Reproductive Soldier Development Is Controlled by Direct Physical Interactions with Reproductive and Soldier Termites

SIMPLE SUMMARY: Generally, in termites, the soldier caste is sterile, and their reproductive organ formation is suppressed. However, in some primitive taxa, neotenic reproductives with soldier-like mandibles, called reproductive soldiers, occasionally appear in the incipient colony. Our first step in understanding the developmental mechanism of this unique caste was to establish efficient conditions to induce reproductive soldiers in Zootermopsis nevadensis. Removing both the king and soldiers from an incipient colony strongly stimulated the formation of male reproductive soldiers, which possessed soldier-like mandibles and developed testes. Similarly, high differentiation rates of male reproductive soldiers were observed after king-and-soldier separation treatment using wire mesh. However, no male reproductive soldiers were produced without direct interaction with the queen. These results suggest that reproductive soldier development might be initiated and controlled by direct physical interactions with both reproductives (the king and queen) and soldiers. ABSTRACT: In eusocial insects (e.g., ants, bees, and termites), the roles of different castes are assigned to different individuals. These castes possess unique phenotypes that are specialized for specific tasks. The acquisition of sterile individuals with specific roles is considered a requirement for social evolution. In termites, the soldier is a sterile caste. In primitive taxa (family Archotermopsidae and Stolotermitidae), however, secondary reproductives (neotenic reproductives) with their mandibles developed into weapons (so-called reproductive soldiers, also termed as soldier-headed reproductives or soldier neotenics) have been reported. To understand the developmental mechanism of this unique caste, it is necessary to understand the environmental cues and developmental processes of reproductive soldiers under natural conditions. Here, we established efficient conditions to induce reproductive soldiers in Zootermopsis nevadensis. Male reproductive soldiers frequently developed after the removal of both the king and soldiers from an incipient colony. Similarly, high differentiation rates of male reproductive soldiers were observed after king-and-soldier separation treatment using wire mesh. However, no male reproductive soldiers were produced without direct interaction with the queen. These results suggest that male reproductive soldier development is repressed by direct physical interactions with both the king and soldiers and facilitated by direct physical interaction with the queen.