Abstract
Insects protect themselves from microbial infections through innate immune responses, including pathogen recognition, phagocytosis, the activation of proteolytic cascades, and the synthesis of antimicrobial peptides. Termites, eusocial insects inhabiting microbe-rich wood, live in closely-related family groups that are susceptible to shared pathogen infections. To resist pathogenic infection, termite families have evolved diverse immune adaptations at both individual and societal levels, and a strategy of trade-offs between reproduction and immunity has been suggested. Although termite immune-inducible genes have been identified, few studies have investigated the differential expression of these genes between reproductive and neuter castes, and between sexes in each caste. In this study, we compared the expression levels of immune-related genes among castes, sexes, and ages in a Japanese subterranean termite, Reticulitermes speratus. Using RNA-seq, we found 197 immune-related genes, including 40 pattern recognition proteins, 97 signalling proteins, 60 effectors. Among these genes, 174 showed differential expression among castes. Comparing expression levels between males and females in each caste, we found sexually dimorphic expression of immune-related genes not only in reproductive castes, but also in neuter castes. Moreover, we identified age-related differential expression of 162 genes in male and/or female reproductives. In addition, although R. speratus is known to use the antibacterial peptide C-type lysozyme as an egg recognition pheromone, we determined that R. speratus has not only C-type, but also P-type and I-type lysozymes, as well as other termite species. Our transcriptomic analyses revealed immune response plasticity among all castes, and sex-biased expression of immune genes even in neuter castes, suggesting a sexual division of labor in the immune system of R. speratus. This study heightens the understanding of the evolution of antimicrobial strategies in eusocial insects, and of sexual roles in insect societies as a whole.
Highlights
Insects are exposed to a variety of infectious microbes in their habitats throughout their life cycle [1]
The expressions of CTL17 and LPSBP4 in young reproductives (PKs and primary queens (PQs)) were more than twice as high as those in other castes, and those of CTL9 and LPSBP1 in young reproductives, mature reproductives (PKs and secondary queens (SQs)), and soldiers were more than 1.3 times as high as those in alates and workers (FDR < 0.05; Fig 1 and S2 Table)
The expression levels of 16 genes differed significantly between reproductive statuses, i.e. reproductive castes and neuter castes, and 12 genes showed sexually dimorphic expression patterns regardless of reproductive status
Summary
Insects are exposed to a variety of infectious microbes in their habitats throughout their life cycle [1]. Insects need to prevent infection in order to survive, and so they must recognize and eliminate pathogens if they become infected with any microbes. Social insects form colonies consisting of a large number of siblings, and they are all susceptible to the same pathogenic infections [2]. Social insects eliminate pathogens by innate cellular and humoral immunity [3]. Social insects have developed behavioral and social immunity such as allogrooming, trophallaxis, isolation, canibalism [2]. Passive immuniazation, which is characterized by sharing immune factors between infected individuals and naive nestmates, is considered a type of social immunity in insect societies [4], the mechanisms of passive immunization remains to be explored [5]. Recent studies revealed an active immunization, which is characterized by social transfer to low-dose infectious pathogens and active up-regulation of nestmates’ immune systems, in ants [6] and termites [7]
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