The evolution of same-sex sexual behaviour in mammals

Article https://doi.org/10.1038/s41467-023-41290-x The evolution of same-sex sexual behaviour in mammals Received: 9 October 2022 José M. Gómez 1,2 , A. Gónzalez-Megías 2,3 & M. Verdú 4 Accepted: 29 August 2023 1234567890():,; 1234567890():,; Check for updates Same-sex sexual behaviour has attracted the attention of many scientists working in disparate areas, from sociology and psychology to behavioural and evolutionary biology. Since it does not contribute directly to reproduction, same-sex sexual behaviour is considered an evolutionary conundrum. Here, using phylogenetic analyses, we explore the evolution of same-sex sexual behaviour in mammals. According to currently available data, this behaviour is not randomly distributed across mammal lineages, but tends to be particularly prevalent in some clades, especially primates. Ancestral reconstruction suggests that same-sex sexual behaviour may have evolved multiple times, with its appearance being a recent phenomenon in most mammalian lineages. Our phylogenetically informed analyses testing for associations between same-sex sexual behaviour and other species characteristics suggest that it may play an adaptive role in maintaining social relationships and mitigating conflict. Same-sex sexual behaviour, that is, any attempted sexual activity between members of the same sex1–4, has been reported in over 1500 animal species, including all main groups from invertebrates such as insects, spiders, echinoderms, and nematodes, to vertebrates such as fish, amphibians, reptiles, birds, and mammals1–3. Same-sex sexual behaviour is particularly prevalent in nonhuman primates5,6, where it has been observed in at least 51 species from lemurs to apes7. This sexual behaviour is not limited to one sex or to the existence of artificial conditions, as it has been observed in males and females both in captivity and in wild conditions1–3,8. Same-sex sexual behaviour is also frequent in humans, existing throughout most of our history and in many societies and cultures9,10. Same-sex sexual behaviour has been argued to incur higher costs than different-sex sexual behaviour11. First, sexual interactions with members of the same sex can have similar mating costs as sexual interactions with members of the opposite sex in terms of energy expenditure, time use, disease transmission, injuries, etc8,12,13. Second, because it does not directly contribute to reproduction, same-sex sexual behaviour additionally has the opportunity cost of not producing offspring, if same-sex sexual behaviour occurs instead of different-sex sexual behaviour8,11. For these reasons, the evolution and prevalence of same-sex sexual behaviour is often considered a Darwinian paradox3,4,11,14–16. Several hypotheses have been proposed to explain the evolution and prevalence of same-sex sexual behaviour in human and nonhuman animals2,8,11,17,18. Some of these hypotheses are non-adaptive, suggesting that same-sex sexual behaviour is the consequence of mistaken identity19,20, the limited availability of individuals of the opposite sex21–23, the consequences of sexual frustration when individuals are refused by members of the other sex20, or the byproduct of selection acting on a separate trait, such as high sexual responsiveness24. A recently proposed hypothesis that is attracting much attention states that indiscriminate sexual behaviour (that is, the co-occurrence of different-sex sexual behaviour and same-sex sexual behaviour) is the ancestral condition for sexually reproducing animals and this explains the widespread occurrence of same-sex sexual behaviour in animals3,16. Under this view, indiscriminate sexual behaviour is proposed as the null hypothesis against which to test the occurrence of both different-sex sexual behaviour and same-sex sexual behaviour3. Contrasting with these non-adaptive explanations, other hypotheses are adaptive and suggest that same-sex sexual behaviour 1 Dpto de Ecología Funcional y Evolutiva, Estación Experimental de Zonas Áridas (EEZA-CSIC), Carretera de Sacramento s/n, La Cañada de San Urbano, 0-4120 Almería, Spain. 2Research Unit Modeling Nature (MNat), Facultad de Ciencias, Universidad de Granada, Granada, Spain. 3Dpto de Zoología, Facultad de Ciencias, Universidad de Granada, Avda Fuentenueva s/n, 18071 Granada, Spain. 4Centro de Investigaciones sobre Desertificación (CSIC-UV-GV), Crta e-mail: ; ; Moncada-Náquera km 4.5, 46113 Moncada, Valencia, Spain. Nature Communications | (2023)14:5719 1 Article can be directly favoured by natural selection8,18. For nonhuman mammals, two of the main adaptive hypotheses postulated to explain the origin, evolution and prevalence of same-sex sexual behaviour are:18,25 (i) Same-sex sexual behaviour contributes to establishing and maintaining positive social relationships18. According to this hypothesis, same-sex sexual interactions can serve to form and maintain bonds and alliances, and to facilitate reconciliation after conflicts between members of the same group18. This hypothesis predicts that same-sex sexual behaviour should be more frequent in social species than in non-social species8. (ii) Same-sex sexual behaviour contributes to diminishing intrasexual aggression and conflict8,18. This hypothesis postulates that same-sex sexual interactions may serve to communicate social status and establish and reinforce dominance hierarchies, thus preventing future conflicts, or may contribute to diverting aggressive behaviour toward courtship behaviour, providing subordinate males with greater opportunities to furtively copulate with females18. Because same-sex sexual behaviour is suggested to mitigate rather than completely eliminate aggressive behaviour, this second hypothesis predicts that same-sex sexual behaviour should be more frequent in species with aggressive and lethal intrasexual interactions than in more peaceful and nonlethal species. Lethal interactions are expressed in many species of mammals as the killing of conspecific adults (adulticide)26. This phenomenon appears to be mediated in males by mating competition and the establishment of dominance hierarchies. In females, on the other hand, the defence of resources and offspring mediates adulticide26. Therefore, due to these between-sex differences in motivation, the predicted association between same-sex sexual behaviour and adulticide would be expected to occur mainly in males. Most research to date has been focused on examining the adaptive functions and disentangling the proximate causes of same-sex sexual behaviour within particular systems or species4. And several descriptive species-specific studies support these adaptive hypotheses. For example, same-sex sexual behaviour seems to facilitate reconciliation among group members in female bonobos (Pan paniscus)27 and female Japanese macaques (Macaca fuscata)28. Similarly, same-sex sexual behaviour seems to serve to reinforce the alliance between small groups of male bottlenose dolph (...truncated)