Effects of inbreeding and temperature stress on life history and immune function in a butterfly

Theory predicts that inbreeding depression should be more pronounced under environmental stress due to an increase in the expression of recessive deleterious alleles. If so, inbred populations may be especially vulnerable to environmental change. Against this background, we here investigate effects of inbreeding, temperature stress and its interactions with inbreeding in the tropical butterfly Bicyclus anynana. We use a full‐factorial design with three levels of inbreeding (F = 0/0.25/0.38) and three temperature treatments (2 h exposure to 1, 27 or 39 °C). Despite using relatively low levels of inbreeding significant inbreeding depression was found in pupal mass, pupal time, thorax mass, abdomen fat content, egg hatching success and fecundity. However, stress resistance traits (heat tolerance, immune function) were not affected by inbreeding and interactions with temperature treatments were virtually absent. We thus found no support for an increased sensitivity of inbred individuals to environmental stress, and suspect that such patterns are restricted to harsher conditions. Our temperature treatments evidently imposed stress, significantly reducing longevity, fecundity, egg hatching success and haemocyte numbers, while fat content, protein content and lysozyme activity remained unaffected. Males and females differed in all traits measured except pupal time, protein content and phenoloxidase (PO) activity. Correlation analyses revealed, among others, a trade‐off between PO and lysozyme activity, and negative correlations between fat content and several other traits. We stress that more data are needed on the effects of inbreeding, temperature variation and sexual differences on insect immune function before more general conclusions can be drawn.     

MAINTENANCE OF GENETIC VARIATION IN IMMUNE DEFENSE OF A FRESHWATER SNAIL: ROLE OF ENVIRONMENTAL HETEROGENEITY

Natural populations often show genetic variation in pathogen resistance, which is paradoxal because natural selection is expected to erode genetic variation in fitness‐related traits. Several different factors have been suggested to maintain such variation, but their relative importance is still poorly understood. Here we examined if environmental heterogeneity and genetic trade‐offs could contribute to the maintenance of genetic variation in immune function of a freshwater snail Lymnaea stagnalis. We assessed the immunocompetence of snails originating from different families and maintained in different feeding treatments (ad libitum feeding, no food) by measuring the density of circulating hemocytes, phenoloxidase activity, and antibacterial activity of snail hemolymph. Food limitation reduced snail immune function, and we found significant among‐family variation in hemocyte concentration and PO activity, but not in antibacterial activity. Interestingly, food availability modified the family‐level variation observed in PO activity so that the relative immunocompetence of different snail families changed over environmental conditions (G × E interaction). We found no evidence for genetic trade‐offs between snail growth and immune defense nor among immune traits. Thus, our findings support the idea that environmental heterogeneity may promote maintenance of genetic variation in immune defense, but also suggest that different immune traits might not respond similarly to environmental variation.     

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.     

Resilience to heat waves in the aquatic snail Lymnaea stagnalis: Additive and interactive effects with micropollutants

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Responses to a warming world: Integrating life history,immune investment,and pathogen resistance in a model insect species

Environmental temperature has important effects on the physiology and life history of ectothermic animals, including investment in the immune system and the infectious capacity of pathogens. Numerous studies have examined individual components of these complex systems, but little is known about how they integrate when animals are exposed to different temperatures. Here, we use the Indian meal moth (Plodia interpunctella) to understand how immune investment and disease resistance react and potentially trade‐off with other life‐history traits. We recorded life‐history (development time, survival, fecundity, and body size) and immunity (hemocyte counts, phenoloxidase activity) measures and tested resistance to bacterial (E. coli) and viral (Plodia interpunctella granulosis virus) infection at five temperatures (20–30°C). While development time, lifespan, and size decreased with temperature as expected, moths exhibited different reproductive strategies in response to small changes in temperature. At cooler temperatures, oviposition rates were low but tended to increase toward the end of life, whereas warmer temperatures promoted initially high oviposition rates that rapidly declined after the first few days of adult life. Although warmer temperatures were associated with strong investment in early reproduction, there was no evidence of an associated trade‐off with immune investment. Phenoloxidase activity increased most at cooler temperatures before plateauing, while hemocyte counts increased linearly with temperature. Resistance to bacterial challenge displayed a complex pattern, whereas survival after a viral challenge increased with rearing temperature. These results demonstrate that different immune system components and different pathogens can respond in distinct ways to changes in temperature. Overall, these data highlight the scope for significant changes in immunity, disease resistance, and host–parasite population dynamics to arise from small, biologically relevant changes to environmental temperature. In light of global warming, understanding these complex interactions is vital for predicting the potential impact of insect disease vectors and crop pests on public health and food security.     

Fitness costs associated with different frequencies and magnitudes of temperature change in the butterfly Bicyclus anynana

Plastic responses to changes in environmental conditions are ubiquitous and typically highly effective, but are predicted to incur costs. We here investigate the effects of different frequencies and magnitudes of temperature change in the tropical butterfly Bicyclus anynana, considering developmental (Experiment 1) and adult stage plasticity (Experiment 2). We predicted negative effects of more frequent temperature changes on development, immune function and/or reproduction. Results from Experiment 1 showed that repeated temperature changes during development, if involving large amplitudes, negatively affect larval time, larval growth rate and pupal mass, while adult traits remained unaffected. However, results from treatment groups with smaller temperature amplitudes yielded no clear patterns. In Experiment 2 prolonged but not repeated exposure to 39 °C increased heat tolerance, potentially reflecting costs of repeatedly activating emergency responses. At the same time fecundity was more strongly reduced in the group with prolonged heat stress, suggesting a trade-off between heat tolerance and reproduction. Clear effects were restricted to conditions involving large temperature amplitudes or high temperatures.     

Responses to selection on phenoloxidase activity in yellow dung flies

Maintaining an immune system is costly. Resource allocation to immunity should therefore trade off against other fitness components. Numerous studies have found phenotypic trade-offs after immune challenge, but few have investigated genetic correlations between immune components and other traits. Furthermore, empirical evidence for the costs of maintaining an innate immune system in the absence of challenges is rare. We examined responses to artificial selection on phenoloxidase (PO) activity, an important part of the insect innate defense against multicellular pathogens, in yellow dung flies, Scathophaga stercoraria (L.). After 15 generations of successful selection on PO activity, we measured reproductive characters: clutch size, egg hatching rates, adult emergence rates, and adult longevity. We found no evidence for negative genetic correlations between PO activity and reproduction. In fact, flies of lines selected for increased PO activity had larger first clutches, and flies of lines selected for decreased PO activity had smaller ones. However, flies from high-PO lines died earlier than did low-PO flies when no food was available; that is, there is a survival cost of running at high PO levels in the absence of challenge. Variation in resource acquisition or use may lead to positive genetic correlations between PO and fertility and fecundity. The negative correlation between PO and longevity under starvation may indicate that variation for resource acquisition is maintained by a cost of acquisition, based on a genotype-environment interaction.     

Exposure to natural pathogens reveals costly aphid response to fungi but not bacteria

Immune responses are costly, causing trade‐offs between defense and other host life history traits. Aphids present a special system to explore the costs associated with immune activation since they are missing several humoral and cellular mechanisms thought important for microbial resistance, and it is unknown whether they have alternative, novel immune responses to deal with microbial threat. Here we expose pea aphids to an array of heat‐killed natural pathogens, which should stimulate immune responses without pathogen virulence, and measure changes in life‐history traits. We find significant reduction in lifetime fecundity upon exposure to two fungal pathogens, but not to two bacterial pathogens. This finding complements recent genomic and immunological studies indicating that pea aphids are missing mechanisms important for bacterial resistance, which may have important implications for how aphids interact with their beneficial bacterial symbionts. In general, recent exploration of the immune systems of non‐model invertebrates has called into question the generality of our current picture of insect immunity. Our data highlight that taking an ecological approach and measuring life‐history traits to a broad array of pathogens provides valuable information that can complement traditional approaches.     

Behavioral constraints on local adaptation and counter‐gradient variation: Implications for climate change

Resource allocation to growth, reproduction, and body maintenance varies within species along latitudinal gradients. Two hypotheses explaining this variation are local adaptation and counter‐gradient variation. The local adaptation hypothesis proposes that populations are adapted to local environmental conditions and are therefore less adapted to environmental conditions at other locations. The counter‐gradient variation hypothesis proposes that one population out performs others across an environmental gradient because its source location has greater selective pressure than other locations. Our study had two goals. First, we tested the local adaptation and counter‐gradient variation hypotheses by measuring effects of environmental temperature on phenotypic expression of reproductive traits in the burying beetle, Nicrophorus orbicollis Say, from three populations along a latitudinal gradient in a common garden experimental design. Second, we compared patterns of variation to evaluate whether traits covary or whether local adaptation of traits precludes adaptive responses by others. Across a latitudinal range, N. orbicollis exhibits variation in initiating reproduction and brood sizes. Consistent with local adaptation: (a) beetles were less likely to initiate breeding at extreme temperatures, especially when that temperature represents their source range; (b) once beetles initiate reproduction, source populations produce relatively larger broods at temperatures consistent with their local environment. Consistent with counter‐gradient variation, lower latitude populations were more successful at producing offspring at lower temperatures. We found no evidence for adaptive variation in other adult or offspring performance traits. This suite of traits does not appear to coevolve along the latitudinal gradient. Rather, response to selection to breed within a narrow temperature range may preclude selection on other traits. Our study highlights that N. orbicollis uses temperature as an environmental cue to determine whether to initiate reproduction, providing insight into how behavior is modified to avoid costly reproductive attempts. Furthermore, our results suggest a temperature constraint that shapes reproductive behavior.     

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.     

Immunotoxic effect of Benzo[α]Pyrene and chrysene in juvenile white shrimp Litopenaeus vannamei

The effects of benzo(a)pyrene (Bap) (0.03, 0.3 and 3 μg L^?1) and chrysene (CHR) (0.3, 2.1 and 14.7 μg L^?1) on the function of the immune system of juvenile white shrimp Litopenaeus vannamei were determined under laboratory conditions. This included the total hemocyte count (THC) in the hemolymph, phagocytic activityand pro-phenoloxidase (pro-PO) activity of the hemocyte, phenoloxidase (PO) activity, α₂-macroglobulin (α₂-M) activity, bacteriolytic activity and antibacterial activity in the hemolymph. The results showed that BaP and CHR could inhibit the immune function of L. vannamei significantly under high concentration BaP and CHR exposure. The results of this study indicated that the immunotoxicity of PAHs in a descending order was BaP>CHR. Moreover, the results indicated the THC in hemolymph, pro-PO activity and phagocytic activity of hemocyte, and bacteriolytic activity in hemolymphcould be used as potentially suitable biomarkersfor early warning indication of PAHs toxicity, this could provide useful information for toxic risk assessment of environmental pollutants.     

Experimental evolution reveals differences between phenotypic and evolutionary responses to population density

Group living can select for increased immunity, given the heightened risk of parasite transmission. Yet, it also may select for increased male reproductive investment, given the elevated risk of female multiple mating. Trade‐offs between immunity and reproduction are well documented. Phenotypically, population density mediates both reproductive investment and immune function in the Indian meal moth, Plodia interpunctella. However, the evolutionary response of populations to these traits is unknown. We created two replicated populations of P. interpunctella, reared and mated for 14 generations under high or low population densities. These population densities cause plastic responses in immunity and reproduction: at higher numbers, both sexes invest more in one index of immunity [phenoloxidase (PO) activity] and males invest more in sperm. Interestingly, our data revealed divergence in PO and reproduction in a different direction to previously reported phenotypic responses. Males evolving at low population densities transferred more sperm, and both males and females displayed higher PO than individuals at high population densities. These positively correlated responses to selection suggest no apparent evolutionary trade‐off between immunity and reproduction. We speculate that the reduced PO activity and sperm investment when evolving under high population density may be due to the reduced population fitness predicted under increased sexual conflict and/or to trade‐offs between pre‐ and post‐copulatory traits.     

Reproductive consequences of transient pathogen exposure across host genotypes and generations

To maximize fitness upon pathogenic infection, host organisms might reallocate energy and resources among life‐history traits, such as reproduction and defense. The fitness costs of infection can result from both immune upregulation and direct pathogen exploitation. The extent to which these costs, separately and together, vary by host genotype and across generations is unknown. We attempted to disentangle these costs by transiently exposing wild isolates and a lab‐domesticated strain of Caenorhabditis elegans nematodes to the pathogen Staphylococcus aureus, using exposure to heat‐killed pathogens to distinguish costs due to immune upregulation and pathogen exploitation. We found that host nematodes exhibit a short‐term delay in offspring production when exposed to live and heat‐killed pathogen, but their lifetime fecundity (total offspring produced) recovered to control levels. We also found genetic variation between host isolates for both cumulative offspring production and magnitude of fitness costs. We further investigated whether there were maternal pathogen exposure costs (or benefits) to offspring and revealed a positive correlation between the magnitude of the pathogen‐induced delay in the parent''s first day of reproduction and the cost to offspring population growth. Our findings highlight the capacity for hosts to recover fecundity after transient exposure to a pathogen.     

Sexual conflict and female immune suppression in the cricket, Allonemobious socius

In many animal systems, females exhibit a localized immune response to insemination that helps defend against sexually transmitted disease. However, this response may also kill sperm, reducing a male's reproductive potential. If males could suppress this response, they may be able to increase their sperm's representation in the female's reproductive tract, thereby increasing their fitness. Here we address the hypothesis that, under conditions of sperm competition, males interfere with female immunity. To test our hypothesis, we manipulated levels of female mating frequency (single vs. multiply mated) and seminal diversity (monandrous vs. polyandrous) in the cricket, Allonemobius socius and measured female immune response. As mating frequency increased, female hemocyte load decreased, indicating a general reproductive cost. As seminal diversity increased, phenoloxidase (PO) activity (in vitro measure of 'potential' macroparasitic defense) increased and encapsulation ability (in vivo measure of 'realized' macroparasitic defense) decreased in polyandrous females. These results suggest that males may manipulate female immunity by interrupting the pro-PO cascade, which begins with the activation of PO and ends in the encapsulation of invading foreign bodies. In other words, female immune function may serve as a battleground over which a sexual conflict is fought.     

The more the merrier: Conspecific density improves performance of gregarious larvae and reduces susceptibility to a pupal parasitoid

Aggregation can confer advantages in animal foraging, defense, and thermoregulation. There is a tight connection between the evolution of insect sociality and a highly effective immune system, presumably to inhibit rapid disease spread in a crowded environment. This connection is less evident for animals that spend only part of their life cycle in a social environment, such as noneusocial gregarious insects. Our aim was to elucidate the effects of group living by the gregarious larvae of the Glanville fritillary butterfly with respect to individual performance, immunity, and susceptibility to a parasitoid. We were also interested in the role of family relative to common postdiapause environment in shaping life‐history traits. Larvae were reared at high or low density and then exposed to the pupal parasitoid wasp Pteromalus apum, either in presence or absence of a previous immune challenge that was used to measure the encapsulation immune response. Surviving adult butterflies were further tested for immunity. The wasp offspring from successfully parasitized butterfly pupae were counted and their brood sex ratios assessed. Larvae reared at high density grew larger and faster than those at low density. Despite high mortality due to parasitism, survival was greater among individuals with high pupal immunity in both density treatments. Moreover, butterfly pupae reared at high density were able to kill a larger fraction of individuals in the parasitoid broods, although this did not increase survival of the host. Finally, a larger proportion of variation observed in most of the traits was explained by butterfly family than by common postdiapause rearing environment, except for adult survival and immunity, for which this pattern was reversed. This gregarious butterfly clearly benefits from high conspecific density in terms of developmental performance and its ability to fight a parasitoid. These positive effects may be driven by cooperative interactions during feeding.     

Developmental timing of extreme temperature events (heat waves) disrupts host–parasitoid interactions

1. When thermal tolerances differ between interacting species, extreme temperature events (heat waves) will alter the ecological outcomes. The parasitoid wasp Cotesia congregata suffers high mortality when reared throughout development at temperatures that are nonstressful for its host, Manduca sexta. However, the effects of short‐term heat stress during parasitoid development are unknown in this host–parasitoid system.
2. Here, we investigate how duration of exposure, daily maximum temperature, and the developmental timing of heat waves impact the performance of C. congregata and its host¸ M. sexta. We find that the developmental timing of short‐term heat waves strongly determines parasitoid and host outcomes.
3. Heat waves during parasitoid embryonic development resulted in complete wasp mortality and the production of giant, long‐lived hosts. Heat waves during the 1st‐instar had little effect on wasp success, whereas heat waves during the parasitoid''s nutritionally and hormonally critical 2nd instar greatly reduced wasp emergence and eclosion. The temperature and duration of heat waves experienced early in development determined what proportion of hosts had complete parasitoid mortality and abnormal phenotypes.
4. Our results suggest that the timing of extreme temperature events will be crucial to determining the ecological impacts on this host–parasitoid system. Discrepancies in thermal tolerance between interacting species and across development will have important ramifications on ecosystem responses to climate change.

     

Impact of field‐realistic doses of glyphosate and nutritional stress on mosquito life history traits and susceptibility to malaria parasite infection

Glyphosate is the world's most widely used herbicide. The commercial success of this molecule is due to its nonselectivity and its action, which would supposedly target specific biosynthetic pathways found mainly in plants. Multiple studies have however provided evidence for high sensitivity of many nontarget species to glyphosate and/or to formulations (glyphosate mixed with surfactants). This herbicide, found at significant levels in aquatic systems through surface runoffs, impacts life history traits and immune parameters of several aquatic invertebrates' species, including disease‐vector mosquitoes. Mosquitoes, from hatching to emergence, are exposed to aquatic chemical contaminants. In this study, we first compared the toxicity of pure glyphosate to the toxicity of glyphosate‐based formulations for the main vector of avian malaria in Europe, Culex pipiens mosquito. Then we evaluated, for the first time, how field‐realistic dose of glyphosate interacts with larval nutritional stress to alter mosquito life history traits and susceptibility to avian malaria parasite infection. Our results show that exposure of larvae to field‐realistic doses of glyphosate, pure or in formulation, did not affect larval survival rate, adult size, and female fecundity. One of our two experimental blocks showed, however, that exposure to glyphosate decreased development time and reduced mosquito infection probability by malaria parasite. Interestingly, the effect on malaria infection was lost when the larvae were also subjected to a nutritional stress, probably due to a lower ingestion of glyphosate.     

The influence of immune activation on thermal tolerance along a latitudinal cline

Global change is shifting both temperature patterns and the geographic distribution of pathogens, and infection has already been shown to substantially reduce host thermal performance, potentially placing populations at greater risk that previously thought. But what about individuals that are able to successfully clear an infection? Whilst the direct damage a pathogen causes will likely lead to reductions in host's thermal tolerance, the response to infection often shares many underlying pathways with the general stress response, potentially acting as a buffer against subsequent thermal stress. Here, by exposing Drosophila melanogaster to heat‐killed bacterial pathogens, we investigate how activation of a host's immune system can modify any response to both heat and cold temperature stress. In a single focal population, we find that immune activation can improve a host's knockdown times during heat shock, potentially offsetting some of the damage that would subsequently arise as an infection progresses. Conversely, immune activation had a detrimental effect on CT_max and did not influence lower thermal tolerance as measured by chill‐coma recovery time. However, we also find that the influence of immune activation on heat knockdown times is not generalizable across an entire cline of locally adapted populations. Instead, immune activation led to signals of local adaptation to temperature being lost, erasing the previous advantage that populations in warmer regions had when challenged with heat stress. Our results suggest that activation of the immune system may help buffer individuals against the detrimental impact of infection on thermal tolerance; however, any response will be population specific and potentially not easily predicted across larger geographic scales, and dependent on the form of thermal stress faced by a host.