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Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2004 Aug 22;271(1549):1723–1728. doi: 10.1098/rspb.2004.2773

Facultative adjustment of mammalian sex ratios in support of the Trivers-Willard hypothesis: evidence for a mechanism.

Elissa Z Cameron 1
PMCID: PMC1691777  PMID: 15306293

Abstract

Evolutionary theory predicts that mothers of different condition should adjust the birth sex ratio of their offspring in relation to future reproductive benefits. Published studies addressing variation in mammalian sex ratios have produced surprisingly contradictory results. Explaining the source of such variation has been a challenge for sex-ratio theory, not least because no mechanism for sex-ratio adjustment is known. I conducted a meta-analysis of previous mammalian sex-ratio studies to determine if there are any overall patterns in sex-ratio variation. The contradictory nature of previous results was confirmed. However, studies that investigated indices of condition around conception show almost unanimous support for the prediction that mothers in good condition bias their litters towards sons. Recent research on the role of glucose in reproductive functioning have shown that excess glucose favours the development of male blastocysts, providing a potential mechanism for sex-ratio variation in relation to maternal condition around conception. Furthermore, many of the conflicting results from studies on sex-ratio adjustment would be explained if glucose levels in utero during early cell division contributed to the determination of offspring sex ratios.

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Selected References

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  1. Bazer F. W., Spencer T. E., Ott T. L. Interferon tau: a novel pregnancy recognition signal. Am J Reprod Immunol. 1997 Jun;37(6):412–420. doi: 10.1111/j.1600-0897.1997.tb00253.x. [DOI] [PubMed] [Google Scholar]
  2. Brameld J. M., Gilmour R. S., Buttery P. J. Glucose and amino acids interact with hormones to control expression of insulin-like growth factor-I and growth hormone receptor mRNA in cultured pig hepatocytes. J Nutr. 1999 Jul;129(7):1298–1306. doi: 10.1093/jn/129.7.1298. [DOI] [PubMed] [Google Scholar]
  3. Burén Jonas, Liu Hui-Xia, Jensen Jørgen, Eriksson Jan W. Dexamethasone impairs insulin signalling and glucose transport by depletion of insulin receptor substrate-1, phosphatidylinositol 3-kinase and protein kinase B in primary cultured rat adipocytes. Eur J Endocrinol. 2002 Mar;146(3):419–429. doi: 10.1530/eje.0.1460419. [DOI] [PubMed] [Google Scholar]
  4. Clutton-Brock T. H., Iason G. R. Sex ratio variation in mammals. Q Rev Biol. 1986 Sep;61(3):339–374. doi: 10.1086/415033. [DOI] [PubMed] [Google Scholar]
  5. Crawford M. A., Doyle W., Meadows N. Gender differences at birth and differences in fetal growth. Hum Reprod. 1987 Aug;2(6):517–520. doi: 10.1093/oxfordjournals.humrep.a136581. [DOI] [PubMed] [Google Scholar]
  6. Diskin M. G., Mackey D. R., Roche J. F., Sreenan J. M. Effects of nutrition and metabolic status on circulating hormones and ovarian follicle development in cattle. Anim Reprod Sci. 2003 Oct 15;78(3-4):345–370. doi: 10.1016/s0378-4320(03)00099-x. [DOI] [PubMed] [Google Scholar]
  7. Dominko T., First N. L. Relationship between the maturational state of oocytes at the time of insemination and sex ratio of subsequent early bovine embryos. Theriogenology. 1997 Apr 1;47(5):1041–1050. doi: 10.1016/s0093-691x(97)00061-7. [DOI] [PubMed] [Google Scholar]
  8. Enright W. J., Spicer L. J., Kelly M., Culleton N., Prendiville D. J. Energy level in winter diets of Fallow deer: effect on plasma levels of insulin-like growth factor-I and sex ratio of their offspring. Small Rumin Res. 2001 Mar;39(3):253–259. doi: 10.1016/s0921-4488(00)00199-1. [DOI] [PubMed] [Google Scholar]
  9. Flint A. P., Albon S. D., Jafar S. I. Blastocyst development and conceptus sex selection in red deer Cervus elaphus: studies of a free-living population on the Isle of Rum. Gen Comp Endocrinol. 1997 Jun;106(3):374–383. doi: 10.1006/gcen.1997.6879. [DOI] [PubMed] [Google Scholar]
  10. Folmer Vanderlei, Soares Júlio C. M., Gabriel Diogo, Rocha João B. T. A high fat diet inhibits delta-aminolevulinate dehydratase and increases lipid peroxidation in mice (Mus musculus). J Nutr. 2003 Jul;133(7):2165–2170. doi: 10.1093/jn/133.7.2165. [DOI] [PubMed] [Google Scholar]
  11. Gutiérrez-Adán A., Behboodi E., Andersen G. B., Medrano J. F., Murray J. D. Relationship between stage of development and sex of bovine IVM-IVF embryos cultured in vitro versus in the sheep oviduct. Theriogenology. 1996 Aug;46(3):515–525. doi: 10.1016/0093-691x(96)00173-2. [DOI] [PubMed] [Google Scholar]
  12. Gutiérrez-Adán A., Granados J., Pintado B., De La Fuente J. Influence of glucose on the sex ratio of bovine IVM/IVF embryos cultured in vitro. Reprod Fertil Dev. 2001;13(5-6):361–365. doi: 10.1071/rd00039. [DOI] [PubMed] [Google Scholar]
  13. Hahn T., Barth S., Graf R., Engelmann M., Beslagic D., Reul J. M., Holsboer F., Dohr G., Desoye G. Placental glucose transporter expression is regulated by glucocorticoids. J Clin Endocrinol Metab. 1999 Apr;84(4):1445–1452. doi: 10.1210/jcem.84.4.5607. [DOI] [PubMed] [Google Scholar]
  14. Hasler J. F., Cardey E., Stokes J. E., Bredbacka P. Nonelectrophoretic PCR-sexing of bovine embryos in a commercial environment. Theriogenology. 2002 Nov;58(8):1457–1469. doi: 10.1016/s0093-691x(02)01044-0. [DOI] [PubMed] [Google Scholar]
  15. Hedricks C., McClintock M. K. Timing of insemination is correlated with the secondary sex ratio of Norway rats. Physiol Behav. 1990 Nov;48(5):625–632. doi: 10.1016/0031-9384(90)90201-e. [DOI] [PubMed] [Google Scholar]
  16. Hewison AJ, Gaillard JM. Successful sons or advantaged daughters? The Trivers-Willard model and sex-biased maternal investment in ungulates. Trends Ecol Evol. 1999 Jun;14(6):229–234. doi: 10.1016/s0169-5347(99)01592-x. [DOI] [PubMed] [Google Scholar]
  17. James W. H. Evidence that mammalian sex ratios at birth are partially controlled by parental hormone levels at the time of conception. J Theor Biol. 1996 Jun 21;180(4):271–286. doi: 10.1006/jtbi.1996.0102. [DOI] [PubMed] [Google Scholar]
  18. Krackow S., Burgoyne P. S. Timing of mating, developmental asynchrony and the sex ratio in mice. Physiol Behav. 1997 Dec 31;63(1):81–84. doi: 10.1016/s0031-9384(97)00393-4. [DOI] [PubMed] [Google Scholar]
  19. Krackow S. Potential mechanisms for sex ratio adjustment in mammals and birds. Biol Rev Camb Philos Soc. 1995 May;70(2):225–241. doi: 10.1111/j.1469-185x.1995.tb01066.x. [DOI] [PubMed] [Google Scholar]
  20. Krackow S., Schmidt T. A., Elepfandt A. Sexual growth dimorphism affects birth sex ratio in house mice. Proc Biol Sci. 2003 May 7;270(1518):943–947. doi: 10.1098/rspb.2002.2310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Krackow S. The developmental asynchrony hypothesis for sex ratio manipulation. J Theor Biol. 1995 Sep 21;176(2):273–280. doi: 10.1006/jtbi.1995.0197. [DOI] [PubMed] [Google Scholar]
  22. Larson M. A., Kimura K., Kubisch H. M., Roberts R. M. 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. 2001 Jul 31;98(17):9677–9682. doi: 10.1073/pnas.171305398. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Machado A. F., Zimmerman E. F., Hovland D. N., Jr, Weiss R., Collins M. D. Diabetic embryopathy in C57BL/6J mice. Altered fetal sex ratio and impact of the splotch allele. Diabetes. 2001 May;50(5):1193–1199. doi: 10.2337/diabetes.50.5.1193. [DOI] [PubMed] [Google Scholar]
  24. Milki Amin A., Jun Sunny H., Hinckley Mary D., Westphal Lynn W., Giudice Linda C., Behr Barry. Comparison of the sex ratio with blastocyst transfer and cleavage stage transfer. J Assist Reprod Genet. 2003 Aug;20(8):323–326. doi: 10.1023/A:1024861624805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Packer C., Collins D. A., Eberly L. E. Problems with primate sex ratios. Philos Trans R Soc Lond B Biol Sci. 2000 Nov 29;355(1403):1627–1635. doi: 10.1098/rstb.2000.0725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Pegoraro L. M., Thuard J. M., Delalleau N., Guérin B., Deschamps J. C., Marquant Le Guienne B., Humblot P. Comparison of sex ratio and cell number of IVM-IVF bovine blastocysts co-cultured with bovine oviduct epithelial cells or with Vero cells. Theriogenology. 1998 Jun;49(8):1579–1590. doi: 10.1016/s0093-691x(98)00103-4. [DOI] [PubMed] [Google Scholar]
  27. Pratt N. C., Lisk R. D. Dexamethasone can prevent stress-related litter deficits in the golden hamster. Behav Neural Biol. 1990 Jul;54(1):1–12. doi: 10.1016/0163-1047(90)91201-l. [DOI] [PubMed] [Google Scholar]
  28. Pratt N. C., Lisk R. D. Effects of social stress during early pregnancy on litter size and sex ratio in the golden hamster (Mesocricetus auratus). J Reprod Fertil. 1989 Nov;87(2):763–769. doi: 10.1530/jrf.0.0870763. [DOI] [PubMed] [Google Scholar]
  29. Reist Martin, Erdin Daniel K., von Euw Daniel, Tschümperlin Kaspar M., Leuenberger Hans, Hammon Harald M., Morel Claudine, Philipona Chantal, Zbinden Yolande, Künzi Niklaus. Postpartum reproductive function: association with energy, metabolic and endocrine status in high yielding dairy cows. Theriogenology. 2003 Apr 15;59(8):1707–1723. doi: 10.1016/s0093-691x(02)01238-4. [DOI] [PubMed] [Google Scholar]
  30. Rjasanowski I., Klöting I., Kovacs P. Altered sex ratio in offspring of mothers with insulin-dependent diabetes mellitus. Lancet. 1998 Feb 14;351(9101):497–498. doi: 10.1016/S0140-6736(05)78685-2. [DOI] [PubMed] [Google Scholar]
  31. Rosenfeld Cheryl S., Grimm Kristie M., Livingston Kimberly A., Brokman Angela M., Lamberson William E., Roberts R. Michael. Striking variation in the sex ratio of pups born to mice according to whether maternal diet is high in fat or carbohydrate. Proc Natl Acad Sci U S A. 2003 Apr 2;100(8):4628–4632. doi: 10.1073/pnas.0330808100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Seematter G., Battilana P., Tappy L. Effects of dexamethasone on the metabolic responses to mental stress in humans. Clin Physiol Funct Imaging. 2002 Mar;22(2):139–144. doi: 10.1046/j.1365-2281.2002.00409.x. [DOI] [PubMed] [Google Scholar]
  33. Shamay A, Mabjeesh SJ, Shapiro F, Silanikove N. Adrenocorticotrophic hormone and dexamethasone failed to affect milk yield in dairy goats: comparative aspects. Small Rumin Res. 2000 Nov 1;38(3):255–259. doi: 10.1016/s0921-4488(00)00152-8. [DOI] [PubMed] [Google Scholar]
  34. Sheldon Ben C. Maternal dominance, maternal condition, and offspring sex ratio in ungulate mammals. Am Nat. 2004 Jan 14;163(1):40–54. doi: 10.1086/381003. [DOI] [PubMed] [Google Scholar]
  35. Trivers R. L., Willard D. E. Natural selection of parental ability to vary the sex ratio of offspring. Science. 1973 Jan 5;179(4068):90–92. doi: 10.1126/science.179.4068.90. [DOI] [PubMed] [Google Scholar]

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