Sex ratios of births conceived during wartime

William H. James

The Galton Laboratory, University College London, 4 Stephenson Way, London NW1 2HE, UK

Dear Sir,

There can be no reasonable doubt that sex ratios (proportions male at birth) have risen during and just after major wars. This happened to the sex ratios of all the belligerent countries in both World Wars. During the same period, the sex ratios of the non-belligerent countries rose to a lesser extent or remained stable (James, 1987Go). I have adduced very large quantities of evidence to support the hypothesis that the sexes of mammalian (including human) offspring are partly dependent on the hormone levels of both parents around the time of conception (James, 1996Go). Ex hypothesi, high parental levels of testosterone and estrogen around the time of conception are associated with the subsequent births of boys and high levels of gonadotrophins and progesterone with girls. This hypothesis is capable of explaining the wartime rise in sex ratios as follows: (i) It may be presumed that there is an unusually high coital frequency during demobilization leaves and short wartime leaves; (ii) it may be shown mathematically that higher coital rates are associated with (slightly) earlier fertilization in the fertile interval within the menstrual cycle (Roberts, 1978Go); (iii) the regression of women’s estrogen/gonadotrophin ratio is U-shaped across this interval, and (iv) the regression of sex ratio of the resulting offspring is also U-shaped across this interval (James, 2000Go), ex hypothesi as a consequence of this variation of the estrogen/gonadotrophin ratio across this interval. The high wartime sex ratios are thus ex hypothesi due to earlier fertilizations because of the high coital rates.

This explanation has been called into question by two recent reports of low offspring sex ratios associated with war viz in Iran during the Iran–Iraq war of 1980–88 (Ansari-Lari and Saadat, 2002Go) and the 10-day war in Slovenia in 1991 (Zorn et al., 2002Go). I deal separately with them here.

(i) The Iran–Iraq War of 1980–88. It is well documented that in this conflict, chemical weapons were used and that Iranian men were exposed to mustard gas (sulphur mustard; dichloroethylsulphide) (Azizi et al., 1995Go; Safarinejad, 2001Go). It is also reported that exposure to mustard gas is subsequently associated with low testosterone/gonadotrophin ratios in male survivors (Azizi et al., 1995Go; Safarinejad, 2001Go). Accordingly I suggest that one cause of the low sex ratio was low testosterone/gonadotrophin ratios in exposed men. The point could be tested if workers in Iran were to examine the sex ratio of offspring of exposed men.

(ii) The 10-day War in Slovenia, 1991. As far as I know, no chemical weapons were used in this operation. So why should the reported trend in associated sex ratio differ from all those reported in the two World Wars? I think Zorn et al. (2002Go) themselves offer a clue. They cited evidence that sex ratios declined after the Kobe earthquake (Fukuda et al., 1998Go), and after severe periconceptional life events (death of a spouse or child etc) (Hansen et al., 1999Go). They write that..."War in Slovenia consisted mainly of psychological pressure with constant menace of a military attack"... and ..."Considering the fall in sex ratio was more pronounced in the capital Ljubljana, where the menace was most intense with the possibility of air raids and constant threat of sabotage or direct assault from the Yugoslav army forces, we presume that a gradation in subjective stress and adaptation argues for the direct effect of psychological stress on the changes in sex ratio". These authors offer evidence that severe psychological stress adversely affects sperm quality which (they suggest) directly lowers the sex ratio. However they cite evidence that sperm quality is not directly associated with offspring sex ratio (Jacobsen et al., 2000Go). This latter evidence weakens their argument, so I should like to amend it. I suggest that it is not variations in sperm quality per se, but in testosterone levels, that are responsible for variations in offspring sex ratio.

Testosterone concentrations are intimately connected with human experience and behaviour (Kemper, 1990Go). They reportedly rise when we win games and fall when we lose them. They are high in dominant people. They fall when we are depressed and, in particular, they fall when men are ill (Semple, 1986Go) or afraid (Rose et al., 1969Go).

Let us now consider a difference between the two World Wars and the Slovenian War. In the former, (with one obvious exception, see below) conceptions usually occurred well away from scenes of violence and terror but according to Zorn et al. (2002Go) this was not so in the Slovenian operation. The exception relates to bombing raids on civilian populations. During World War II, a number of large cities repeatedly became the targets of such bombing. However these bombing raids did not occur randomly in time across the whole period of the War. Rather, individual cities were targeted for several consecutive days or weeks, and then there would be a lull. If I am correct, conceptions which occurred in cities during such targeting would have low sex ratios. All other conceptions would have high sex ratios. In principle, this suggestion may be tested if the dates of bombing raids and of births are still available.

References

Ansari-Lari, M. and Saadat, M. (2002) Changing sex ratio in Iran 1976–2000. J. Epidemiol. Community Health, 56, 622–623.[Free Full Text]

Azizi, F., Keshvarz, A., Roshanzamir, F. and Nafarabadi, M. (1995) Reproductive function in men following exposure to chemical warfare with sulphur mustard. Med. War, 11, 34–44.[Medline]

Fukuda, M., Fukuda, K., Shimizu, T. and Moller, H. (1998) Decline in sex ratio at birth after Kobe earthquake. Hum. Reprod., 13, 2321–2322.[Abstract]

Hansen, D., Moller, H. and Olsen, J. (1999) Severe periconceptional life events and the sex ratio in offspring: follow-up study on five national registries. Br. Med. J., 319, 548–549.[Free Full Text]

Jacobsen, R., Bostofte, E., Skakkebaek, N.E., Hansen, J. and Moller, H. (2000) Offspring sex ratio of subfertile men and men with abnormal sperm characteristics. Hum. Reprod., 15, 2369–2370.[Abstract/Free Full Text]

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James, W.H. (1996) Evidence that mammalian sex ratios at birth are partially controlled by parental hormone levels at the time of conception. J. Theor. Biol., 180, 271–286.[CrossRef][ISI][Medline]

James, W.H. (2000) Analysing data on the sex ration of human births by cycle day of conception. Hum. Reprod., 15, 1206–1207.[Free Full Text]

Kemper, T.D. (1990) Social Structure and Testosterone. Rutgers University Press, London.

Roberts, A.M. (1978) The origins of fluctuations in the human secondary sex ratio. J. Biosoc. Sci., 10, 169–182.[ISI][Medline]

Rose, R.M., Bourne, P.G., Poe, R.O., Mougey, E.H., Collins, D.R. and Mason, J.W. (1969) Androgen responses to stress. II. Excretion of testosterone, epitestosterone, androsterone, and etiocholanone during basic combat training and under threat of attack. Psychosom. Med., 31, 418–436.[ISI][Medline]

Safarinejad, M.R. (2001) Testicular effect of mustard gas. Urology, 58, 90–94[CrossRef][ISI][Medline]

Semple, C.G. (1986) Hormonal changes in non-endocrine diseases. Br. Med. J., 293, 1049–1052.[ISI][Medline]

Zorn, B., Sucur, V., Stare, J. and Meden-Vrtovec, H. (2002) Decline in sex ratio at birth after 10-day war in Slovenia. Hum. Reprod., 17, 3173–3177.[Abstract/Free Full Text]