Milk Composition during Lactation Suggests a Mechanism for Male Biased Allocation of Maternal Resources in the Tammar Wallaby (Macropus eugenii)

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Robert, Kylie A ^a   Braun, Shannon ^a  

^a LA TROBE UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOHYDRATE; LIPID; MILK PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; DAUGHTER; ENERGY METABOLISM; FEMALE; FOOD ANALYSIS; FOOD COMPOSITION; LACTATION; MALE; MARSUPIAL; MILK; MILK PRODUCTION; MILK YIELD; MOTHER; NONHUMAN; PROGENY; PROTEIN CONTENT; REARING; SEX ALLOCATION; SEX DIFFERENCE; SON; TAMMAR WALLABY;

ANALYSIS OF VARIANCE; ANIMALS; BODY SIZE; FEMALE; LACTATION; MACROPODIDAE; MALE; MILK; MILK PROTEINS; MOTHERS; SEX CHARACTERISTICS; SEXISM;

MACROPODIDAE; MACROPUS EUGENII; METATHERIA;

EID: 84870597484     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0051099     Document Type: Article

References (53)

1. Cockburn A, Legge S, Double MC (2002) Sex ratios in birds and mammals: can the hypotheses be disentangled? In Sex ratios: concepts and research methods (ed. I. C. W. Hardy), 266-286. Cambridge, UK: Cambridge University Press.
2. 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: 1723-1728 (doi:10.1098/rspb.2004.2773).
3. Leimar O, (1996) Life-history analysis of the Trivers and Willard sex-ratio problem. Behav. Ecol. 7: 316-325.
4. Trivers RL, Willard DE, (1973) Natural selection of parental ability to vary the sex ratio of offspring. Science. 179: 90-92 (doi:10.1126/science.179.4068.90).
5. Lindstrom J, (1999) Early development and fitness in birds and mammals. Trends Ecol. Evol. 14: 343-348.
6. Clutton-Brock TH, Albon SD, Guinness FE, (1984) Maternal dominance, breeding success, and birth sex ratios in red deer. Nature. 308: 358-360.
7. Stamps JA, (1990) When should avian parents differentially provision sons and daughters? Am. Nat. 135: 671-685.
8. Oftedal OT, (1984) Milk composition, milk yield and energy output at peak lactation: a comparative review. Symp. Zool. Soc. Lond. 51: 33-85.
9. Martin RD, (1984) Scaling effects and adaptive strategies in mammalian lactation. Symp. Zool. Soc. Lond. 51: 87-117.
10. Landete-Castillejos T, García AJ, Gomez JA, Gallego L, (2003) Subspecies and body size effect on lactation biology in red deer: comparison of Cervus elaphus hispanicus and C. e. scoticus. Physiol. Biochem. Zool. 76: 594-602.
11. Landete-Castillejos T, García AJ, Carrión D, Estevez JA, Ceacero F, et al. (2009) Age-related body weight constraints on prenatal and milk provisioning in Iberian red deer (Cervus elaphus hispanicus) affect allocation of maternal resources. Theriogenology 71: 400-407.
12. Landete-Castillejos T, Garcia A, Gallego L, (2001) Calf growth in captive Iberian red deer (Cervus elaphus hispanicus): effect of birth date and hind milk production and composition. J. An. Sci. 79: 1085-1092.
13. Landete-Castillejos T, Garcia A, Lopez-Serrano FR, Gallego L, (2005) Maternal quality and differences in milk production and composition for male and female Iberian red deer calves (Cervus elaphus hispanicus). Behav. Ecol. Sociobiol. 57: 267-274.
14. Gallego L, Gómez JA, Landete-Castillejos T, Garcia AJ, Estevez JA, et al. (2009) Effect of milk minerals on calf gains and sex differences in mineral composition of milk from Iberian red deer (Cervus elaphus hispanicus). Reprod. 138: 859-865.
15. Hinde K, (2007) First time macaque mothers bias milk composition in favor of sons. Curr. Biol. 17: 958-959.
16. Hinde K, (2009) Richer milk for sons but more milk for daughters: sex-biased investment during lactation varies with maternal life history in Rhesus Macaques. Am J. Human Biol. 21: 512-519.
17. Cockburn A, (1990) Sex ratio variation in marsupials. Aust. J. Zool. 37: 467-479.
18. Johnson KA, Burbidge AA, Mckenzie NL (1989) Australian macropodoitea: status, causes of decline and future management. In Kangaroos, Wallabies and Rat-Kangaroos, vol. 2, Grigg, G., Jarman, P. & Hume, I. (Eds), Surrey Beatty, Chipping Norton 641-657.
19. Robert KA, Schwanz LE, (2011) Emerging sex allocation research in mammals: marsupials and the pouch advantage. Mam. Rev. 41: 1-22.
20. Poole WE, Merchant JC, Carpenter SM Calaby JH, (1985) Reproduction, growth and age determination of the yellow footed rock wallaby Petrogale xanthopus gray, in captivity. Aust. Wildlife Res. 12: 127-136.
21. Robert KA, Schwanz LE, Mills HR, (2010) Offspring sex varies with maternal investment ability: empirical demonstration based on cross-fostering. Biol. Lett. 6: 242-245.
22. Sunnucks P, Taylor AC, (1997) Sex of pouch young related to maternal weight in Macropus eugenii and M. parma. Aust. J. Zool. 45: 573-578 (doi:10.1071/ZO97038).
23. Rutkowska J, Koskela E, Mappes T, Speakman JR (2010) A trade-off between current and future sex allocation revealed by maternal energy budget in a small mammal. Proc. R. Soc. B. (doi:10.1098/rspb.2010.2654).
24. Tyndale-Biscoe H, Renfree M (1987) Reproductive physiology of marsupials. Cambridge University Press, Sydney.
25. Tyndale-Biscoe H, Hinds L, (1990) Control of seasonal reproduction in the Tammar and Bennett's wallabies. Prog. Clin. Biol. Res. 342: 659-667.
26. Green B, Merchant J, Newgrain K, (1988) Milk consumption and energetics of growth in pouch young of the Tammar Wallaby, Macropus eugenii. Aust. J. Zool. 36: 217-227.
27. Trott JF, Simspons KJ, Moyle RLC, Hearn CM, Shaw G, et al. (2003) Maternal regulation of milk composition, milk production, and pouch young development during lactation in the Tammar Wallaby (Macropus eugenii). Biol. Reprod. 68: 929-936.
28. Poole WE, Simms NG, Wood JT, Luboloa M (1991) Tables for age determination of the Kangaroo Island Wallaby (Tammar) Macropus eugenii, from body measurements. Technical Memorandum no. 32. CSIRO (Division of Wildlife and Ecology), Canberra, Australia.
29. Inns RW, (1982) Age determination in the Kangaroo Island wallaby, Macropus eugenii (Desmarest). Aust. Wild. Res. 9: 213-220.
30. Chambers BK (2008) Human disturbance affects the ecology and population dynamics of the tammar wallaby, Macropus eugenii, on Garden Island Western Australia. PhD Thesis, The University of Western Australia, Perth.
31. Inns RW (1980) Ecology of the Kangaroo Island wallaby, Macropus eugenii (Desmarest), in Flinders Chase National Park, Kangaroo Island. Ph.D. thesis, University of Adelaide.
32. Taggart DA, Shimmin GA, Underwood G, Phillips K, (2002) Survival of very small macropod pouch young following short-term isolation from the pouch at various environmental temperatures. Anim. Cons. 5: 275-282 (doi:10.1017/S136794300200402X).
33. Atwood CS, Hartman PE, (1992) Collection of fore and hind milk from the sow and the changes in milk composition during suckling. J. Dairy Res. 59: 287-298.
34. Messer M, Crisp EA, Newgrain K, (1988) Studies on the carbohydrate content of milk of the crabeater seal (Lobodon carcinophagus). Comp. Biochem. Physiol. B. 90: 367-370.
35. Schwanz L, Robert K (2012) Reproductive ecology of wild tammar wallabies in natural and developed habitats on Garden Island, Western Australia. Aust. J. Zool. In press.
36. Powe C, Knott CD, Conklin-Brittain N, (2010) Infant sex predicts breast milk energy content. Am. J. Hum. Biol. 22: 50-54.
37. Fujita M, Roth E, Lo Y, Hurst C, Vollner J, et al. (2012) In poor families, mothers' milk is richer for daughters than sons: A test of Trivers-Willard Hypothesis in agropastoral settlements in Northern Kenya. Am. J. Phys. Anthropology. (doi:10.1002/ajpa.22092).
38. Merchant JC, Sharman GB, (1966) Observations on the attachment of marsupial pouch young to the teats and on the rearing of pouch young by foster-mothers of the same or different species. Aust. J. Zool. 14: 593-609.
39. Metges CC, (2001) Does dietary protein in early life affect the development of adiposity in mammals? J. Nutr. 131: 2062-2066.
40. Rudd CD, (1994) Sexual behabiour of male and female tammar wallabies (Macropus eugenii) at post-partum oestrus. J. Zool. Lond. 232: 151-162.
41. Daly KA, Digby M, Lefevre C, Mailer S, Thomson P, et al. (2007) Analysis of the expression of immunoglobulins throughout lactation suggests two periods of immune transfer in the tammar wallaby (Macropus eugenii). Vet. Immunol. Immunop. 120: 187-200.
42. Landete-Castillejos T, García A, Gómez JA, Laborda J, Gallego L, (2002) Effects of nutritional stress during lactation on immunity costs and indices of future reproduction in Iberian red deer (Cervus elaphus hispanicus). Biol. Repro. 67: 1613-1620.
43. Clutton-Brock TH (1991) The evolution of Parental Care. Princeton NJ: Princeton University Press.
44. Stearns SC (1992) The evolution of life-histories. Oxford: Oxford University Press.
45. Hinde K, Power ML, Oftedal T, (2009) Rhesus Macaque milk: Magnitude, sources, and consequences of individual variation over lactation. Am. J. Phys. Anthropology. 138: 148-157 (doi.10.1002/ajpa.20911).
46. Rose RW, Flowers K, (2005) Milk composition and growth in wild and captive Tasmanian pademelons, Thylogale billardierii (Marsupialia). Aust. J. Zool. 53: 241-248.
47. Sutton JD, (1989) Altering milk composition by feeding. J. Dairy Sci. 72: 2801-2814.
48. Gopalan C, (1962) Effect of nutrition on pregnancy and lactation. Bull. Wld. Hlth. Org. 26: 203-211.
49. Rasmussen KM, (1992) The influence of maternal nutrition on lactation. Annu. Rev. Nutr. 12: 103-117.
50. Gittleman JL, Thompson SD, (1988) Energy allocation in mammalian reproduction. Amer. Zool. 28: 863-875.
51. Wang J, Wong ESW, Whitley JC, Li J, Stringer JM, et al. (2011) Ancient Antimicrobial Peptides Kill Antibiotic-Resistant Pathogens: Australian Mammals Provide New Options. PLoS ONE 6(8): e24030 doi:10.1371/journal.pone.0024030.
52. Green SW, Renfree MB, (1982) Changes in the Milk Proteins during Lactation in the Tammar Wallaby, Macropus eugenii. Aust. J. Bioi. Sci. 35: 145-152.
53. Dove H, Cork S, (1989) Lactation in the tammar wallaby (Macropus eugenii). I. Milk consumption and the algebraic description of the lactation curve. J. Zool. 219: 385-397.