Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-05T02:57:44.819Z Has data issue: false hasContentIssue false
  • English
  • Français

BEHAVIOURAL AND BIOLOGICAL DETERMINANTS OF HUMAN SEX RATIO AT BIRTH

Published online by Cambridge University Press:  03 June 2010

WILLIAM H. JAMES
WILLIAM H. JAMES
Affiliation:
The Galton Laboratory, Department of Genetics, Evolution and Environment, University College London, UK
Get access Rights & Permissions [Opens in a new window]

Summary

The human sex ratio SR (proportion male) at birth has been reported to vary with many variables. The explanation of this variation is not established, but I have hypothesized that it is partially caused by the hormonal concentrations of both parents around the time of conception. The present note suggests how this hypothesis might accommodate recent sex ratio findings relating to ‘psychosexual restriction’, female genital cutting, sexes of prior sibs, finger length ratios, the autism spectrum disorder, parental occupation and maternal eating disorders. Tests of such suggestions are offered, and it is hypothesized that: (a) in women, Manning's R (the ratio of the lengths of the 2nd and 4th digits) is positively correlated with offspring sex ratio (proportion male); (b) women who have undergone female genital cutting (FGC) have high androgen levels; (c) offspring sex ratio correlates positively with ‘masculinity’ of parental occupation, the correlation being mediated by testosterone levels. It is noted that the lines of evidence for three hypotheses (James', Manning's and Baron-Cohen's) are mutually supportive.

Type
Research Article
Information
Journal of Biosocial Science , Volume 42 , Issue 5 , September 2010 , pp. 587 - 599
Copyright
Copyright © Cambridge University Press 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Auyeung, B., Baron-Cohen, S., Ashwin, E., Knickmeyer, R., Taylor, K. & Hackett, G. (2009a) Fetal testosterone and autistic traits. British Journal of Psychology 100, 1–22.CrossRefGoogle ScholarPubMed
Baron-Cohen, S. (2003) The Essential Difference. Penguin, London.Google Scholar
Baron-Cohen, S., Knickmeyer, R. C. & Belmonte, M. K. (2005) Sex differences in the brain: implications for explaining autism. Science 310, 819–823.CrossRefGoogle ScholarPubMed
Behrendt, A. & Moritz, S. (2005) Post-traumatic stress disorder and memory problems after female genital mutilation. American Journal of Psychiatry 162, 1000–1002.CrossRefGoogle ScholarPubMed
Bernstein, M. E. (1951) Action of genes affecting the secondary sex ratio in man. Science 114, 181–182.CrossRefGoogle ScholarPubMed
Bernstein, M. E. (1981) Sex distributions in sibships according to occupation of parents. Genus 37, 179–188.Google ScholarPubMed
Bernstein, M. E. & Martinez-Gustin, M. (1961) Physical and psychological variation and the sex ratio. Journal of Heredity 52, 109–112.CrossRefGoogle Scholar
Bogaert, A. F. & Fisher, W. A. (1995) Predictors of university men's number of sexual partners. Journal of Sex Research 32, 119–130.CrossRefGoogle Scholar
Brambilla, F., Monteleone, P., Bortolotti, P., Dalle, G. R., Todisco, P., Favoro, A. et al. (2003) Persistent amenorrhoea in weight-recovered anorexics: psychological and biological aspects. Psychiatric Research 118, 249–257.CrossRefGoogle ScholarPubMed
Bulik, C. M., Holle, A. V., Gendall, K., Lie, K. K., Hoffman, E., Mo, X. et al. (2008) Maternal eating disorders influence sex ratio at birth. Acta Obstetricia et Gynecologica 87, 979–981.CrossRefGoogle ScholarPubMed
Bulik, C. M., Torgersen, L., Reichborn-Kjennerud, T., Gendall, K. & Von Holle, A. (2009) Maternal eating disorders and offspring sex ratio at birth. Acta Obstetricia et Gynecologica 88, 489.CrossRefGoogle Scholar
Burger, H. G. (1989) Estradiol: the physiological basis of the fertile period. International Journal of Gynecology and Obstetrics, Supplement 1, 5–9.Google Scholar
Chapman, E., Baron-Cohen, S., Auyeung, B., Knickmeyer, R., Taylor, K. & Hackett, G. (2006) Fetal testosterone and empathy: evidence from the empathy quotient (EQ) and the “reading the mind in the eyes” test. Social Neuroscience 1, 135–148.CrossRefGoogle ScholarPubMed
Dabbs, J. M., de la Rue, D. & Williams, P. M. (1990) Testosterone and occupational choice: actors, ministers and other men. Journal of Personality and Social Psychology 59, 1261–1265.CrossRefGoogle ScholarPubMed
Dabbs, J. M. & Morris, R. (1990) Testosterone, social class and antisocial behavior in a sample of 4462 men. Psychological Science 1, 209–211.CrossRefGoogle Scholar
Daitzman, R. & Zuckerman, M. (1980) Disinhibitory sensation seeking and gonadal hormones. Personality and Individual Differences 1, 103–110.CrossRefGoogle Scholar
Edler, C., Lipson, S. F. & Keel, P. K. (2007) Ovarian hormones and binge eating in bulimia nervosa. Psychological Medicine 37, 131–141.CrossRefGoogle ScholarPubMed
Edwards, A. W. F. (1958) An analysis of Geissler's data on the human sex ratio. Annals of Human Genetics 23, 6–15.CrossRefGoogle ScholarPubMed
Edwards, A. W. F. (1960) The meaning of binomial distribution. Nature 186, 1074.CrossRefGoogle ScholarPubMed
Eisner, J. R., Barnett, M. A., Dumesic, D. A. & Abbott, D. H. (2002) Ovarian hyperandrogenism in adult female rhesus monkeys exposed to prenatal androgen excess. Fertility and Sterility 77, 167–172.CrossRefGoogle ScholarPubMed
Emaus, A., Espetvedt, S., Veirod, M. B., Ballard-Barbash, R., Furberg, A-S., Ellison, P. T. et al. (2008) 17-Beta estradiol in relation to age at menarche and adult obesity in premenopausal women. Human Reproduction 23, 919–927.CrossRefGoogle ScholarPubMed
Gangestad, S. W. & Simpson, J. A. (1990) Toward an evolutionary history of female sociosexual variation. Journal of Personality 58, 69–96.CrossRefGoogle ScholarPubMed
Garenne, M. (2009) Sex ratio at birth and family composition in sub-Saharan Africa: inter-couple variations. Journal of Biosocial Science 41, 399–407.CrossRefGoogle ScholarPubMed
Garenne, M. (in press) Heterogeneity in the sex ratio at birth in European populations. Genus.Google Scholar
Gooren, L. J. G. & Giltay, E. J. (2008) Review of studies of androgen treatment of female-to-male transsexuals: effects and risks of administration of androgens to females. Journal of Sexual Medicine 5, 765–776.CrossRefGoogle ScholarPubMed
Harlow, S. D., Baird, D. D., Weinberg, C. R. & Wilcox, A. J. (2000) Urinary estrogen patterns in long follicular phases. Human Reproduction 15, 11–16.CrossRefGoogle ScholarPubMed
Hausmann, M., Slabbekoorn, D., Van Goozen, S. H., Cohen-Kettenis, P. T. & Gunturkun, O. (2000) Sex hormones affect spatial abilities during the menstrual cycle. Behavioral Neuroscience 114, 1245–1250.CrossRefGoogle ScholarPubMed
Helle, S. & Lilley, T. (2008) Maternal 2nd to 4th digit ratio does not predict lifetime offspring sex ratio at birth. American Journal of Human Biology 20, 700–703.CrossRefGoogle Scholar
Hermans, E. J., Putnam, P. & Van Honk, J. (2006) Testosterone administration reduces empathetic behaviour: a facial mimicry study. Psychoneuroendocrinology 31, 859–866.CrossRefGoogle ScholarPubMed
Hooven, C. K., Chabris, C. F., Ellison, P. T. & Kossleyn, S. M. (2004) The relationship of male testosterone to components of mental rotation. Nueropsychologia 42, 782–790.CrossRefGoogle ScholarPubMed
Inqudomnukul, E., Baron-Cohen, S., Wheelwright, S. & Knickmeyer, R. (2007) Elevated rates of testosterone related disorders in women with autism spectrum conditions. Hormones and Behavior 51, 597–604.CrossRefGoogle Scholar
James, W. H. (1975) Sex ratio and the sex composition of the existing sibs. Annals of Human Genetics 38, 371–378.CrossRefGoogle ScholarPubMed
James, W. H. (1987) The human sex ratio. Part 1: a review of the literature. Human Biology 59, 721–752.Google ScholarPubMed
James, W. H. (1996) Evidence that mammalian sex ratios at birth are partially controlled by parental hormone levels at the time of conception. Journal of Theoretical Biology 180, 271–286.CrossRefGoogle ScholarPubMed
James, W. H. (2000a) The variation of the probability of a son within and across couples. Human Reproduction 15, 1184–1188.CrossRefGoogle ScholarPubMed
James, W. H. (2000b) Analysing data on the sex ratio of human births by cycle day of conception. Human Reproduction 15, 1206–1207.CrossRefGoogle ScholarPubMed
James, W. H. (2001) Finger length ratios, sexual orientation and offspring sex ratios. Journal of Theoretical Biology 212, 273–274.CrossRefGoogle ScholarPubMed
James, W. H. (2004) Further evidence that mammalian sex ratios at birth are partially controlled by parental hormone levels around the time of conception. Human Reproduction 19, 1250–1256.CrossRefGoogle ScholarPubMed
James, W. H. (2006a) Possible constraints on adaptive variation in sex ratio at birth in humans and other primates. Journal of Theoretical Biology 238, 383–394.CrossRefGoogle ScholarPubMed
James, W. H. (2006b) Offspring sex ratios at birth as markers of paternal endocrine disruption. Environmental Research 100, 77–85.CrossRefGoogle ScholarPubMed
James, W. H. (2008a) Further support for the hypothesis that parental hormone levels around the time of conception are associated with human sex ratios at birth. Journal of Biosocial Science 40, 855–861.CrossRefGoogle ScholarPubMed
James, W. H. (2008b) Evidence that mammalian sex ratios at birth are partially controlled by parental hormone levels around the time of conception. Journal of Endocrinology 198, 3–15.CrossRefGoogle ScholarPubMed
James, W. H. (2008c) Further evidence that some male-based neurodevelopmental disorders are associated with high intrauterine testosterone concentrations. Developmental Medicine and Child Neurology 50, 15–18.CrossRefGoogle ScholarPubMed
James, W. H. (2009a) Variation of the probability of a male birth within and between sibships. Human Biology 81, 13–22.CrossRefGoogle ScholarPubMed
James, W. H. (2009 b) Maternal eating disorders and sex ratio at birth. Acta Obstetricia et Gynecologica 88, 488.CrossRefGoogle Scholar
Kanazawa, S. & Apari, P. (2009) Sociosexually unrestricted parents have more sons: a further application of the generalized Trivers–Willard hypothesis (gTWH). Annals of Human Biology, epub 21.3.09.CrossRefGoogle Scholar
Kanazawa, S. & Vandermassen, G. (2005) Engineers have more sons, nurses have more daughters: an evolutionary psychological extension of Baron-Cohen's extreme male brain theory of autism. Journal of Theoretical Biology 233, 589–599.CrossRefGoogle ScholarPubMed
Kemper, T. D. (1990) Social Structure and Testosterone. Rutgers University Press, London, p. 137.CrossRefGoogle Scholar
McIntyre, M. H., Chapman, J. F., Lipson, S. F. & Ellison, P. T. (2007) Index-to-ring finger length ratio (2D: 4D) predicts levels of salivary estradiol, but not progesterone, over the menstrual cycle. American Journal of Human Biology 19, 434–436.CrossRefGoogle Scholar
Malinvaud, E. (1955) Relations entre la composition des familles et le taux de masculinite. Journal de la Societe de Statistique de Paris 96, 49.Google Scholar
Manning, J. T. (2002) Digit Ratio: a Pointer to Fertility, Behavior and Health. Rutgers University Press, New Jersey.Google Scholar
Manning, J. T., Baron-Cohen, S., Wheelwright, S. & Sanders, G. (2001) The 2nd to 4th digit ratio and autism. Developmental Medicine and Child Neurology 43, 160–164.CrossRefGoogle ScholarPubMed
Manning, J. T. & Fink, B. (2008) Digit ratio (2D: 4D), dominance, reproductive success, asymmetry and sociosexuality in the BBC Internet Study. American Journal of Human Biology 20, 451–461.CrossRefGoogle ScholarPubMed
Manning, J. T., Martin, S., Trivers, R. L. & Soler, M. (2002) 2nd to 4th digit ratio and offspring sex ratio. Journal of Theoretical Biology 217, 93–95.CrossRefGoogle ScholarPubMed
Manning, J. T., Scutt, D., Wilson, J. & Lewis-Jones, D. I. (1998) The ratio of 2nd to 4th digit length: a predictor of sperm numbers and concentrations of testosterone, luteinizing hormone and oestrogen. Human Reproduction 13, 3000–3004.CrossRefGoogle ScholarPubMed
Manning, J. T., Wood, S., Vang, E., Walton, J., Bundred, P. E., van Heyningen, C. & Lewis-Jones, D. I. (2004) Second to fourth digit ratio (2D: 4D) and testosterone in men. Asian Journal of Andrology 6, 211–215.Google ScholarPubMed
Mantzoras, C. S., Georgiadis, E. I. & Trichopoulos, D. (1995) Contribution of dihydrotestosterone to male sexual behaviour. British Medical Journal 310, 1289–1291.CrossRefGoogle Scholar
Martin, D. M., Wittert, G. & Burns, N. R. (2007) Gonadal steroids and visuo-spatial abilities in adult males: implications for generalized age-related cognitive decline. Aging Male 10, 17–29.CrossRefGoogle ScholarPubMed
Martin, J. F. & Williams, R. C. (2008) Female genital cutting and mother's age at birth are associated with the sex of offspring. Biodemography and Social Biology 54, 141–151.CrossRefGoogle Scholar
Mealey, L. (1995) The socio-biology of sociopathy: an integrated evolutionary model. Behavioral and Brain Sciences 18, 523–599.CrossRefGoogle Scholar
Mouridsen, S. E., Rich, B. & Isager, T. (in press) Sibling sex ratio of individuals diagnosed with autism spectrum disorder as children. Developmental Medicine and Child Neurology.Google Scholar
Pickles, A. R., Crouchley, R. & Davies, R. B. (1982) New methods for the analysis of sex ratio data independent of the effects of family limitation. Annals of Human Genetics 46, 75–81.CrossRefGoogle ScholarPubMed
Potter, R. G. & Millman, S. R. (1986) Fecundability and the frequency of marital intercourse: new models incorporating the aging of gametes. Population Studies 40, 159–170.CrossRefGoogle Scholar
Powell, L. H., Lovallo, W. R., Matthews, K. A., Meyer, P., Baum, A., Stone, A. A. et al. (2002) Physiological markers of chronic stress in premenopausal middle aged women. Psychosomatic Medicine 64, 502–509.CrossRefGoogle ScholarPubMed
Purifoy, F. E. & Koopmans, L. H. (1979) Androstenedione, testosterone and free testosterone concentrations in women of various occupations. Social Biology 26, 179–188.CrossRefGoogle ScholarPubMed
Reimers, S. (2007) The BBC Internet Study: general methodology. Archives of Sexual Behavior 36, 147–161.CrossRefGoogle ScholarPubMed
Schutzenberger, M. P. (1950) Nouvelles recherches sur la distribution du sexe a la naissance. Semaine des Hopitaux de Paris 26, 4458–4465.Google Scholar
Smalley, S. L., Loo, S. K., Yang, M. H. & Cantor, R. M. (2005) Towards localizing genes underlying cerebral asymmetry and mental health. American Journal of Medical Genetics B: Neuropsychiatric Genetics 135, 79–84.CrossRefGoogle Scholar
Sorenson, J. C., Meier, R. J. & Campbell, B. C. (1993) Dermatoglyphic asymmetry and testosterone levels in normal males. American Journal of Physical Anthropology 90, 185–195.Google Scholar
Stewart, H., Morison, L. & White, R. (2002) Determinants of coital frequency among married women in Central African Republic: the role of female genital cutting. Journal of Biosocial Science 34, 525–539.CrossRefGoogle ScholarPubMed
Swaab, D. F., Bao, A. M. & Lucassen, P. J. (2005) The stress system in the human brain in depression and neurodegeneration. Ageing Research Reviews 4, 141–194.CrossRefGoogle ScholarPubMed
Terman, L. M. & Miles, C. C. (1936) Sex and Personality. McGraw Hill, New York.Google Scholar
Thilers, P. P., MacDonald, S. W. S. & Herlitz, A. (2006) The association between endogenous free testosterone and cognitive performance: a population-based study in 35- to 90-year-old men and women. Psychoneuroendocrinology 31, 565–576.CrossRefGoogle ScholarPubMed
Trivers, R. L. & Willard, D. E. (1973) Natural selection of parental ability to vary the sex ratio of offspring. Science 179, 90–91.CrossRefGoogle ScholarPubMed
Von Horn, A., Backman, L., Davidsson, T. & Hansen, S. (in press). Empathizing, systemizing and finger length ratio in a Swedish sample. Scandinavian Journal of Psychology, epub 7.4.09.Google Scholar
Vermeersch, H., T'Sjoen, G., Kaufman, J-M. & Vincke, J. (2008) Estradiol, testosterone, differential association aggressive and non-aggressive risk-taking in adolescent girls. Psychoneuroendocrinology 33, 897–908.CrossRefGoogle ScholarPubMed
Voracek, M., Manning, J. T. & Dressler, S. G. (2007) Repeatability and interobserver error of digit ratio (2D: 4D) measurements made by experts. American Journal of Human Biology 19, 142–146.CrossRefGoogle ScholarPubMed
Windham, G. C., Elkin, E., Fenster, L., Waller, K., Anderson, M., Mitchell, P. R. et al. (2002) Ovarian hormones in premenopausal women and menstrual cycle characteristics. Epidemiology 13, 675–684.CrossRefGoogle ScholarPubMed
Zalata, A., Hafez, T., Verdonck, L., Vermeulen, L. & Comhaire, F. (1995) Androgens in seminal plasma: markers of the surface epithelium of the male reproductive tract. International Journal of Andrology 18, 271–277.CrossRefGoogle ScholarPubMed
Zuckerman, M. (1994) Behavioral Expressions and Biosocial Bases of Sensation Seeking. Cambridge University Press, New York.Google Scholar