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Hum. Reprod. Advance Access originally published online on February 23, 2006
Human Reproduction 2006 21(7):1659-1661; doi:10.1093/humrep/del050
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© The Author 2006. Published by Oxford University Press on behalf of the European Society of Human Reproduction and Embryology. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

OPINIONS

Sex predetermination and the ethics of sex selection

V.J. Grant

Department of Psychological Medicine, Faculty of Medical and Health Sciences, University of Auckland, Auckland, New Zealand

To whom correspondence should be addressed at: Department of Psychological Medicine, Faculty of Medical and Health Sciences, University of Auckland, Private Bag 92019, Auckland 1, New Zealand. E-mail: vj.grant{at}auckland.ac.nz


    Abstract
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 Abstract
 Introduction
 An evolutionary dimension
 What if the sex...
 Implications for ethics of...
 References
 
At present there appear to be two main categories of problems involved in the ethics of sex selection. The first has to do with the status of the embryo, and the second has to do with the social consequences of making sex selection widely available. However, these may not be the only issues. There is growing evidence from evolutionary psychology and biology, which suggests that the sex of the offspring in mammals may not, after all, be a matter of chance. Instead, sex allocation in mammals may be the result of a finely tuned adaptive process involving the current suitability of a mother to conceive an offspring of a particular sex. If so, we need to know more about this process before embarking on a social policy that could have disadvantageous outcomes for children, their parents and society as a whole.

Key words: ethics/sex allocation/sex determination/sex preferences


    Introduction
 Top
 Abstract
 Introduction
 An evolutionary dimension
 What if the sex...
 Implications for ethics of...
 References
 
After decades of controversy, the problems surrounding the ethics of sex selection are still being debated. The underlying difficulties can be divided into two main areas – the ethical problems that arise from conflicting viewpoints on the status of the embryo (the extent to which an embryo should be considered fully human) and the ethical problems involved in the possible social consequences of sex selection (the likelihood or otherwise that the numbers of the sexes would be unequal at the time of reproductive maturity).

At present the most reliable method of sex selection is by means of PGD. The ethical question here is about the status and rights of an embryo and whether or not these should be the same as those which apply to a human foetus. This appears to be a matter of conscience in the same way that abortion is. The process is anathema to some (often on religious grounds) but is acceptable to others who believe human rights should not be fully bestowed till later in the pregnancy, and/or to those who believe that the needs and rights of parents outweigh those of the embryo.

The second problem concerns the ethical status of sex preferences and the social consequences of implementing such preferences. At the level of the individual, there appears to be some consensus that a sex preference is ethical if the existing family is a single-sex sibship, or occasionally, if parents seek to replace a deceased daughter or son (McMillan, 2002Go). But at the societal level, generalized sex preferences can become sexist and contrary to humans rights legislation. Furthermore over-valuing one sex can lead to distortions in the tertiary (reproductive) sex ratio. In 1993 Ridley described the problem of unequal sex preferences as a ‘tragedy of the commons: a collective harm that results from the rational pursuit of self-interest by individuals. One person choosing to have only sons does nobody any harm. But if everybody does it, everybody suffers’ (Ridley, 1993Go). Today this prediction has come true in several countries (Ramanamma and Bambawale, 1980Go; Allahbadia, 2002Go; Arnold et al., 2002Go). Further, the situation could have serious implications even for neighbouring countries in the near future (Hudson and den Boer, 2004Go).

The argument about collective harm would be less relevant in European countries if, first, roughly half the prospective parents preferred girls, and/or secondly, donations (Seibel et al., 1994Go) and/or regulations (Harris, 2005Go) kept population sex ratios in check. Thus, although the problem of sex preferences and its possible consequence of imbalanced sex ratios at the time of reproductive maturity is an important one, it appears that at present, in most western countries, regulating sex selection could solve the problem. If so, then one might argue in favour of permitting sex selection for social reasons such as family balancing.


    An evolutionary dimension
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 Abstract
 Introduction
 An evolutionary dimension
 What if the sex...
 Implications for ethics of...
 References
 
But wait! Before going ahead and liberalizing sex selection, it may be that we should take into account a completely new dimension of the problem. Sex determination in mammals is commonly viewed as a matter of chance, depending on whether an X- or a Y-chromosome-bearing spermatozoon arrives at the ovum first. The new hypothesis does not question the sex-determining role of the spermatozoon; it does, however, query the ‘gets there first’ part of this commonly accepted description of sex determination.

This new perspective comes from sex allocation theory, which in turn arises from evolutionary biology and psychology. It suggests that the sex of the offspring in mammals may not, after all, be a matter of chance. Instead, sex allocation may be a finely tuned adaptation which depends on both the characteristics of the mother and the quality of her immediate environment at the time of conception.

There are at least three major research areas currently pointing in this direction. The first is in sex allocation theory. In many non-mammalian species there is evidence of a high degree of adaptive control of the sex of the offspring. Species with such control include fish (for example Conover and Van Voorhees, 1990Go), birds (for example Komdeur et al., 2002Go; Veiga et al., 2004Go) and insects (Hardy, 2002Go). Although methods of sex determination differ between species, some theorists believe that in principle, to be consistent, mammals too should have some measure of control of the sex of their offspring (Krackow, 1995Go).

Secondly, the chance view of sex allocation is not consistent with known variations in the sex ratio of mammalian offspring. More than 40 major studies (see Hiraiwa-Hasegawa, 1993Go; Brown and Silk, 2002Go; Cameron, 2004Go; Sheldon and West, 2004Go; for reviews) now document statistically significant departures from the usual 100 : 100 sex ratio in mammals in a variety of species and contexts. Although theorists have not yet found a way of interpreting seemingly contradictory findings, almost all the studies cited in their reviews have shown statistically significant atypical offspring sex ratios according to various characteristics of the mother and her environment. The chief of these have been good condition, high status and dominance in the mother, and/or stressful or non-stressful environments.

In humans there is the unexplained puzzle of the normal secondary (birth) sex ratio being 105 : 100 in favour of males, even though recent research has shown that X- and Y-chromosome-bearing spermatozoa are present in equal numbers in human semen (Graffelman et al., 1999Go). This problem is exacerbated by the evidence which supports a much higher primary (conception) sex ratio (Hassold et al., 1983Go).

Thirdly, almost all the evidence concerning dominance and the sex ratio is based on mothers. This is partly because of paternal uncertainty (especially in studies of animals in the wild) but mainly because the maternal effects are so pronounced. Given the vastly greater amount of maternal investment in nurturing mammalian young, both before and after birth, it seems reasonable to consider the possibility of a maternal role in predetermining the sex of offspring.

Arguments from theory and observations, however, are not entirely persuasive. To convince, one needs to be able to describe and demonstrate a proximate mechanism. A current hypothesis runs as follows. In animals, both good condition and high status are positively correlated with the behavioural characteristic dominance which in turn is underpinned in a predictable way by variations in serum testosterone – the more dominant the female, the higher her testosterone levels (Bouissou, 1978Go). Dominance in humans also appears to be underpinned by testosterone (Udry et al., 1995Go; Grant and France, 2001Go). High testosterone levels are thought to be the link between the observed preponderance of dominance behaviours on the one hand and the increased likelihood of conceiving male offspring on the other.

Furthermore, since female (although not male) testosterone rises under chronic stress (Christiansen, 1998Go) there is the possibility that raised testosterone levels could provide the physiological variable which leads to raised sex ratios under conditions of chronic stress in mammals. If so, this would provide a mechanism whereby more males were conceived during stressful periods, thus making up for increased male losses due to male vulnerability (Kraemer, 2000Go) and providing for equal numbers of the sexes at the time of reproductive maturity. Such a system would fulfil the requirements for Fisher’s (1958Go) frequency-dependent sex selection.

A possible mechanism has already been described in general terms (Grant, 1996Go) and is now being explored in detail. The hypothesis is that in each oestrus or menstrual cycle, ova develop in follicles containing either high or low amounts of testosterone in the follicular fluid. Although not yet demonstrated, it is possible that an ovum exposed to high levels of follicular testosterone may emerge already adapted to receive a Y-chromosome bearing spermatozoon and an ovum exposed to low levels of follicular testosterone could be more likely to receive an X-chromosome bearing spermatozoon (Grant and Irwin, 2005Go).


    What if the sex of the infant is not a matter of chance?
 Top
 Abstract
 Introduction
 An evolutionary dimension
 What if the sex...
 Implications for ethics of...
 References
 
In humans, such a system of sex allocation and sex predetermination, under the adaptive control of the mother, could have important implications for the ethics of sex selection. Research shows that dominant females (both human and non-human) conceive significantly more sons. There is also evidence to suggest that males gain a reproductive advantage from being dominant (see, for example, Sadalla et al., 1987Go; Ellis, 1995Go).

Since male testosterone is generated in the testes it is unlikely females could pass on a genetic tendency to high testosterone levels to their sons. Therefore it may be that dominant mothers make up for this by being especially suited, behaviourally, to bringing up male infants. There are more than a dozen studies which demonstrate behavioural differences in mothers’ interactions with their neonates according to the sex of their infants (for a review, see Grant, 1994Go). (These differences occur in the absence of differences in the babies’ behaviours.) Thus it could be that dominant women are specially adapted, both physically and psychologically, for conceiving and raising male infants, and non-dominant women female infants, with these maternal characteristics being of particular importance during the very first weeks and months of life.

The hypothesis is that women conceive male or female infants according to both their genetic predisposition to a particular baseline level of testosterone and the conditions in the environment at the time of conception. In this way, normal fluctuations in testosterone levels could provide the means by which most women conceive both male and female infants. However, women whose testosterone levels lie at one or the other extreme of the normal distribution curve may continue to conceive all male or all female infants in spite of normal fluctuations. Thus there is a strong possibility that at a particular time and in a particular place, a woman is specially suited to conceiving and raising either a male or a female infant.


    Implications for ethics of sex selection
 Top
 Abstract
 Introduction
 An evolutionary dimension
 What if the sex...
 Implications for ethics of...
 References
 
If such predetermination of the sex of the offspring is the result of an evolutionarily stable strategy that has served the human race well over evolutionary time, perhaps we should think some more before trying to override it. What would happen if a woman who was particularly suited to conceiving and raising male infants was instead asked to raise a female infant? At present there is little scientific evidence on what the consequences might be. Anecdotal evidence from adoptions suggests it may not be a good idea, but studies would need to show that the difficulties did not arise from the other factors involved in adoption (Shapiro et al, 2001Go). Parents of single-sex families adopting a child of the opposite sex have found many difficulties, but studies would need to show that the difficulties did not arise from the other factors involved in adoption.

If mothers of boys behave differently to mothers of girls, we need to know more about these differences before allowing people who are particularly suited to raising one sex to try their hand at the other. Thus family balancing may be among the worst reasons for attempting sex selection. Rather, parents who have two, three or more children of one sex and none of the other should regard themselves as being particularly suited to raising that sex and be proud of it.


    References
 Top
 Abstract
 Introduction
 An evolutionary dimension
 What if the sex...
 Implications for ethics of...
 References
 
Allahbadia GN. (2002) The 50 million missing women. J Assist Reprod Genet 19:411–416.[CrossRef][Web of Science][Medline]

Arnold F, Kishor S, Roy TK. (2002) Sex-selective abortions in India. Popul Dev Rev 28:759–785.[CrossRef]

Bouissou MF. (1978) Effects of testosterone propionate on dominance relationships in a group of cows. Horm Behav 11:388–400.[CrossRef][Medline]

Brown GR and Silk JB. (2002) Reconsidering the null hypothesis: is maternal rank associated with birth sex ratios in primate groups? Proc Natl Acad Sci U S A 99:11252–11255.[Abstract/Free Full Text]

Cameron EZ. (2004) Facultative adjustment of mammalian sex ratios in support of the Trivers – Willard hypothesis: evidence for a mechanism. Proc R Soc Lond B Biol Sci 271:1723–1728.[Medline]

Christiansen K. (1998) Behavioural correlates of testosterone. In Nieschlag E and Behre HM (Eds.). Testosterone: Action, Deficiency, Substitution (Springer-Verlag, Heidelberg).

Conover DO and Van Voorhees DA. (1990) Evolution of a balanced sex ratio by frequency-dependent selection in a fish. Science 250:1556–1558.[Abstract/Free Full Text]

Ellis L. (1995) Dominance and reproductive success among nonhuman animals. Ethol Sociobiol 16:257–333.

Fisher RA. (1958) The General Theory of Natural Selection 2nd rev. edn. (Dover, New York).

Graffelman J, Fugger EF, Keyvanfar K, Schulman JD. (1999) Human live birth and sperm-sex ratios compared. Hum Reprod 14:2917–2919.[Abstract/Free Full Text]

Grant VJ. (1994) Sex of infant differences in mother–infant interaction: a reinterpretation of past findings. Dev Rev 14:1–26.

Grant VJ. (1996) Sex determination and the maternal dominance hypothesis. Hum Reprod 11:2371–2375.[Abstract/Free Full Text]

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Grant VJ and Irwin RJ. (2005) Follicular fluid steroid levels and subsequent sex of bovine embryos. J Exp Zool 303A:1120–1125.[CrossRef]

Hardy ICW. (2002) The birds and the wasps: a sex-ratio meta-analysis. Trends Ecol Evol 17:207.

Harris J. (2005) Sex selection and regulated hatred. J Med Ethics 31:291–294.[Abstract/Free Full Text]

Hassold T, Quillen SD, Yamane JA. (1983) Sex ratio in spontaneous abortions. Ann Hum Genet 47:39–47.[Web of Science][Medline]

Hiraiwa-Hasegawa M. (1993) Skewed birth sex ratios in primates: should high-ranking mothers have sons or daughters? Trends Ecol Evol 8:395–400.[CrossRef]

Hudson V and den Boer AM. (2004) Bare Branches: The Security Implications of Asia’s Surplus Male Population (MIT Press, Cambridge, MA.).

Komdeur J, Magrath MJL, Krackow S. (2002) Pre-ovulation control of hatchling sex ratio in the Seychelles warbler. Proc Biol Sci 269:1067–1072.

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Kraemer S. (2000) The fragile male. BMJ 321:1609–1612.[Free Full Text]

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Ramanamma A and Bambawale U. (1980) The mania for sons: an analysis of social values in South Asia. Soc Sci Med 14B:107–110.

Ridley M. (1993) The Red Queen: Sex and the Evolution of Human Nature (Viking Press, London) pp. 122.

Sadalla EK, Kenrick DT, Vershure B. (1987) Dominance and heterosexual attraction. J Pers Soc Psychol 52:730–738.[CrossRef]

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Submitted on December 20, 2005; resubmitted on January 22, 2006; accepted on January 28, 2006.


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