Jens Rolff

Copulation corrupts immunity: A mechanism for a cost of mating in insects

There are well documented costs of mating in insects but little evidence for underlying mechanisms. Here, we provide experimental evidence for a hormone-based mechanism that reduces immunity as a result of mating. We examined the mealworm beetle Tenebrio molitor and show that (i) mating reduces a major humoral immune effector-system (phenoloxidase) in both sexes, and (ii) that this down-regulation is mediated by juvenile hormone. Because both juvenile hormone and phenoloxidase have highly conserved functions across all insects, the identified mechanism is similarly likely to be highly conserved. The positive physiological function of mating-induced juvenile hormone secretion is gamete and accessory gland production: we propose that its negative effects on immune function are the consequence of physiological antagonism. Therefore, we have identified a physiological tradeoff between mating and immunity. Our results suggest that increasing mating success can result in increasing periods of immune suppression, which in turn implies that reproductively successful individuals may be more vulnerable to infection by, and the negative fitness effects of, pathogens.

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.

On sexual dimorphism in immune function

Sexual dimorphism in immune function is a common pattern in vertebrates and also in a number of invertebrates. Most often, females are more ‘immunocompetent’ than males. The underlying causes are explained by either the role of immunosuppressive substances, such as testosterone, or by fundamental differences in male and female life histories. Here, we investigate some of the main predictions of the immunocompetence handicap hypothesis (ICHH) in a comparative framework using mammals. We focus specifically on the prediction that measures of sexual competition across species explain the observed patterns of variation in sex-specific immunocompetence within species. Our results are not consistent with the ICHH, but we do find that female mammals tend to have higher white blood cell counts (WBC), with some further associations between cell counts and longevity in females. We also document positive covariance between sexual dimorphism in immunity, as measured by a subset of WBC, and dimorphism in the duration of effective breeding. This is consistent with the application of ‘Batemans principle’ to immunity, with females maximizing fitness by lengthening lifespan through greater investment in immune defences. Moreover, we present a meta-analysis of insect immunity, as the lack of testosterone in insects provides a means to investigate Batemans principle for immunity independently of the ICHH. Here, we also find a systematic female bias in the expression of one of the two components of insect immune function that we investigated (phenoloxidase). From these analyses, we conclude that the mechanistic explanations of the ICHH lack empirical support. Instead, fitness-related differences between the sexes are potentially sufficient to explain many natural patterns in immunocompetence.

Examining costs of induced and constitutive immune investment in Tenebrio molitor

Central to the conceptual basis of ecological immunity is the notion that immune effector systems are costly to produce, run, and/or maintain. Using the mealworm beetle, Tenebrio molitor, as a model we investigated two aspects of the costs of innate immunity. We conducted an experiment designed to identify the cost of an induced immune response, and the cost of constitutive investment in immunity, as well as potential interactions. The immune traits under consideration were the encapsulation response and prophylactic cuticular melanization, which are mechanistically linked by the melanin‐producing phenoloxidase cascade. If immunity is costly, we predicted reduced longevity and/or fecundity as a consequence of investment in either immune trait. We found a measurable longevity cost associated with producing an inducible immune response (encapsulation). In contrast to other studies, this cost was expressed under ad libitum feeding conditions. We found no measurable costs for constitutive investment in immunity (prophylactic investment in cuticular colour).

TIME CONSTRAINTS MEDIATE PREDATOR-INDUCED PLASTICITY IN IMMUNE FUNCTION, CONDITION, AND LIFE HISTORY

The simultaneous presence of predators and a limited time for development imposes a conflict: accelerating growth under time constraints comes at the cost of higher predation risk mediated by increased foraging. The few studies that have addressed this tradeoff have dealt only with life history traits such as age and size at maturity. Physiological traits have largely been ignored in studies assessing the impact of environmental stressors, and it is largely unknown whether they respond independently of life history traits. Here, we studied the simultaneous effects of time constraints, i.e., as imposed by seasonality, and predation risk on immune defense, energy storage, and life history in lestid damselflies. As predicted by theory, larvae accelerated growth and development under time constraints while the opposite occurred under predation risk. The activity of phenoloxidase, an important component of insect immunity, and investment in fat storage were reduced both under time constraints and in the presence of predators. These reductions were smaller when time constraints and predation risk were combined. This indicates that predators can induce sublethal costs linked to both life history and physiology in their prey, and that time constraints can independently reduce the impact of predator-induced changes in life history and physiology.

Life histories and parasite pressure across the major groups of social insects.

Animal societies are aggregations of cooperating individuals that are isolated from other societies by limitations of dispersal and/or hostile exclusion mechanisms. The individuals within them are more related to the members of their own society than to random individuals in the population at large and quite often this relatedness is high because societies are families or groups of families. For parasites and diseases, however, animal societies are merely patches of suitable hosts to be colonized and exploited and to ultimately produce dispersing propagules to reach other similar patches (Freeland, 1979). Living in groups or societies has generally been thought to be associated with increased parasitism (Alexander, 1974; Freeland, 1976; Hamilton, 1987; Sherman et al., 1988; Schmid-Hempel, 1998; Côté and Poulin, 1995). However, several recent studies have questioned the generality of this assertion (Watve and Jog, 1997; Lewis, 1998; Naug and Camazine, 2002; Wilson et al., 2003). Others have provided data to show that social behaviour can also be associated with reduced parasite load, due to either behavioural interactions providing an effective defence (Rosengaus et al., 1998; Hughes et al., 2002; Traniello et al., 2002), or density-dependent immune responses (Reeson et al., 1998, Barnes and Siva-Jothy, 2000, Wilson et al., 2003). These discrepancies may result from the exact mode of transmission. In fact, a meta-analysis by Côté and Poulin (1995) has shown that rates of parasitism tend to be positively correlated with group size

Time Constraints Decouple Age and Size at Maturity and Physiological Traits

Life‐history theory predicts changes in age and size at maturity in response to constraints in animals with complex life cycles. A critical underlying assumption is that only these traits are optimized during ontogeny. However, it is not clear how altered life histories mechanistically translate into survival and fecundity. Here we present data from damselflies reared from egg to adult under day lengths mimicking the start or end (time constrained) of the season at high and low food level. These data show that an important component of immunity is suppressed under time‐constrained development as well as under low food conditions and that fat storage is affected only by food availability. Intriguingly, the physiological responses are partly decoupled from age and size at maturity, which indicates that the predictive value of traits such as age and size at maturity might well be restricted.

Priming and memory of stress responses in organisms lacking a nervous system.

Experience and memory of environmental stimuli that indicate future stress can prepare (prime) organismic stress responses even in species lacking a nervous system. The process through which such organisms prepare their phenotype for an improved response to future stress has been termed ‘priming’. However, other terms are also used for this phenomenon, especially when considering priming in different types of organisms and when referring to different stressors. Here we propose a conceptual framework for priming of stress responses in bacteria, fungi and plants which allows comparison of priming with other terms, e.g. adaptation, acclimation, induction, acquired resistance and cross protection. We address spatial and temporal aspects of priming and highlight current knowledge about the mechanisms necessary for information storage which range from epigenetic marks to the accumulation of (dormant) signalling molecules. Furthermore, we outline possible patterns of primed stress responses. Finally, we link the ability of organisms to become primed for stress responses (their ‘primability’) with evolutionary ecology aspects and discuss which properties of an organism and its environment may favour the evolution of priming of stress responses.

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.