Relationship between urinary estrogen levels before conception and sex ratio at birth in a primate, the gray mouse lemur

Angelo Cagnacci

Ginecologia e Ostetricia, Dipartimento Integrato Materno-Infantile, Policlinico di Modena, via del Pozzo 71, 41100 Modena, Italy

E-mail: cagnacci{at}unimore.it

Sir,

In her recent paper, Dr Perret (2005)Go concluded that estradiol levels of late follicular but not pre-ovulatory phase play a major role in determining secondary sex ratio of gray mouse lemur offspring. This conclusion is supported only by some of her analyses, i.e. by grouping mother according to litter composition. On the other hand, this conclusion cannot be reached by looking at his Table I where young, adult and old mothers are compared. In this table secondary sex ratio, reported in real values, is low only in young mothers, whose only difference from adult mothers is, despite the age, in body mass. Estrogen levels are similar. Throughout the article, body mass is never considered a major determinant of sex ratio, although at least two recent papers in humans have claimed its possible importance in sex ratio modulation (Gibson and Mace, 2003Go; Cagnacci et al., 2004Go). Indeed, body mass may influence follicle growth, independently or in conjunction with estradiol, via modifications of adipose tissue secretory products, such as leptin, or indirectly through associate endocrine modifications of insulin, insulin-like growth factors and growth hormone (Poretzky et al., 1999Go). In some of her calculations Dr Perret tried to control for body mass, by regression analysis, but if body mass modulates secondary sex ratio via a threshold effect, this control can be insufficient. By stratifying women’s body weight in quartiles, we did not show a linear relationship between body weight and sex ratio, but only a reduced sex ratio in women of the first in comparison to those of the other three quartiles (Cagnacci et al., 2004Go). It should be useful to see values of secondary sex ratio and of estradiol (the ones reported in Table I of Dr Perret’s paper), stratified for tertiles/quartiles of maternal body mass.

Perret’s conclusions that low estrogen levels favour male conceptions are in contrast with those reported in humans (James, 2001Go). Similarly, the increase of sex ratio in aged animals is in contrast with some human data, as she correctly mentions. Dr Perret maintains that human data showing higher production of males under favourable conditions are challenged by several data: the decline of sex ratio in medically assisted reproduction with high estrogen levels (but also gonadotrophin); the increase of sex ratio during the first and second world wars (stress), and the similar decline of sex ratio observed in industrialized/polluted and rural areas in recent decades. These arguments are weak. For all the evidence cited by Dr Perret there are data showing the exact opposite. An increase of sex ratio in medically assisted reproduction was reported by some authors (Pergament et al., 1994Go; Tarin et al., 1995Go). The increase of sex ratio during the two world wars can be explained by alternative mechanisms, as an increased coital rate or a greater age difference between partners (Gaffelman and Hoestra, 2000Go; Manning et al., 1997Go), while a decline of sex ratio was observed during highly distressing recent wars (Zorn et al., 2002Go; James, 2003Go). Similarly a decline of sex ratio was observed following destructive earthquakes (Fukuda et al., 1998Go), or following emotional stress (Hansen et al., 1999Go). A difference in the decline of sex ratio between metropolitan/polluted areas and non-metropolitan rural areas was indeed observed in recent decades, in non-metropolitan areas sex ratio not declining and instead increasing (Astolfi and Zonta, 1999Go). Finally, an increase of sex ratio was reported in conjunction with the seasonal peak of conceptions (Cagnacci et al., 2003Go), i.e. in the best environmental conditions to conceive. Accordingly, either Dr Perret’s data have another explanation (body mass) or they do not seem to be in line with most of the available data in humans. Dr Perret performed her study in the mouse gray lemur kept in captivity, which is a small primate, seasonal breeding, with poly-ovulatory cycles and with a short time of gestation (2 months). In addition to a major difference in social organization and mating system, humans are large primates, not seasonal breeding, with mono-ovulatory cycles and with a long gestation (9 months). For these considerations, extrapolation of Dr Perret’s data to the human species is, in my opinion, inappropriate and probably misleading.

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