Department of Epidemiology and Biostatistics,University Medical Centre Nijmegen, P.O.Box 9101,6500 HB Nijmegen, The Netherlands. e-mail: p.jongbloet{at}epib.umcn.nl
Dear Sir,
The conclusion of Cagnacci et al. (2003) that more males than females are conceived in seasons with more favourable reproductive conditions challenges the well-known V-shaped probability of delivering more male offspring at both the onset and the end of the fertile window, versus equal gender proportions at the time of ovulation in the mid-cycle (Guerrero, 1974
; Harlap, 1979
; James, 1996
). It even seems opposite to the general experience of increasing sex ratio (SR) at younger and advanced maternal age in animals, versus the approach to equity during prime reproductive age, independent of birth order and paternal age (King and Stotsenburg, 1915
; Clutton-Brock and Jason, 1986
; Kojola and Eloranta, 1989
). The former conditions are characterized by an irregular ovulation rate, the latter by a regular one. Still more worrying is the other general tendency in amphibians, birds and mammals of rather equal numbers of male and female births when mating occurs at the peak(s) of seasonally bound heat periods, versus high SR at the breakthrough and breakdown of the ovulatory pattern (Heape, 1908
; King and Stotsenburg, 1915
; Wolda, 1935
; Coulson and Hickling, 1961
; Stirling, 1971
; Lambin, 1994
). The peaks of reproductive performance appear to go hand in hand with more optimal progeny; the transitional stages with more disabled progeny. The conclusion of Cagnacci et al. is incompatible with these general experiences, and therefore embarrassing for any researcher into modulation of the SR.
The overripeness ovopathy concept (Jongbloet et al., 1996, 2001, 2002) might reconcile the present controversy. At the mid-cycle, optimal maturation of the oocyte and optimal liquefaction of the cervical mucus are modulated by the estrogens, which promotes equity of male and female conceptuses. In contrast, non-optimal maturation of the oocyte or pre-ovulatory overripeness ovopathy (PrOO) entails impossibility of fertilization, defective implantation, transitory retardation in the rate of development, and a wide spectrum of anomalies in organogenesis and in differentiation of various tissues and organ systems, as evidenced after experimental delay of the ovulation in animals (Mikamo, 1968
; Butcher, 1981
). Y-Bearing sperm are smaller than X-bearing ones (Cui, 1997
) and their fertilization capacity will therefore be advantaged in the case of non-optimal liquefaction of the cervical mucus. Preferential fertilization of aged oocytes by Y-bearing sperm thus induces an excess of male-biased (non-optimal) embryos and loss of them before implantation or birth. In extreme circumstances, accumulation of the rate of ovopathy will result in a reversal of the SR after having surpassed a certain threshold, i.e. again a decrease of the SR.
The interesting data of Cagnacci et al., and particularly their theoretical phases in the periodogram, do not perhaps represent what they seem to. Instead of comparing these curves in their Figure, one can follow the SR per month corresponding to the conception rate. This reveals a double hump surge: the SR appears to increase in May during the rise of the conception rate (corresponding to the breakthrough of the ovulation rate), to decrease in June/July at the peak (corresponding to optimal ovulation rate), again to increase in August/September during the descent of the conception rate (corresponding with the breakdown of the ovulation rate) and finally to become inverted in the feminine direction from December to April (corresponding with the season of a more constrained ovulation rate).
Lower SR at the zenith of the seasonally bound birth peaks and, in contrast, more male births at the transitional stages have not only been recorded in animals, as mentioned already, but also in naturally conceiving populations (van Eyk, 1904; Heape, 1909
; Wolda, 1927
; Huntington, 1938a
; Underwood, 1995
). Similar configurations were always present in contemporary populations from the Netherlands, Germany and the USA, or from Australia in the Southern hemisphere (Jongbloet et al., 1996
).
The seasonal birth (or conception) peaks concur not only with this equity trend in the SR, but also with optimal weight and length at birth, at school age and even at adulthood (Noack and Otto, 1957; Henneberg and Louw, 1993
; Matsuda et al., 1995
; Weber, 1998
; Banegas et al., 2001
), with brightness (Huntington, 1938b
) and longevity (Jongbloet, 1992
; Doblhammer and Vaupel, 2001
). This is opposed to the conclusion of Cagnacci et al., but in line with superior developmental competence of the related oocytes; pathological progeny and male excesses always concur with the slopes of these birth peaks in line with constrained developmental competence of the oocytes.
All these phenomena persuade us to adjust the conclusion of Cagnacci et al.: at the peaks of the seasonally bound ovulatory rate there is a tendency to equity in the sex distribution (and to optimal conceptuses); at the breakthrough and breakdown, more males than females are conceived (and less optimal conceptuses); and, in the most constrained conditions, the SR becomes inverted due to excessive loss of male-biased (pathological) fetuses.
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