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The evolution of same-sex sexual behaviour in mammals.

ABSTRACT: 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.

SUBMITTER: Gomez JM

PROVIDER: S-EPMC10547684 | biostudies-literature | 2023 Oct

REPOSITORIES: biostudies-literature

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The evolution of same-sex sexual behaviour in mammals.

Gómez José M JM Gónzalez-Megías A A Verdú M M

Nature communications 20231003 1

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, ...[more]

PMID: 37788987

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Project description:Animal behaviours that are superficially similar can express different intents in different contexts, but how this flexibility is achieved at the level of neural circuits is not understood. For example, males of many species can exhibit mounting behaviour towards same- or opposite-sex conspecifics1, but it is unclear whether the intent and neural encoding of these behaviours are similar or different. Here we show that female- and male-directed mounting in male laboratory mice are distinguishable by the presence or absence of ultrasonic vocalizations (USVs)2-4, respectively. These and additional behavioural data suggest that most male-directed mounting is aggressive, although in rare cases it can be sexual. We investigated whether USV+ and USV- mounting use the same or distinct hypothalamic neural substrates. Micro-endoscopic imaging of neurons positive for oestrogen receptor 1 (ESR1) in either the medial preoptic area (MPOA) or the ventromedial hypothalamus, ventrolateral subdivision (VMHvl) revealed distinct patterns of neuronal activity during USV+ and USV- mounting, and the type of mounting could be decoded from population activity in either region. Intersectional optogenetic stimulation of MPOA neurons that express ESR1 and vesicular GABA transporter (VGAT) (MPOAESR1∩VGAT neurons) robustly promoted USV+ mounting, and converted male-directed attack to mounting with USVs. By contrast, stimulation of VMHvl neurons that express ESR1 (VMHvlESR1 neurons) promoted USV- mounting, and inhibited the USVs evoked by female urine. Terminal stimulation experiments suggest that these complementary inhibitory effects are mediated by reciprocal projections between the MPOA and VMHvl. Together, these data identify a hypothalamic subpopulation that is genetically enriched for neurons that causally induce a male reproductive behavioural state, and indicate that reproductive and aggressive states are represented by distinct population codes distributed between MPOAESR1 and VMHvlESR1 neurons, respectively. Thus, similar behaviours that express different internal states are encoded by distinct hypothalamic neuronal populations.

Dataset Information

The evolution of same-sex sexual behaviour in mammals.

Publications

The evolution of same-sex sexual behaviour in mammals.

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