0000000000114890
AUTHOR
Yannick Moret
Limiting immunopathology: Interaction between carotenoids and enzymatic antioxidant defences.
The release of reactive oxygen and nitrogen species (ROS and RNS) during the inflammatory response generates damages to host tissues, referred to as immunopathology, and is an important factor in ecological immunology. The integrated antioxidant system, comprising endogenous antioxidant enzymes (e.g. superoxide dismutase SOD, and catalase CAT) and dietary antioxidants (e.g. carotenoids), helps to cope with immune-mediated oxidative stress. Crustaceans store large amounts of dietary carotenoids for yet unclear reasons. While being immunostimulants and antioxidants, the interaction of these pigments with antioxidant enzymes remains unclear. Here, we tested the interaction between dietary supp…
Trans-generational immune priming in the mealworm beetle protects eggs through pathogen-dependent mechanisms imposing no immediate fitness cost for the offspring.
8 pages; International audience; Immune-challenged mothers can improve their offspring immunity through trans-generational immune priming (TGIP). In insects, TGIP endows the offspring with lifetime immunity, including the eggs, which are likely exposed soon after maternal infection. Egg protection may rely on the transfer of maternal immune effectors to the egg or/and the induction of egg immune genes. These respective mechanisms are assumed to have early-life fitness costs of different magnitude for the offspring. We provide evidence in the mealworm beetle Tenebrio molitor that enhanced egg immunity following a maternal immune challenge is achieved by both of these mechanisms but in a path…
Temporal patterns in immune responses to a range of microbial insults (Tenebrio molitor).
8 pages; International audience; 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 …
Rapid induction of immune density-dependent prophylaxis in adult social insects.
The innate immune system provides defence against parasites and pathogens. This defence comes at a cost, suggesting that immune function should exhibit plasticity in response to variation in environmental threats. Density-dependent prophylaxis (DDP) has been demonstrated mostly in phase-polyphenic insects, where larval group size determines levels of immune function in either adults or later larval instars. Social insects exhibit extreme sociality, but DDP has been suggested to be absent from these ecologically dominant taxa. Here we show that adult bumble-bee workers ( Bombus terrestris ) exhibit rapid plasticity in their immune function in response to social context. These results sugges…
Personality, immune response and reproductive success: an appraisal of the pace-of-life syndrome hypothesis.
11 pages; International audience; The pace-of-life syndrome (POLS) hypothesis is an extended concept of the life-history theory that includes behavioural traits. The studies challenging the POLS hypothesis often focus on the relationships between a single personality trait and a physiological and/or life-history trait. While pathogens represent a major selective pressure, few studies have been interested in testing relationships between behavioural syndrome, and several fitness components including immunity. The aim of this study was to address this question in the mealworm beetle, Tenebrio molitor, a model species in immunity studies. The personality score was estimated from a multidimensi…
The immune role of the arthropod exoskeleton.
7 pages; International audience; The exoskeleton or cuticle of arthropods is an important feature that contributes to their great success in colonising numerous habitats on earth. It has numerous functions among which to provide protection against parasites. Whereas often regarded as a simple physical barrier to the outside world, the immune protection of the cuticle is slightly more complex than that. Here, we provide an overview of the cuticle defensive traits against parasites and examine their variation as a response to parasitism. It appears that the cuticle is an efficient line of defense, which includes physical, biochemical and physiological defensive components that are potentially…
Immune response affects ant trophallactic behaviour.
5 pages; International audience; Sociality is associated with many benefits that have favoured its evolution in social insects. However, sociability also presents disadvantages like crowding of large numbers of individuals, which may favour the spread of infections within colonies. Adaptations allowing social insects to prevent and/or control pathogen infections range from behavioural responses to physiological ones including their immune systems. In a state of infection, social interactions with nestmates should be altered in a way which might prevent its spreading. We simulated a microbial infection in workers of the ant Camponotus fellah by the administration of peptidoglycan (PGN) and t…
Variation in the immune state of Gammarus pulex (Crustacea, Amphipoda) according to temperature: are extreme temperatures a stress?
9 pages; International audience; Temperature is known to impact host-parasite interactions in various ways. Such effects are often regarded as the consequence of the increased metabolism of parasites with increasing temperature. However, the effect of temperature on hosts' immune system could also be a determinant. Here we assessed the influence of temperature on the immunocompetence of the crustacean amphipod Gammarus pulex. Amphipods play a key ecological role in freshwater ecosystems that can be altered by several parasites. We investigated the consequences of three weeks of acclimatization at four temperatures (from 9 °C to 17 °C) on different immunological parameters. Temperature influ…
Lobesia botrana larvae develop faster in the presence of parasitoids.
3 pages; International audience; To combat parasitism hosts often rely on their immune system, which is the last line of defense. However, the immune system may not always be effective, and other non-immunological defenses might be favored to reduce the cost of parasite infection. Here we report that larvae of the moth Lobesia botrana can rapidly accelerate their development and reach maturity earlier in response to cues perceived at a distance from parasitoids. Such a phenotypically plastic life history shift, induced by the perception of deadly enemies in the environment, is likely to be an adaptive defensive strategy to prevent parasitoid attack, and has important implications in host-pa…
Variation in the risk of being wounded: an overlooked factor in studies of invertebrate immune function?
In invertebrates, wounding can trigger an immune response, and will often expose organisms to parasites and pathogens. Here we show that in the amphipod Gammarus pulex, wounding abundance is negatively correlated with PhenolOxidase activity (a major component of the invertebrate immune response), and that the occurrence and abundance of wounding is extremely high and varies significantly between five natural populations. In some populations the prevalence and abundance of wounds also varied between sexes. Given that, using and maintaining an efficient immune system is costly, we suggest that the frequency of wounding may be an important selective pressure influencing an organism's optimal i…
Chromosome-scale assembly of the yellow mealworm genome
Background: The yellow mealworm beetle, Tenebrio molitor, is a promising alternative protein source for animal and human nutrition and its farming involves relatively low environmental costs. For these reasons, its industrial scale production started this century. However, to optimize and breed sustainable new T. molitor lines, the access to its genome remains essential. Methods: By combining Oxford Nanopore and Illumina Hi-C data, we constructed a high-quality chromosome-scale assembly of T. molitor. Then, we combined RNA-seq data and available coleoptera proteomes for gene prediction with GMOVE. Results: We produced a high-quality genome with a N50 = 21.9Mb with a completeness of 99.5% an…
No evidence of an immune adjustment in response to a parasitoid threat in Lobesia botrana larvae.
5 pages; International audience; Immune function is a key determinant of an organism's fitness, and natural insect populations are highly variable for this trait, mainly due to environmental heterogeneity and pathogen diversity. We previously reported a positive correlation between infection prevalence by parasitoids and host immunity in natural populations of the vineyard pest Lobesia botrana. Here, we tested whether this correlation reflects a plastic adjustment of host immunity in response to the local presence of parasites. To this end, we measured immunity of non-parasitized L. botrana larvae exposed, respectively, to one of the two most common species of parasitoids in vineyards, over…
Larval personality does not predict adult personality in a holometabolous insect.
10 pages; International audience; Although personality (consistent inter-individual differences in behavioural traits across time and/or contexts) and behavioural syndromes (suites of correlated personality traits) have been widely studied in the last decades, the origin and development of these traits during ontogeny are still underexplored. In this context, species undergoing metamorphosis are of special interest. To date, however, the persistence of personality traits has been only little investigated in organisms undergoing complete metamorphosis such as in holometabolous insects, although this kind of studies may provide important insights from a functional point of view. Here, we test…
Contrôle des ravageurs de cultures par les ennemis naturels : la plante hôte facteur régulateur du système immunitaire des chenilles de vers de la grappe.
10 pages; National audience; En raison des nombreux dégâts occasionnés par les vers de la grappe dans les vignobles, trouver un moyen de lutte efficace est devenu un réel challenge. A l’heure actuelle, la lutte biologique apparaît comme une alternative possible à la lutte chimique. Cependant, les résultats obtenus suite aux lâchers de parasitoïdes sont extrêmement variables dans leur efficacité. Des études approfondies de la biologie des vers de la grappe et de leurs parasitoïdes sont donc nécessaires afin d’affiner les méthodes de lutte biologique. Le système immunitaire des insectes représente la dernière ligne de défense des phytophages contre les parasitoïdes. Dans cette étude nous mett…
Immune depression induced by acanthocephalan parasites in their intermediate crustacean host: consequences for the risk of super-infection and links with host behavioural manipulation.
9 pages; International audience; Parasite survival in hosts mainly depends on the capacity to circumvent the host immune response. Acanthocephalan infections in gammarids are linked with decreased activity of the prophenoloxidase (ProPO) system, suggesting an active immunosuppression process. Nevertheless, experimental evidence for this hypothesis is lacking: whether these parasites affect several immune pathways is unknown and the consequences of such immune change have not been investigated. In particular, the consequences for other pathogens are not known; neither are the links with other parasite-induced manipulations of the host. Firstly, using experimental infections of Pomphorhynchus…
Defense strategies used by two sympatric vineyard moth pests.
8 pages; International audience; Natural enemies including parasitoids are the major biological cause of mortality among phytophagous insects. In response to parasitism, these insects have evolved a set of defenses to protect themselves, including behavioral, morphological, physiological and immunological barriers. According to life history theory, resources are partitioned to various functions including defense, implying trade-offs among defense mechanisms. In this study we characterized the relative investment in behavioral, physical and immunological defense systems in two sympatric species of Tortricidae (Eupoecilia ambiguella, Lobesia botrana) which are important grapevine moth pests. …
Immunocompetence increases with larval body size in a phytophagous moth
Despite the obvious benefit of an immune system, its efficacy against pathogens and parasites may show great variation among individuals, populations and species. Understanding the causes of this variation is becoming a central theme in ecology. Many biotic and abiotic factors are known to influence immunocompetence (temperature, age, etc.). However, for a given age, size among individuals varies, probably as a result of accumulated resources. Thus, these variable resources could be allocated to immune defence and, consequently, body size may explain part of the variation in immune responsiveness. However, the influence of body size on immune defence is often overlooked. The present study i…
Food-mediated modulation of immunity in a phytophagous insect: An effect of nutrition rather than parasitic contamination.
7 pages; International audience; Inherent to the cost of immunity, the immune system itself can exhibit tradeoffs between its arms. Phytophagous insects face a wide range of microbial and eukaryotic parasites, each activating different immune pathways that could compromise the activity of the others. Feeding larvae are primarily exposed to microbes, which growth is controlled by antibiotic secondary metabolites produced by the host plant. The resulting variation in abundance of microbes on plants is expected to differentially stimulate the insect antimicrobial immune defenses. Under the above tradeoff hypothesis, stimulation of the insect antimicrobial defenses is expected to compromise imm…
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 insect's 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 f…
Relationship between maternal transfer of immunity and mother fecundity in an insect.
Trans-generational immune priming (TGIP) corresponds to the plastic adjustment of offspring immunity as a result of maternal immune experience. TGIP is expected to improve mother's fitness by improving offspring individual performance in an environment where parasitism becomes more prevalent. However, it was recently demonstrated that maternal transfer of immunity to the offspring is costly for immune-challenged female insects. Thus, these females might not provide immune protection to all their offspring because of the inherent cost of other fitness-related traits. Females are therefore expected to adjust their investment to individual offspring immune protection in ways that maximize the…
Immunoécologie des vertébrés et invertébrés : recherche sur la variabilité naturelle de la résistance parasitaire.
1 page; National audience
Introduction. Ecological immunology.
12 pages; International audience; An organism's 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 organism's 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 popula…
The presence of conifer resin decreases the use of the immune system in wood ants.
5 pages; International audience; 1. Wood ants ( Formica paralugubris ) incorporate large amounts of solidified conifer resin into their nest, which reduces the density of many bacteria and fungi and protects the ants against some detrimental micro-organisms. By inducing an environment unfavourable to pathogens, the presence of resin may allow workers to reduce the use of their immune system. 2. The present study tested the hypothesis that the presence of resin decreases the immune activity of wood ants. Specifically, three components of the humoral immune defences of workers kept in resin-rich and resin-free experimental nests (antibacterial, lytic, and prophenoloxidase activities) were com…
Host plant variation plastically impacts different traits of the immune system of a phytophagous insect
Summary 1. Host plant quality affects herbivorous insect performance and consequently their susceptibility to natural enemies. Recently, it has been hypothesized that the immune function of herbivorous insects can be altered by their host plant, thus generating variation in their susceptibility to entomopathogens. Previous studies testing this hypothesis provided contradictory outcomes, mainly as a result of the differences in methodology such as measuring a single-immune parameter rather than considering trade-off-mediated interactions between immune defence systems of the insect. Here, we hypothesized that plant-mediated changes in insect immunity could result from the alteration of physi…
Trans-generational immune priming is constrained by the maternal immune response in an insect.
5 pages; International audience; Immune-challenged vertebrate and invertebrate females can transfer immunity to their off spring. Th is trans-generational immune priming (TGIP) is benefi cial for the off spring if the maternal infection risk persists across generations. However, because immunity is costly, fi tness consequences of TGIP have been found in primed off spring. Furthermore, transferring immunity to off spring may be costly for immune-challenged females who are also carrying the costs of their immune response. A negative relationship between levels of immunity between mothers and off spring might therefore be expected. Consistent with this hypothesis, we show that in the insect, …
Condition-dependent ecdysis and immunocompetence in the amphipod crustacean, Gammarus pulex.
The exoskeleton of arthropods forms an efficient protection against pathogens, but this first line of defence is periodically weakened during ecdysis, increasing the opportunity for surrounding pathogens to invade the body cavity. Since the richness of pathogens in the environment can be spatially and temporally variable, arthropods may have a fitness advantage in moulting in a place and time of low infection risk. Consistent with this hypothesis, we found that the amphipod crustacean, Gammarus pulex , exhibits temporal adjustment of the moult cycle in response to elevated risks of infection. Interestingly, this phenomenon is variable between two populations and independent of levels of im…
Is there a role for antioxidant carotenoids in limiting self-harming immune response in invertebrates?
Innate immunity relies on effectors, which produce cytotoxic molecules that have not only the advantage of killing pathogens but also the disadvantage of harming host tissues and organs. Although the role of dietary antioxidants in invertebrate immunity is still unknown, it has been shown in vertebrates that carotenoids scavenge cytotoxic radicals generated during the immune response. Carotenoids may consequently decrease the self-harming cost of immunity. A positive relationship between the levels of innate immune defence and circulating carotenoid might therefore be expected. Consistent with this hypothesis, we show that the maintenance and use of the prophenoloxidase system strongly cor…
Biological invasion and parasitism: invaders do not suffer from physiological alterations of the acanthocephalan Pomphorhynchus laevis.
SUMMARYBiological invasions expose parasites to new invasive hosts in addition to their local hosts. However, local parasites are often less successful in infecting and exploiting their new hosts. This may have major consequences for the competitive ability of hosts, and finally on the fate of the parasite-host community. In Burgundy (Eastern France), the acanthocephalan parasite,Pomphorhynchus laevis, infects 2 amphipod species living in sympatry: the nativeGammarus pulexand the invasiveGammarus roeseli. WhileP. laevisaffects the behaviour and the immunity ofG. pulex,G. roeseliseems unaffected by the infection. In this study, we examined in detail the ability of the parasite to affect the …
The relative abundance of hemocyte types in a polyphagous moth larva depends on diet.
7 pages; International audience; Hemocytes are crucial cells of the insect immune system because of their involvement in multiple immune responses including coagulation, phagocytosis and encapsulation. There are various types of hemocytes, each having a particular role in immunity, such that variation in their relative abundance affects the outcome of the immune response. This study aims to characterize these various types of hemocytes in larvae of the grapevine pest insect Eupoecilia ambiguella, and to assess variation in their concentration as a function of larval diet and immune challenge. Four types of hemocytes were found in the hemolymph of 5th instar larvae: granulocytes, oenocytoids…
Should grape moth larval immunity help explaining resistance against natural enemies?
National audience; In tritrophic systems (plants, phytophagous insects and natural enemies), host plant variation often keys the relative performance of both the herbivore and its associated natural enemies. In bottom-up effects, host plants could affect the fitness of phytophagous insects including growth rate and adult fertility. These effects are indirectly reflected in parasitoids whose success depends on their host quality. For instance, nutrient deficiency or/and toxic defensive compounds of the plants could slow-down the development of herbivorous insects, thus extending the window of vulnerability of attacks by natural enemies. The immune system is arguably the most common resistanc…
Is the host or the parasite the most locally adapted in an amphipod–acanthocephalan relationship? A case study in a biological invasion context
8 pages; International audience; Manipulative endoparasites with complex life cycles can alter their intermediate host immunity and behaviour in ways that increase survival probability within the host body cavity and enhance successful transmission to the definitive host. These parasitic manipulations are variable among and within parasite species and may result from co-evolutionary processes, in which the parasite is constrained for adaptation to the local intermediate host. Hence, arrival of a new host species in a local host population may promote local parasite maladaptation. This study tested the occurrence of local adaptation in two distantly located populations of the acanthocephalan…
Differential phenoloxidase activity between native and invasive gammarids infected by local acanthocephalans: differential immunosuppression?
Manipulative endoparasites can alter the behaviour and the physiology of their intermediate hosts in ways that increase the probability of successful transmission to the final host. This requires that the parasite is able to circumvent its host's immune defence. Successful immune evasion may depend on host-parasite coevolutionary history and the appearance of new hosts invading the local host population may promote local parasite maladaptation. To test this hypothesis, we examined the effect of 2 acanthocephalan parasites, Pomphorhynchus laevis and Polymorphus minutus, on the immunity of their local and new invasive gammarid intermediate hosts, respectively Gammarus pulex and Gammarus roese…
DYNAMIC TRANSMISSION, HOST QUALITY, AND POPULATION STRUCTURE IN A MULTIHOST PARASITE OF BUMBLEBEES
The evolutionary ecology of multihost parasites is predicted to depend upon patterns of host quality and the dynamics of transmission networks. Depending upon the differences in host quality and transmission asymmetries, as well as the balance between intra- and interspecific transmission, the evolution of specialist or generalist strategies is predicted. Using a trypanosome parasite of bumblebees, we ask how host quality and transmission networks relate to parasite population structure across host species, and thus the potential for the evolution of specialist strains adapted to different host species. Host species differed in quality, with parasite growth varying across host species. High…
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 in…
Behavioural and physiological effects of the trophically transmitted cestode parasite, Cyathocephalus truncatus, on its intermediate host, Gammarus pulex
SUMMARYSome parasites with complex life-cycles are able to manipulate the behaviour of their intermediate hosts in a way that increases their transmission to the next host. Gammarids infected by the tapeworm Cyathocephalus truncatus (Cestoda: Spathebothriidea) are known to be more predated by fish than uninfected ones, but potential behavioural manipulation by the parasite has never been investigated. In this study, we tested the hypothesis that C. truncatus is able to manipulate the behaviour of one of its intermediate hosts, Gammarus pulex (Crustacea: Amphipoda). To assess if any behavioural change was linked to other phenotypic alterations, we also measured the immunity of infected and u…
Origin of the natural variation in the storage of dietary carotenoids in freshwater amphipod crustaceans
16 pages; International audience; Carotenoids are diverse lipophilic natural pigments which are stored in variable amounts by animals. Given the multiple biological functions of carotenoids, such variation may have strong implications in evolutionary biology. Crustaceans such as Gammarus amphipods store large amounts of these pigments and inter-population variation occurs. While differences in parasite selective pressure have been proposed to explain this variation, the contribution of other factors such as genetic differences in the gammarid ability to assimilate and/or store pigments, and the environmental availability of carotenoids cannot be dismissed. This study investigates the relati…
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 ulti…
Origin of the natural variation in the storage of dietary carotenoids in freshwater amphipod crustaceans
Carotenoids are diverse lipophilic natural pigments which are stored in variable amounts by animals. Given the multiple biological functions of carotenoids, such variation may have strong implications in evolutionary biology. Crustaceans such as Gammarus amphipods store large amounts of these pigments and inter-population variation occurs. While differences in parasite selective pressure have been proposed to explain this variation, the contribution of other factors such as genetic differences in the gammarid ability to assimilate and/or store pigments, and the environmental availability of carotenoids cannot be dismissed. This study investigates the relative contributions of the gammarid g…
Data from: Dynamic transmission, host quality and population structure in a multi-host parasite of bumble bees
The evolutionary ecology of multi-host parasites is predicted to depend upon patterns of host quality and the dynamics of transmission networks. Depending upon the differences in host quality and transmission asymmetries, as well as the balance between intra- and inter-specific transmission, the evolution of specialist or generalist strategies is predicted. Using a trypanosome parasite of bumble bees we ask how host quality and transmission networks relate to parasite population structure across host species, and thus the potential for the evolution of specialist strains adapted to different host species. Host species differed in quality, with parasite growth varying across host species. Hi…
Data from: Personality, immune response and reproductive success: an appraisal of the pace-of-life syndrome hypothesis
The pace-of-life syndrome (POLS) hypothesis is an extended concept of the life-history theory that includes behavioural traits. The studies challenging the POLS hypothesis often focus on the relationships between a single personality trait and a physiological and/or life-history trait. While pathogens represent a major selective pressure, few studies have been interested in testing relationships between behavioural syndrome, and several fitness components including immunity. The aim of this study was to address this question in the mealworm beetle, Tenebrio molitor, a model species in immunity studies. The personality score was estimated from a multidimensional syndrome based of four repeat…