Relish as a Candidate Marker for Transgenerational Immune Priming in a Dampwood Termite (Blattodae: Archeotermopsidae) (original) (raw)
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PLOS ONE, 2017
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.
No Evidence for Single-Copy Immune-Gene Specific Signals of Selection in Termites
Frontiers in Ecology and Evolution
Selection pressures from pathogens appear to play an important role in shaping social evolution. Social behavior, in particular brood care, is associated with pathogen pressure in wood-dwelling "lower" termites. Yet, generally pathogen pressure is predicted to be low in wood-dwelling termite species that never leave the nest except for the mating flight. In comparison, pathogen pressure is predicted to be higher in species that leave the nest to forage, and thus constantly encounter a diversity of microbes from their environment. We hypothesized that such differences in predicted pathogen pressure are also reflected by differences in the intensity of natural selection on immune genes. We tested this hypothesis in a phylogenetic framework, analyzing rates of non-synonymous and synonymous substitutions on single-copy immune genes. Therefore, we leveraged recent genomic and transcriptomic data from eight termite species, representing wooddwelling and foraging species as well as 14 additional species spanning the winged insects (Pterygota). Our results provide no evidence for a role of pathogen pressure in selection intensity on single-copy immune genes. Instead, we found evidence for a genome-wide pattern of relaxed selection in termites.
PLoS pathogens, 2015
In many vertebrates and invertebrates, offspring whose mothers have been exposed to pathogens can exhibit increased levels of immune activity and/or increased survival to infection. Such phenomena, called "Trans-generational immune priming" (TGIP) are expected to provide immune protection to the offspring. As the offspring and their mother may share the same environment, and consequently similar microbial threats, we expect the immune molecules present in the progeny to be specific to the microbes that immune challenged the mother. We provide evidence in the mealworm beetle Tenebrio molitor that the antimicrobial activity found in the eggs is only active against Gram-positive bacteria, even when females were exposed to Gram-negative bacteria or fungi. Fungi were weak inducers of TGIP while we obtained similar levels of anti-Gram-positive activity using different bacteria for the maternal challenge. Furthermore, we have identified an antibacterial peptide from the defensin ...
Paternally derived immune priming for offspring in the red flour beetle, Tribolium castaneum
Journal of Animal …, 2010
1. Parasitized females in mammals, fish and birds can enhance the immune defence of their offspring by transferring specific antibodies for the embryo. Likewise, social insect mothers transfer immunity despite the fact that invertebrates lack antibodies. 2. Female trans-generational immune priming is consistent with parental investment theory, because mothers invest more into rearing their offspring than fathers. However, when immune priming is not directly linked to parental care, as is often the case in insects that abandon their eggs after oviposition, both sexes might benefit from protecting their offspring. 3. Using the red flour beetle, Tribolium castaneum, we show that after parental exposure to heatkilled bacteria, trans-generational immune priming occurs through fathers as well as mothers. 4. This novel finding challenges the traditional view that males provide only genes to their offspring in species without paternal care, and raises the possibility of a division of tasks with respect to immune protection between parents.
Parents invest in their offspring by transmitting acquired resistance against pathogens that only the parents have encountered, a phenomenon known as trans-generational immune priming (TGIP). Examples of TGIP are widespread in the animal kingdom. Female vertebrates achieve TGIP by passing antibodies to their offspring, but the mechanisms of sex-specific TGIP in invertebrates are unclear despite increasing evidence suggesting that both male-specific and female-specific TGIP occurs in insects. We used the tobacco hornworm (Manduca sexta) to investigate sex-specific TGIP in insects because it is a model host for the analysis of insect immunity and the complete genome sequence is available. We found that feeding larvae with non-pathogenic Escherichia coli or the entomopathogen Serratia entomophila triggered immune responses in the infected host associated with shifts in both DNA methylation and histone acetylation. Maternal TGIP was mediated by the translocation of bacterial structures from the gut lumen to the eggs, resulting in the microbe-specific transcriptional reprogramming of genes encoding immunity-related effector molecules and enzymes involved in the regulation of histone acetylation as well as DNA methylation in larvae of the F1 generation. The third-instar F1 larvae displayed sex-specific differences in the expression profiles of immunity-related genes and DNA methylation. We observed crosstalk between histone acetylation and DNA methylation, which mediated sex-specific immune responses in the F1 generation derived from parents exposed to a bacterial challenge. Multiple routes for TGIP seem to exist in M. sexta and-partially sex-specific-effects in the offspring depend on the microbial exposure history of their parents. Crucially, the entomopathogen S. entomophila appears to be capable of interfering with TGIP in the host.
Insect immune priming: ecology and experimental evidences
Ecological Entomology, 2016
1. Immune priming refers to improved protection of the host after a second encounter with the same parasite or pathogen. This phenomenon is similar to that of adaptive immunity in vertebrates. 2. There is evidence to suggest that this improved protection can be species/ strain-specific and can protect organisms for a lifetime. These two attributes, along with a biphasic immune response, are essential characteristics of immune priming and form the basis for the effectiveness of resistance to parasites and pathogens. 3. This paper considers the effect of immune priming within and across generations, the influence of a heterologous challenge during immune priming and the importance of testing the immune response with natural pathogens. 4. The analysis presented takes into account the multifaceted nature of the invertebrate immune response. The lack of evidence suggesting that the bacterial microbiome plays a complementary role in the immune priming outcome is discussed. 5. Finally, the cost of immune priming is explored. This is a poorly investigated issue, which could help to explain why there is a paucity of evidence in support of immune priming.
The evolutionary dynamics of within-generation immune priming in invertebrate hosts
Journal of The Royal Society Interface, 2012
While invertebrates lack the machinery necessary for ‘acquired immunity’, there is increasing empirical evidence that exposure to low levels of disease may ‘prime’ an invertebrate's immune response, increasing its defence to subsequent exposure. Despite this increasing empirical data, there has been little theoretical attention paid to immune priming. Here, we investigate the evolution of immune priming, focusing on the role of the unique feedbacks generated by a newly developed susceptible–primed–infected epidemiological model. Contrasting our results with previous models on the evolution of acquired immunity, we highlight that there are important implications to the evolution of immunity through priming owing to these different epidemiological feedbacks. In particular, we find that in contrast to acquired immunity, priming is strongly selected for at high as well as intermediate pathogen virulence. We also find that priming may be greatest at either intermediate or high host l...