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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.
The evolution and mechanistic underpinnings of termite immunity are not well understood. Given the intimate relationship between sociality and disease, this represents a major gap in understanding, particularly since termites represent the only animal group outside of Hymenoptera to have evolved such advanced forms of social living. We explore the evolution of termite immunity by conducting qualitative and quantitative transcriptomic analyses from twelve cockroach and termite species occurring along a gradient of sociality. We incorporate lineages spanning the origin of eusociality, and include species from a key transitional subsocial group: the wood roaches. Firstly, we analyze immune characteristics in the context of termite phylogeny. Here, we examine the evolution of immune traits during the transition to eusociality, and explore the extent to which immune adaptations are associated with evolutionary shifts in social complexity and ecology. Secondly, we conduct a quantitative analysis of responses to a common immune stimulus to examine the role of both sociality and caste in immunity. Here, we test the hypothesis that the evolution of division of labour – and associated increases in investment into costly altruistic (immune) traits – occurred at the expense of individual immunity in the sterile caste.
The evolution and mechanistic underpinnings of termite immunity are not well understood. Given the intimate relationship between sociality and disease, this represents a major gap in understanding, particularly since termites represent the only animal group outside of Hymenoptera to have evolved such advanced forms of social living. We explore the evolution of termite immunity by conducting qualitative and quantitative transcriptomic analyses from twelve cockroach and termite species occurring along a gradient of sociality. We incorporate lineages spanning the origin of eusociality, and include species from a key transitional subsocial group: the wood roaches. Firstly, we analyze immune characteristics in the context of termite phylogeny. Here, we examine the evolution of immune traits during the transition to eusociality, and explore the extent to which immune adaptations are associated with evolutionary shifts in social complexity and ecology. Secondly, we conduct a quantitative analysis of responses to a common immune stimulus to examine the role of both sociality and caste in immunity. Here, we test the hypothesis that the evolution of division of labour – and associated increases in investment into costly altruistic (immune) traits – occurred at the expense of individual immunity in the sterile caste.
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.
The evolution and mechanistic underpinnings of termite immunity are not well understood. Given the intimate relationship between sociality and disease, this represents a major gap in understanding, particularly since termites represent the only animal group outside of Hymenoptera to have evolved such advanced forms of social living. We explore the evolution of termite immunity by conducting qualitative and quantitative transcriptomic analyses from twelve cockroach and termite species occurring along a gradient of sociality. We incorporate lineages spanning the origin of eusociality, and include species from a key transitional subsocial group: the wood roaches. Firstly, we analyze immune characteristics in the context of termite phylogeny. Here, we examine the evolution of immune traits during the transition to eusociality, and explore the extent to which immune adaptations are associated with evolutionary shifts in social complexity and ecology. Secondly, we conduct a quantitative analysis of responses to a common immune stimulus to examine the role of both sociality and caste in immunity. Here, we test the hypothesis that the evolution of division of labour – and associated increases in investment into costly altruistic (immune) traits – occurred at the expense of individual immunity in the sterile caste.
Diverse animal species consume toxins, minerals or secondary compounds as an adaptive response to pathogen infection – a process termed self-medication. Recent studies have also shown that macronutrients can play an important role in an individual’s infection response. For instance African army worm caterpillars select a diet rich in protein and low in carbohydrate upon baculovirus infection. Here we investigate whether dietary choice of macronutrients also plays a role in immunity in the omnivorous cockroach: Blatta orientalis. After challenging individual cockroaches with a common entomopathogenic soil bacterium, Pseudomonas entomophila, we conducted food-choice experiments using two artificial diets differing in their relative protein to carbohydrate ratio. We show for the first time that cockroaches are able to self-select a protein-enriched diet as a response to bacterial infection. This is driven by a sharp decline in carbohydrate intake rather than an increase in protein intake. Additionally, infected cockroaches reduced their overall nutrient intake, which is consistent with an illness-induced anorexia-like response. The feeding pattern of bacteria-challenged individuals returned to normality approx 4 days after challenge. We also investigate whether cockroach survival and hemolymph immunity are enhanced in individuals when restricted to a protein-rich vs. carbohydrate-rich diet. Overall, our findings demonstrate that macronutrient preferences follow a general pattern independent of pathogen type. Furthermore, we show that interactions between nutrition and immunity are highly conserved in evolution, highlighted by the fact that caterpillars and cockroaches diverged some 386 million years ago.
The termites are a derived eusocial lineage of otherwise non-social cockroaches. Understanding the proximal and ultimate drivers of this major evolutionary transition represents an important goal in biology. One outstanding question concerns the evolution of termite immunity, which is thought to have undergone broad-sweeping adaptations in order to enhance group-level immune protection. To understand the evolutionary origins of termite immunity, we conducted qualitative and quantitative transcriptome analyses along a gradient of sociality. Firstly, we aimed to identify large-scale genetic shifts in immune traits linked to eusociality by comparing immune gene repertoires in solitary and subsocial cockroaches and across a range of eusocial termite lineages. Secondly, we compared the responses of a solitary cockroach, a subsocial wood-roach and different castes of a lower termite species to a non-specific immune challenge, in order to understand how sociality may have influenced the evolution of immune gene regulation. Firstly, we found that termites have a broadly representative repertoire of canonical immune genes as compared to gregarious cockroaches and subsocial wood-roaches. Secondly, with respect to immune challenge, the solitary cockroach and the subsocial wood-roach displayed a similarly comprehensive induced response, while the termite response was considerably dampened by comparison and strongly influenced by caste; with reproductives displaying a generally higher constitutive level of immune-gene expression compared to sterile castes. In summary we did not find termite eusociality to be associated with significant changes in immune gene diversity, but rather to be linked with significant modifications to the regulation of immunity following the origin of division of labour.
The termites are a derived eusocial lineage of otherwise non-social cockroaches. Understanding the proximal and ultimate drivers of this major evolutionary transition represents an important goal in biology. One outstanding question concerns the evolution of termite immunity, which is thought to have undergone broad-sweeping adaptations in order to enhance group-level immune protection. To understand the evolutionary origins of termite immunity, we conducted qualitative and quantitative transcriptome analyses along a gradient of sociality. Firstly, we aimed to identify large-scale genetic shifts in immune traits linked to eusociality by comparing immune gene repertoires in solitary and subsocial cockroaches and across a range of eusocial termite lineages. Secondly, we compared the responses of a solitary cockroach, a subsocial wood-roach and different castes of a lower termite species to a non-specific immune challenge, in order to understand how sociality may have influenced the evolution of immune gene regulation. Firstly, we found that termites have a broadly representative repertoire of canonical immune genes as compared to gregarious cockroaches and subsocial wood-roaches. Secondly, with respect to immune challenge, the solitary cockroach and the subsocial wood-roach displayed a similarly comprehensive induced response, while the termite response was considerably dampened by comparison and strongly influenced by caste; with reproductives displaying a generally higher constitutive level of immune-gene expression compared to sterile castes. In summary we did not find termite eusociality to be associated with significant changes in immune gene diversity, but rather to be linked with significant modifications to the regulation of immunity following the origin of division of labour.
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.