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 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.     

Fraternal birth order and the maternal immune hypothesis of male homosexuality

In men, sexual orientation correlates with an individual's number of older brothers, each additional older brother increasing the odds of homosexuality by approximately 33%. It has been hypothesized that this fraternal birth order effect reflects the progressive immunization of some mothers to Y-linked minor histocompatibility antigens (H-Y antigens) by each succeeding male fetus and the concomitantly increasing effects of such maternal immunization on the future sexual orientation of each succeeding male fetus. According to this hypothesis, anti-H-Y antibodies produced by the mother pass through the placental barrier to the fetus and affect aspects of sexual differentiation in the fetal brain. This explanation is consistent with a variety of evidence, including the apparent irrelevance of older sisters to the sexual orientation of later born males, the probable involvement of H-Y antigen in the development of sex-typical traits, and the detrimental effects of immunization of female mice to H-Y antigen on the reproductive performance of subsequent male offspring. The maternal immune hypothesis might also explain the recent finding that heterosexual males with older brothers weigh less at birth than heterosexual males with older sisters and homosexual males with older brothers weigh even less than heterosexual males with older brothers.     

Is male homosexuality maintained via kin selection?

We tested the kin selection hypothesis of male homosexuality using questionnaire data in a community sample of homosexual and heterosexual men. Homosexual men were no more likely than heterosexual men to channel resources toward family members. Indeed, heterosexual men tended to give more financial resources to siblings than homosexual men. Furthermore, homosexual men were somewhat more estranged from family members, especially from fathers and oldest siblings.     

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.     

Sequence variation in the androgen receptor gene is not a common determinant of male sexual orientation.

To test the hypothesis that DNA sequence variation in the androgen receptor gene plays a causal role in the development of male sexual orientation, we have (1) measured the degree of concordance of androgen receptor alleles in 36 pairs of homosexual brothers, (2) compared the lengths of polyglutamine and polyglycine tracts in the amino-terminal domain of the androgen receptor in a sample of 197 homosexual males and 213 unselected subjects, and (3) screened the the entire androgen receptor coding region for sequence variation by PCR and denaturing gradient-gel electrophoresis (DGGE) and/or single-strand conformation polymorphism analysis in 20 homosexual males with homosexual or bisexual brothers and one homosexual male with no homosexual brothers, and screened the amino-terminal domain of the receptor for sequence variation in an additional 44 homosexual males, 37 of whom had one or more first- or second-degree male relatives who were either homosexual or bisexual. These analyses show that (1) homosexual brothers are as likely to be discordant as concordant for androgen receptor alleles; (2) there are no large-scale differences between the distributions of polyglycine or polyglutamine tract lengths in the homosexual and control groups; and (3) coding region sequence variation is not commonly found within the androgen receptor gene of homosexual men. The DGGE screen identified two rare amino acid substitutions, ser205-to-arg and glu793-to-asp, the biological significance of which is unknown.     

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.     

Homosexual incest avoidance among females in captive Japanese macaques

This paper reports a systematic pattern of homosexual incest avoidance among females in a captive group of Japanese macaques (Macaca fuscata) culled from the Arashiyama-West troop known for its high rates of female homosexuality. The study group included three matrilines and two generations. Between eight and 11 females were sexually active over four consecutive mating seasons, and all engaged in both heterosexual and homosexual activity. While all females performed homosexual acts with almost all possible non-kin partners, they systematically avoided homosexual interactions with their mother, daughters, and sisters. This pattern could not be explained either in terms of kin not being simultaneously in estrus, kin avoiding affiliative interactions in general, or non-kin utilizing the tension-reducing effect of estrus to affiliate exclusively with each other. In contrast to homosexual females, heterosexual pairs of relatives (brother-sister, mother-son) were sometimes incestuous. Assuming that female homosexuality expresses the reproductive strategy of females unconstrained by male influence, the present results point to the strong tendency of females to avoid incest and suggest that males are primarily responsible for the reported exceptions to incest avoidance.     

Perceived Sexual Orientation Based on Vocal and Facial Stimuli Is Linked to Self-Rated Sexual Orientation in Czech Men

Previous research has shown that lay people can accurately assess male sexual orientation based on limited information, such as face, voice, or behavioral display. Gender-atypical traits are thought to serve as cues to sexual orientation. We investigated the presumed mechanisms of sexual orientation attribution using a standardized set of facial and vocal stimuli of Czech men. Both types of stimuli were rated for sexual orientation and masculinity-femininity by non-student heterosexual women and homosexual men. Our data showed that by evaluating vocal stimuli both women and homosexual men can judge sexual orientation of the target men in agreement with their self-reported sexual orientation. Nevertheless, only homosexual men accurately attributed sexual orientation of the two groups from facial images. Interestingly, facial images of homosexual targets were rated as more masculine than heterosexual targets. This indicates that attributions of sexual orientation are affected by stereotyped association between femininity and male homosexuality; however, reliance on such cues can lead to frequent misjudgments as was the case with the female raters. Although our study is based on a community sample recruited in a non-English speaking country, the results are generally consistent with the previous research and thus corroborate the validity of sexual orientation attributions.     

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.     

Possible Balancing Selection in Human Female Homosexuality

A growing number of researchers suggest that female homosexuality is at least in part influenced by genetic factors. Unlike for male homosexuality, few familial studies have attempted to explore maintenance of this apparently fitness-detrimental trait in the population. Using multiple recruitment methods, we explored fecundity and sexual orientation within the pedigrees of 1,458 adult female respondents. We compared 487 homosexual and 163 bisexual with 808 heterosexual females and 30,203 of their relatives. Our data suggest that the direct fitness of homosexual females is four times lower than the direct fitness of heterosexual females of corresponding ages. The prevalence of nonheterosexuality within the homosexual female respondents’ families (2.83%) appear to be more than four times higher than the basal prevalence in the Italian population (0.63%). Pedigree size and relative fecundity in both the paternal and maternal sides of the homosexual women’s families were significantly higher than in the heterosexuals’ families. If confirmed, the relative average fecundity increase within the family seems to offset the loss in fitness due to the low direct fitness of homosexual females. Therefore, the balanced fecundity in the homosexual females’ families may allow the trait to be maintained at a low-frequency equilibrium in the population.     

Intestinal parasitic infections in homosexual men: prevalence,symptoms and factors in transmission.

In a controlled study 67.5% of 200 homosexual men but only 16% of 100 heterosexual men were found to be infected with intestinal parasites. Entamoeba histolytica was isolated from 27% of the homosexual and 1% of the heterosexual men, and Giardia lamblia was isolated from 13% of the homosexual and 3% of the heterosexual men. The presence of symptoms could not be correlated with infection except when the infection was caused by more than one organism, including G. lamblia. Symptoms were much more common in both infected and uninfected homosexuals than in heterosexuals. Among the homosexual men recent foreign travel, living in a homosexual household and promiscuity were not correlated with intestinal parasitic infection, but cleansing of the anus before and sex was associated with a significantly lower prevalence of infection. These findings suggest that the male homosexual community may be an important reservoir of potentially pathogenic protozoa.     

A new group-selection model for the evolution of homosexuality

Abstract. Scientists have long puzzled over how homosexual orientation has evolved, given the assumed low relative fitness of homosexual individuals compared to heterosexual individuals. A number of theoretical models for the evolution of homosexuality have been postulated including balance polymorphism, "Fertile females", hypervariability of DNA sequences, kin selection, and "parental manipulation". In this paper, I propose a new group-selection model for the evolution of homosexuality which offers two advantages over existing models: (1) its non-assumption of genetic determinism, and (2) its lack of dependency on an inefficient altruism relation and family dynamics theory.     

Endocrine Function in Male and Female Homosexuals

Serial assays of hormones and their metabolites are reported in the urine of three male and four female homosexuals. Urinary testosterone levels were abnormally low in the two men who practised exclusive homosexuality and were within the normal range in the third, who had both homosexual and heterosexual relationships. In the women assays were generally performed throughout one menstrual cycle; in three the pattern of hormone excretion was ovulatory in character, while in the fourth evidence for ovulation was equivocal. Levels of testosterone and luteinizing hormone (L.H.) were raised in the female homosexuals, while those for oestrogens, particularly oestrone, were below the range for normal heterosexual subjects during their reproductive life; readings of follicle-stimulating hormone (F.S.H.) and pregnanediol were normal in three women. The data reported here are in keeping with the view that abnormalities in endocrine function may occur in both male and female homosexuals.     

Sexually antagonistic selection in human male homosexuality

Several lines of evidence indicate the existence of genetic factors influencing male homosexuality and bisexuality. In spite of its relatively low frequency, the stable permanence in all human populations of this apparently detrimental trait constitutes a puzzling 'Darwinian paradox'. Furthermore, several studies have pointed out relevant asymmetries in the distribution of both male homosexuality and of female fecundity in the parental lines of homosexual vs. heterosexual males. A number of hypotheses have attempted to give an evolutionary explanation for the long-standing persistence of this trait, and for its asymmetric distribution in family lines; however a satisfactory understanding of the population genetics of male homosexuality is lacking at present. We perform a systematic mathematical analysis of the propagation and equilibrium of the putative genetic factors for male homosexuality in the population, based on the selection equation for one or two diallelic loci and Bayesian statistics for pedigree investigation. We show that only the two-locus genetic model with at least one locus on the X chromosome, and in which gene expression is sexually antagonistic (increasing female fitness but decreasing male fitness), accounts for all known empirical data. Our results help clarify the basic evolutionary dynamics of male homosexuality, establishing this as a clearly ascertained sexually antagonistic human trait.     

The effect of luteinizing hormone releasing hormone (LRH) on pituitary gonadotropins in male homosexuals.

Basal serum LH and FSH values were found to be within normal limits in 9 homosexual men. The mean LH and FSH responses following the intravenous administration of 100 microgram of LRH were not significantly different from that of heterosexual controls. In addition, the mean basal plasma serum testosterone was similar in the two groups. There is thus no definite implication of endocrine factors in the genesis of male homosexuality.     

Evidence against a relationship between dermatoglyphic asymmetry and male sexual orientation

Hall and Kimura (1994) studied the relation between dermatoglyphic asymmetry and male sexual orientation in a sample of 66 homosexual and 182 heterosexual men. They found that more homosexual men possessed a leftward dermatoglyphic asymmetry than did heterosexual men. In this paper, we report a comparative study about the relationship between sexual orientation and dermatoglyphic characteristics, including 60 homosexual men, 76 heterosexual men, and 60 heterosexual women, recruited from the general population, and also from a gay-rights nongovernmental organization, in Salvador, Brazil. Ulnar loops were the most frequent dermatoglyphic pattern in all groups, followed by whorls, arches, and radial loops. A chi-square analysis comparing the frequencies of the patterns in the three groups only showed an excess of ulnar loops in women (p < 0.05) and arches in men (p < 0.01), but did not reveal significant differences between homosexuals and the other groups studied. There was no significant difference between gay and straight men on total ridge count. We found a preponderance of rightward asymmetry in homosexual and heterosexual men, as well as in heterosexual women. Our results do not agree with Hall and Kimura's data indicating that more gay men possessed the minority leftward asymmetry than did straight men. There was no significant difference in leftward asymmetry in the sample studied. The results reported in this paper do not support any relation between dermatoglyphic asymmetry and male sexual orientation, and, thus, any hypothesis concerning a biological intrauterine contribution to adult sexual orientation somehow associated with dermatoglyphic development.     

Face perception is modulated by sexual preference

Face perception is mediated by a distributed neural system in the human brain . The response to faces is modulated by cognitive factors such as attention, visual imagery, and emotion ; however, the effects of gender and sexual orientation are currently unknown. We used fMRI to test whether subjects would respond more to their sexually preferred faces and predicted such modulation in the reward circuitry. Forty heterosexual and homosexual men and women viewed photographs of male and female faces and assessed facial attractiveness. Regardless of their gender and sexual orientation, all subjects similarly rated the attractiveness of both male and female faces. Within multiple, bilateral face-selective regions in the visual cortex, limbic system, and prefrontal cortex, similar patterns of activation were found in all subjects in response to both male and female faces. Consistent with our hypothesis, we found a significant interaction between stimulus gender and the sexual preference of the subject in the thalamus and medial orbitofrontal cortex, where heterosexual men and homosexual women responded more to female faces and heterosexual women and homosexual men responded more to male faces. Our findings suggest that sexual preference modulates face-evoked activation in the reward circuitry.     

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.     

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.