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

Recent attempts to explain the evolutionary prevalence of same-sex sexual behaviour (SSB) have focused on the role of indiscriminate mating. However, in many cases, SSB involves plastically adjusting sex roles to achieve successful courtship or pairing. To evaluate this overlooked factor, we tested whether ancestral sex-role plasticity facilitated the evolution of SSB in the termite Reticulitermes speratus . Male termites follow females in paired ‘tandems’ before mating, and movement patterns are sexually dimorphic. Adaptive same-sex tandems occur in both sexes. We show that in such cases, one partner adopts the other sex’s movement patterns, resulting in behavioural dimorphism. Data-based simulations confirmed that this socially-cued plasticity contributes to pair maintenance because dimorphic movements improve reunion success upon accidental separation. Phylogenetic analysis indicated that the ancestors of modern termites lack consistent sex roles during pairing, indicating that R. speratus inherited the plasticity from the ancestor. Socio-environmental induction of ancestral behavioural potential may be of widespread importance to the evolutionary maintenance of SSB.