Why Same-Sex Orientation Persists: A New Map of Genes, Development and Culture

Same-sex attraction has puzzled evolutionary biologists for decades: if sexual orientation partly shapes reproductive output, why do androphilic men and gynephilic women recur in every culture and historical period rather than being trimmed away by selection? A conceptual analysis published in Frontiers in Psychology by Andrea S. Camperio Ciani of the University of Padua argues that the paradox dissolves only when the question is split into distinct but interacting levels: genetic architecture, evolutionary maintenance, developmental assembly, motivational organization, and socioecological context. The paper, a targeted narrative synthesis rather than a systematic review, proposes that same-sex orientation is best understood as a plural, phenotype-specific phenomenon in which no single mechanism explains persistence across sexes or populations.

The framework’s central move is to treat these explanatory levels as analytical tools rather than isolated causes. Following Tinbergen’s classic distinction between ultimate and proximate questions, the analysis separates why a trait persists in populations from how it is assembled in individuals, while insisting that development generates the variation on which selection acts and evolutionary history constrains developmental systems. Genetic, hormonal, neural, behavioral, and cultural influences are therefore modeled as interacting components of a developmental system, not as separable additive factors. Crucially, the author introduces the concept of a motivational architecture: an emergent, progressively stabilized organization of attraction-related dispositions that links developmental processes to relatively stable adult orientation and to context-sensitive behavior and identity. Canalization, in this view, means relative stabilization of a trajectory, not insulation from environmental influence, and plasticity and stability can coexist within the same person.

For male androphilia, the most specific evolutionary hypothesis on the table is X-linked sexually antagonistic selection. Because a male inherits his single X chromosome from his mother, the model predicts that variants reducing direct reproduction in some male carriers should be maintained if they raise reproductive output in female carriers, producing elevated fecundity preferentially among maternal-line female relatives with little or no corresponding increase on the paternal side. The Italian research program associated with Camperio Ciani has repeatedly reported exactly this pattern. In a foundational study of 98 homosexual and 100 heterosexual men with more than 4,600 relatives, mothers of homosexual men averaged 2.69 versus 2.32 offspring, maternal aunts 1.98 versus 1.51, and descendants of maternal grandparents 2.17 versus 1.83, while paternal aunts showed no significant difference. An enlarged sample of 152 homosexual and 98 heterosexual men replicated the asymmetry, and a comparison of first-born mothers, whose fecundity advantage cannot be an artifact of having older sons, strengthened the case. A separately collected sample including bisexual probands found maternal-line elevation in both bisexual and homosexual families, while an excess of older brothers appeared only in homosexual probands, dissociating the two signals.

Independent evidence, however, is far more heterogeneous. A study of 301 gay and 404 heterosexual White British men found only a marginal family-size difference that could not isolate female-line fecundity. Rahman and colleagues reported elevated maternal-aunt fecundity in a White British subsample but a different pattern in the non-White stratum. Schwartz and colleagues did not interpret their data as maternal transmission, and a later secondary reanalysis suggesting maternal-aunt superiority is not an independent replication. Most strikingly, recent large-scale analyses have turned negative: a Czech study of more than 7,300 straight men and 459 gay men found no maternal or maternal-grandmother advantage and a small paternal-grandmother effect, and an extended-kin study found no effect in mothers or maternal aunts but a modest paternal-grandparent increase. The author concludes that the X-linked model remains a falsifiable submodel, not an established fact, and that the decisive test requires comparing mothers, maternal aunts, maternal grandmothers, and homologous paternal-line relatives within the same pedigrees while modeling birth order, sibship composition, cohort, background fertility, and ascertainment.

A critical methodological distinction underlies much of this confusion. Mother- or sibship-based measures of female fecundity share the proband’s sibship structure and are statistically entangled with the fraternal birth-order effect, the well-replicated finding that each additional older brother increases the odds of male homosexuality, plausibly through maternal immune responses to male-specific antigens. Joint analyses show the two can come apart. Across 14 archived samples of 5,390 men, the older-brother effect persisted while a sibship-based fecundity proxy showed no increase. Dutch population-register data covering more than nine million individuals found a robust older-brother association with later same-sex union but no positive fecundity effect, and a study of 1,061 Samoans confirmed the fraternal birth-order effect while the total-sibship fecundity parameter was absent. By contrast, the fecundity of maternal aunts and grandmothers is not mechanically determined by the proband’s older brothers, making extended-kin tests the sharper discriminator, though such data remain vulnerable to familial, demographic, and cultural confounding.

Contemporary genomics reframes the whole question. Twin, family, and genome-wide studies indicate that sexual orientation is partly heritable and highly polygenic, with many variants of individually small effect rather than a single deterministic locus. Large-scale genomic analyses reported that genetic variants associated with same-sex sexual behavior also predicted a greater number of opposite-sex partners among people reporting exclusively opposite-sex behavior, and evolutionary simulations suggested such a mating advantage could help maintain the associated alleles. This supports antagonistic pleiotropy as a broad maintenance principle: variants imposing a reproductive cost in some carriers can persist if they confer advantages in others. Earlier population-genetic modeling reached a compatible conclusion, finding that simple one-locus models could not reproduce the observed combination of trait frequency, reduced male reproduction, and maternal-line asymmetry, whereas a two-locus sexually antagonistic model containing at least one X-linked component fit better. The X-linked hypothesis thus sits as a narrower pedigree-generating prediction inside a broader polygenic framework, and repeated failure of the maternal-line signature would weaken only that submodel, not heritability itself.

Female same-sex orientation follows a different empirical logic. A large pedigree study of 1,458 women and 30,203 relatives found markedly reduced direct reproduction among lesbian women, 0.09 versus 0.33 offspring in the full sample and 0.31 versus 1.54 among women aged 45 or older. But the compensatory pattern in relatives was bilateral rather than maternal: significant increases appeared in parents, paternal aunts, and maternal uncles, while maternal aunts, paternal uncles, and grandparents showed no significant elevation. Lesbian respondents also reported more siblings and a higher prevalence of non-heterosexual female relatives in their pedigrees, 2.83 percent versus a 0.63 percent reference. This structure is compatible with balancing selection, in which fitness costs in a low-reproduction minority are offset by increased reproduction elsewhere in the pedigree, but the evidence derives largely from one research program and requires independent replication before the interpretation can be considered established.

Stable lesbian orientation must also be distinguished from broader gynephilic motivation. Cross-cultural studies using implicit and explicit measures found that gynephilic responses are widespread among women, frequently coexist with attraction to men, are only weakly coupled to non-heterosexual identity, and show no distinctive fecundity signature, suggesting a broadly distributed and developmentally plastic motivational dimension rather than a discrete low-frequency reproductive phenotype. Functional hypotheses for female sexual fluidity operate at yet another level. An alloparenting account proposes that flexible same-sex attraction may have facilitated pair-bonds with unrelated female alloparents when paternal investment was unreliable, while a co-wife hypothesis links fluidity to reduced conflict in polygynous marriages; analyses of Add Health data found that women, but not men, showing greater fluidity had more children, though the proposed causal pathway remains untested. Evidence for either function would not validate the pedigree-level balancing model, and vice versa.

Developmental mechanisms add further variance without replacing genetic liability. The fraternal birth-order effect and its maternal immune interpretation, prenatal endocrine variation, neural differentiation, and developmental stochasticity all contribute probabilistically to phenotypic realization. Childhood gender nonconformity is among the most consistent developmental correlates of later non-heterosexual orientation, particularly in males, yet it is neither necessary nor sufficient for any adult outcome. Average developmental stability differs by sex: male attraction shows stronger continuity and resistance to redirection attempts, while female attraction, behavior, and identity are more variably coupled across relationships and life stages. The author stresses this is a difference in average plasticity and coupling among components, not a contrast between biologically determined male orientation and socially determined female orientation.

Cross-cultural evidence completes the picture by showing that social institutions modify expression, kin-directed behavior, identity, and realized fitness without constituting a universal maintenance mechanism. Samoan fa’afafine, feminine androphilic males in a culturally recognized gender category, repeatedly show elevated avuncular tendencies toward nieces and nephews, yet this does not establish kin selection as a general explanation. Among the Urak-Lawoi of Ko Lipe, Thailand, androphilic na-ning showed no greater avuncularity than gynephilic men, with higher altruism characterizing the population generally. The framework closes with explicit testable predictions: extended maternal-line asymmetry surviving joint statistical controls, genomic antagonistic effects tied to realized fitness, reproducible bilateral compensation for lesbian orientation, functional mediators for female fluidity, and attraction-based measures showing greater cross-context continuity than identity labels. The evidence, the author concludes, favors plural, phenotype-specific maintenance rather than any single evolutionary story.

Subject of Research: Evolutionary and developmental architecture of human sexual orientation

Article Title: The motivational architecture of sexual orientation across development and evolutionary persistence

Article References: Camperio Ciani, A. S. (2026). The motivational architecture of sexual orientation across development and evolutionary persistence. Frontiers in Psychology, 17, Article 1906479. https://doi.org/10.3389/fpsyg.2026.1906479

Image Credits: AI Generated

DOI: 10.3389/fpsyg.2026.1906479

Keywords: sexual orientation, evolutionary psychology, sexually antagonistic selection, polygenic architecture, fraternal birth order effect, balancing selection, female sexual fluidity, developmental systems, fa'afafine, antagonistic pleiotropy, kin selection, socioecological context