Termite Soldier Differentiation in Incipient Colonies is Related to Parental Proctodeal Trophallactic Behavior

Caste polyphenism in social insects is regulated by social interactions among colony members. Trophallaxis is one of the most frequently observed interactions, but no studies have been conducted identifying the intrinsic factors involved in this behaviour and caste differentiation. Dopamine (DA) has multiple roles in the modulation of behaviours and physiology, and it produces species-specific behaviours in animals. Here, to verify the role of DA in termite soldier differentiation, we focused on the first soldier in an incipient colony of Zootermopsis nevadensis , which always differentiates from the oldest 3rd instar (No. 1 larva) via a presoldier. First, brain DA levels of the No. 1 larva at day 3 after its appearance were significantly higher than day 0. Second, DA synthesis gene expression levels were extraordinarily high in the No. 1 larva at day 0–1 after appearance. Finally, injection of a DA receptor antagonist into the No. 1 larva resulted in the inhibition of presoldier differentiation. Behavioural observations of the antagonist or control-injected larvae suggested that brain DA and signalling activity regulate the frequencies of trophallaxis from reproductives and presoldier differentiation. Because trophallaxis is a social behaviour frequently observed in natural conditions, the role of DA should be investigated in other social insects with frequent trophallactic and allogrooming behaviour.

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A lipocalin protein, Neural Lazarillo, is key to social interactions that promote termite soldier differentiation

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2018.0707 ◽

2018 ◽

Vol 285 (1883) ◽

pp. 20180707 ◽

Cited By ~ 4

Author(s):

Hajime Yaguchi ◽

Shuji Shigenobu ◽

Yoshinobu Hayashi ◽

Satoshi Miyazaki ◽

Kouhei Toga ◽

...

Keyword(s):

Social Communication ◽

Social Evolution ◽

Differentially Expressed Gene ◽

Social Signals ◽

Crucial Component ◽

Insect Societies ◽

Termite Soldier ◽

Molecular Phylogenetic ◽

Incipient Colony ◽

Soldier Differentiation

Social communication among castes is a crucial component of insect societies. However, the genes involved in soldier determination through the regulation of inter-individual interactions are largely unknown. In an incipient colony of the damp-wood termite Zootermopsis nevadensis , the first larva to develop into a third instar always differentiates into a soldier via frequent trophallactic feeding from the reproductives. Here, by performing RNA-seq analysis of third instar larvae, a homologue of Neural Lazarillo (named ZnNLaz1 ) was found to be the most differentially expressed gene in these soldier-destined larvae, compared with worker-destined larvae. This gene encodes a lipocalin protein related to the transport of small hydrophobic molecules. RNAi-induced knockdown of ZnNLaz1 significantly inhibited trophallactic interactions with the queen and decreased the soldier differentiation rates. This protein is localized in the gut, particularly in the internal wall, of soldier-destined larvae, suggesting that it is involved in the integration of social signals from the queen through frequent trophallactic behaviours. Based on molecular phylogenetic analysis, we suggest that a novel function of termite NLaz1 has contributed to social evolution from the cockroach ancestors of termites. These results indicated that a high larval NLaz1 expression is crucial for soldier determination through social communication in termites.

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TGFβ signaling related genes are involved in hormonal mediation during termite soldier differentiation

PLoS Genetics ◽

10.1371/journal.pgen.1007338 ◽

2018 ◽

Vol 14 (4) ◽

pp. e1007338 ◽

Cited By ~ 8

Author(s):

Yudai Masuoka ◽

Hajime Yaguchi ◽

Kouhei Toga ◽

Shuji Shigenobu ◽

Kiyoto Maekawa

Keyword(s):

Tgfβ Signaling ◽

Termite Soldier ◽

Soldier Differentiation

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Multi-functional roles of a soldier-specific volatile as a worker arrestant, primer pheromone and an antimicrobial agent in a termite

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2017.1134 ◽

2017 ◽

Vol 284 (1859) ◽

pp. 20171134 ◽

Cited By ~ 13

Author(s):

Yuki Mitaka ◽

Naoki Mori ◽

Kenji Matsuura

Keyword(s):

Communication Systems ◽

Division Of Labour ◽

Primer Pheromone ◽

Evolutionary Mechanisms ◽

Functional Roles ◽

Eusocial Insects ◽

Fungistatic Activity ◽

Termite Soldier ◽

Fungistatic Agent ◽

Soldier Differentiation

Division of labour in eusocial insects is characterized by efficient communication systems based on pheromones. Among such insects, termites have evolved specialized sterile defenders, called soldiers. Because they are incapable of feeding themselves, it has been suggested that soldiers are sustained by workers and emit the pheromone arresting workers. However, such a soldier pheromone has not been identified in any termite species, and the details of the soldier–worker interaction remain to be explored. Here, we identified a soldier-specific volatile sesquiterpene as a worker arrestant, which also acts as a primer pheromone regulating soldier differentiation and fungistatic agent in a termite Reticulitermes speratus . Chemical analyses revealed that (−)- β -elemene is the major component of soldier extract, and its authentic standard exhibited arrestant activity to workers and inhibited the differentiation from workers to soldiers. This compound also showed fungistatic activity against entomopathogenic fungi. These suggest that (−)- β -elemene secreted by soldiers acts not only as a worker arrestant but also as one component of inhibitory primer pheromone and an anti-pathogenic agent. Our study provides novel evidence supporting the multi-functionality of termite soldier pheromone and provides new insights into the role of soldiers and the evolutionary mechanisms of pheromone compounds.

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