Andrea Camperio Ciani

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 adaptive value of personality differences revealed by small island population dynamics

Whether differences in personality among populations really exist and, if so, whether they are only due to cultural and linguistic differences or have a genetically selected adaptive value, is a controversial issue. In this research, we compared three Italian populations living on three small archipelagos in the Tyrrhenian Sea (n = 993), with their corresponding neighbouring mainlanders (n = 598), i.e. sharing the same geographical origin, culture and language. We used an adjective‐based Big Five questionnaire in order to measure personality traits in four categories of individuals for each archipelago/mainland population: (1) original islanders; (2) non‐original islanders; (3) mainlanders and (4) immigrants to the islands. We further analysed original and non‐original islanders who had or had not emigrated from the islands. We found that islanders had different personality traits from mainlanders, the former being more conscientious and emotionally stable and less extraverted and open to experience. We also found that the subgroup of islanders whose ancestors had inhabited their island for about 20 generations in isolation (original islanders, n = 624) were less extraverted and open to experience than immigrants (n = 193). In contrast, immigrants retained the typical personality profile of the mainland populations. Lastly, emigrants from the islands (n = 209) were significantly more extraverted and open to experience than original and non‐original islanders who had never left their island (n = 741). We hypothesise that population differences in extraversion and openness to experience are more probably related to genetic differences which evolved rapidly, presumably through an active gene flow produced by selective emigration from the islands. Copyright

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.

Factors associated with higher fecundity in female maternal relatives of homosexual men.

INTRODUCTION Recent evidence suggests that sexually antagonistic genetic factors in the maternal line promote homosexuality in men and fecundity in female relatives. However, it is not clear if and how these genetic factors are phenotypically expressed to simultaneously induce homosexuality in men and increased fecundity in their mothers and maternal aunts. AIMS The aim of the present study was to investigate the phenotypic expression of genetic factors that could explain increased fecundity in the putative female carriers. METHODS Using a questionnaire-based approach, which included also the Big Five Questionnaire personality inventory based on the Big Five theory, we investigated fecundity in 161 female European subjects and scrutinized possible influences, including physiological, behavioral, and personality factors. We compared 61 female probands who were either mothers or maternal aunts of homosexual men. One hundred females who were mothers or aunts of heterosexual men were used as controls. MAIN OUTCOME MEASURES Personality traits, retrospective physiological and clinical data, behavior and opinions on fecundity-related issues were assessed and analyzed to illustrate possible effects on fecundity between probands and control females. RESULTS Our analysis showed that both mothers and maternal aunts of homosexual men show increased fecundity compared with corresponding maternal female relatives of heterosexual men. A two-step statistical analysis, which was based on t-tests and multiple logistic regression analysis, showed that mothers and maternal aunts of homosexual men (i) had fewer gynecological disorders; (ii) had fewer complicated pregnancies; (iii) had less interest in having children; (iv) placed less emphasis on romantic love within couples; (v) placed less importance on their social life; (vi) showed reduced family stability; (vii) were more extraverted; and (viii) had divorced or separated from their spouses more frequently. CONCLUSIONS Our findings are based on a small sample and would benefit from a larger replication, however they suggest that if sexually antagonistic genetic factors that induce homosexuality in males exist, the factors might be maintained in the population by contributing to increased fecundity greater reproductive health, extraversion, and a generally relaxed attitude toward family and social values in females of the maternal line of homosexual men.

Reaching and grasping behavior in Macaca fascicularis: a kinematic study

The prehensile hand is one of the major traits distinguishing primates from other mammal species. All primates, in fact, are able to grasp an object and hold it in part or entirely using a single hand. Although there is a wealth of behavioral data regarding grasping movements in humans and apes, there is relatively little material on macaques, the animal model often used to investigate neuronal mechanisms responsible for grip control in humans. To date, evidence regarding free-ranging macaques is confined to observational data, while quantitative reports describe studies carried out in laboratory settings or in captivity. The purpose of the present study was to provide the first kinematic descriptions of basic grip behavior with regard to precision and power grips in free-ranging macaque monkeys. Video footage of those animals grasping objects was analyzed frame-by-frame using digitalization techniques. The results revealed that the two types of grips considered are each characterized by specific kinematic signatures. It was also found that hand kinematics was scaled depending on the type of grasp needing to be adopted and the intrinsic properties of the object to be grasped. In accordance with data concerning humans, these findings indicate that the intrinsic features of an object affect the planning and control of reach-to-grasp movements even in free-ranging macaques. The data presented here take research in the field of comparative reach-to-grasp kinematics in human and non-human primates another step forward as they are based on precise measurements of spontaneous grasping movements by animals living/acting in their natural environment.

Gene flow by selective emigration as a possible cause for personality differences between small islands and mainland populations.

Whether personality differences exist between populations is a controversial question. Even though such differences can be measured, it is still not clear whether they are due to individual phenotypic responses to the environment or whether they have a genetic influence. In a population survey we compared the personality traits of inhabitants of an Italian archipelago (the three Egadi islands; N = 622) with those of the closest mainland population (Trapani area; N = 106) and we found that personality differences between small populations can be detected. Islanders scored significantly lower on the personality traits of openness to experience and extraversion and higher on conscientiousness. We suggest that these personality trait differences could be an adaptive response to a confined socio–environmental niche, genetically produced by a strong, non–random gene flow in the last 20–25 generations, rather than the flexible response of islanders to environmental variables. To test this hypothesis, we compared subsets of the islander population classified by ancestry, birthplace, immigration and emigration and found that differences in extraversion can be accounted for by gene flow, while openness to experience and conscientiousness can also be accounted for by some gene–environment interactions. We propose a Personality Gene Flow hypothesis suggesting that, in small isolated communities, whenever there is strong, non–random emigration, paired with weak and random immigration, we can expect rapid genetic personality change within the population. Copyright

Societal Norms Rather Than Sexual Orientation Influence Kin Altruism and Avuncularity in Tribal Urak-Lawoi, Italian, and Spanish Adult Males

Homosexual males could balance their low fitness by increasing benefits to relatives either through kin-directed altruism or by avuncularity (altruistic behavior toward the children of siblings). Evidence in support of kin selection and avuncularity includes the fact that homosexuals seem to be more empathic and altruistic than heterosexuals. Other studies have not confirmed behaviors that increase kin altruism in homosexuals. We explored altruistic behavior and avuncularity in a sample of 278 subjects, either homosexual or heterosexual, from three populations: Italian, Spanish, and Urak-Lawoi, a Southeast Asian tribal population. Among the Urak-Lawoi, the kathoeys, androphilic men who dress and behave as women, were compared with heterosexuals. All populations were rated for societal norms on the expression of affiliative behavior. No greater kin altruism or avuncularity among the kathoeys or in homosexuals in either Mediterranean population was found. Greater avuncularity and kin-directed altruism, independent of sexual orientation, were found among the Urak-Lawoi, and these traits were the least prevalent among the Italians, corresponding to different societal norms. The increase in kin altruism and avuncularity was associated in all males with societal differences and norms on general altruism toward nonkin children, suggesting it is not an adaptive design to maintain homosexuality in humans.

Human Homosexuality: A Paradigmatic Arena for Sexually Antagonistic Selection?

Sexual conflict likely plays a crucial role in the origin and maintenance of homosexuality in our species. Although environmental factors are known to affect human homosexual (HS) preference, sibling concordances and population patterns related to HS indicate that genetic components are also influencing this trait in humans. We argue that multilocus, partially X-linked genetic factors undergoing sexually antagonistic selection that promote maternal female fecundity at the cost of occasional male offspring homosexuality are the best candidates capable of explaining the frequency, familial clustering, and pedigree asymmetries observed in HS male proband families. This establishes male HS as a paradigmatic example of sexual conflict in human biology. HS in females, on the other hand, is currently a more elusive phenomenon from both the empirical and theoretical standpoints because of its fluidity and marked environmental influence. Genetic and epigenetic mechanisms, the latter involving sexually antagonistic components, have been hypothesized for the propagation and maintenance of female HS in the population. However, further data are needed to truly clarify the evolutionary dynamics of this trait.

Implicit Measurements of Sexual Preference in Self‐Declared Heterosexual Men: A Pilot Study on the Rate of Androphilia in Italy

INTRODUCTION An unambiguous measurement of the rate of nonheterosexuality in the male population (male bisexuality and homosexuality) is essential to estimate the health risks associated with same-sex sexual behavior and to scale social and health programs for these citizens. However, self-reported questionnaires on explicit measures of sexual orientation yield significant underestimations of nonheterosexuality. A necessary prerequisite for nonheterosexual preference is androphilia (sexual-erotic attraction to males), which can be explored through psychological tests. AIMS This study, using a pilot sample, investigates the possibility to inventory the frequency of male androphilia in the general population through a sexual preference implicit association test (sp-IAT). This test is a classical IAT that is based on an association of pictures and words and is easily portable. METHODS First we conducted a preliminary validation of the specific IAT protocol on 24 control subjects; then, we examined a sample of 150 adult males in Italy as a pilot study. The subjects responded to the sp-IAT and completed the explicit Kinsey scale questionnaire. MAIN OUTCOME MEASURES Kinsey scale scores and D value of sp-IAT for both preliminary and pilot sample. RESULTS On the explicit Kinsey scale, 2.7% of the sample declared themselves to be sexually attracted to men, corresponding to previous explicit samplings of the Italian homosexual male population. However, the sp-IAT identified that 11.3% of self-declared gynephilic heterosexuals showed a moderate to strong androphilia with a significant effect size (D) always below -0.2, and another 5.6% of the heterosexual sample showed no preference for females (D between -0.2 and 0). CONCLUSION The Kinsey questionnaire strongly dichotomized the responses as either attracted to females or attracted to men, whereas the sp-IAT showed a wider distribution of responses from gynephilia to androphilia. In conclusion, the sp-IAT could be a novel and unambiguous instrument useful to ascertain androphilia population prevalence as a proxy for possible male nonheterosexuality. Camperio Ciani A and Battaglia U. Implicit measurements of sexual preference in self-declared heterosexual men: A pilot study on the rate of androphilia in Italy. J Sex Med 2014;11:2207-2217.

The Dopamine D4 Receptor (DRD4) Exon 3 VNTR Contributes to Adaptive Personality Differences in an Italian Small Island Population

The search for evolutionary forces shaping the diversity of human personality traits encouraged studies that have found that islanders are relatively closed and introverted, with little interest in the external world. The ‘personality gene flow’ hypothesis was proposed to explain the mechanism underlying this difference, suggesting that the frequency of alleles that influence islander personality traits might progressively increase in the gene pools on islands because of selective emigration of individuals not displaying these alleles. We genotyped 96 individuals from the Italian mainland and 117 from Giglio Island, whose residents were previously assessed regarding their personality traits. We genotyped three polymorphisms: the dopamine D4 receptor (DRD4) exon 3 repeat region, the serotonin–transporter SLC6A4 5–HTTLPR indel and the dopamine transporter SLC6A3 DAT1 3′UTR repeat region. Only the DRD4 exon 3 repeat was hypothesised to show varying allele frequencies because this polymorphism could be associated with human migration and personality traits such as extraversion, openness and novelty seeking. As predicted, no differences in allele frequencies were found for the SLC6A4 and SLC6A3 polymorphisms, whereas significant differences were observed in the frequency of the DRD4 exon 3 alleles. The DRD4.2 repeat was more common in mainlanders, as expected, whereas the DRD4.7 allele was over–represented among islanders who never emigrated. This last result contradicts the suggested association of this allele with long–distance migrations. We suggest that emigration might have caused gene flow out the island that resulted in somewhat unpredictable changes in the frequencies of specific alleles, thus influencing islander personality traits. Copyright