Hum. Reprod. Advance Access originally published online on June 13, 2006
Human Reproduction 2006 21(10):2486-2490; doi:10.1093/humrep/del226
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OPINION |
Are there preconceptional determinants of mammalian sex? A response to Boklage (2005)
The Galton Laboratory, University College London, London, UK
To whom correspondence should be addressed at: The Galton Laboratory, University College London, Wolfson House, 4 Stephenson Way, London NW 12HE, UK. E-mail: whjames{at}waitrose.com
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Abstract |
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 Top Abstract IntroductionPolytocous mammalsMonotocous mammalsAmerican bisonSpringbokDomestic cattleBarbary macaqueHumanSo what causes the...References |
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Boklage (2005
, Hum Reprod 20,583–587) wrote: ‘Changes in, or mediated by, the epigenetic environment of embryogenesis provide the most plausible prospects for causes of changes in secondary sex ratio’. Without impugning this notion, I suggest here that other causes of variation in secondary sex ratio antedate fertilization or, in other words, that there are circumstances under which unequal numbers of male and female zygotes are formed. It will be documented here that this suggestion has repeatedly been made on the basis of data on many mammalian species (golden hamster, sheep, mouse, white-tailed deer, American bison, springbok, domestic cattle and Barbary macaque). It may be acknowledged that the causes of this hypothesized preconceptional variation are not established. I have suggested one (parental hormones around the time of conception). But the truth of that hypothesis is not germane to the thrust of the present argument—which is to document the strong suspicions that such preconceptional determinants do, indeed, exist. Efforts should be made to confirm or discredit these suspicions.
Key words: preconceptional determinants/sex ratio
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Introduction |
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TopAbstractIntroductionPolytocous mammalsMonotocous mammalsAmerican bisonSpringbokDomestic cattleBarbary macaqueHumanSo what causes the...References |
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The argument of Boklage (2005)
may be summarized in the form of seven numbered propositions:
- The numbers of X- and Y-bearing sperm produced by men are equal.
- X- and Y-bearing sperm have equal probabilities of fertilizing the ovum.
- Hence, at the time of fertilization, equal numbers of male and female zygotes are formed.
- The sex ratio (proportion male) at birth is in excess of 0.5.
- The sex ratio of recognized spontaneously aborted fetuses is also in excess of 0.5.
- There is a substantial quantity of unrecognized embryonic and early fetal losses (viz. those occurring roughly before the eighth week of pregnancy).
- Hence, there must be an excess of females among these early unrecognized losses.
I take this argument to be valid; however, I shall argue that its conclusion is false because one of its premises [Proposition (ii)] is false. To sustain my case, I shall assume that sex is controlled by similar mechanisms across the mammalian species. In doing so, I follow Boklage (2005) who wrote of his own argument: ‘The evidence provided by these results is indirect. That is unlikely to change. Ethical, technical and financial considerations argue against the destruction for karyotyping of statistically sufficient numbers of products of natural human fertilizations’. Different forms of argument will be deployed here in regard to data relating to (i) polytocous and (ii) monotocous mammals.
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Polytocous mammals |
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TopAbstractIntroductionPolytocous mammalsMonotocous mammalsAmerican bisonSpringbokDomestic cattleBarbary macaqueHumanSo what causes the...References |
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The variances of the distributions of the sexes within mammalian litters
It has been shown that the variances of the distributions of the sexes within litters are sub-binomial in the pig, rabbit, mouse (James, 1975
) and sheep (James, 1976), and data have been cited showing the same phenomenon in the golden hamster and rat (James, 1996a). In other words, as contrasted with binomial expectation, there are
- significantly more litters in which the two sexes are evenly balanced and
- fewer unisexual litters.
A possible cause of this sub-binomial variance is as follows: if P (the probability that a zygote will be male) were to vary from one zygote to another within litters, then that would constitute an example of Poisson variation (not to be confused with Poisson distribution). And it is a standard result in probability theory that Poisson variation is associated with sub-binomial variance (Edwards, 1960). So, the question arises: is the established sub-binomial variance the consequence of such Poisson variation? Other possibilities have been discussed (James, 1975):
- differential fetal mortality preferentially affecting the more numerous sex in a litter (regardless of whether that sex is male or female);
- the individual X- and Y-bearing sperm have a common origin and subsequently may not get the chance to distribute themselves randomly in space and
- defective reporting (in herdbooks and elsewhere).
In view of the lack of evidence for any of these three alternatives, I proposed that there is Poisson variation of the sort described (James, 1975). It is not clear how such variation would be consistent with Boklage’s (2005) proposal. So, I suggest that the onus is on Boklage either to reconcile his proposal with the sub-binomial variance or to give grounds for espousing at least one of these three alternatives.
Sex ratio and litter size
As I understand it, if Boklage’s hypothesis were correct, then there would be a negative correlation between sex ratio and litter size in polytocous mammalian species. (Ex hypothesi, small litters would be the consequence of female-biased embryonic and fetal losses.) In fact, there seems no general relationship between litter size and sex ratio across species (Trivers, 1985). In the rabbit, for instance, there is reportedly a lower proportion of males in large litters (Hammond, 1934), whereas in the mouse, there is a rise in sex ratio with litter size (Howard et al., 1955). Of course, it is possible that in some species, the male zygote is the more vulnerable, whereas in others, it is the female.
Sex ratio, maternal condition and the hypothesis of Trivers and Willard
Trivers and Willard (1973) (henceforth TW) noted that under some circumstances, there would be reproductive advantage if females were to skew their offspring sex ratio in one direction or the other. The circumstances were that
- males have a greater reproductive variance than females;
- reproductive success correlates with mother’s ‘condition’ and
- offspring inherit their mothers’ ‘condition’.
Under these circumstances, females would have more grandchildren if mothers in good ‘condition’ were to have disproportionately more sons and those in poor ‘condition’ more daughters. These authors hypothesized that under these circumstances, such skewed offspring sex ratios actually exist. It is accepted that these three circumstances are very generally fulfilled in a wide range of species, including ours. The hypothesis has occasioned much subsequent research. This has been reviewed by Brown and Silk (2002), with respect to 35 studies on 15 non-human primate species, and by Lazarus (2002), with respect to 54 studies on humans. About 50% of the above 89 studies were interpreted as offering confirmatory evidence for TW. Moreover, Cameron (2004) showed in a further meta-analysis that when maternal condition was assessed at the time of conception (rather than during gestation or at birth), 22 of 25 studies gave statistically significant support for TW. Thus, one would infer that TW has a kernel of truth. I have suggested that the frequent failures to confirm are partially consequent on ‘constraints’ (James, 2004). Regardless of the correctness of that suggestion, the ‘kernel of truth’ remains. In short, there is a tendency for women (female primates generally) in good ‘condition’ to produce excesses of sons. If Boklage’s (2005) hypothesis were correct, they would do so via spontaneous female embryonic and early fetal loss. So, his hypothesis apparently commits him to the view that women in good condition on the average have higher rates of spontaneous reproductive loss than women in poor condition. This seems implausible from an evolutionary viewpoint.
Experimental work on polytocous mammals
Boklage (2005) wrote: ‘There has been a sizeable number of sound research efforts that would have discovered any consistent bias in spermatogenesis or fertilization, but did not’. By this, I take him to mean that, inter alia, there are no grounds for supposing that, at the time of fertilization, there are circumstances under which the proportions of male and female zygotes differ. This contention has been questioned by many workers. I shall illustrate my point by directly quoting from work on several species.
Golden hamster
Pratt et al. (1987) found that in this species, litter sex ratios (proportions male) increase with time of mating vis-à-vis onset of estrus. However, they wrote (p. 313): ‘The increase in sex ratio of litters resulting from later matings is probably not due to differential female mortality in utero, since there is only evidence for differential male mortality in this species (Sundell, 1962)’. Members of this research group also found significantly sub-binomial variances in the distributions of the combinations of the sexes within litters of golden hamsters (Huck et al., 1990), and they wrote (p. 99): ‘The main features of the distribution of litter sex ratios can be generated from a causal model in which different probabilities of producing a male apply to "early" and "late" conceptions within each litter’ [italics in the original]. This suggestion had previously been made in respect of several other species (James, 1975) and implies the existence of determinants of sex at or before fertilization.
Sheep
Ewes were inseminated at different times before or after ovulation (Gutierrez-Adan et al., 1999). Gutierrez-Adan et al. reported that more females resulted from inseminations before ovulation and that more males resulted from inseminations after ovulation. They wrote: ‘Our results suggest that the differential ability of X- or Y-bearing spermatozoa to fertilize oocytes depending on time of insemination or oocyte maturation state, may be due, at least partially, to "intrinsic" differences in the physiological activity of X- or Y-bearing spermatozoa before fertilization’ [italics added].
Mouse
Tarin et al. (1999) artificially inseminated female mice at 13 h (controls) or 22 h (oocyte aged) after GnRH injection. Litter size was not associated with the sex ratio of offspring. These authors interpreted this as evidence against the developmental asynchrony hypothesis of Krackow (1995) and the sex-related fetal mortality hypothesis.
Jimenez et al. (2003) examined mouse embryos developmentally synchronic or asynchronic with recipient female endometrium. They concluded that their results were ‘the first experimental evidence supporting the view that both pre- and post-conceptional mechanisms of sex ratio distortion in polytocous species are not mutually exclusive’. (A similar conclusion was also reached in regard to an avian species; Komdeur et al., 2002.)
White-tailed deer
Verme and Ozoga (1981) reported on the variation of sex ratio by the timing of insemination within the estrus cycle of the white-tailed deer. Their data are summarized in Table I. It may be acknowledged that the number of fawns per mother is slightly less in the two extreme time intervals. But one may calculate that these differences cannot be reconciled with the hypothesis that secondary sex ratio is controlled by sex-selective losses. Accordingly, De Young et al. (2004) tested whether white-tailed bucks produce Y-chromosome-biased ejaculates. These authors failed to find any evidence for bias. One may conclude that, taken together, these data provide strong evidence that there are preconceptional determinants of sex in this species.
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Monotocous mammals |
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In two species, fetuses have been sexed after their mothers had been randomly culled, viz the American bison (Rutberg, 1986
) and the springbok (Kruger et al., 2005). |
American bison |
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TopAbstractIntroductionPolytocous mammalsMonotocous mammalsAmerican bisonSpringbokDomestic cattleBarbary macaqueHumanSo what causes the...References |
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The data of Rutberg (1986)
are summarized in Table II. The cows were dichotomized by whether they were lactating or not at the time of slaughter. This author wrote: ‘The sex ratio bias among non-lactating cows is too strong to be plausibly accounted for by selective mortality on female fetuses. Even under the extreme assumption that all seven non-pregnant, non-lactating cows conceived and aborted female fetuses, the resultant hypothetical primary sex ratio (25 male:11 female) still differs significantly from 1:1’. One may infer that some form of preconceptional mechanism was operating.
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Springbok |
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TopAbstractIntroductionPolytocous mammalsMonotocous mammalsAmerican bisonSpringbokDomestic cattleBarbary macaqueHumanSo what causes the...References |
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Springboks were studied on a farm of 113 km2 in South Africa, 1972–2001. In the course of random culling, 3974 embryos were ascertained and sexed. Kruger et al. (2005)
wrote: ‘Sex specific foetal mortality is unlikely to be the mechanism behind the variation in offspring sex ratio between years in the springbok. Although we cannot categorically rule out the possibility that females might have reabsorbed their embryos at a very early stage, the number of non-pregnant females in many years is simply too small to affect qualitatively the results of the population-level analysis’. These authors concluded that either differential implantation occurs or females are able to influence the sex of the sperm fertilizing an oocyte. |
Domestic cattle |
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TopAbstractIntroductionPolytocous mammalsMonotocous mammalsAmerican bisonSpringbokDomestic cattleBarbary macaqueHumanSo what causes the...References |
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Several articles documented substantial variation in calf sex ratio by the estimated time of insemination vis-à-vis ovulation (Wehner et al., 1997
; Pursley et al., 1998; Gutierrez-Adan et al., 1999). Gutierrez-Adan et al., (1999) were so impressed by this variation that they suggested that it was caused by physiological differences between X- and Y-bearing spermatozoa before fertilization (rather than by sex-related early losses). In other words, they were hypothesizing preconceptional mechanisms for sex determination. |
Barbary macaque |
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TopAbstractIntroductionPolytocous mammalsMonotocous mammalsAmerican bisonSpringbokDomestic cattleBarbary macaqueHumanSo what causes the...References |
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Paul and Kuester (1987)
reported on the sex ratios of offspring of Barbary macaques by maternal dominance status. High-ranking females produced offspring with a significantly higher sex ratio than low-ranking females. These authors noted that 88% of all infants resulted from conceptions in the first estrus in the season, this being so for high- and low-ranking females. These authors wrote (p. 129): ‘The rate of abortion was far too low for causing [sic] the rank related differences in secondary sex ratio. There were no indications that abortion rates of low ranking females were higher than those of high ranking females. Also there were no indications that low ranking females had more estrous periods until conception than did high ranking females. Most infants were conceived in the first estrous period of a mating season where no post-conceptional adjustment of infant’s sex was possible’. These authors inferred (p. 129) that their data ‘strongly indicated that the proportion of male and female offspring was modified by preconceptional adjustment mechanisms working via timing of mating in relation to ovulation’. |
Human |
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TopAbstractIntroductionPolytocous mammalsMonotocous mammalsAmerican bisonSpringbokDomestic cattleBarbary macaqueHumanSo what causes the...References |
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There are many points in the epidemiology of sex ratio on which Boklage’s comments would be useful.
- Boldrini (1936) and Colombo (1957) found that the sex ratio of the offspring of women who have never had a (recognized) spontaneous abortion is very close to that of the surviving offspring of women who have had a recognized spontaneous abortion. I assume that Boklage would dismiss this evidence as irrelevant to his argument because the spontaneous abortions were recognized. However, Renkonen (1970) reported on the sex ratio of first marital births by the duration of time since marriage. He found that the sex ratio at birth declined monotonically with this duration. Since long delays to conception are partially due to spontaneous abortions (recognized and unrecognized), I would suppose that this phenomenon is contrary to Boklage’s expectation.
- As Boklage (2005) remarked, there is a huge and sometimes contradictory literature on human sex ratio variation. But not all of it is contradictory, although it may be further acknowledged that some of the established variation is so minuscule as to defy decisive explanation (e.g. that with war, maternal age, parity, paternal age, region, season and smoking). However, some of the variation is both established and substantial, e.g. with the time of insemination within the cycle, the duration of gestation, male and female occupational and chemical exposures and with pathological conditions in men and women (James, 2004). Some of these variables are associated with high sex ratios and others with low sex ratios. It is not clear to me how Boklage would explain
- why women with some categories of obstetric illness (e.g. pre-eclampsia) have a tendency to produce sons, whereas those with other forms of obstetric illness (e.g. hyperemesis gravidarum) have a predominance of daughters (e.g. James, 1995) and
- why some forms of paternal illnesses have been repeatedly reported to be associated with the production of sons, e.g. hepatitis B carriers (Chahnazarian et al., 1988), and others with daughters, e.g. testicular cancer (Moller, 1998; Jacobsen et al., 2000; Gundy et al., 2004).
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So what causes the excess of males among human births? |
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TopAbstractIntroductionPolytocous mammalsMonotocous mammalsAmerican bisonSpringbokDomestic cattleBarbary macaqueHumanSo what causes the...References |
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There is good evidence that P (the probability of a male birth) varies across human parents (Lexis variation) (James, 1990
). On the plausible assumption that there is a genetic component to this Lexis variation, Kumm et al. (1994) examined the effects of sex prejudice (e.g. sex-selective infanticide or sex-selective abortion) on the evolution of the sex ratio at conception. These authors showed mathematically that when the total number of offspring of a mating pair is significantly reduced as a consequence of that prejudice, the primary sex ratio will be expected to evolve to favour the preferred sex. These authors concluded their article with the words: ‘Generations of female infanticide amongst our ancestors may explain the universally male biased primary sex ratio, if such practices were associated with significant fitness cost’. Confirmation of this hypothesis came from an unexpected quarter. Kumm et al. (1994) and Boklage (2005) were incorrect in supposing that there is always an excess of boys at birth. Clark et al. (1995) reported the births of 2429 boys and 2629 girls during the years 1956–91 in a group of Tonga speakers in southern Zambia. This is a highly significant excess of daughters when contrasted with an expected sex ratio of 0.507 for newborns of African ancestry (James, 1987). Clark et al. (1995) offered no evidence to impugn the reporting of their data. Moreover, they documented sexual prejudice in the Tonga. This is a matrilineal society in which both fathers and mothers want daughters. These continue their mothers’ lines, and to their fathers, daughters represent bride price in the future. Clark et al. (1995) also offered evidence that in this society, daughters are favoured over sons in access to medical care and in mortality rates. Thus, the Tonga may be interpreted as providing strong support for the hypothesis of Kumm et al. (1994) by constituting the exception that proves their rule (James, 1996b).
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