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

Abstract

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.

Wasted efforts impair random search efficiency and reduce choosiness in mate-pairing termites

“…All 40 individuals were maintained for 30 min (just after swarming) or 72 hours (extended mate search) separately in a 24-well plate before the observation. Note that the results of the 30-minute treatment were reported in a previous study (see Text S1 of (Mizumoto et al, 2022)). We introduced 40 individuals to the experimental arena (ø = 600 mm).…”

“…Note that males, rather than females, actively choose partners in termite species with female-led tandems. Tandem runs do not start without males following females (Mizumoto et al, 2022), and females do not change their behavior according to their partners (Mizumoto et al, 2021(Mizumoto et al, , 2020.…”

The significance of social interactions in synchronized swarming flight in a termite

“…Our finding on the association between colony size and the synchronicity of swarming has a vital implication for understanding the evolution of termite mating behavior (Figs 1 and 4). The mating behavior of termites is diverse across lineages (Mizumoto et al, 2022a; Nutting, 1979). Some species show a short and concentrated swarming season in dispersal flight, where dispersal flights are highly synchronized within and across colonies (Nutting, 1979).…”

“…1), species with smaller colony sizes may not use synchronized swarming flights as a mating mechanism but develop other unknown alternative behavioral mechanisms. Interestingly, with several exceptions, tandem running behavior is lacking for several one-piece nesting termite genera, such as, Bifiditermes , Neotermes , Pterotermes and Stolotermes (summarized in (Mizumoto et al, 2022a)).…”

“…All pairs were from the same colony, and each individual was observed only once. Pairing colony mates does not affect the tandem running success in R. speratus (Mizumoto et al, 2022a).…”