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A fundamental yet seemingly contradictory aspect of biological individuals is their capacity to remain the same while changing through time. This self-regulatory ability is facilitated by a number of factors that are shared by all complex multicellular life-forms. One such essential trait is an effective immune system. Here, I use concepts of individuality and immunity to explore the blurred line between society and individual in termite “superorganisms”. I discuss our current understanding of the breadth and mechanistic underpinnings of collective immunity in termites, before going on to explore the evolution of the immune system during the transition from a cockroach-like ancestor to a fully-fledged termite society. I end by discussing the possibly crucial role played by immunity during the emergence of eusociality, and in transitions in organismal complexity generally.
A broad suite of immune adaptations have evolved in social insects which hold close parallels with the immune systems of multicellular individuals. However, comparatively little is known about the evolutionary origins of immunity in social insects. We tackle this by identifying immune genes from 18 cockroach and termite species, spanning a gradient of social lifestyles. Termites have undergone contractions of major immune gene families during the early origin of the group, particularly in antimicrobial effector and receptor proteins, followed by later re-expansions in some lineages. In a comparative gene expression analysis, we find that reproductive individuals of a termite invest more in innate immune regulation than other castes. When colonies encounter immune-challenged nestmates, gene expression responses are weak in reproductives but this pattern is reversed when colony members are immune-challenged individually, with reproductives eliciting a greater response to treatment than other castes. Finally, responses to immune challenge were more comprehensive in both subsocial and solitary cockroaches compared to termites, indicating a reduced overall ability to respond to infection in termites. Our study indicates that the emergence of termite sociality was associated with the evolution of a tapered yet caste-adapted immune system.
The first sterile caste to evolve in termites was the soldier. While the importance of soldiers to termite society defense has long been recognized, the contribution of soldiers to other societal functions, such as colony immunity, is less well understood. We explore this issue by examining the role of soldiers in protecting nestmates against pathogen infection. Even though they are unable to engage in grooming behavior, we find that the presence of soldiers of the Darwin termite, Mastotermes darwiniensis, significantly improves the survival of nestmates following entomopathogenic infection. We also show that the copious exocrine oral secretions produced by Darwin termite soldiers contain a high concentration of proteins involved in digestion, chemical biosynthesis, and immunity. The oral secretions produced by soldiers are sufficient to protect nestmates against infection, and they have potent inhibitory activity against a broad spectrum of microbes. Our findings support the view that soldiers may play an important role in colony immunity, and broaden our understanding of the possible function of soldiers during the origin of soldier-first societies.
The first sterile caste to evolve in termites was the soldier. While the importance of soldiers to termite society defense has long been recognized, the contribution of soldiers to other societal functions, such as colony immunity, is less well understood. We explore this issue by examining the role of soldiers in protecting nestmates against pathogen infection. Even though they are unable to engage in grooming behavior, we find that the presence of soldiers of the Darwin termite, Mastotermes darwiniensis, significantly improves the survival of nestmates following entomopathogenic infection. We also show that the copious exocrine oral secretions produced by Darwin termite soldiers contain a high concentration of proteins involved in digestion, chemical biosynthesis, and immunity. The oral secretions produced by soldiers are sufficient to protect nestmates against infection, and they have potent inhibitory activity against a broad spectrum of microbes. Our findings support the view that soldiers may play an important role in colony immunity, and broaden our understanding of the possible function of soldiers during the origin of soldier-first societies.
Differentiation of immune response with castes in termites by de novo transcriptome sequencing
(2017)
Eusociality is one major evolutionary transitions, during which the division of labor is considered as the hallmark feature. This character of evolution, also interpreted as task specialization, is associated with multiple morphological, physiological and behavioral adaptations required for brood care, foraging, and defense. With these adaptations which ultimately cause the formation of castes in insect sociality (mostly in termites, ants, some bees and wasps), while whether immune system is related to eusociality in termites is rare understood. We hypothesis that immune system in termite sociality had also differentiation along with the formation of castes. We address this issue by exploring the immune responses of different castes with de novo transcriptome sequencing. After injection with cocktail of heat-killed pathogens (Pseudomonas entomophila, Bacillus thuringiensis, Saccharomyces cerevisiae), the mRNAs from false workers, soldiers and reproductive of Neotermes canstaneus were sequenced. We found much more genes are regulated (1420 genes downregulated and 398 genes upregulated) in reproductives compared to soldiers (90 genes downregulated and 108 genes upregulated) and false workers (135 genes downregulated and 71 genes upregulated). In these upregulated genes, reproductives had 54 same genes as soldiers, while only 7 same genes as workers which almost is same number between soldiers and workers. In the downregulated genes, reproductives shared 50 and 41 same genes as soldiers
and workers, respectively. Besides, soldiers and workers had 29 same downregulated genes. From these findings, it is indicated that the immune system differentiates with division of labor during eusociality in termites.