The evolution of same-sex sexual behaviour in mammals

Same-sex sexual behavior (SSB), encompassing any sexual activity between members of the same sex, has been documented in over 1500 animal species, spanning various taxa from invertebrates to mammals. Its prevalence, particularly in nonhuman primates (observed in at least 15 species), presents an evolutionary puzzle. SSB, unlike different-sex sexual behavior, doesn't directly contribute to reproduction, incurring costs such as energy expenditure, time investment, disease transmission, and injuries. Furthermore, the opportunity cost of forgoing offspring production presents an additional evolutionary challenge, leading to the characterization of SSB as a Darwinian paradox. Existing hypotheses attempting to explain SSB's evolution range from non-adaptive explanations such as mistaken identity, limited availability of opposite-sex partners, sexual frustration, or byproducts of selection on other traits to adaptive hypotheses suggesting beneficial roles in social interactions and conflict mitigation. This study seeks to address this evolutionary puzzle by investigating the phylogenetic patterns of SSB in mammals and testing the plausibility of adaptive hypotheses in a broader phylogenetic context.

The existing literature on same-sex sexual behavior in animals is extensive and varied. Early studies often focused on anecdotal observations and species-specific analyses, leading to a range of hypotheses. Non-adaptive hypotheses posit that SSB is a result of factors such as mistaken identity, limited access to opposite-sex partners, sexual frustration, or a byproduct of selection for high sexual responsiveness. Conversely, adaptive hypotheses propose that SSB enhances social bonds, facilitates alliances, mitigates conflict, or improves reproductive success indirectly. This study builds upon this existing literature by employing a phylogenetic approach to examine the evolutionary history of SSB in mammals and formally test these hypotheses across a broader taxonomic scale. The review acknowledges the limitations of previous research focusing on individual species or limited taxa, emphasizing the need for a more comprehensive, phylogenetically informed analysis.

This study compiled data on the presence or absence of SSB in mammals. The data included courtship, mounting, genital contact, copulation, and pair bonding, mostly focusing on adult behaviors observed in wild or semi-wild conditions. To account for potential biases caused by differences in research intensity, four subsets of species were employed, with increasingly stringent criteria for data inclusion. Phylogenetic analyses, including ancestral state reconstruction, stochastic character mapping, and Pagel's directional test for trait evolution, were conducted to infer the evolutionary history of SSB in mammals and test hypotheses linking SSB to sociality and adulticide (intraspecific lethal aggression). The analyses employed several statistical methods and controlled for potential confounding factors using different approaches: including sampling effort as a covariate in phylogenetic logistic regressions; using sampling effort as a weighting factor; using subsets of species where reproductive and sexual behavior have been extensively studied; and using subsets of species with high overall research intensity. Phylogenetic signal was assessed using the phylo.signal algorithm, while phylogenetic correlation between male and female SSB was determined using the approach from ref. 42 as implemented in the R package "diversitree". Ancestral state reconstruction utilized maximum likelihood for discrete characters, and the number of independent gains and losses of SSB was estimated using stochastic character mapping. To test adaptive hypotheses, phylogenetic models were constructed with SSB as the dependent variable and sociality and adulticide as independent variables.

The study documented SSB in 261 mammalian species (approximately 4%), representing 62 families (about 50%) and 12 orders (63%). SSB was primarily observed as mounting/genital contact, courtship, or pair bonding, mostly among adults and in wild or semi-wild conditions. Phylogenetic analysis revealed a significant phylogenetic signal, indicating non-random distribution across the mammalian phylogeny. SSB was particularly prevalent in even-toed ungulates, carnivores, kangaroos, rodents, and primates. Ancestral state reconstruction suggested that SSB is not an ancestral trait in mammals and that it evolved multiple times independently in various lineages, often in more recently evolved lineages. The age of nodes where SSB was inferred as present was significantly younger than those where it was absent. Analysis revealed a significant association between SSB prevalence and sociality in both males and females. Pagel's directional test supported the hypothesis that the evolution of SSB depended on the shift from solitary to social living, suggesting a role in establishing and strengthening social relationships. A significant association between male SSB and adulticide was also observed, with the directional test indicating that the evolution of male SSB was contingent upon male adulticide. This association supports the role of SSB in mitigating intrasexual aggression and conflict. The absence of such a relationship between female SSB and female adulticide is discussed. Table 1 summarizes the results from various phylogenetic models testing the effects of sociality and adulticide on SSB, controlling for sampling effort. Table 2 presents a comparison of various evolutionary models using AIC and likelihood ratio tests.

The findings challenge the hypothesis that indiscriminate sexual behavior is an ancestral condition for sexually reproducing animals in mammals, suggesting instead that SSB evolved multiple times independently within different mammalian lineages. The strong association between SSB and sociality across both sexes suggests an adaptive role in social bonding, alliance formation, and conflict resolution. The association between male SSB and adulticide further strengthens the hypothesis that SSB serves to mitigate intrasexual aggression and conflict, possibly contributing to social stability. The contrast between the sexes regarding the relationship between SSB and adulticide aligns with the observation that adulticide in mammals is more strongly linked to intrasexual conflicts in males than females. While the study strongly suggests a role for sociality and conflict mitigation in the evolution of SSB, it acknowledges that other factors may also be involved and warrants further research.

This study provides compelling evidence for the adaptive evolution of SSB in mammals. The phylogenetic analyses revealed that SSB is not a randomly distributed trait, but rather is associated with sociality and, in males, with adulticide, suggesting that these factors have played a role in the repeated evolution of SSB across various mammalian lineages. The findings underscore the importance of considering both adaptive and non-adaptive explanations and the need for further research to fully understand the complexity of SSB's evolution across different mammalian groups. Future studies should focus on increasing data on SSB prevalence across various species to enhance the robustness of phylogenetic analyses and explore other potential selective pressures that could explain the observed patterns.

The study acknowledges potential limitations related to data availability and incomplete information on SSB in many mammalian species. The reliance on existing literature may have introduced bias due to uneven research effort across different species. The study attempted to mitigate these limitations through various statistical controls and the use of different data subsets, but the possibility of false negatives remains. Additionally, the study focuses on mammals, and the conclusions may not be generalizable to other animal groups.