Quantitative and theoretical analyses of the relation between older brothers and homosexuality in men

Meta-analysis of aggregate data from 14 samples representing 10,143 male subjects shows that homosexuality in human males is predicted by higher numbers of older brothers, but not by higher numbers of older sisters, younger brothers, or younger sisters. The relation between number of older brothers and sexual orientation holds only for males. This phenomenon has therefore been called the fraternal birth order effect. Research on birth order, birth weight, and sexual orientation suggests that the developmental pathway to homosexuality initiated by older brothers operates during prenatal life. Calculations assuming a causal relation between older brothers and sexual orientation have estimated the proportion of homosexual men who owe their sexual orientation to fraternal birth order at 15% in one study and 29% in another. The maternal immune hypothesis proposes that the fraternal birth order effect reflects the progressive immunization of some mothers to male-specific antigens by each succeeding male fetus and the increasing effects of such immunization on sexual differentiation of the brain in each succeeding male fetus. There are at least three possible mechanisms by which the mother's immune response could influence the fetus: the transfer of anti-male antibodies across the placenta from the maternal into the fetal compartment, the transfer of maternal cytokines across the placenta, and maternal immune reactions affecting the placenta itself. This hypothesis is consistent with recent studies showing that the quantity of fetal cells that enter the maternal circulation is greater than previously thought, and that the number of male-specific proteins encoded by Y-chromosome genes is greater than previously thought.     

Birth weight, sexual orientation and the sex of preceding siblings.

This study's first objective was to compare the mean birth weights of homosexual and heterosexual men and women. Its second objective was to investigate whether prior male and female fetuses have different effects on the birth weight of subsequent fetuses. The subjects were 3229 adult men and women (the probands), who weighed at least 2500 g at birth, and whose mothers knew the sex of the child (or fetus) for each pregnancy prior to the proband. Information on birth weight, maternal gravidity and other demographic variables was reported on questionnaires completed by the probands' mothers. The results confirmed earlier reports that boys with older brothers weigh less at birth than boys with older sisters, but they did not confirm reports that girls with older brothers weigh less than girls with older sisters. The results did not show across-the-board differences in the mean birth weights of homosexual versus heterosexual women or homosexual versus heterosexual men. However, the homosexual males with older brothers weighed about 170 g less at birth than the heterosexual males with older brothers. It is suggested that this pattern of results may reflect a maternal immune response to Y-linked minor histocompatibility antigens (H-Y antigens). According to this hypothesis, when the maternal immune response is mild, it produces only a slightly reduced birth weight, but when it is stronger, it produces a markedly reduced birth weight as well as an increased probability of homosexuality.     

The association between the fraternal birth order effect in male homosexuality and other markers of human sexual orientation

Later fraternal birth order (FBO) is a well-established correlate of homosexuality in human males and may implicate a maternal immunization response in the feminization of male sexuality. This has led to the suggestion that FBO may relate to other markers of male sexual orientation which are robustly sexually dimorphic. If so, among homosexual males the number of older brothers should strongly correlate with traits such as spatial ability and psychological gender, indicative of greater behavioural feminization, compared to heterosexual males. The present study failed to find significant associations between number of older brothers and these traits.     

Fraternal birth order and birth weight in probably prehomosexual feminine boys

The purpose of this study was to confirm a previous finding that homosexual males with older brothers weigh less at birth than do heterosexual males with older brothers. The subjects comprised 250 feminine boys referred to a child psychiatry service because of extreme cross-gender wishes or behavior and assumed, on the basis of previous research, to be prehomosexual, plus 739 control boys and 261 control girls referred to the same service for reasons unrelated to sexual orientation or gender identity disorder and assumed, from base-rate probabilities, to be preheterosexual. The feminine boys with two or more older brothers weighed 385 g less at birth than did the control boys with two or more older brothers (P = 0.005). In contrast, the feminine and control boys with fewer than two older brothers did not differ in birth weight. This finding suggests that the mechanism by which older brothers increase the odds of homosexuality in later-born males operates prior to the individual's birth. We hypothesize that this mechanism may be immunologic, that antimale antibodies produced by human mothers in response to immunization by male fetuses could decrease the birth weight of subsequent male fetuses as well as increase their odds of homosexuality.     

The cause(s) of the fraternal birth order effect in male homosexuality

It has been established that the probability that a man is homosexual is positively related to his number of older brothers, but not older sisters when the brothers are accounted for. This is known as the 'fraternal birth order' effect. In the past, efforts have been made to explain this phenomenon in terms of several alternative biological hypotheses and a psychosocial hypothesis. This note examines how well these hypotheses accommodate the fraternal birth order effect. It is concluded that: (1) the evidence for the hypothesis of maternal immunoreactivity to the male fetus is weak; (2) the evidence for the intrauterine hormone exposure hypothesis is also weak; (3) the evidence for the hypothesis of postnatal learning is stronger. Lastly, there seem likely to be causes common to male homosexuality and paedophilia. They may include sexual (or quasi-sexual) experience in childhood or adolescence.     

The influence of birth order on birth weight: does the sex of preceding siblings matter?

The purpose of this study was to investigate whether the well-established relationship between parity and birth weight is affected by the sex composition of siblings, especially for male newborns. Subjects were 856 male and 862 female newborns who weighed at least 2500 g at birth, who were born after 37 completed weeks of gestation, who obtained an Apgar score of 7 or higher, who had the same biological parents as all other children in the sibship, and who lived in the same household. Information on birth weight was collected from hospital records. Results showed that male newborns with older brothers weighed less than male newborns with older sisters. In contrast, the weight of female newborns with older brothers did not differ from the weight of female newborns with older sisters. One explanation of these results is that maternal immunoreactivity to some male-specific feature of the fetus affects prenatal development and consequently reduces birth weight in males. The relation between older brothers and birth weight may have theoretical significance for behavioural variables.     

Two hypotheses on the causes of male homosexuality and paedophilia

This note considers two hypotheses on the causes of homosexuality and paedophilia in men, viz. the hypotheses of maternal immunity and of postnatal learning. According to the maternal immune hypothesis, there is progressive immunization of some mothers to male-specific antigens by each succeeding male fetus, and there are concomitantly increasing effects of anti-male antibodies on the sexual differentiation of the brain in each succeeding male fetus. An attempt is made to assess the status of this hypothesis within immunology. Knowledge of the properties of anti-male antibodies is meagre and there has been little direct experimentation on them, let alone on their effects on the developing male fetal brain. Moreover until the relevant antigens are identified, it will not be possible to test mothers of male homosexuals or paedophiles for the presence of such antibodies. Yet until this experimentation has been done, it would seem premature to regard the hypothesis as more than a very provisional explanatory tool. The evidence in relation to the postnatal learning hypothesis is quite different. There is an abundance of data suggesting that male homosexuals and paedophiles report having experienced more sexual abuse (however defined) in childhood (CSA) than do heterosexual controls. The question revolves round the interpretation of these data. Many (though not all) of these studies are correlational and thus subject to the usual qualifications concerning such data. However, there are grounds for supposing that some of the reports are veridical, and there is support from a longitudinal study reporting a small but significant increase in paedophilia in adulthood following CSA. To summarize: most boys who experience CSA do not later develop into homosexuals or paedophiles. However, the available evidence suggests that a few do so as a result of the abuse.     

Birth order and male androphilia in Samoan fa'afafine

The manner in which male androphilia is publicly expressed varies cross-culturally. As such, it is unclear whether distinct or common underlying causal processes characterize male androphilia in different cultures. Establishing the existence of cross-cultural universals in male androphilia is one means of ascertaining whether common biological bases underlie this phenomenon despite its culturally distinct forms. The evidence that the number of older biological brothers increases the odds of androphilia in later-born males has been well documented for Western samples (i.e. the fraternal birth order effect); but there is little evidence for this effect in non-Western samples. Here, we compare the birth order of androphilic males (i.e. fa'afafine) and gynephilic males from the politically autonomous Polynesian nation of Independent Samoa. Results indicate that relative to gynephilic males, fa'afafine tend to have more siblings and are generally later born when birth order is quantified using Slater, fraternal and sororal indices. More specifically, fa'afafine tend to have a greater number of older brothers, older sisters and younger brothers. We discuss the observed effects in relation to the differing reproductive patterns exhibited by the mothers of fa'afafine and gynephilic males, and to existing social and biological theories for sexual orientation.     

Evidence for maternally inherited factors favouring male homosexuality and promoting female fecundity

The Darwinian paradox of male homosexuality in humans is examined, i.e. if male homosexuality has a genetic component and homosexuals reproduce less than heterosexuals, then why is this trait maintained in the population? In a sample of 98 homosexual and 100 heterosexual men and their relatives (a total of over 4600 individuals), we found that female maternal relatives of homosexuals have higher fecundity than female maternal relatives of heterosexuals and that this difference is not found in female paternal relatives. The study confirms previous reports, in particular that homosexuals have more maternal than paternal male homosexual relatives, that homosexual males are more often later-born than first-born and that they have more older brothers than older sisters. We discuss the findings and their implications for current research on male homosexuality.     

Birth order and fluctuating asymmetry: a first look

We investigated the hypothesis that maternal immunoreactivity to male-specific features of the foetus can increase developmental instability. We predicted that the participants' number of older brothers would be positively related to the fluctuating asymmetry of ten bilateral morphological traits. The participants were 40 adult male psychiatric patients and 31 adult male hospital employees. Consistent with the hypothesis, the participants' number of older brothers--but not number of older sisters, younger brothers or younger sisters--was positively associated with fluctuating asymmetry. The patients had significantly larger fluctuating asymmetry scores and tended to have more older brothers than the employees, but the positive relationship between the number of older brothers and fluctuating asymmetry was observed in both groups.     

Sexual orientation, handedness, sex ratio and fetomaternal tolerance-rejection

Fraternal birth order (FBO) appears as a prenatal cause of 15% of homosexual males (gays) through mnemonic maternal anti-male factors. Non-right-handed men seem to be protected from homosexuality. Four hypotheses are proposed: (1) androgenic factors of non-right-handedness neutralize anti-male factors; (2) non-right-handedness and homosexuality are lethal or produce mental impairment; (3) non-right-handed male embryos are insensitive to anti-male factors; (4) mothers of non-right-handed fetuses do not produce anti-male factors. Studies of the sex ratio (SR) of older and younger siblings show: (1) a significant heterogeneity in the SR of siblings of right or non-right handed heterosexual men and women; (2) lesbians are born among siblings with high SR; (3) siblings of right-handed gays show a higher SR than non-right-handed gays that present a low SR. Based on our discovery of maternal tolerance-rejection processes, associated with genetic systems (ABO, Rh), where zygotes or embryos different from their mother induce better pregnancy and maternal tolerance than do those that share antigens with their mothers, I propose a new explanation for sexual relationships, sexual orientation, handedness and sibling SR. Lesbian embryos could induce tolerance from mothers with anti-female factors. Non-right-handedness could induce maternal tolerance, or change the maternal compatibility of "gay" embryos. Alternatively, gay embryos could be poor inducers of maternal tolerance towards male traits.     

Patrilineal family values,family planning and variation in stature among Taiwanese six-year-olds

It has been argued that patrilineal joint family systems tend to bias family planning decisions in favour of sons. A simple model suggests that in such societies, any given son will be more highly valued by his parents (1) the fewer his brothers and (2) the earlier his birth is in the brother series. A daughter's value will be greater (1) the fewer brothers she has and (2) the earlier her birth is relative to other sisters. This study first addresses the extent of son preference as inferred from family composition data for 772 Taiwanese first-graders born in the mid-1970s in two socioeconomically distinct communities in Taipei, Taiwan. It then uses linear regression to consider whether the model criteria help account for statural variation among children in each study area when controlling for differences in measurement age, parental education and housing. With respect to family composition and gender preference, available evidence was consistent with previous surveys. While better-educated parents in the more affluent study area had significantly fewer children (p < 0.0005) and were more willing to stop without a son, girls there, as in the less affluent area, were still significantly more likely than boys to belong to large sibships (p < or = 0.005). Evidence from mean height of males and females partially accords with hypothetical predictions. In the less affluent area, the interaction effect of male birth order and the presence of younger siblings was significantly associated with mean stature (p = 0.002). Males without brothers were 2.0 cm taller than males with either an older or a younger brother (116.3 +/- 0.5 cm vs 114.3 +/- 0.4 cm). Males who had both younger and older brothers, but often no sisters, were about as tall, however, as those without brothers. A similar, but less pronounced, pattern was found among males in the more affluent area, but only among those who had sisters. These boys were also consistently shorter than boys without sisters (115.6 +/- 0.6 cm vs 117.7 +/- 0.6 cm; p = 0.001). Patterns of mean female stature did not clearly support the hypothesis. Girls in the more affluent area were relatively tall and did not show significant variation. Results among less affluent girls showed significant contrasts, but not necessarily in the predicted direction.     

Rank relations of juvenile and subadult natal males of Barbary macaques (Macaca sylvanus) at Affenberg Salem

Rank relations of more than 100 juvenile and subadult natal Barbary macaque males were analyzed. Hierarchical relations among individuals of the same age were established early during the first year of life. With few exceptions concerning infants from very high-ranking genealogies, males dominated female peers regardless of maternal rank. Males started to outrank females from older cohorts during the second year of life and completed the process of rank reversal with adult females at 5-6 years of age. An age-graded dominance pattern existed among males from different birth cohorts. Only 3 rank reversals between males from different cohorts were observed. Rank reversals among males of the same birth cohort occurred more frequently. Rank position of a male among his male peers was influenced by birth order, by maternal rank, and by the presence of juvenile brothers. Most males without juvenile brothers had low positions, regardless of maternal rank. Males born late in the birth season were also low-ranking, even when juvenile brothers were present. There was no cohort where ranking among males was determined by maternal rank alone, as is the case in rhesus monkeys and Japanese macaques. Adult/subadult male carriers had no noticeable effect on rank positions of 'their' infants. It is suggested that a weaker influence of Barbary macaque mothers on rank of their sons is related to very early integration of male infants in male social/play groups.     

Sexual dichronism and intersexual phoresy in gall-forming coccoids

Summary Coccoid gall-formers from the genus Cystococcus exhibit sexual dichronism, producing the males of a brood well before their sisters. This ensures the coexistence in the maternal gall of winged adult males and their first instar wingless sisters. Females disperse by clinging to the attenuate abdomens of their brothers, and the efficiency of this dispersal is reflected in an even dispersion on host trees. Evolution of this form of phoresy may be associated with the paternal genome loss prevalent in the Coccoidea.     

Fecundity of Paternal and Maternal Non-Parental Female Relatives of Homosexual and Heterosexual Men

A variety of social, developmental, biological and genetic factors influence sexual orientation in males. Thus, several hypotheses have attempted to explain the sustenance of genetic factors that influence male homosexuality, despite decreased fecundity within the homosexuals. Kin selection, the existence of maternal effects and two forms of balancing selection, sexually antagonistic selection and overdominance, have been proposed as compensatory mechanisms for reduced homosexual fecundity. Here, we suggest that the empirical support for kin selection and maternal effects cannot account for the low universal frequency and stability of the distribution of homosexuals. To identify the responsible compensatory mechanism, we analyzed fecundity in 2,100 European female relatives, i.e., aunts and grandmothers, of either homosexual or heterosexual probands who were matched in terms of age, culture and sampling strategy. Female relatives were chosen to avoid the sampling bias of the fraternal birth order effect, which occurs when indirectly sampling mothers though their homosexual sons. We observed that the maternal aunts and grandmothers of homosexual probands were significantly more fecund compared with the maternal aunts and maternal grandmothers of the heterosexual probands. No difference in fecundity was observed in the paternal female lines (grandmothers or aunts) from either of the two proband groups. Moreover, due to the selective increase in maternal female fecundity, the total female fecundity was significantly higher in homosexual than heterosexual probands, thus compensating for the reduced fecundity of homosexuals. Altogether, these data support an X-linked multi-locus sexually antagonistic hypothesis rather than an autosomal multi-locus overdominance hypothesis.     

Review lecture. Immunology of H-Y antigen and its role in sex determination

H-Y was originally discovered as a transplantation antigen that caused female mice of certain inbred strains to reject skin from otherwise identical males. The ability to make the skin graft rejection response and, in vitro, cytotoxic T cell responses against H-Y is controlled by genes within the major histocompatibility complex, H-2, and by non-H-2 genes. H-Y belongs to a class of weak transplantation antigens characterized by an inability to elicit responses under many conditions. Although genetic factors are very important in determining responsiveness, their action can be modified by immunization procedures. H-Y has been proposed as the differentiation signal that causes the formation of the testes from the undifferentiated gonad in the developing embryo. This hypothesis has been explored by using a series of mice whose karyotype and phenotypic sex are paradoxical.     

H-Y Antigen Expression in Temperature Sex-Reversed Turtles (Emys orbicularis)

H-Y antigen has been used as a marker for the heterogametic sex and is assumed to be an organizing factor for the heterogametic gonad. In the turtle Emys orbicularis , H-Y antigen is restricted to the female cells, indicating a female heterogamety (ZZ/ZW) sex-determining mechanism. Moreover, the sexual differentiation of the gonads is temperature sensitive, and complete sex reversal can be obtained at will. In this framework the relationships between H-Y antigen, temperature, and gonadal phenotype were studied. Mouse H-Y antiserum was absorbed with blood and gonadal cells of control wild male and female adults, and with blood and gonadal cells from three lots of young turtles from eggs incubated at 25–26°C (100% phenotypic males), at 30–30.5°C (100% phenotypic females), or at 28.5–29°C (majority of females with some males and intersexes). The residual activity of H-Y antiserum was then estimated using an immunobacterial rosette technique. In adults, both blood cells and gonadal cells were typed as H-Y negative in males and as H-Y positive in females. In each of the three lots of young, blood cells were H-Y negative in some individuals and H-Y positive in others. The proposed interpretation is that the H-Y negative individuals were genotypic males (ZZ) and the H-Y positive were genotypic females (ZW). The gonads of these animals were then pooled in different sets according to their sexual phenotype and to the presumed genotypic sex (i.e., blood H-Y phenotype). Testicular cells were typed as H-Y negative in genotypic males as well as in the presumed sex-reversed genotypic females; likewise, ovarian cells were typed as H-Y positive in genotypic females as well as in the presumed sex-reversed genotypic males. These results provide additional evidence that H-Y antigen expression is closely associated with ovarian structure in vertebrates displaying a ZZ/ZW sex-determining mechanism.     

Correlation between the number of sex chromosomes and the H-Y antigen titer

Summary H-Y antigen was studied serologically on blood cells and cultured fibroblasts of patients with numerical aberrations of the sex chromosomes. As compared with normal males, patients with the karyotypes 48,XXXY and 49,XXXXY have reduced H-Y antigen titrs; a tendency toward reduced titers can also be detected in the 47,XXY Klinefelter syndrome. The existence of an intermediary titer was further substantiated by a quantitative absorption test applied to cells with the 49,XXXXY karyotype. It appears that in the presence of one Y chromosome, the H-Y antigen titer decreases with an increasing number of X chromosomes. In contrast, the H-Y antigen titer is increased if, at a given number of X chromosomes, the number of Y chromosomes is increased, as in the 47,XYY male. Consequently, patients with 48,XXYY chromosomes are in the male control range. The findings are interpreted under the hypothesis of a controlling or modifying influence of the sex chromosomes on the titer of H-Y antigen.     

Interaction of fraternal birth order and handedness in the development of male homosexuality

The present study investigated evidence for an interaction between two of the best established etiologic factors, or markers of etiologic factors, in the literature on male homosexuality: fraternal birth order and hand preference. By combining five samples, the authors produced study groups of 1774 right-handed heterosexuals, 287 non-right-handed heterosexuals, 928 right-handed homosexuals, and 157 non-right-handed homosexuals. The results showed a significant (P = 0.004) handedness by older brothers interaction, such that (a) the typical positive correlation between homosexuality and greater numbers of older brothers holds only for right-handed males, (b) among men with no older brothers, homosexuals are more likely to be non-right-handed than heterosexuals; among men with one or more older brothers, homosexuals are less likely to be non-right-handed than heterosexuals, and (c) the odds of homosexuality are higher for men who have a non-right hand preference or who have older brothers, relative to men with neither of these features, but the odds for men with both features are similar to the odds for men with neither. These findings have at least two possible explanations: (a) the etiologic factors associated with non-right-handedness and older brothers-hypothesized to be hyperandrogenization and anti-male antibodies, respectively-counteract each other, yielding the functional equivalent of typical masculinization, and (b) the number of non-right-handed homosexuals with older brothers is smaller than expected because the combination of the older brothers factor with the non-right-handedness factor is toxic enough to lower the probability that the affected fetus will survive.     

Immunodominance in the T cell response to multiple non-H-2 histocompatibility antigens. III. Single histocompatibility antigens dominate the male antigen

Immunization of mice with multiple non-H-2 histocompatibility antigens results in the generation of cytolytic T lymphocytes that are specific for a limited number of immunodominant antigens. The experiments presented in this communication were designed to reveal immunodominance in pairwise combinations of autosomal and sex-linked non-H-2 histocompatibility (H) antigens. Priming and boosting responders with the male antigen, H-Y, paired with the H-4.2, H-7.1, or H-3.1 antigens, resulted in the generation of cytolytic T cells specific for the autosomal H antigens but not the H-Y antigen. Furthermore, co-immunization and boosting of C57BL/6 female responder spleen cells with BALB.B male cells resulted in the generation of cytolytic T cells specific for the BALB.B immunodominant antigens but not H-Y. No dominance was observed in H-4-plus H-7-incompatible combinations. Co-immunization of three different H-3 congenic strains with H-3.1 plus H-Y demonstrated that an efficient anti-H-3.1 T cell response is required for observing H-3.1 immunodominance over H-Y. Co-expression of H-3.1 and H-Y on the same priming and boosting cells was required for immunodominance. In fact, immunization with H-3.1 and H-Y presented on different cells resulted in normal generation of H-Y-specific cytolytic T cells, but no generation of H-3.1-specific cytolytic T cells resulted unless H-Y-specific cells were stimulated in the mixed lymphocyte cultures. These observations suggest that in vitro T cell responses to paired, non-H-2 H antigens may be independent, competitive, or synergistic, depending on the identity of the antigens and the priming and boosting conditions.