Studying basal taxa often allows shedding a light on the evolution of advanced representatives. The most basal termite species, Mastotermes darwiniensis, possesses unique morphological and behavioural traits, of which many remain scarcely studied. For these reasons, we conducted a comprehensive study of the alarm communication in this species and compared its components to behavioural modes described in other termites. In M. darwiniensis, the alarm is communicated by substrate-borne vibrations resulting from vertical vibratory movements. Another similar behaviour consists in longitudinal movements, by which the alarm is delivered to other termites in contact with alerted individual. Both these two behavioural modes could be used in synergy to create complex movements. M. darwiniensis also uses chemical alarm signals produced by labial gland secretion, in contrast to Neoisoptera in which this function is fulfilled exclusively by the frontal gland secretion. Moreover, we demonstrated in M. darwiniensis the presence of a positive feedback mechanism thought to occur exclusively in the crown group Termitidae. This positive feedback consists in both oscillatory movements of alerted individuals in response to alarm signals and release of alarm pheromone by excited soldiers. Our results confirm that M. darwiniensis is a remarkable example of mosaic evolution, as it combines many primitive and advanced features, and its alarm communication clearly belongs to the latter category.

In termites, as in many social insects, some individuals specialize in colony defense, developing diverse weaponry. As workers of the termite Neocapritermes taracua (Termitidae: Termitinae) age, their efficiency to perform general tasks decreases, while they accumulate defensive secretions and increase their readiness to fight. This defensive mechanism involves self-sacrifice through body rupture during which an enzyme, stored as blue crystals in dorsal pouches, converts precursors produced by the labial glands into highly toxic compounds. Here, we identify both components of this activated defense system and describe the molecular basis responsible for the toxicity of N. taracua worker autothysis. The blue crystals are formed almost exclusively by a specific protein named BP76. By matching N. taracua transcriptome databases with amino acid sequences, we identified BP76 to be a laccase. Following autothysis, the series of hydroquinone precursors produced by labial glands get mixed with BP76, resulting in the conversion of relatively harmless hydroquinones into toxic benzoquinone analogues. Neocapritermes taracua workers therefore rely on a two-component activated defense system, consisting of two separately stored secretions that can react only after suicidal body rupture, which produces a sticky and toxic cocktail harmful to opponents.

BackgroundThe frontal gland is a unique adaptation of advanced termite families. It has been intensively studied in soldiers with respect to its anatomy and chemistry, with numerous novel compounds being discovered within the tremendous richness of identified products. At the same time, the presence of the frontal gland in non-soldier castes received only negligible attention in the past.Principal FindingsHere, we report on the development of the frontal gland in alate imagoes of 10 genera and 13 species of Rhinotermitidae and Serritermitidae, in order to shed light on the evolution and function of this gland in imagoes. All investigated species possess a frontal gland. In most cases, it is well-developed and equipped with a sac-like reservoir, located in the postero-dorsal part of cranium, but reaching as far as the seventh abdominal segment in some Rhinotermitinae. The only exception is the genus Psammotermes, in which the gland is very small and devoid of the reservoir.ConclusionsOur direct observations and comparisons with soldiers suggest a defensive role of the gland in imagoes of all studied species. This functional analogy, along with the anatomic homology between the frontal gland in soldiers and imagoes, make it likely that the gland appeared once during the early evolution of rhinotermitid ancestors, and remained as a defensive organ of prime importance in both, soldiers and imagoes.

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