Immune Investment Research Articles

Distinct immune and transcriptomic profiles in dominant versus subordinate males in mouse social hierarchies

Social status is a critical factor determining health outcomes in human and nonhuman social species. In social hierarchies with reproductive skew, individuals compete to monopolize resources and increase mating opportunities. This can come at a significant energetic cost leading to trade-offs between different physiological systems. In particular, changes in energetic investment in the immune system can have significant short and long-term effects on fitness and health. We have previously found that dominant alpha male mice living in social hierarchies have increased metabolic demands related to territorial defense. In this study, we tested the hypothesis that high-ranking male mice favor adaptive immunity, while subordinate mice show higher investment in innate immunity. We housed 12 groups of 10 outbred CD-1 male mice in a social housing system. All formed linear social hierarchies and subordinate mice had higher concentrations of plasma corticosterone (CORT) than alpha males. This difference was heightened in highly despotic hierarchies. Using flow cytometry, we found that dominant status was associated with a significant shift in immunophenotypes towards favoring adaptive versus innate immunity. Using Tag-Seq to profile hepatic and splenic transcriptomes of alpha and subordinate males, we identified genes that regulate metabolic and immune defense pathways that are associated with status and/or CORT concentration. In the liver, dominant animals showed a relatively higher expression of specific genes involved in major urinary production and catabolic processes, whereas subordinate animals showed relatively higher expression of genes promoting biosynthetic processes, wound healing, and proinflammatory responses. In spleen, subordinate mice showed relatively higher expression of genes facilitating oxidative phosphorylation and DNA repair and CORT was negatively associated with genes involved in lymphocyte proliferation and activation. Together, our findings suggest that dominant and subordinate animals adaptively shift immune profiles and peripheral gene expression to match their contextual needs.

The developmental high wire: Balancing resource investment in immunity and reproduction.

The strategic allocation of resources into immunity poses a unique challenge for individuals, where infection at different stages of development may result in unique trade‐offs with concurrent physiological processes or future fitness‐enhancing traits. Here, we experimentally induced an immune challenge in female Gryllus firmus crickets to test whether illness at discrete life stages differentially impacts fitness. We injected heat‐killed Serratia marcescens bacteria into antepenultimate juveniles, penultimate juveniles, sexually immature adults, and sexually mature adults, and then measured body growth, instar duration, mating rate, viability of stored sperm, egg production, oviposition rate, and egg viability. Immune activation significantly impacted reproductive traits, where females that were immune challenged as adults had decreased mating success and decreased egg viability compared to healthy individuals or females that were immune challenged as juveniles. Although there was no effect of an immune challenge on the other traits measured, the stress of handling resulted in reduced mass gain and smaller adult body size in females from the juvenile treatments, and females in the adult treatments suffered from reduced viability of sperm stored within their spermatheca. In summary, we found that an immune challenge does have negative impacts on reproduction, but also that even minor acute stressors can have significant impacts on fitness‐enhancing traits. These findings highlight that the factors affecting fitness can be complex and at times unpredictable, and that the consequences of illness are specific to when during an individual's life an immune challenge is induced.

Mechanisms and potential immune tradeoffs of accelerated coral growth induced by microfragmentation.

Microfragmentation is the act of cutting corals into small pieces (~1 cm2) to accelerate the growth rates of corals relative to growth rates observed when maintaining larger-sized fragments. This rapid tissue and skeletal expansion technique offers great potential for supporting reef restoration, yet the biological processes and tradeoffs involved in microfragmentation-mediated accelerated growth are not well understood. Here we compared growth rates across a range of successively smaller fragment sizes in multiple genets of reef-building corals, Orbicella faveolata and Montastraea cavernosa. Our results confirm prior findings that smaller initial sizes confer accelerated growth after four months of recovery in a raceway. O. faveolata transcript levels associated with growth rate include genes encoding carbonic anhydrase and glutamic acid-rich proteins, which have been previously implicated in coral biomineralization, as well as a number of unannotated transcripts that warrant further characterization. Innate immunity enzyme activity assays and gene expression results suggest a potential tradeoff between growth rate after microfragmentation and immune investment. Microfragmentation-based restoration practices have had great success on Caribbean reefs, despite widespread mortality among wild corals due to infectious diseases. Future studies should continue to examine potential immune tradeoffs throughout the microfragmentation recovery period that may affect growout survival and disease transmission after outplanting.

Density-Dependent Prophylaxis in Freshwater Snails Driven by Oxylipin Chemical Cues.

While animal aggregations can benefit the fitness of group members, the behaviour may also lead to higher risks of parasite infection as group density increases. Some animals are known to moderate their investment in immunity relative to the risk of infection. These animals exhibit density-dependent prophylaxis (DDP) by increasing their immune investment as group density increases. Despite being documented in many taxa, the mechanisms of DDP remain largely unexplored. Snails are known to aggregate and experience large fluctuations in density and serve as required hosts for many parasites. Further, they are known to use chemical cues to aggregate. To test whether freshwater snails exhibit DDP and investigate the role that chemical signaling compounds may play in triggering this phenomenon, we performed four experiments on the freshwater snail Stagnicola elodes, which is a common host for many trematode parasite species. First, we tested if DDP occurred in snails in laboratory-controlled conditions (control vs snail-conditioned water) and whether differences in exposure to chemical cues affected immune function. Second, we used gas chromatography to characterize fatty acids expressed in snail-conditioned water to determine if precursors for particular signaling molecules, such as oxylipins, were being produced by snails. Third, we characterized the oxylipins released by infected and uninfected field-collected snails, to better understand how differences in oxylipin cocktails may play a role in inducing DDP. Finally, we tested the immune response of snails exposed to four oxylipins to test the ability of specific oxylipins to affect DDP. We found that snails exposed to water with higher densities of snails and raised in snail-conditioned water had higher counts of haemocytes. Additionally, lipid analysis demonstrated that fatty acid molecules that are also precursors for oxylipins were present in snail-conditioned water. Trematode-infected snails emitted 50 oxylipins in higher amounts, with 24 of these oxylipins only detected in this group. Finally, oxylipins that were higher in infected snails induced naïve snails to increase their immune responses compared to sham-exposed snails. Our results provide evidence that snails exhibit DDP, and the changes in oxylipins emitted by infected hosts may be one of the molecular mechanisms driving this phenomenon.

Realism in Immune Ecology Studies: Artificial Diet Enhances a Caterpillar's Immune Defense but Does Not Mask the Effects of a Plastic Immune Strategy.

The immune system is considered a functional trait in life-history theory and its modulation is predicted to be costly and highly dependent on the host's nutrition. Therefore, the nutritional status of an individual has a great impact on an animal's immune ecology. Herbivorous insects are commonly used as model organisms in eco-immunology studies and the use of an artificial diet is the predominant rearing procedure to test them. However, this diet differs from what herbivores experience in nature and it is unclear to what degree this distinction might impact on the relevance of these studies for the real world. Here, we compared plant-based vs. artificial diet in a set of three experiments to investigate the interaction of both diets with a plastic immune strategy known as Density-Dependent Prophylaxis (DDP). We used as a model organism the velvetbean caterpillar Anticarsia gemmatalis, which is known to adjust its immune defense in line with the DDP hypothesis. Our main results showed that larvae fed with artificial diet had 20.5% more hemocytes circulating in the hemolymph and died 20% more slowly when infected with an obligate (viral) pathogen. Crucially, however, we did not find any indication of fitness costs related to DDP. The use of artificial diet did not interact with that of DDP except in the case of host survival after infection, where the DDP effect was only observable in this diet. Our findings suggest the use of an artificial diet does not mask resource allocation conflicts between immune investment and fitness related traits, but to some extent it might lead to an overestimation of immune parameters and host survival time after infection. We believe that this is the first study to compare an artificial diet and a host plant covering all these aspects: immune parameters, life-history traits, and host survival after infection. Here we provide evidence that, besides the quantitative effects in immune parameters and host survival time, the use of artificial diet interacts only marginally with a density-dependent immune response. This provides support for the use of artificial diets in eco-immunology studies with insects.

Indications of symbiotic state influencing melanin-synthesis immune response in the facultative coral Astrangia poculata.

Increased ocean warming is causing detrimental impacts to tropical corals worldwide. Compounding the effects of heat stress, incidences of tropical coral disease have risen concurrently. While tropical coral responses to these impacts are well studied, temperate coral responses remain largely unknown. The present study focused on the immune response of the temperate coral Astrangia poculata to increased temperature and disease. Symbiotic and aposymbiotic A. poculata were collected from Narragansett Bay, Rhode Island (USA) in summer and winter seasons and exposed to control (18°C) versus elevated temperatures (26°C) in the presence of an immune stimulant (i.e. lipopolysaccharide) for a 12 h period. Prophenoloxidase (PPO) and melanin concentrations from the melanin-synthesis pathway were assessed via spectrophotometry to examine immune responses. While PPO measurements were higher on average in symbiotic corals compared with aposymbiotic corals, temperature and season did not significantly affect this metric. Melanin was significantly higher in symbiotic compared to aposymbiotic corals, implying that symbiotic state may be important for melanin-synthesis response. Conversely, melanin as an immune response may be of less importance in aposymbiotic A. poculata due to the potential capacity of other immune responses in this species. In addition, differences in resource allocation to immune investment as a result of symbiosis is plausible given melanin production observed within the present study. However, thermal stressors may reduce the overall influence of symbiosis on melanin production. Future studies should build upon these results to further understand the entirety of innate immunity responses in temperate coral species.

Sex Matters: Effects of Sex and Mating in the Presence and Absence of a Protective Microbe.

In most animals, female investment in offspring production is greater than for males. Lifetime reproductive success (LRS) is predicted to be optimized in females through extended lifespans to maximize reproductive events by increased investment in immunity. Males, however, maximize lifetime reproductive success by obtaining as many matings as possible. In populations consisting of mainly hermaphrodites, optimization of reproductive success may be primarily influenced by gamete and resource availability. Microbe-mediated protection (MMP) is known to affect both immunity and reproduction, but whether sex influences the response to MMP remains to be explored. Here, we investigated the sex-specific differences in survival, behavior, and timing of offspring production between feminized hermaphrodite (female) and male Caenorhabditis elegans following pathogenic infection with Staphylococcus aureus with or without MMP by Enterococcus faecalis. Overall, female survival decreased with increased mating. With MMP, females increased investment into offspring production, while males displayed higher behavioral activity. MMP was furthermore able to dampen costs that females experience due to mating with males. These results demonstrate that strategies employed under pathogen infection with and without MMP are sex dependent.

The effects of host plant species and larval density on immune function in the polyphagous moth Spodoptera littoralis.

Immune functions are costly, and immune investment is usually dependent on the individual's condition and resource availability. For phytophagous insects, host plant quality has large effects on performance, for example growth and survival, and may also affect their immune function. Polyphagous insects often experience a large variation in quality among different host plant species, and their immune investment may thus vary depending on which host plant species they develop on. Larvae of the polyphagous moth Spodoptera littoralis have previously been found to exhibit density‐dependent prophylaxis as they invest more in certain immune responses in high population densities. In addition, the immune response of S. littoralis has been shown to depend on nutrient quality in experiments with artificial diet. Here, I studied the effects of natural host plant diet and larval density on a number of immune responses to understand how host plant species affects immune investment in generalist insects, and whether the density‐dependent prophylaxis could be mediated by host plant species. While host plant species in general did not mediate the density‐dependent immune expression, particular host plant species was found to increase larval investment in certain functions of the immune system. Interestingly, these results indicate that different host plants may provide a polyphagous species with protection against different kinds of antagonisms. This insight may contribute to our understanding of the relationship between preference and performance in generalists, as well as having applied consequences for sustainable pest management.

Larvae and adults exhibit contrasting patterns of immune gene expression and infection resistance in wild flour beetle populations

1. In nature, hosts face shifting patterns of parasite exposure and life history trade‐offs, as they develop from birth to old age. As a result, the net fitness benefit of immunological investment can change dramatically from one life stage to the next.2. Previous work has revealed a puzzling diversity of relative immune investment patterns among juvenile and adult stages, and it is not clear whether lessons learned from one particular population or species can be generalised to wild populations, after accounting for local adaptation and other variance‐generating processes.3. In this study, we quantify larval and adult immune gene expression and resistance to bacterial infection in two flour beetle species (Tribolium castaneum and Tribolium confusum) from seven wild‐derived populations.4. Our results provide a clear signal of higher infection‐induced immunological investment and resistance in adults relative to larvae, despite variation among species in immune gene regulation.5. Better characterisation of stage‐specific investment in infection resistance in natural populations can inform our understanding of life history evolution and improve predictions of disease dynamics in the wild.

Environmental variability affects optimal trade‐offs in ecological immunology

AbstractThe costs of mounting and maintaining an immune response lead to trade‐offs with investment in (or maintenance of) other organ systems or functions such as reproduction, as has been observed in several taxa, including birds, insects, and mammals. Given these trade‐offs, optimal strategies can be affected by biotic and abiotic conditions; however, how these trade‐offs are affected by environmental variability remains unclear. Using a deterministic within‐host model of disease dynamics, we analyzed the effect of environmental variability (here, the coefficient of variation in the host’s background survival distribution) on the optimal resolution to a trade‐off between investment in reproduction and the immune system. We found that higher variability led to increased investment in the immune system at the cost of decreased early‐life reproduction when the immune investment strategy was assumed to be constant through life. Since we manipulated the distribution of lifespans while keeping the mean lifespan constant, our results suggest that even the small probability of living far past the mean lifespan for individuals in highly variable environments has a large effect on the optimal investment strategy. When immune investment was able to change over the age of the organism, the optimal investment strategies were again contingent on the level of environmental variability experienced by individuals. Our results support and extend previous work on optimal life‐history theory in variable environments by showing that in the context of ecological immunology, the most fit individuals in constant environments are not the most fit individuals in variable environments. The effects of environmental variability on optimal immune investment are likely to have consequences for other aspects of infectious disease such as transmission dynamics, virulence evolution, and the likelihood of epidemics occurring.

Who Rules Over Immunology? Seasonal Variation in Body Temperature, Steroid Hormones, and Immune Variables in a Tegu Lizard.

Multiple factors can influence the immune response of ectothermic vertebrates, including body temperature (Tb), gonadal steroids, and seasonality, in ways that are thought to reflect trade-offs between energetic investment in immunity versus reproduction. Hibernating tegu lizards (Salvator merianae) are a unique model to investigate how immunocompetence might be influenced by different factors during their annual cycle. We assessed immunological measures (plasma bacterial killing ability, total and differential leukocyte count), plasma hormone levels (testosterone in males, estradiol and progesterone in females, and corticosterone [CORT] in both sexes), Tb, and body condition from adult tegus during each stage of their annual cycle: reproduction, post-reproduction/preparation for hibernation, and hibernation. Our hypothesis that immune traits present higher values during the reproductive phase, and a sharp decrease during hibernation, was partially supported. Immune variables did not change between life history stages, except for total number of leukocytes, which was higher at the beginning of the reproductive season (September) in both males and females. Average Tb of the week prior to sampling was positively correlated with number of eosinophils, basophils, monocytes, and azurophils, corroborating other studies showing that when animals maintain a high Tb, there is an increase in immune activity. Surprisingly, no clear relationship between immune traits and gonadal steroids or CORT levels was observed, even when including life history stage in the model. When gonadal hormones peaked in males and females, heterophil: lymphocyte ratio (which often elevates during physiological stress) also increased. Additionally, we did not observe any trade-off between reproduction and immunity traits, sex differences in immune traits, or a correlation between body condition and immune response. Our results suggest that variation in patterns of immune response and correlations with body condition and hormone secretion across the year can depend upon the specific hormone and immune trait, and that experienced Tb is an important variable determining immune response in ectotherms.

Urinary neopterin of wild chimpanzees indicates that cell-mediated immune activity varies by age, sex, and female reproductive status

The study of free-living animal populations is necessary to understand life history trade-offs associated with immune investment. To investigate the role of life history strategies in shaping proinflammatory cell-mediated immune function, we analyzed age, sex, and reproductive status as predictors of urinary neopterin in 70 sexually mature chimpanzees (Pan troglodytes) at Ngogo, Kibale National Park, Uganda. In the absence of clinical signs of acute infectious disease, neopterin levels significantly increased with age in both male and female chimpanzees, as observed in humans and several other vertebrate species. Furthermore, males exhibited higher neopterin levels than females across adulthood. Finally, females with full sexual swellings, pregnant females, and post-reproductive females, the oldest individuals in our sample, exhibited higher neopterin levels than lactating females and cycling females without full swellings. Variation in females’ neopterin levels by reproductive status is consistent with post-ovulatory and pregnancy-related immune patterns documented in humans. Together, our results provide evidence of ample variation in chimpanzee immune activity corresponding to biodemographic and physiological variation. Future studies comparing immune activity across ecological conditions and social systems are essential for understanding the life histories of primates and other mammals.

Current and time-lagged effects of climate on innate immunity in two sympatric snake species.

Changing environments result in alterations at all levels of biological organization, from genetics to physiology to demography. The increasing frequency of droughts worldwide is associated with higher temperatures and reduced precipitation that can impact population persistence via effects on individual immune function and survival.We examined the effects of annual climate variation on immunity in two sympatric species of garter snakes from four populations in California over a seven‐year period that included the record‐breaking drought.We examined three indices of innate immunity: bactericidal competence (BC), natural antibodies (NABs), and complement‐mediated lysis (CL).Precipitation was the only climatic variable explaining variation in immune function: spring precipitation of the current year was positively correlated to Thamnophis sirtalis BC and NABs, whereas spring precipitation of the previous year was positively correlated to T. elegans BC and NABs. This suggests that T. elegans experiences a physiological time‐lag in response to reduced precipitation, which may reflect lack of capital for investment in immunity in the year following a dry year.In general, our findings demonstrate compelling evidence that climate can influence wild populations through effects on physiological processes, suggesting that physiological indices such as these may offer valuable opportunities for monitoring the effects of climate.

Spatial Patterns of Thalassia testudinum Immune Status and Labyrinthula spp. Load Implicate Environmental Quality and History as Modulators of Defense Strategies and Wasting Disease in Florida Bay, United States.

Seagrass wasting disease, caused by protists of the genus Labyrinthula, is an important stressor of the dominant macrophyte in Florida Bay (FB), United States, Thalassia testudinum. FB exhibits countervailing gradients in plant morphology and resource availability. A synoptic picture of the Thalassia-Labyrinthula relationship was obtained by assessing the activity of four immune biomarkers in conjunction with pathogen prevalence and load [via quantitative PCR (qPCR)] at 15 sites across FB. We found downregulated immune status paired with moderate pathogen load among larger-bodied host phenotypes in western FB and upregulated immunity for smaller-bodied phenotypes in eastern FB. Among the highest immune response sites, a distinct inshore-offshore loading pattern was observed, where coastal basins exposed to freshwater runoff and riverine inputs had the highest pathogen loads, while adjacent offshore locations had the lowest. To explain this, we propose a simple, conceptual model that defines a framework for testable hypotheses based on recent advances in resistance-tolerance theory. We suggest that resource availability has the potential to drive not only plant size, but also tolerance to pathogen load by reducing investment in immunity. Where resources are more scarce, plants may adopt a resistance strategy, upregulating immunity; however, when physiologically challenged, this strategy appears to fail, resulting in high pathogen load. While evidence remains correlative, we argue that hyposalinity stress, at one or more temporal scales, may represent one of many potential drivers of disease dynamics in FB. Together, these data highlight the complexity of the wasting disease pathosystem and raise questions about how climate change and ongoing Everglades restoration might impact this foundational seagrass species.

Increased immune marker variance in a population of invasive birds

Immunity and parasites have been linked to the success of invasive species. Especially lower parasite burden in invasive populations has been suggested to enable a general downregulation of immune investment (Enemy Release and Evolution of Increased Competitive Ability Hypotheses). Simultaneously, keeping high immune competence towards potentially newly acquired parasites in the invasive range is essential to allow population growth. To investigate the variation of immune effectors of invasive species, we compared the mean and variance of multiple immune effectors in the context of parasite prevalence in an invasive and a native Egyptian goose (Alopochen aegyptiacus) population. Three of ten immune effectors measured showed higher variance in the invasive population. Mean levels were higher in the invasive population for three effectors but lower for eosinophil granulocytes. Parasite prevalence depended on the parasite taxa investigated. We suggest that variation of specific immune effectors, which may be important for invasion success, may lead to higher variance and enable invasive species to reduce the overall physiological cost of immunity while maintaining the ability to efficiently defend against novel parasites encountered.

Fitness outcomes in relation to individual variation in constitutive innate immune function.

Although crucial for host survival when facing persistent parasite pressure, costly immune functions will inevitably compete for resources with other energetically expensive traits such as reproduction. Optimizing, but not necessarily maximizing, immune function might therefore provide net benefit to overall host fitness. Evidence for associations between fitness and immune function is relatively rare, limiting our potential to understand ultimate fitness costs of immune investment. Here, we assess how measures of constitutive immune function (haptoglobin, natural antibodies, complement activity) relate to subsequent fitness outcomes (survival, reproductive success, dominance acquisition) in a wild passerine (Malurus coronatus). Surprisingly, survival probability was not positively linearly predicted by any immune index. Instead, both low and high values of complement activity (quadratic effect) were associated with higher survival, suggesting that different immune investment strategies might reflect a dynamic disease environment. Positive linear relationships between immune indices and reproductive success suggest that individual heterogeneity overrides potential resource reallocation trade-offs within individuals. Controlling for body condition (size-adjusted body mass) and chronic stress (heterophil-lymphocyte ratio) did not alter our findings in a sample subset with available data. Overall, our results suggest that constitutive immune components have limited net costs for fitness and that variation in immune maintenance relates to individual differences more closely.

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.

Weak relationships of parasite infection with sexual and life‐history traits in wild‐caught Texas field crickets (Gryllus texensis)

Sex differences in immune investment and infection rate are predicted due to the divergent life histories of males and females, where females invest more toward immunity due to the fitness consequences of a reduced lifespan and males allocate less toward immunity due to increased resource investment in traits critical to sexual selection. Consequently, males are expected to fight infection less adeptly, resulting in higher parasite loads relative to females across all taxa. Wild animals rarely face a single parasite within their given environment, yet nearly all studies on sex‐biased infection rates have focused on a single host–parasite relationship. Here, we investigate how simultaneous natural infections of ecto‐ and endosymbionts (i.e. both parasitic and phoretic taxa) correlate with sex biases in host immune response and reproductive investment in a field‐caught cricket, Gryllus texensis. Our comprehensive analysis found no significant sex differences in two measures of immune response (melanization and nodulation), and found no strong evidence of a sex bias in the prevalence or intensity of parasitism by the three most common parasites infecting wild G. texensis field crickets (Eutrombidiidae, gregarines, and nematodes). Two traits related to female fitness, egg number and egg size, showed no relation to parasitic infection; however, males having wider heads and poorer body condition were significantly more infected by eutrombidiid mites, gregarines, and nematodes. Despite frequent predictions of male‐biased parasitism in the literature, our results concur with many other studies indicating that the divergent life histories of males and females alone are not sufficient to explain natural infection rates in wild insects.

An immune challenge of female great tits decreases offspring survival and has sex-specific effects on offspring body size

Investment in immunity is expected to decrease (costly immunity) or enhance (terminal investment) reproductive performance. Here, we tested the effects of activation of the immune system in female great tits (Parus major) on (1) their reproductive effort and (2) the survival and body condition of their offspring, controlling for chick sex. We injected females tending 3-day-old chicks with sheep red blood cells (SRBC) or saline (control) and recorded their provisioning rates 6 days later, during the expected peak of antibody production. We measured tarsus length and body mass in 11-day-old chicks and monitored changes in brood size. We found that female provisioning rates were unaffected by the SRBC challenge. An analysis without an outlier, however, showed a significant challenge-by-hatch date interaction. This interaction indicated that female provisioning rates decreased with hatch dates in the SRBC but not in the control nests, suggesting a stronger effect in later breeders. Chick body mass was not affected by female immunisation nor by its interaction with chick sex. However, we found a significant challenge-by-sex interaction on offspring tarsus. In SRBC nests, the difference in tarsus length between male and female chicks was lower than in controls, suggesting sex-dependent effects of the challenge on offspring structural growth. Finally, chick mortality was greater in SRBC nests compared with controls, but chick survival probability was not affected by sex. Overall, our results support the costly immunity but not the terminal investment hypothesis in the great tit.

Pro-inflammatory immune response is linked to wintering habitat in a migratory shorebird

AbstractMigratory shorebirds (Charadrii) show a strong dichotomy in their breeding and wintering strategies: Arctic-breeding species typically spend the wintering season in marine habitats, while more southerly breeding species tend to do so in freshwater habitats where pathogens and parasites, particularly vector-borne blood parasites, are generally more abundant. Thus, it has been hypothesized that the former group may reduce their investment in immunity, but experimental data supporting this hypothesis are lacking. Moreover, whether this contrasting habitat selection can shape investments in immunocompetence among populations within a species is uncertain. We experimentally tested the hypothesis that there is a significant association between habitat occupancy and the strength of a pro-inflammatory immune response in the Dunlin (Calidris alpina), a widely distributed long-distance migratory shorebird that breeds in (sub-)arctic areas and winters mainly, but not exclusively, in coastal habitats. Overwintering Dunlins occupying inland freshwater and marine habitats at a similar latitude were captured and acclimated under identical conditions in outdoor aviaries. After an acclimation period, they were challenged with phytohemagglutinin to assess the pro-inflammatory immune response and its associated energetic costs, measured by basal metabolic rate (BMR) and body mass changes. We found that freshwater Dunlins exhibited a higher (63%) pro-inflammatory immune response than marine Dunlins. Although this difference did not involve significant BMR changes, the time course of body mass response differed between freshwater and marine individuals. Our findings point to the existence of different pro-inflammatory immune responses and body mass adjustments associated with the wintering habitat. These intraspecific differences are likely due to population adaptation rather than phenotypic plasticity, where not only disease risk but also physiological adaptations to different salinity levels could play an important role.