Immune Defense Traits Research Articles

Ecological determinants of variation in phenotypic selection on quantitative immune defence traits

Immune defence is an important determinant of organismal fitness. While theoretical models based on tradeoffs in resource allocation predict quantitative immune traits to be subject to stabilizing selection due to associated energetic costs and self‐harm, empirical studies report mainly positive directional selection. This discrepancy may arise from multiple ecological factors that vary in nature and could influence selection. We examined if selection on immune activity varies depending on immune challenge/infection risk, between immune traits and among populations in the freshwater snail Lymnaea stagnalis. We assessed selection on the phenoloxidase‐like and antibacterial activity of snail haemolymph while manipulating the level of immune challenge imposed by environmental microbes. We did this using snails from multiple populations and also quantified within‐population family‐level variation (i.e. evolutionary potential) in the snails' immune activity. We found that the strength of immune challenge and the examined immune trait determined selection on the snails' immune function. Thus, variation in infection risk can be an important factor in maintaining genetic variation in defence traits. Additionally, immune traits showed low among‐population differentiation but high within‐population genetic variation. This pattern could arise if natural snail populations are exposed to higher temporal than spatial variation in infection risk.

Examining adaptive evolution of immune activity: opportunities provided by gastropods in the age of 'omics'.

Parasites threaten all free-living organisms, including molluscs. Understanding the evolution of immune defence traits in natural host populations is crucial for predicting their long-term performance under continuous infection risk. Adaptive trait evolution requires that traits are subject to selection (i.e. contribute to organismal fitness) and that they are heritable. Despite broad interest in the evolutionary ecology of immune activity in animals, the understanding of selection on and evolutionary potential of immune defence traits is far from comprehensive. For instance, empirical observations are only rarely in line with theoretical predictions of immune activity being subject to stabilizing selection. This discrepancy may be because ecoimmunological studies can typically cover only a fraction of the complexity of an animal immune system. Similarly, molecular immunology/immunogenetics studies provide a mechanistic understanding of immunity, but neglect variation that arises from natural genetic differences among individuals and from environmental conditions. Here, we review the current literature on natural selection on and evolutionary potential of immune traits in animals, signal how merging ecological immunology and genomics will strengthen evolutionary ecological research on immunity, and indicate research opportunities for molluscan gastropods for which well-established ecological understanding and/or 'immune-omics' resources are already available. This article is part of the Theo Murphy meeting issue 'Molluscan genomics: broad insights and future directions for a neglected phylum'.

Effects of immune challenge on expression of life-history and immune trait expression in sexually reproducing metazoans\u2014a meta-analysis

BackgroundLife-history theory predicts a trade-off between investment into immune defence and other fitness-related traits. Accordingly, individuals are expected to upregulate their immune response when subjected to immune challenge. However, this is predicted to come at the expense of investment into a range of other traits that are costly to maintain, such as growth, reproduction and survival. Currently, it remains unclear whether the magnitude of such costs, and trade-offs involving immune investment and other traits, manifests consistently across species and sexes. To address this, we conducted a meta-analysis to investigate how changes in sex, ontogenetic stage and environmental factors shape phenotypic trait expression following an immune challenge.ResultsWe explored the effects of immune challenge on three types of traits across sexually reproducing metazoans: life-history, morphological and proximate immune traits (235 effect sizes, 53 studies, 37 species [21 invertebrates vs. 16 vertebrates]). We report a general negative effect of immune challenge on survival and reproduction, a positive effect on immune trait expression, but no effect on morphology or development time. The negative effects of immune challenge on reproductive traits and survival were larger in females than males. We also report a pronounced effect of the immune treatment agent used (e.g. whether the treatment involved a live pathogen or not) on the host response to immune challenge, and find an effect of mating status on the host response in invertebrates.ConclusionThese results suggest that costs associated with immune deployment following an immune challenge are context-dependent and differ consistently in their magnitude across the sexes of diverse taxonomic lineages. We synthesise and discuss the outcomes in the context of evolutionary theory on sex differences in life-history and highlight the need for future studies to carefully consider the design of experiments aimed at disentangling the costs of immune deployment.

Balancing Life History Investment Decisions in Founding Ant Queens

Reproduction is a very critical step in the life of an organism. Females must balance their investment in different life-history traits while reproducing. During the process of colony founding in social organisms, such as ants or bees, a trade-off between reproduction and immunity might be very stringent, because queens might be constrained to invest into immune protection of themselves and their developing offspring until the first workers emerge. Here we investigate how different levels of microbial pressure affect colony founding success of Lasius niger ant queens and whether investment into immune defense traits comes at a substantial cost to the queens. In a first experiment mated queens were exposed to four different environments: sterile housing, autoclaved soil, untreated soil and soil containing two opportunistic pathogens. In this experiment, we investigated an immediate cost, i.e., the success of producing the first brood, and a potential delayed cost, i.e., queen survival and colony founding success after hibernation. For the latter, we removed the first brood after hibernation to reveal hidden costs via the application of an additional stressor. We found that irrespective of the microbial environment all queens successfully managed to start a colony, with queens in the soil treatments showing a higher worker production than the queens in the sterile environment. This suggests that either soil components or soil microbes benefit colony growth. After hibernation queens in microbe soil showed significantly lower survival and could not replace a lost brood. In a second experiment, we investigated whether external immune defense in the form of formic acid use can explain part of the costs imposed on queens. We found that queens used formic acid to sanitize their new nest suggesting that queens founding a colony under high microbial pressure are forced to pay a substantial cost by investing in both reproduction and immunity simultaneously. Our results suggest that early, simultaneous investment in reproduction and immunity can allow colony growth under microbial pressure but may be costly in terms of resistance to later challenges. Ant queens may thus be trading off insurance against future challenges for increased pathogen immunity.

Diurnal variation around an optimum and near-critically high temperature does not alter the performance of an ectothermic aquatic grazer.

The growing threat of global climate change has led to a profusion of studies examining the effects of warming on biota. Despite the potential importance of natural variability such as diurnal temperature fluctuations, most experimental studies on warming are conducted under stable temperatures. Here, we investigated whether the responses of an aquatic invertebrate grazer (Lymnaea stagnalis) to an increased average temperature differ when the thermal regime is either constant or fluctuates diurnally. Using thermal response curves for several life‐history and immune defense traits, we first identified the optimum and near‐critically high temperatures that Lymnaea potentially experience during summer heat waves. We then exposed individuals that originated from three different populations to these two temperatures under constant or fluctuating thermal conditions. After 7 days, we assessed growth, reproduction, and two immune parameters (phenoloxidase‐like activity and antibacterial activity of hemolymph) from each individual. Exposure to the near‐critically high temperature led to increased growth rates and decreased antibacterial activity of hemolymph compared to the optimum temperature, whilst temperature fluctuations had no effect on these traits. The results indicate that the temperature level per se, rather than the variability in temperature was the main driver altering trait responses in our study species. Forecasting responses in temperature‐related responses remains challenging, due to system‐specific properties that can include intraspecific variation. However, our study indicates that experiments examining the effects of warming using constant temperatures can give similar predictions as studies with fluctuating thermal dynamics, and may thus be useful indicators of responses in nature.

Inbreeding does not alter the response to an experimental heat wave in a freshwater snail.

Global climate change affects natural populations of many species by increasing the average temperature and the frequency of extreme weather events (e.g. summer heat waves). The ability of organisms to cope with these environmental changes can, however, depend on their genetic properties. For instance, genetic load owing to inbreeding could alter organisms’ responses to climate change-mediated environmental changes but such effects are often overlooked. We investigated the effects of an experimental heat wave (25°C versus 15°C) on life history (reproduction, size) and constitutive immune defence traits (phenoloxidase-like and antibacterial activity of haemolymph) in relation to inbreeding by manipulating the mating type (outcrossing, self-fertilization) in two populations of a hermaphroditic freshwater snail, Lymnaea stagnalis. High temperature increased reproduction and size of snails but impaired their immune function. In one of the two study populations, inbreeding reduced reproductive output of snails indicating inbreeding depression. Furthermore, this effect did not depend on the temperature snails were exposed to. Our results suggest that L. stagnalis snails can be negatively affected by inbreeding but it may not alter their responses to heat waves.

Rodeo™ Herbicide Negatively Affects Blanchard's Cricket Frogs (Acris blanchardi) Survival and Alters the Skin-Associated Bacterial Community

Abstract Disease-associated mortality is a leading cause of amphibian declines and extinctions worldwide. Understanding the influence of land-management practices, like herbicide use, on amphibian immune defense traits could guide changes to improve conservation outcomes. Amphibians are partially protected from pathogens by two skin-associated immune defense traits: bacterial communities inhabiting their skin, and antimicrobial peptides secreted by the skin. Utilizing the Blanchard's Cricket Frog (Acris blanchardi), a declining North American amphibian species, as our model, we manipulated Rodeo™ aquatic herbicide concentration and the life stage at which Rodeo exposure occurred. We assessed juvenile survival, time to metamorphosis, juvenile mass, and skin-associated immune defense traits. We found a 37% decrease in survival of larvae exposed to 2.5 mg a.e. L−1 (acid equivalent) compared to controls despite that this commercial herbicide formulation does not contain an added surfactant. Surviving larvae e...

Potential for adaptation to climate change: family-level variation in fitness-related traits and their responses to heat waves in a snail population

BackgroundOn-going global climate change poses a serious threat for natural populations unless they are able to evolutionarily adapt to changing environmental conditions (e.g. increasing average temperatures, occurrence of extreme weather events). A prerequisite for evolutionary change is within-population heritable genetic variation in traits subject to selection. In relation to climate change, mainly phenological traits as well as heat and desiccation resistance have been examined for such variation. Therefore, it is important to investigate adaptive potential under climate change conditions across a broader range of traits. This is especially true for life-history traits and defences against natural enemies (e.g. parasites) since they influence organisms’ fitness both directly and through species interactions. We examined the adaptive potential of fitness-related traits and their responses to heat waves in a population of a freshwater snail, Lymnaea stagnalis. We estimated family-level variation and covariation in life history (size, reproduction) and constitutive immune defence traits [haemocyte concentration, phenoloxidase (PO)-like activity, antibacterial activity of haemolymph] in snails experimentally exposed to typical (15 °C) and heat wave (25 °C) temperatures. We also assessed variation in the reaction norms of these traits between the treatments.ResultsWe found that at the heat wave temperature, snails were larger and reproduced more, while their immune defence was reduced. Snails showed high family-level variation in all examined traits within both temperature treatments. The only negative genetic correlation (between reproduction and antibacterial activity) appeared at the high temperature. However, we found no family-level variation in the responses of most examined traits to the experimental heat wave (i.e. largely parallel reaction norms between the treatments). Only the reduction of PO-like activity when exposed to the high temperature showed family-level variation, suggesting that the cost of heat waves may be lower for some families and could evolve under selection.ConclusionOur results suggest that there is genetic potential for adaptation within both thermal environments and that trait evolution may not be strongly affected by trade-offs between them. However, rare differences in thermal reaction norms across families indicate limited evolutionary potential in the responses of snails to changing temperatures during extreme weather events.

Natural selection on immune defense: A field experiment.

Predicting the evolution of phenotypic traits requires an understanding of natural selection on them. Despite its indispensability in the fight against parasites, selection on host immune defense has remained understudied. Theory predicts immune traits to be under stabilizing selection due to associated trade-offs with other fitness-related traits. Empirical studies, however, report mainly positive directional selection. This discrepancy could be caused by low phenotypic variation in the examined individuals and/or variation in host resource level that confounds trade-offs in empirical studies. In a field experiment where we maintained Lymnaea stagnalis snails individually in cages in a lake, we investigated phenotypic selection on two immune defense traits, phenoloxidase (PO)-like activity and antibacterial activity, in hemolymph. We used a diverse laboratory population and manipulated snail resource level by limiting their food supply. For six weeks, we followed immune activity, growth, and two fitness components, survival and fecundity of snails. We found that PO-like activity and growth were under stabilizing selection, while antibacterial activity was under positive directional selection. Selection on immune traits was mainly driven by variation in survival. The form of selection on immune defense apparently depends on the particular trait, possibly due to its importance for countering the present parasite community.

Estimating Genetic and Maternal Effects Determining Variation in Immune Function of a Mixed-Mating Snail.

Evolution of host defenses such as immune function requires heritable genetic variation in them. However, also non-genetic maternal effects can contribute to phenotypic variation, thus being an alternative target for natural selection. We investigated the role of individuals’ genetic background and maternal effects in determining immune defense traits (phenoloxidase and antibacterial activity of hemolymph), as well as in survival and growth, in the simultaneously hermaphroditic snail Lymnaea stagnalis. We utilized the mixed mating system of this species by producing full-sib families in which each parental snail had produced offspring as both a dam and as a sire, and tested whether genetic background (family) and non-genetic maternal effects (dam nested within family) explain trait variation. Immune defense traits and growth were affected solely by individuals’ genetic background. Survival of snails did not show family-level variation. Additionally, some snails were produced through self-fertilization. They showed reduced growth and survival suggesting recessive load or overdominance. Immune defense traits did not respond to inbreeding. Our results suggest that the variation in snail immune function and growth was due to genetic differences. Since immune traits did not respond to inbreeding, this variation is most likely due to additive or epistatic genetic variance.

Landscape and water characteristics correlate with immune defense traits across Blanchard's cricket frog (Acris blanchardi) populations

Due to ease of global transportation, disease threats to amphibians are expected to increase. Therefore it is crucial that we improve our understanding of factors which may depress disease resistance so that we can incorporate this information into long-term conservation planning. Amphibians are protected from disease-causing pathogens by two skin-associated immune defense traits: the skin microbiome and the antimicrobial peptides found within natural peptide secretions (NPS) produced by the skin. Particular environmental characteristics may alter these amphibian immune defense traits and potentially affect disease resistance. We surveyed the skin-associated microbial communities (microbiome) and natural peptide secretions (NPS) of Blanchard's cricket frogs (Acris blanchardi), at each of eleven sites across the species' declining range. We utilized an AICc model selection and model averaging approach to test for potential environmental influence on these traits. We found that populations differed in microbiomes and NPS production, but not NPS bioactivity against Bd (Batrachochytrium dendrobatidis). The microbiome was associated with water conductivity, ratio of natural to managed land, and latitude. Additionally the microbiome was affected by interactions between frog sex and latitude, between frog sex and water surface area, and between the ratio of natural to managed land and water surface area. NPS production was influenced by an interaction between water surface area and conductivity. We found no evidence that NPS influence the microbiome; however, Bd growth rate in culture was positively associated with NPS production. This study indicates that environmental characteristics influence amphibian immune defense traits and may explain population differences in pathogen resistance.

Larval Environment Alters Amphibian Immune Defenses Differentially across Life Stages and Populations.

Recent global declines, extirpations and extinctions of wildlife caused by newly emergent diseases highlight the need to improve our knowledge of common environmental factors that affect the strength of immune defense traits. To achieve this goal, we examined the influence of acidification and shading of the larval environment on amphibian skin-associated innate immune defense traits, pre and post-metamorphosis, across two populations of American Bullfrogs (Rana catesbeiana), a species known for its wide-ranging environmental tolerance and introduced global distribution. We assessed treatment effects on 1) skin-associated microbial communities and 2) post-metamorphic antimicrobial peptide (AMP) production and 3) AMP bioactivity against the fungal pathogen Batrachochytrium dendrobatidis (Bd). While habitat acidification did not affect survival, time to metamorphosis or juvenile mass, we found that a change in average pH from 7 to 6 caused a significant shift in the larval skin microbial community, an effect which disappeared after metamorphosis. Additionally, we found shifts in skin-associated microbial communities across life stages suggesting they are affected by the physiological or ecological changes associated with amphibian metamorphosis. Moreover, we found that post-metamorphic AMP production and bioactivity were significantly affected by the interactions between pH and shade treatments and interactive effects differed across populations. In contrast, there were no significant interactions between treatments on post-metamorphic microbial community structure suggesting that variation in AMPs did not affect microbial community structure within our study. Our findings indicate that commonly encountered variation in the larval environment (i.e. pond pH and degree of shading) can have both immediate and long-term effects on the amphibian innate immune defense traits. Our work suggests that the susceptibility of amphibians to emerging diseases could be related to variability in the larval environment and calls for research into the relative influence of potentially less benign anthropogenic environmental changes on innate immune defense traits.

Natural selection on quantitative immune defence traits: a comparison between theory and data.

Parasites present a threat for free-living species and affect several ecological and evolutionary processes. Immune defence is the main physiological barrier against infections, and understanding its evolution is central for predicting disease dynamics. I review theoretical predictions and empirical data on natural selection on quantitative immune defence traits in the wild. Evolutionary theory predicts immune traits to be under stabilizing selection owing to trade-offs between immune function and life-history traits. Empirical data, however, support mainly positive directional selection, but also show variation in the form of selection among study systems, immune traits and fitness components. I argue that the differences between theory and empirical data may at least partly arise from methodological difficulties in testing stabilizing selection as well as measuring fitness. I also argue that the commonness of positive directional selection and the variation in selection may be caused by several biological factors. First, selection on immune function may show spatial and temporal variation as epidemics are often local/seasonal. Second, factors affecting the range of phenotypic variation in immune traits could alter potential for selection. Third, different parasites may impose different selective pressures depending on their characteristics. Fourth, condition dependence of immune defence can obscure trade-offs related to it, thus possibly modifying observed selection gradients. Fifth, nonimmunological defences could affect the form of selection by reducing the benefits of strong immune function. To comprehensively understand the evolution of immune defence, the role of above factors should be considered in future studies.

Effects of interaction between temperature conditions and copper exposure on immune defense and other life-history traits of the blow fly Protophormia terraenovae.

Environmental pollution is considered one of the major threats to organisms. Direct effects of heavy metal pollution on various life-history traits are well recognized, while the effects of potential interactions between two distinct environmental conditions on different traits are poorly understood. Here, we have tested the effects of interactions between temperature conditions and heavy metal exposure on innate immunity and other life-history traits. Maggots of the blow fly Protophormia terraenovae were reared on either copper-contaminated or uncontaminated food, under three different temperature environments. Encapsulation response, body mass, and development time were measured for adult flies that were not directly exposed to copper. We found that the effects of copper exposure on immunity and other traits are temperature-dependent, suggesting that the ability to regulate toxic compounds in body tissues might depend on temperature conditions. Furthermore, we found that temperature has an effect on sex differences in immune defense. Males had an encapsulation response at higher temperatures stronger than that of females. Our results indicate that the effects of environmental conditions on different traits are much more intricate than what can be predicted. This is something that should be considered when conducting immunological experiments or comparing results of previous studies.

An experimental heat wave changes immune defense and life history traits in a freshwater snail

The predicted increase in frequency and severity of heat waves due to climate change is expected to alter disease dynamics by reducing hosts' ability to resist infections. This could take place via two different mechanisms: (1) through general reduction in hosts' performance under harsh environmental conditions and/or (2) through altered resource allocation that reduces expression of defense traits in order to maintain other traits. We tested these alternative hypotheses by measuring the effect of an experimental heat wave (25 vs. 15°C) on the constitutive level of immune defense (hemocyte concentration, phenoloxidase [PO]-like activity, antibacterial activity of hemolymph), and life history traits (growth and number of oviposited eggs) of the great pond snail Lymnaea stagnalis. We also manipulated the exposure time to high temperature (1, 3, 5, 7, 9, or 11 days). We found that if the exposure to high temperature lasted <1 week, immune function was not affected. However, when the exposure lasted longer than that, the level of snails' immune function (hemocyte concentration and PO-like activity) was reduced. Snails' growth and reproduction increased within the first week of exposure to high temperature. However, longer exposures did not lead to a further increase in cumulative reproductive output. Our results show that short experimental heat waves do not alter immune function but lead to plastic responses that increase snails' growth and reproduction. Thus, although the relative expression of traits changes, short experimental heat waves do not impair snails' defenses. Negative effects on performance get pronounced when the heat waves are prolonged suggesting that high performance cannot be maintained over long time periods. This ultimately reduces the levels of defense traits.

Genetic and phenotypic relationships between immune defense, melanism and life-history traits at different temperatures and sexes in Tenebrio molitor

Insect cuticle melanism is linked to a number of life-history traits, and a positive relationship is hypothesized between melanism and the strength of immune defense. In this study, the phenotypic and genetic relationships between cuticular melanization, innate immune defense, individual development time and body size were studied in the mealworm beetle (Tenebrio molitor) using three different temperatures with a half-sib breeding design. Both innate immune defense and cuticle darkness were higher in females than males, and a positive correlation between the traits was found at the lowest temperature. The effect of temperature on all the measured traits was strong, with encapsulation ability and development time decreasing and cuticle darkness increasing with a rise in temperature, and body size showing a curved response. The analysis showed a highly integrated system sensitive to environmental change involving physiological, morphological and life-history traits.

Life History Trade-Offs Between Longevity and Immunity in the Parasitic Brown-Headed Cowbird?

Life history theory predicts evolutionary trade-offs between investing in immune defense and other traits. We investigated whether reduced longevity was associated with increased investment in immunity in an avian brood parasite, the brown-headed cowbird (Molothrus ater). Previously we had found that the brown-headed cowbird was unusually re- sistant to infection with West Nile virus and other pathogenic arboviruses when compared with three closely related spe- cies in the same Family, Icteridae, the New World blackbirds. In this study, we hypothesized that the cowbird's more ef- fective immune responses may be associated with a trade-off in somatic maintenance that results in a shorter lifespan. We measured lifespan using the North American bird banding database and compared the lifespan of the cowbird with the lifespan of red-winged blackbird (Agelaius phoeniceus) and Brewer's blackbird (Euphagus cyanocephalus), two related species whose immune defenses were previously found less effective against West Nile virus. The cowbird lifespan was significantly shorter than those of both the red-winged blackbird and Brewer's blackbird. We also found that both male and female cowbirds had a shorter lifespan than the males and females in the two non-parasitic blackbird species. These data suggest that the brown-headed cowbird is a good study species for examining the trade-offs between immunity and longevity.

Variation in immune defence among populations of Gammarus pulex (Crustacea: Amphipoda)

Despite intensive studies in ecological immunology, few have investigated variation in immune defence among natural populations; in particular, there is a lack of knowledge of the sources of spatial variability in immune defence in the wild. Here we documented variation among twelve populations of the freshwater crustacean Gammarus pulex in the activity of the prophenoloxidase (ProPO) system, which is an important component of invertebrate immunity. We then tested for trade-offs between investment in immune defence and fitness-related traits such as survival and fecundity, as well as for environmental causes of variability (water temperature and conductivity, parasite prevalence). Levels of immune defence differed among populations, with environment partly explaining this population effect, as immune activities were negatively related to water conductivity and acanthocephalan parasite prevalence. There was a strong variation among populations for the maintenance of the ProPO system, while variation in its use was relatively weak. Such a pattern could be partly explained by the relative costs associated with the maintenance and/or the use of the ProPO system. Investment in the ProPO system was negatively correlated to survival, whereas it was positively related to female fecundity and resource storage. However, variation in immunity did not predict resistance to bacterial infection among populations, suggesting that measuring the activity of the ProPO system might not be sufficient to estimate immunocompetence at the population level. These results suggest that investment in immune function is a variable trait, which might be locally optimized as a result of both life history trade-offs and environmental conditions, highlighting the need to combine them in a common framework.

Natural host‐plant quality affects immune defence of an insect herbivore

AbstractWe examined the effect of natural host‐plant quality on immune resistance in the autumnal moth, Epirrita autumnata (Borkhausen) (Lepidoptera: Geometridae). The division of mountain birches [Betula pubescens ssp. czerepanovii (Orlova) Hämet‐ahti (Betulaceae)] into two categories, high‐ and low‐quality food for larvae, was based on previous years’ results on the relative growth rate of the autumnal moth on the trees selected. The strength of the immune defence of autumnal moths was determined by measuring their encapsulation rate to exposure to a foreign antigen and the phenoloxidase (PO) activity of the pupal haemolymph. We found that individuals reared as larvae on naturally low‐quality food had a significantly higher encapsulation rate at the pupal stage than individuals reared on high‐quality food. Females also had a higher encapsulation rate than males. Food quality did not have statistically significant effect on PO activity, nor did this response variable show any differences between the sexes. Using half‐sib analyses, we found significant heritable variation in the encapsulation rate; the heritable variation in PO activity was near to significant, although equally strong. Heritability estimates (h2: 0.19–0.27) for immune defence traits were relatively low and only moderate when compared to other studies with insects. We also found a negative genetic correlation between pupal mass and PO activity, but not between PO activity and encapsulation rate. Our results suggest that the quality of food affects immune defence in the autumnal moth. Thus an intricate tritrophic relationship exists between the folivorous insect, the host tree, and the insect's natural enemies (e.g., pathogens, parasites, and parasitoids). This study demonstrates that natural variation within a food plant species has an effect on the innate immune system of an herbivorous insect.

Inbreeding and extreme outbreeding cause sex differences in immune defence and life history traits in Epirrita autumnata

Empirical studies in vertebrates support the hypothesis that inbreeding reduces resistance against parasites and pathogens. However, studies in insects have not found any evidence that inbreeding compromises immune defence. Here we tested whether one generation of brother-sister mating or extreme outbreeding (mating between two populations) have an effect on innate immunity and life history traits in the autumnal moth, Epirrita autumnata. We show that the effect of inbreeding on immune response differed between the sexes: whereas in females, inbreeding significantly reduced encapsulation response against nylon monofilament ability, it did not have a significant effect on male immune response. There were also differences in the correlation of the immune response with other traits: in females increased immune response was positively correlated with large size, whereas in males immune response increased with a reduction in development time. Immune response differed significantly among families in males but not in females, both for the inbreeding and extreme outbreeding experiments. In conjunction with the observed immune responses to inbreeding, these data suggest that in males genetic variation for immune response is largely additive or non-directional with respect to dominance, whereas in females variation is much reduced and consists of directional dominance variance. Further, we show that encapsulation response against nylon monofilament is associated with the resistance against real pathogens suggesting that this widely used method to measure the strength of immune defence in insects is also a biologically relevant method.