, Paranko J, Huitu O (2008) Female field voles with high testosterone and glucose levels produce male-biased litters. Anim Behav 75:1031–1039CrossRefGoogle Scholar
  30. Hewison AJM, Gaillard J-M (1999) Successful sons or advantaged daughters? The Trivers–Willard model and sex-biased maternal investment in ungulates. Trends Ecol Evol 14:229–234PubMedCrossRefGoogle Scholar
  31. Hiraiwa-Hasegawa M (1993) Skewed sex ratios in primates: should high-ranking mothers have daughters or sons? Trends Ecol Evol 8:395–400PubMedCrossRefGoogle Scholar
  32. Hume ID (1982) Digestive physiology and nutrition of marsupials. Cambridge University Press, CambridgeGoogle Scholar
  33. Hynes EF (2005) Mating sequence, dominance and paternity success in captive male tammar wallabies. Reproduction 130:123–130PubMedCrossRefGoogle Scholar
  34. Inns RW (1980) Ecology of the Kangaroo Island wallaby, Macropus eugenii (Desmarest) in Flinders Chase National Park. Dissertation, University of Adelaide, Kangaroo IslandGoogle Scholar
  35. Isaac JL, Krockenberger AK, Johnson CN (2005) Adaptive sex allocation in relation to life-history in the Common brushtail possum, Trichosurus vulpecula. J Anim Ecol 74:552–558CrossRefGoogle Scholar
  36. Janssens PA, Hinds LA (1981) Long-term effects of corticosteroid administration in the tammar wallaby, Macropus eugenii. Gen Comp Endocrinol 45:56–60PubMedCrossRefGoogle Scholar
  37. Johnson CN (1988) Dispersal and the sex ratio at birth in primates. Nature 332:726–728PubMedCrossRefGoogle Scholar
  38. Johnson CN (1989) Dispersal and philopatry in the Macropodoids. In: Grigg G, Jarman P, Hume I (eds) Kangaroos, wallabies and rat-kangaroos. Surrey Beatty & Sons Pty Limited, Chipping Norton, pp 593–602Google Scholar
  39. Johnson CN, Ritchie EG (2002) Adaptive biases in offspring sex ratios established before birth in a marsupial, the Common brushtail possum Trichosurus vulpecula. Behav Ecol 13:653–656CrossRefGoogle Scholar
  40. Johnson CN, Clinchy M, Taylor AC, Krebs CJ, Jarman PJ, Payne A, Ritchie EG (2001) Adjustment of offspring sex ratios in relation to the availability of resources for philopatric offspring in the Common brushtail possum. Proc R Soc Lond B 268:2001–2005CrossRefGoogle Scholar
  41. Julliard R (2000) Sex-specific dispersal in spatially varying environments leads to habitat-dependent evolutionary stable offspring sex ratios. Behavioral Ecology 11:421–428Google Scholar
  42. Kruuk LE, Clutton-Brock TH, Albon SD, Pemberton JM, Guinness FE (1999) Population density affects sex ratio variation in red deer. Nature 399:459–461PubMedCrossRefGoogle Scholar
  43. Larson MA, Kimura K, Kubisch HM, Roberts RM (2001) Sexual dimorphism among bovine embryos in their ability to make the transition to expanded blastocyst and in the expression of the signaling molecule IFN-tau. Proc Natl Acad Sci U S A 98:9677–9682PubMedCentralPubMedCrossRefGoogle Scholar
  44. Love OP, Chin EH, Wynne‐Edwards KE, Williams TD (2005) Stress hormones: a link between maternal condition and sex‐biased reproductive investment. Am Nat 166:751–766PubMedCrossRefGoogle Scholar
  45. MacDonald AJ, FitzSimmons NN, Chambers B, Renfree MB, Sarre SD (2013) Sex-linked and autosomal microsatellites provide new insights into island populations of the tammar wallaby. Heredity 2013:1–10Google Scholar
  46. Martin JGA, Festa-Bianchet M (2011) Sex ratio bias and reproductive strategies: what sex to produce when? Ecology 92:441–449PubMedCrossRefGoogle Scholar
  47. McKenzie S, Deane EM (2003) The effects of age, season, and gender on serum cortisol levels in the tammar wallaby, Macropus eugenii. Gen Comp Endocrinol 133:273–278PubMedCrossRefGoogle Scholar
  48. McKenzie S, Deane EM (2005) Faecal corticosteroid levels as an indicator of well-being in the tammar wallaby, Macropus Eugenii. Comp Biochem Phys A 140:81–87CrossRefGoogle Scholar
  49. McKenzie S, Deane EM, Burnett L (2004) Are serum cortisol levels a reliable indicator of wellbeing in the tammar wallaby, Macropus eugenii? Comp Biochem Phys A 138:341–348CrossRefGoogle Scholar
  50. Miller EJ, Eldridge MBD, Herbert CA (2010) Dominance and paternity in the tammar wallaby. In: Coulson G, Eldridge M (eds) Macropods: the biology of kangaroos, wallabies and rat-kangaroos. CSIRO, Collingwood, pp 77–86Google Scholar
  51. Pelletier F, Réale D, Garant D, Coltman DW, Festa-Bianchet M (2007) Selection on heritable seasonal phenotypic plasticity of body mass. Evolution 61:1969–1979PubMedCrossRefGoogle Scholar
  52. Pike TW, Petrie M (2005) Maternal body condition and plasma hormones affect offspring sex ratio in peafowl. Anim Behav 70:745–751CrossRefGoogle Scholar
  53. Pike TW, Petrie M (2006) Experimental evidence that corticosterone affects offspring sex ratios in quail. Proc R Soc Lond B 273:1093–1098CrossRefGoogle Scholar
  54. Poole WE, Simms NG, Wood JT, Luboloa M (1991) Tables for age determination of the Kangaroo Island tammar wallaby (Macropus eugenii) from body measurements. Technical Memorandum no. 32. CSIRO, CanberraGoogle Scholar
  55. Pryke SR, Rollins LA, Buttemer WA, Griffith SC (2011) Maternal stress to partner quality is linked to adaptive offspring sex ratio adjustment. Behav Ecol 22:717–722CrossRefGoogle Scholar
  56. Robert KA, Braun S (2012) Milk composition during lactation suggests a mechanism for male biased allocation of maternal resources in the tammar wallaby (Macropus eugenii). PLoS ONE 7:e51099PubMedCentralPubMedCrossRefGoogle Scholar
  57. Robert KA, Schwanz LE (2011) Emerging sex allocation research in mammals: marsupials and the pouch advantage. Mammal Rev 41:1–22CrossRefGoogle Scholar
  58. Robert KA, Schwanz LE (2013) Monitoring the health status of free-ranging tammar wallabies using haematology, serum biochemistry and parasite load. J Wildlife Manag 77:1232–1243CrossRefGoogle Scholar
  59. Robert KA, Schwanz LE, Mills HR (2009) Offspring sex varies with maternal investment ability: empirical demonstration based on cross-fostering. Biol Lett 6:242–245PubMedCentralPubMedCrossRefGoogle Scholar
  60. Ryan CP, Anderson WG, Gardiner LE, Hare JF (2012) Stress-induced sex ratios in ground squirrels: support for a mechanistic hypothesis. Behav Ecol 23:160–167CrossRefGoogle Scholar
  61. Schwanz LE, Robert KA (2012) Reproductive ecology of wild tammar wallabies in natural and developed habitats on Garden Island, Western Australia. Aust J Zool 60:111–119CrossRefGoogle Scholar
  62. Schwanz LE, Bragg JG, Charnov EL (2006) Maternal condition and facultative sex ratios in populations with overlapping generations. Am Nat 168:521–530PubMedCrossRefGoogle Scholar
  63. Sheldon BC, West SA (2004) Maternal dominance, maternal condition, and offspring sex ratio in ungulate mammals. Am Nat 163:40–54PubMedCrossRefGoogle Scholar
  64. Silk JB (1983) Local resource competition and facultative adjustment of sex ratios in relation to competitive abilities. Am Nat 121:56–66Google Scholar
  65. Simpson MJA, Simpson AE (1982) Birth sex ratios and social rank in rhesus monkey mothers. Nature 300:440–441Google Scholar
  66. Spindler RE, Renfree MB, Shaw G, Gardner DK (1998) Reactivating tammar wallaby blastocysts oxidize glucose. Biol Reprod 58:1425–1431PubMedCrossRefGoogle Scholar
  67. Sunnucks P, Taylor AC (1997) Sex of pouch young related to maternal weight in Macropus eugenii and M. parma (Marsupialia: Macropodidae). Aust J Zool 45:573–578CrossRefGoogle Scholar
  68. Trivers RL, Willard DE (1973) Natural selection of parental ability to vary the sex ratio of offspring. Science 179:90–92PubMedCrossRefGoogle Scholar
  69. Tyndale-Biscoe H, Renfree MB (1987) Reproductive physiology of marsupials. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  70. Warner DA, Radder RS, Shine R (2009) Corticosterone exposure during embryonic development affects offspring growth and sex ratios in opposing directions in two lizard species with environmental sex determination. Physiol Biochem Zool 82:363–371PubMedCrossRefGoogle Scholar
  71. Wasser SK, Hunt KE, Brown JL, Cooper K, Crockett CM, Bechert U, Millspaugh JJ, Larson S, Monfort SL (2000) A generalized fecal glucocorticoid assay for use in a diverse array of nondomestic mammalian and avian species. Gen Comp Endocrinol 120:260–275PubMedCrossRefGoogle Scholar
  72. West SA (2009) Sex allocation. Princeton University Press, PrincetonGoogle Scholar
  73. Wild G (2006) Sex ratios when helpers stay at the nest. Evolution 60:2012–2022PubMedCrossRefGoogle Scholar
  74. Wild G, West SA (2007) A sex allocation theory for vertebrates: combining local resource competition and condition‐dependent allocation. Am Nat 170:E112–E128PubMedCrossRefGoogle Scholar
  75. Williamson P, Fletcher TP, Renfree MB (1990) Testicular development and maturation of the hypothalamic-pituitary-testicular axis in the male tammar, Macropus eugenii. Reproduction 88:549–557CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.School of Marine and Tropical BiologyJames Cook UniversityTownsvilleAustralia
  2. 2.Institute for Applied EcologyUniversity of CanberraCanberraAustralia
  3. 3.Research School of BiologyAustralian National UniversityCanberraAustralia
  4. 4.School of Animal BiologyUniversity of Western AustraliaPerthAustralia
  5. 5.Department of ZoologyLa Trobe UniversityBundooraAustralia
  6. 6.Evolution & Ecology Research Centre, School of Biological, Earth and Environmental SciencesUniversity of New South WalesSydneyAustralia

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