Yannick Moret

Insect Immunity: An Evolutionary Ecology Perspective

Abstract We review recent advances in our understanding of the mechanisms of insect immune defence, but do so in a framework defined by the ecological and evolutionary forces that shape insect immune defence. Recent advances in genetics and molecular biology have greatly expanded our understanding of the details of the immune mechanisms that enable insects to defend themselves against parasites and pathogens. However, these studies are primarily concerned with discovering and describing how resistance mechanisms work. They rarely address the question of why they are shaped the way they are. Partly because we know so much about the mechanisms that it is now becoming possible to ask such ultimate questions about insect immunity, and they are currently emerging from the developing field of ‘ecological immunology’. In this review we first present an overview of insect immune mechanisms and their coordination before examining the key ecological/evolutionary issues associated with ecological immunity. Finally, we identify important areas for future study in insect immunity that we feel can now be approached because of the insight provided by combining mechanistic and ecological approaches.

Antimicrobial defense and persistent infection in insects.

During 400 million years of existence, insects have rarely succumbed to the evolution of microbial resistance against their potent antimicrobial immune defenses. We found that microbial clearance after infection is extremely fast and that induced antimicrobial activity starts to increase only when most of the bacteria (99.5%) have been removed. Our experiments showed that those bacteria that survived exposure to the insects constitutive immune response were subsequently more resistant to it. These results imply that induced antimicrobial compounds function primarily to protect the insect against the bacteria that persist within their body, rather than to clear microbial infections. These findings suggest that understanding of the management of antimicrobial peptides in natural systems might inform medical treatment strategies that avoid the risk of drug resistance.

Adaptive innate immunity? Responsive-mode prophylaxis in the mealworm beetle, Tenebrio molitor.

A primary infection by a parasite may indicate a higher risk of being reinfected in the near future (since infection may indicate that enemies are becoming more abundant). Acquired immunity does not exist in invertebrates despite the fact that they also face increased risks of reinfection following primary exposure. However, when subjected to immune insult, insects can produce immune responses that persist for long enough to provide prophylaxis. Because these immune responses are costly, persistence must be maintained through a selective advantage. We tested for the possibility that these long–lasting immune responses provided increased resistance to later infections by experimentally mimicking a primary immune insult (pre–challenge) in larvae of the mealworm beetle, Tenebrio molitor, with lipopolysaccharides (LPS) prior to early or late exposure to spores of the entomopathogenic fungus Metarhizium anisopliae. We found that pre–challenged larvae produced a long–lasting antimicrobial response, which provided a survival benefit when the larvae were exposed to fungal infection. These results suggest that the observed response is functionally ‘adaptive’.

Introduction. Ecological immunology.

An organisms fitness is critically reliant on its immune system to provide protection against parasites and pathogens. The structure of even simple immune systems is surprisingly complex and clearly will have been moulded by the organisms ecology. The aim of this review and the theme issue is to examine the role of different ecological factors on the evolution of immunity. Here, we will provide a general framework of the field by contextualizing the main ecological factors, including interactions with parasites, other types of biotic as well as abiotic interactions, intraspecific selective constraints (life-history trade-offs, sexual selection) and population genetic processes. We then elaborate the resulting immunological consequences such as the diversity of defence mechanisms (e.g. avoidance behaviour, resistance, tolerance), redundancy and protection against immunopathology, life-history integration of the immune response and shared immunity within a community (e.g. social immunity and microbiota-mediated protection). Our review summarizes the concepts of current importance and directs the reader to promising future research avenues that will deepen our understanding of the defence against parasites and pathogens.

‘Trans-generational immune priming’: specific enhancement of the antimicrobial immune response in the mealworm beetle, Tenebrio molitor

Encounters with parasites and pathogens are often unpredictable in time. However, experience of an infection may provide the host with reliable cues about the future risk of infection for the host itself or for its progeny. If the parental environment predicts the quality of the progenys environment, then parents may further enhance their net reproductive success by differentially providing their offspring with phenotypes to cope with potential hazards such as pathogen infection. Here, I test for the occurrence of such an adaptive transgenerational phenotypic plasticity in the mealworm beetle, Tenebrio molitor. A pathogenic environment was mimicked by injection of bacterial lipopolysaccharides for two generations of insects. I found that parental challenge enhanced offspring immunity through the inducible production of antimicrobial peptides in the haemolymph.

Immune defence in bumble-bee offspring.

Immune-challenged vertebrate females transfer specific antibodies to their offspring, but this gratuitous immunity cannot operate in invertebrates. Here we show that constitutive immune defence is enhanced in sexual offspring of the bumble-bee Bombus terrestris L. when the parental colony is immune-challenged. Our findings indicate that invertebrates may use a different component of the immune system to generate a facultative trans-generational increase in the immune response.

Senescence of immune defence in Bombus workers

Abstract 1. Senescence in workers of social insects is a particularly intriguing life‐history trait as the future fitness of workers relies primarily on age‐dependent survival rate. The pattern of senescence of immune defence traits was investigated under laboratory conditions in workers of two bumble bees: Bombus terrestris and B. lucorum.

Differential expression and costs between maternally and paternally derived immune priming for offspring in an insect

1. When parasitized, both vertebrates and invertebrates can enhance the immune defence of their offspring, although this transfer of immunity is achieved by different mechanisms. In some insects, immune-challenged males can also initiate trans-generational immune priming (TGIP), but its expressions appear qualitatively different from the one induced by females similarly challenged. 2. The existence of male TGIP challenges the traditional view of the parental investment theory, which predicts that females should invest more into their progeny than males. However, sexual dimorphism in life-history strategies and the potential costs associated with TGIP may nevertheless lead to dissymmetric investment between males and females into the immune protection of the offspring. 3. Using the yellow mealworm beetle, Tenebrio molitor, we show that after parental exposure to a bacterial-like infection, maternal and paternal TGIP are associated with the enhancement of different immune effectors and different fitness costs in the offspring. While all the offspring produced by challenged mothers had enhanced immune defence, only those from early reproductive episodes were immune primed by challenged fathers. 4. Despite the fact that males and females may share a common interest in providing their offspring with an immune protection from the current pathogenic threat, they seem to have evolved different strategies concerning this investment.

Temporal patterns in immune responses to a range of microbial insults (Tenebrio molitor).

Much work has elucidated the pathways and mechanisms involved in the production of insect immune effector systems. However, the temporal nature of these responses with respect to different immune insults is less well understood. This study investigated the magnitude and temporal variation in phenoloxidase and antimicrobial activity in the mealworm beetle Tenebrio molitor in response to a number of different synthetic and real immune elicitors. We found that antimicrobial activity in haemolymph increased rapidly during the first 48h after a challenge and was maintained at high levels for at least 14 days. There was no difference in the magnitude of responses to live or dead Escherichia coli or Bacillus subtilis. While peptidoglylcan also elicited a long-lasting antimicrobial response, the response to LPS was short lived. There was no long-lasting upregulation of phenoloxidase activity, suggesting that this immune effector system is not involved in the management of microbial infections over a long time scale.

Activation of host constitutive immune defence by an intestinal trypanosome parasite of bumble bees.

Many parasites, including important species that affect humans and livestock, must survive the harsh environment of insect guts to complete their life-cycle. Hence, understanding how insects protect themselves against such parasites has immediate practical implications. Previously, such protection has been thought to consist mainly of mechanical structures and the action of lectins. However, recently it has become apparent that gut infections may interact with the host immune system in more complex ways. Here, using bumble bees, Bombus terrestris and their non-invasive gut trypanosome, Crithidia bombi, as a model system we investigated the effects of parasitic infection, host resources and the duration of infections on the host immune system. We found that infection doubled standing levels of immune defence in the haemolymph (the constitutive pro-phenoloxidase system), which is used as a first, general defence against parasites. However, physical separation of the parasite from the haemolymph suggests the presence of a messenger system between the gut and the genes that control the pro-phenoloxidase system. Surprisingly, we found no direct effect of host resource-stress or duration of the infection on the immune system. Our results suggest a novel and tactical response of insects to gut infections, demonstrating the complexity of such host-parasite systems.