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Termite gut flagellates are colonized by host-specific lineages of ectosymbiotic and endosymbiotic bacteria. Previous studies have shown that flagellates of the genus Trichonympha may harbour more than one type of symbiont. Using a comprehensive approach that combined cloning of SSU rRNA genes with fluorescence in situ hybridization and electron microscopy, we investigated the phylogeny and subcellular locations of the symbionts in a variety of Trichonympha species from different termites. The flagellates in Trichonympha Cluster I were the only species associated with 'Endomicrobia', which were located in the posterior part of the cell, confirming previous results. Trichonympha species of Cluster II from the termite genus Incisitermes (family Kalotermitidae) lacked 'Endomicrobia' and were associated with endosymbiotic Actinobacteria, which is highly unusual. The endosymbionts, for which we suggest the name 'Candidatus Ancillula trichonymphae', represent a novel, deep-branching lineage in the Micrococcineae that consists exclusively of clones from termite guts. They preferentially colonized the anterior part of the flagellate host and were highly abundant in all species of Trichonympha Cluster II except Trichonympha globulosa. Here, they were outnumbered by a Desulfovibrio species associated with the cytoplasmic lamellae at the anterior cell pole. Such symbionts are present in both Trichonympha clusters, but not in all species. Unlike the intracellular location reported for the Desulfovibrio symbionts of Trichonympha agilis (Cluster I), the Desulfovibrio symbionts of T. globulosa (Cluster II) were situated in deep invaginations of the plasma membrane that were clearly connected to the exterior of the host cell.
The surface of many termite gut flagellates is colonized with a dense layer of bacteria, yet little is known about the evolutionary relationships of such ectosymbionts and their hosts. Here we investigated the molecular phylogenies of devescovinid flagellates (Devescovina spp.) and their symbionts from a wide range of dry-wood termites (Kalotermitidae). From species-pure flagellate suspensions isolated with micropipettes, we obtained SSU rRNA gene sequences of symbionts and host. Phylogenetic analysis showed that the Devescovina spp. present in many species of Kalotermitidae form a monophyletic group, which includes also the unique devescovinid flagellate Caduceia versatilis. All members of this group were consistently associated with a distinct lineage of Bacteroidales, whose location on the cell surface was confirmed by fluorescence in situ hybridization. The well-supported congruence of the phylogenies of devescovinids and their ectosymbionts documents a strict cospeciation. In contrast, the endosymbionts of the same flagellates (´Endomicrobia´) were clearly polyphyletic and must have been acquired independently by horizontal transfer from other flagellate lineages. Also the Bacteroidales ectosymbionts of Oxymonas flagellates present in several Kalotermitidae belonged to several distantly related lines of descent, underscoring the general perception that the evolutionary history of flagellate-bacteria symbioses in the termite gut is complex.
Social insects employ a range of behaviours to protect their colonies against disease, but little is known about how such collective behaviours are orchestrated. This is especially true for the social Blattodea (termites). We developed an experimental approach that allowed us to explore how the social response to disease is co-ordinated by multistep host-pathogen interactions. We infected the eastern subterranean termite Reticulitermes flavipes with the entomopathogenic fungus Metarhizium anisopliae, and then, at different stages of infection, reintroduced them to healthy nestmates and recorded behavioural responses. As expected, termites groomed pathogen-exposed individuals significantly more than controls; however, grooming was significantly elevated after fungal germination than before, demonstrating the importance of fungal status to hygienic behaviour. Significantly, we found that cannibalism became prevalent only after exposed termites became visibly ill, highlighting the importance of host condition as a cue for social hygienic behaviour. Our study reveals the presence of a coordinated social response to disease that depends on stage of infection. Specifically, we show how the host may play a key role in triggering its own sacrifice. Sacrificial self-flagging has been observed in other social insects: our results demonstrate that termites have independently evolved to both recognize and destructively respond to sickness.
The soil-feeding habit is an evolutionary novelty found in some advanced groups of termites. The study of such groups is important to revealing interesting adaptations to this way-of-life. The genus Verrucositermes is one such example, characterized by peculiar outgrowths on the head capsule, antennae and maxillary palps, which are not found in any other termite. These structures have been hypothesized to be linked to the presence of a new exocrine organ, the rostral gland, whose structure has remained unexplored.
We have thus studied the ultrastructure of the epidermal layer of the head capsule of Verrucositermes tuberosus soldiers.We describe the ultrastructure of the rostral gland, which consists of class 3 secretory cells only. The dominant secretory organelles comprise rough endoplasmic reticulum and Golgi apparatus, which provide secretions delivered to the surface of the head, likely made of peptide-derived components of unclear function. We discuss a possible role of the rostral gland of soldiers as an adaptation to the frequent encounter with soil pathogens during search for new food resources.