Regulation of neotenic differentiation through direct physical contact in the damp-wood termite Hodotermopsis sjostedti

eusocial insects exhibit reproductive division of labor, in which only a fraction of colony members differentiate into reproductives. In termites, reproductives of both sexes are present in a colony and constantly engaged in reproduction. It has been suggested that the sex ratio of reproductives is maintained by social interactions. The presence of reproductives is known to inhibit the additional differentiation of same-sex reproductives, while it promotes the differentiation of opposite-sex reproductives. In this study, using the damp-wood termite Hodotermopsis sjostedti, physiological effects of male/female reproductives on the differentiation of supplementary reproductives (neotenics) were examined. The results showed that the only male-neotenic condition, i.e., the presence of male neotenics in the absence of female neotenics, accelerated the neotenic differentiation from female workers (i.e., pseudergates). Under this condition, the rise of juvenile hormone (JH) titer was repressed in females, and the application of a JH analog inhibited the female neotenic differentiation, indicating that the low JH titer leads to rapid differentiation. Thus, the only male-neotenic condition that actively promotes reproductive differentiation by manipulating physiological condition of females is suggested to be a mechanism underlying sexual asymmetry in reproductive function, which may lead the femalebiased sex allocation of reproductives. Eusocial insects construct sophisticated social systems via the reproductive division of labor, in which only a fraction of colony members occupy reproductive status, while the others, known as workers, are engaged in non-reproductive roles such as brooding, maintaining nest, and foraging 1. In many species, non-reproductive individuals retain their reproductive potential, implying that there are mechanisms that maintain reproductive division of labor, and it has been reported that these mechanisms involve managing conflicts over reproductive status 2,3. In termites (order Blattodea, superfamily Termitoidea), however, little is known about the mechanisms that regulate the number of reproductives. It has been suggested, though, that the regulatory mechanisms underlying reproductive differentiation in termites differ from those in hymenopterans, since their respective social and developmental systems are so different 4. One of the major distinctions is the presence of males in the colony; in termites, male reproductives continue to attend female reproductives after colony foundation, while males in hymenopterans die immediately after their nuptial flight 5. Due to the hemimetabolous development of termites, non-adult individuals can perform worker roles 6,7. In addition to these individuals, there are two types of reproductives: primary reproductives, which are derives from alates that experienced nuptial flights 8 , and neotenics, which develop from non-adult individuals through special molt (neotenic molt) and remain in their natal nest to perform reproduction 2,9,10 (Fig. 1a). Caste comp...

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“…the same sex, indicating the existence of a suppression effect on the differentiation of neotenics from the same sex [13][14][15] (Fig. 1b).…”

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confidence: 99%

Male neotenic reproductives accelerate additional differentiation of female reproductives by lowering JH titer in termites

Oguchi

Sugime

Shimoji

et al. 2020

Sci Rep

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“…In basal termite species, the elder instar larvae, known as pseudergates, have the potential to differentiate into alates, neotenics (supplementary reproductives) or soldiers (Roisin & Korb, ). Because the elder instar larvae serve as the worker caste (Shimoji et al ., ), we use the term ‘worker’ for larvae of the fourth or older instars in the present study. Hodotermopsis sjostedti provides a useful model system to study caste differentiation, as morphological caste differentiation is regulated by nestmate interactions that induce hormonal changes in individuals (Cornette et al ., ; Shimoji et al ., ).…”

Section: Methodsmentioning

confidence: 99%

“…For example, the soldier caste, a specialist in colony defence, has a distinctly larger body size and better developed mandibles compared with those of workers. All immature individuals basically remain totipotent and can differentiate into the reproductive caste or soldier caste, and this differentiation is regulated by social interactions, especially direct physical contact between individuals (Dong et al ., ; Watanabe et al ., ; Maekawa et al ., ; Shimoji et al ., ). Given that morphology itself affects the locomotor activity of insects (Kaspari & Weiser, ; Wittlinger et al ., ; Hurlbert et al ., ; Crumière et al ., ), measuring morphological differences among termite castes, both quantitative and qualitative, would be important when assessing the influence of caste identity on locomotor activity.…”

Section: Introductionmentioning

confidence: 97%

Caste‐biased locomotor activities in isolated termites

et al. 2019

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Eusocial insects are characterized by a well-developed division of labour among castes. Although the successful division of labour should stem from behavioural differentiation depending on caste identity, caste-specific intrinsic behavioural characteristics might be masked by social interactions within colonies. The present study explores caste-specific intrinsic locomotive activities of termites by quantifying them in isolation. We track individual movement trajectories of the damp-wood termite Hodotermopsis sjostedti over 30 min and extract individual locomotion parameters. Multivariate statistical analyses reveal significant differences among castes: soldiers move more actively than workers and neotenic reproductives. The morphometric data of test individuals indicate that locomotor activities reflected caste identity more strongly compared with quantitative morphological variations among individuals. We find that the different locomotor activities of soldiers compared with those of neotenics and workers probably reflect their physiological differentiation. The present study provides a basis for a deeper understanding of the roles of individual locomotor activities in social behaviours.

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“…Accumulating 55 evidence indicates that social interactions among nestmates alter individual hormone levels 56 that regulate molecular mechanisms involved in caste differentiation, thus optimizing caste 57 have the potential to differentiate into alates, neotenics (supplementary reproductives), and 76 soldiers (Miura, 2001). Because the fourth instar and older larvae behave as the worker caste 77 (Shimoji et al, 2017), we use the term "worker" instead of "elder instar larva" in this paper. 78…”

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confidence: 99%

“…This species provides a good model system to study caste differentiation, as morphological 79 caste differentiation is regulated by nestmate interactions that induce hormonal changes in 80 individuals (Cornette et al, 2008;Shimoji et al, 2017). 81…”

mentioning

confidence: 99%