Beyond mistakes: same-sex partner acceptance and broad mating filters coexist in termite pairing

Nobuaki Mizumoto , Elijah P. Carroll

Same-sex sexual behavior is often interpreted either as a mistake arising from indiscriminate attempts or as an adaptive behavior directed towards same-sex partners. These explanations are typically considered mutually exclusive. Here we challenge this assumption using an adaptive same-sex pairing system in Reticulitermes termites. Long-term male-male pairings originate from tandem running, in which one male follows another. We found that males discriminate partner sex and rarely form male-male tandems upon first encounter, whereas male-female tandems form immediately. However, male-male pairing frequency increases over time, indicating that males progressively accept male partners despite recognizing their sex. At the same time, males frequently follow non-mating individuals, including workers and soldiers, which partially share cues with females. Such interactions are costly because workers attack following males. Males subsequently refine their decisions, reducing these interactions and ceasing them entirely after experiencing an attack. Our results show that adaptive same-sex pairing and mistaken partner choice arise from different stages of the same behavioral sequence. Rather than alternative explanations, adaptation and mistakes can coexist because partner recognition and acceptance occur sequentially in the pairing process. These findings highlight the importance of behavioral sequences when interpreting the causes of same-sex sexual behavior and other apparently misdirected behaviors.