Ancestral sex-role plasticity facilitates the evolution of same-sex sexual behavior

Recent attempts to explain the evolutionary prevalence of same-sex sexual behavior (SSB) have focused on the role of indiscriminate mating. However, in many cases, SSB may be more complex than simple mistaken identity, instead involving mutual interactions and successful pairing between partners who can detect each other's sex. Behavioral plasticity is essential for the expression of SSB in such circumstances. To test behavioral plasticity's role in the evolution of SSB, we used termites to study how females and males modify their behavior in same-sex versus heterosexual pairs. Male termites follow females in paired tandems before mating, and movement patterns are sexually dimorphic. Previous studies observed that adaptive same-sex tandems also occur in both sexes. Here we found that stable same-sex tandems are achieved by behavioral plasticity when one partner adopts the other sex's movements, resulting in behavioral dimorphism. Simulations based on empirically obtained parameters indicated that this socially cued plasticity contributes to pair maintenance, because dimorphic movements improve reunion success upon accidental separation. A systematic literature survey and phylogenetic comparative analysis suggest that the ancestors of modern termites lack consistent sex roles during pairing, indicating that plasticity is inherited from the ancestor. Socioenvironmental induction of ancestral behavioral potential may be of widespread importance to the expression of SSB. Our findings challenge recent arguments for a prominent role of indiscriminate mating behavior in the evolutionary origin and maintenance of SSB across diverse taxa.

Automated summary

Recent studies have found that the prevalence of same-sex sexual behavior is not simply due to mistaken identity, but involves mutual interactions and successful pairing between partners. Behavioral plasticity plays a crucial role in expressing same-sex behavior in such circumstances, as partners are able to modify their behavior to adapt to each other's sex. Through studying termites, it was discovered that stable same-sex pairings are achieved through behavioral plasticity, resulting in behavioral dimorphism. This dimorphism improves reunion success in case of accidental separation. A systematic literature survey and phylogenetic comparative analysis suggest that the ancestors of modern termites lacked consistent sex roles during pairing, indicating that this plasticity is inherited from ancestors. Therefore, socioenvironmental induction of ancestral behavioral potential may be of widespread importance to the expression of same-sex behavior.