Abstract

Simple SummaryGenerally, 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.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.

Highlights

  • The complex society of eusocial insects is maintained by the division of labor among castes

  • Male reproductive soldiers were observed under all experimental conditions except for the control treatment (Figure 1)

  • When removals were performed at the time of first-soldier emergence, male reproductive soldiers were observed in 4.8% of the king removal colonies (1/21)

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Summary

Introduction

The complex society of eusocial insects is maintained by the division of labor among castes. The existence of sterile castes (e.g., the workers in social Hymenoptera and soldiers in termites) that engage in altruistic work without possessing any reproductive abilities is the most crucial characteristic of eusocial insects. Secondary reproductives (called “neotenics”) that possess both reproductive organs and weapons appear occasionally in several species of primitive termite taxa (family Archotermopsidae and Stolotermitidae) [4,5,6]. These individuals are so-called reproductive soldiers ( termed as soldier-headed reproductives or soldier neotenics [7]), and males are more frequently observed than females under natural conditions [4,5,6]. Reproductive soldier-like individuals were artificially induced by the juvenile hormone (JH)

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