Open Access

The evolution of biological complexity is associated with the emergence of bespoke immune systems that maintain and protect organism integrity. Unlike the well-studied immune systems of cells and individuals, little is known about the origins of immunity during the transition to eusociality, a major evolutionary transition comparable to the evolution of multicellular organisms from single-celled ancestors. We aimed to tackle this by characterizing the immune gene repertoire of 18 cockroach and termite species, spanning the spectrum of solitary, subsocial and eusocial lifestyles. We find that key transitions in termite sociality are correlated with immune gene family contractions. In cross-species comparisons of immune gene expression, we find evidence for a caste-specific social defence system in termites, which appears to operate at the expense of individual immune protection. Our study indicates that a major transition in organismal complexity may have entailed a fundamental reshaping of the immune system optimized for group over individual defence.

It is thought that the primary function of soldier castes in insect societies is to protect colonies against macroscale predators and parasites. By comparison, little attention has been paid to the role of soldiers against pathogenic microorganisms. This is a significant gap in knowledge because in non-hymenopteran societies, such as the eusocial termites, the first-evolved, and arguably most important sterile caste, is the soldier. Here, we investigate whether soldiers of the wood-eating termite, Mastotermes darwiniensis, play a significant role in social immunity. Firstly, we show that uninfected soldiers improve the survival of worker nestmates exposed to a lethal dose of a fungal pathogen, despite the fact that soldiers (unlike workers) cannot allogroom. Hazard ratios of pathogen-exposed workers decreased from 6.616 in infected groups to 4.376 and 2.786 in infected groups containing uninfected workers and soldiers, respectively. To explore the basis of soldier protection, we applied soldier-derived oral secretions to infected worker cuticle, resulting in significantly improved worker survival. Soldiers that contacted infected workers were also more active and produced secretions with significantly greater mass variance than soldiers exposed to uninfected workers. Significantly, we show that secretions produced by soldiers inhibit the growth of a broad range of microorganisms, including gram-negative and gram-positive bacteria, in addition to fungi. Our findings demonstrate that soldiers can contribute powerful antimicrobial factors to external immune defenses, effectively complementing behaviour-based protective activities provided by workers.

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.

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.

Virulence determines the impact a pathogen has on the fitness of its host, yet current understanding of the evolutionary origins and causes of virulence of many pathogens is surprisingly incomplete. Here, we explore the evolution of Marek’s disease virus (MDV), a herpesvirus commonly afflicting chickens and rarely other avian species. The history of MDV in the 20th century represents an important case study in the evolution of virulence. The severity of MDV infection in chickens has been rising steadily since the adoption of intensive farming techniques and vaccination programs in the 1950s and 1970s, respectively. It has remained uncertain, however, which of these factors is causally more responsible for the observed increase in virulence of circulating viruses. We conducted a phylogenomic study to understand the evolution of MDV in the context of dramatic changes to poultry farming and disease control. Our analysis reveals evidence of geographical structuring of MDV strains, with reconstructions supporting the emergence of virulent viruses independently in North America and Eurasia. Of note, the emergence of virulent viruses appears to coincide approximately with the introduction of comprehensive vaccination on both continents. The time-dated phylogeny also indicated that MDV has a mean evolutionary rate of ~1.6 × 10−5 substitutions per site per year. An examination of gene-linked mutations did not identify a strong association between mutational variation and virulence phenotypes, indicating that MDV may evolve readily and rapidly under strong selective pressures and that multiple genotypic pathways may underlie virulence adaptation in MDV.