Evolutionary trade-off between innate and acquired immune defences in birds.

BACKGROUND: The development, maintenance, and use of immune defences are costly. Therefore, animals face trade-offs in terms of resource allocation within their immune system and between their immune system and other physiological processes. To maximize fitness, evolution may favour investment in one immunological defence or subsystem over another in a way that matches a species broader life history strategy. Here, we used phylogenetically-informed comparative analyses to test for relationships between two immunological components. Natural antibodies and complement were used as proxies for the innate branch; structural complexity of the major histocompatibility complex (MHC) region was used for the acquired branch. RESULTS: We found a negative association between the levels of natural antibodies (i.e., haemagglutination titre) and the total MHC gene copy number across the avian phylogeny, both at the species and family level. The family-level analysis indicated that this association was apparent for both MHC-I and MHC-II, when copy numbers within these two MHC regions were analysed separately. The association remained significant after controlling for basic life history components and for ecological traits commonly linked to pathogen exposure. CONCLUSION: Our results provide the first phylogenetically robust evidence for an evolutionary trade-off within the avian immune system, with a more developed acquired immune system (i.e., more complex MHC architecture) in more derived bird lineages (e.g., passerines) being accompanied by an apparent downregulation of the innate immune system.

Immunosenescence in the wild? A longitudinal study in a long-lived seabird.

Longitudinal studies of various vertebrate populations have demonstrated senescent declines in reproductive performance and survival probability to be almost ubiquitous. Longitudinal studies of potential underlying proximate mechanisms, however, are still scarce. Due to its critical function in the maintenance of health and viability, the immune system is among the potential (mediators of) proximate mechanisms that could underlie senescence. Here, we studied three innate immune parameters-haemagglutination titre, haemolysis titre and haptoglobin concentration-in a population of common terns (Sterna hirundo) known to undergo actuarial senescence. We repeatedly sampled birds of known sex and age across 11 years and used random regression models to (a) quantify how immune parameters vary among individuals and (b) describe within-individual age-specific changes in, and potential trade-offs between, immune parameters. Our models revealed no differences between males and females in haemagglutination titre and haptoglobin concentration, and very low among-individual variation in these parameters in general. Within individuals, haemagglutination titre increased with age, while haptoglobin concentration did not change. We found no indication for selective (dis)appearance in relation to haemagglutination titre or haptoglobin concentration, nor for the existence of a trade-off between them. Haemolysis was absent in the majority (76%) of samples. Common terns do not exhibit clear senescence in haemagglutination titre and haptoglobin concentration and show very little among-individual variation in these parameters in general. This may be explained by canalisation of the immune parameters or by the colonial breeding behaviour of our study species, but more longitudinal studies are needed to facilitate investigation of links between species' characteristics and immunosenescence in wild animals.

Mammal assemblage composition predicts global patterns in emerging infectious disease risk.

As a source of emerging infectious diseases, wildlife assemblages (and related spatial patterns) must be quantitatively assessed to help identify high-risk locations. Previous assessments have largely focussed on the distributions of individual species; however, transmission dynamics are expected to depend on assemblage composition. Moreover, disease-diversity relationships have mainly been studied in the context of species loss, but assemblage composition and disease risk (e.g. infection prevalence in wildlife assemblages) can change without extinction. Based on the predicted distributions and abundances of 4466 mammal species, we estimated global patterns of disease risk through the calculation of the community-level basic reproductive ratio R0, an index of invasion potential, persistence, and maximum prevalence of a pathogen in a wildlife assemblage. For density-dependent diseases, we found that, in addition to tropical areas which are commonly viewed as infectious disease hotspots, northern temperate latitudes included high-risk areas. We also forecasted the effects of climate change and habitat loss from 2015 to 2035. Over this period, many local assemblages showed no net loss of species richness, but the assemblage composition (i.e. the mix of species and their abundances) changed considerably. Simultaneously, most areas experienced a decreased risk of density-dependent diseases but an increased risk of frequency-dependent diseases. We further explored the factors driving these changes in disease risk. Our results suggest that biodiversity and changes therein jointly influence disease risk. Understanding these changes and their drivers and ultimately identifying emerging infectious disease hotspots can help health officials prioritize resource distribution.

Immune function differs among tropical environments but is not downregulated during reproduction in three year-round breeding equatorial lark populations.

Seasonal variation in immune function can be attributed to life history trade-offs, and to variation in environmental conditions. However, because phenological stages and environmental conditions co-vary in temperate and arctic zones, their separate contributions have not been determined. We compared immune function and body mass of incubating (female only), chick-feeding (female and male), and non-breeding (female and male) red-capped larks Calandrella cinerea breeding year-round in three tropical equatorial (Kenya) environments with distinct climates. We measured four immune indices: haptoglobin, nitric oxide, agglutination, and lysis. To confirm that variation in immune function between breeding (i.e., incubating or chick-feeding) and non-breeding was not confounded by environmental conditions, we tested if rainfall, average minimum temperature (Tmin), and average maximum temperature (Tmax) differed during sampling times among the three breeding statuses per location. Tmin and Tmax differed between chick-feeding and non-breeding, suggesting that birds utilized environmental conditions differently in different locations for reproduction. Immune indices did not differ between incubating, chick-feeding and non-breeding birds in all three locations. There were two exceptions: nitric oxide was higher during incubation in cool and wet South Kinangop, and it was higher during chick-feeding in the cool and dry North Kinangop compared to non-breeding birds in these locations. For nitric oxide, agglutination, and lysis, we found among-location differences within breeding stage. In equatorial tropical birds, variation in immune function seems to be better explained by among-location climate-induced environmental conditions than by breeding status. Our findings raise questions about how within-location environmental variation relates to and affects immune function.

Restless roosts: Light pollution affects behavior, sleep, and physiology in a free-living songbird.

The natural nighttime environment is increasingly polluted by artificial light. Several studies have linked artificial light at night to negative impacts on human health. In free-living animals, light pollution is associated with changes in circadian, reproductive, and social behavior, but whether these animals also suffer from physiologic costs remains unknown. To fill this gap, we made use of a unique network of field sites which are either completely unlit (control), or are artificially illuminated with white, green, or red light. We monitored nighttime activity of adult great tits, Parus major, and related this activity to within-individual changes in physiologic indices. Because altered nighttime activity as a result of light pollution may affect health and well-being, we measured oxalic acid concentrations as a biomarker for sleep restriction, acute phase protein concentrations and malaria infection as indices of immune function, and telomere lengths as an overall measure of metabolic costs. Compared to other treatments, individuals roosting in the white light were much more active at night. In these individuals, oxalic acid decreased over the course of the study. We also found that individuals roosting in the white light treatment had a higher probability of malaria infection. Our results indicate that white light at night increases nighttime activity levels and sleep debt and affects disease dynamics in a free-living songbird. Our study offers the first evidence of detrimental effects of light pollution on the health of free-ranging wild animals.

Personality and innate immune defenses in a wild bird: Evidence for the pace-of-life hypothesis.

We tested the two main evolutionary hypotheses for an association between immunity and personality. The risk-of-parasitism hypothesis predicts that more proactive (bold, exploratory, risk-taking) individuals have more vigorous immune defenses because of increased risk of parasite exposure. In contrast, the pace-of-life hypothesis argues that proactive behavioral styles are associated with shorter lifespans and reduced investment in immune function. Mechanistically, associations between immunity and personality can arise because personality differences are often associated with differences in condition and stress responsiveness, both of which are intricately linked with immunity. Here we investigate the association between personality (measured as proactive exploration of a novel environment) and three indices of innate immune function (the non-specific first line of defense against parasites) in wild superb fairy-wrens Malurus cyaneus. We also quantified body condition, hemoparasites (none detected), chronic stress (heterophil:lymphocyte ratio) and circulating corticosterone levels at the end of the behavioral test (CORT, in a subset of birds). We found that fast explorers had lower titers of natural antibodies. This result is consistent with the pace-of-life hypothesis, and with the previously documented higher mortality of fast explorers in this species. There was no interactive effect of exploration score and duration in captivity on immune indices. This suggests that personality-related differences in stress responsiveness did not underlie differences in immunity, even though behavioral style did modulate the effect of captivity on CORT. Taken together these results suggest reduced constitutive investment in innate immune function in more proactive individuals.

Indices of immune function used by ecologists are mostly unaffected by repeated freeze-thaw cycles and methodological deviations.

BACKGROUND: Over the past couple of decades, measuring immunological parameters has become widespread in studies of ecology and evolution. A combination of different immunological indices is useful for quantifying different parts of the immune system and comprehensively assessing immune function. Running multiple immune assays usually requires samples to be repeatedly thawed and re-frozen. There is some evidence that repeated freezing and thawing can affect assay results, but this has never been comprehensively studied in some common ecological immunology assays. We tested the effect of multiple (1, 2, 3, 4, 5, 10) freeze-thaw cycles on the results of four commonly used immunological assays: haemolysis-haemagglutination titres, haptoglobin concentration, bacterial killing capacity and total immunoglobulins (IgY). We tested five different bird species from four different bird orders (Passeriformes, Columbiformes, Charadriiformes and Galliformes), and we included both captive and free-living individuals. In addition, we tested for haptoglobin concentrations and the haemolysis-haemagglutination assay if re-analysing samples 1 year apart led to different results. For the haemolysis-haemagglutination assay we also tested two different sources of rabbit blood, and we compared untreated microtitre plates with plates that were "blocked" to prevent nonspecific interactions between the plate and assay reagents. RESULTS: Repeated freezing and thawing of plasma had no effect on lysis titres, haptoglobin concentrations, bacterial killing capacity, or total immunoglobulin levels. Agglutination titres were unaffected by up to five cycles but were lower after ten freeze-thaw cycles. For the haemolysis-haemagglutination assay and haptoglobin concentrations, re-analysing samples 1 year apart yielded highly correlated data. For the haemolysis-haemagglutination assay, the source of rabbit blood did not influence the results, and the untreated vs. blocked plates differed slightly overall, but at the individual level assay results were highly correlated. Using different rabbit blood sources or different types of microtitre plates yielded highly correlated data. CONCLUSIONS: Our data suggest that repeated freeze-thaw cycles do not impair assay results to the point of influencing ecological or evolutionary conclusions. Plasma samples can be safely stored in one tube and thawed repeatedly for different assays. Nevertheless, we recommend consistent treatment of samples in terms of freeze-thaw cycles or other laboratory treatments to minimize the potential for introducing a systematic bias.

Geographical and temporal variation in environmental conditions affects nestling growth but not immune function in a year-round breeding equatorial lark.

BACKGROUND: Variation in growth and immune function within and among populations is often associated with specific environmental conditions. We compared growth and immune function in nestlings of year-round breeding equatorial Red-capped Lark Calandrella cinerea from South Kinangop, North Kinangop and Kedong (Kenya), three locations that are geographically close but climatically distinct. In addition, we studied growth and immune function of lark nestlings as a function of year-round variation in breeding intensity and rain within one location. We monitored mass, wing, and tarsus at hatching (day 1) and at 4, 7, and 10 days post-hatch, and we quantified four indices of immune function (haptoglobin, agglutination, lysis and nitric oxide) using blood samples collected on day 10. RESULTS: Nestling body mass and size at hatching, which presumably reflect the resources that females allocated to their eggs, were lowest in the most arid location, Kedong. Contrary to our predictions, nestlings in Kedong grew faster than nestlings in the two other cooler and wetter locations of South and North Kinangop. During periods of peak reproduction within Kedong, nestlings were heavier at hatching, but they did not grow faster over the first 10 days post-hatch. In contrast, rainfall, which did not relate to timing of breeding, had no effect on hatching mass, but more rain did coincide with faster growth post-hatch. Finally, we found no significant differences in nestling immune function, neither among locations nor with the year-round variation within Kedong. CONCLUSION: Based on these results, we hypothesize that female body condition determines nestling mass and size at hatching, but other independent environmental conditions subsequently shape nestling growth. Overall, our results suggest that environmental conditions related to food availability for nestlings are relatively unimportant to the timing of breeding in equatorial regions, while these same conditions do have consequences for nestling size and growth.

Environmental proxies of antigen exposure explain variation in immune investment better than indices of pace of life.

Investment in immune defences is predicted to covary with a variety of ecologically and evolutionarily relevant axes, with pace of life and environmental antigen exposure being two examples. These axes may themselves covary directly or inversely, and such relationships can lead to conflicting predictions regarding immune investment. If pace of life shapes immune investment then, following life history theory, slow-living, arid zone and tropical species should invest more in immunity than fast-living temperate species. Alternatively, if antigen exposure drives immune investment, then species in antigen-rich tropical and temperate environments are predicted to exhibit higher immune indices than species from antigen-poor arid locations. To test these contrasting predictions we investigated how variation in pace of life and antigen exposure influence immune investment in related lark species (Alaudidae) with differing life histories and predicted risks of exposure to environmental microbes and parasites. We used clutch size and total number of eggs laid per year as indicators of pace of life, and aridity, and the climatic variables that influence aridity, as correlates of antigen abundance. We quantified immune investment by measuring four indices of innate immunity. Pace of life explained little of the variation in immune investment, and only one immune measure correlated significantly with pace of life, but not in the predicted direction. Conversely, aridity, our proxy for environmental antigen exposure, was predictive of immune investment, and larks in more mesic environments had higher immune indices than those living in arid, low-risk locations. Our study suggests that abiotic environmental variables with strong ties to environmental antigen exposure can be important correlates of immunological variation.

Are antimicrobial defences in bird eggs related to climatic conditions associated with risk of trans-shell microbial infection?

INTRODUCTION: All bird eggs are exposed to microbes in the environment, which if transmitted to the developing embryo, could cause hatching failure. However, the risk of trans-shell infection varies with environmental conditions and is higher for eggs laid in wetter environments. This might relate to generally higher microbial abundances and diversity in more humid environments, including on the surface of eggshells, as well as the need for moisture to facilitate microbial penetration of the eggshell. To protect against microbial infection, the albumen of avian eggs contains antimicrobial proteins, including lysozyme and ovotransferrin. We tested whether lysozyme and ovotransferrin activities varied in eggs of larks (Alaudidae) living along an arid-mesic gradient of environmental aridity, which we used as a proxy for risk of trans-shell infection. RESULTS: Contrary to expectations, lysozyme activity was highest in eggs from hotter, more arid locations, where we predicted the risk of trans-shell infection would be lower. Ovotransferrin concentrations did not vary with climatic factors. Temperature was a much better predictor of antimicrobial protein activity than precipitation, a result inconsistent with studies stressing the importance of moisture for trans-shell infection. CONCLUSIONS: Our study raises interesting questions about the links between temperature and lysozyme activity in eggs, but we find no support for the hypothesis that antimicrobial protein deposition is higher in eggs laid in wetter environments.

Offspring pay sooner, parents pay later: experimental manipulation of body mass reveals trade-offs between immune function, reproduction and survival.

INTRODUCTION: Life-history theory predicts that organisms trade off survival against reproduction. However, the time scales on which various consequences become evident and the physiology mediating the cost of reproduction remain poorly understood. Yet, explaining not only which mechanisms mediate this trade-off, but also how fast or slow the mechanisms act, is crucial for an improved understanding of life-history evolution. We investigated three time scales on which an experimental increase in body mass could affect this trade-off: within broods, within season and between years. We handicapped adult skylarks (Alauda arvensis) by attaching extra weight during first broods to both adults of a pair. We measured body mass, immune function and return rates in these birds. We also measured nest success, feeding rates, diet composition, nestling size, nestling immune function and recruitment rates. RESULTS: When nestlings of first broods fledged, parent body condition had not changed, but experimental birds experienced higher nest failure. Depending on the year, immune parameters of nestlings from experimental parents were either higher or lower than of control nestlings. Later, when parents were feeding their second brood, the balance between self-maintenance and nest success had shifted. Control and experimental adults differed in immune function, while mass and immune function of their nestlings did not differ. Although weights were removed after breeding, immune measurements during the second brood had the capacity to predict return rates to the next breeding season. Among birds that returned the next year, body condition and reproductive performance a year after the experiment did not differ between treatment groups. CONCLUSIONS: We conclude that the balance between current reproduction and survival shifts from affecting nestlings to affecting parents as the reproductive season progresses. Furthermore, immune function is apparently one physiological mechanism involved in this trade-off. By unravelling a physiological mechanism underlying the trade-offs between current and future reproduction and by demonstrating the different time scales on which it acts, our study represents an important step in understanding a central theory of life-history evolution.

Immune response to an endotoxin challenge involves multiple immune parameters and is consistent among the annual-cycle stages of a free-living temperate zone bird.

Trade-offs between immune function and other physiological and behavioural processes are central in ecoimmunology, but one important problem is how to distinguish a reallocation of resources away from the immune system from a reallocation or redistribution within the immune system. While variation in baseline values of individual immune parameters is well established, studies in wild animals on multiple parameters during an immune response are lacking. It also remains to be tested whether and how immune responses correlate with baseline values that vary, for example, over the course of an annual cycle. We studied immunological responses to an endotoxin challenge in skylarks (Alauda arvensis), a partial migrant bird breeding in temperate zones. We compared birds injected with the endotoxin LPS with un-injected controls, characterizing immunological responses with leukocyte profiles, titres of lytic enzymes and natural antibodies, and concentrations of haptoglobin and heat shock proteins. We did this in five annual-cycle stages to test whether the response varied throughout the year. The endotoxin challenge affected six of 10 measured parameters. Lysis titres and proportions of heterophils increased; haptoglobin concentrations and proportions of lymphocytes, basophils and eosinophils decreased. The variable effects on different immune components demonstrate the complexity of an immune response. We found no evidence that the response differed between annual-cycle stages. The response was independent of baseline measures taken directly upon capture in the field, indicating that birds were facing no immunological ceiling when mounting an immune response. Values of five parameters collected under field conditions were significantly related to values taken under standardized laboratory conditions. We conclude that multiple parts of the immune system are modulated during an immunological response and that responses are not re-organized throughout the annual cycle.

Climate change, host plant availability, and irrigation shape future region-specific distributions of the Sitobion grain aphid complex.

BACKGROUND: Understanding where species occur using species distribution models has become fundamental to ecology. Although much attention has been paid to invasive species, questions about climate change related range shifts of widespread insect pests remain unanswered. Here, we incorporated bioclimatic factors and host plant availability into CLIMEX models to predict distributions under future climate scenarios of major cereal pests of the Sitobion grain aphid complex (Sitobion avenae, S. miscanthi, and S. akebiae). Additionally, we incorporated the application of irrigation in our models to explore the relevance of a frequently used management practice that may interact with effects of climate change of the pest distributions. RESULTS: Our models predicted that the area potentially at high risk of outbreaks of the Sitobion grain aphid complex would increase from 41.3% to 53.3% of the global land mass. This expansion was underlined by regional shifts in both directions: expansion of risk areas in North America, Europe, most of Asia, and Oceania, and contraction of risk areas in South America, Africa, and Australia. In addition, we found that host plant availability limited the potential distribution of pests, while the application of irrigation expanded it. CONCLUSION: Our study provides insights into potential risk areas of insect pests and how climate, host plant availability, and irrigation affect the occurrence of the Sitobion grain aphid complex. Our results thereby support agricultural policy makers, farmers, and other stakeholders in their development and application of management practices aimed at maximizing crop yields and minimizing economic losses. © 2023 Society of Chemical Industry.

Risk factors for Lyme disease: A scale-dependent effect of host species diversity and a consistent negative effect of host phylogenetic diversity.

Biodiversity can influence disease risk. One example of a diversity-disease relationship is the dilution effect, which suggests higher host species diversity (often indexed by species richness) reduces disease risk. While numerous studies support the dilution effect, its generality remains controversial. Most studies of diversity-disease relationships have overlooked the potential importance of phylogenetic diversity. Furthermore, most studies have tested diversity-disease relationships at one spatial scale, even though such relationships are likely scale dependent. Using Lyme disease as a model system, we investigated the effects of host species richness and phylogenetic relatedness on the number of reported Lyme disease cases in humans in the U.S.A. at two spatial scales (the county level and the state level) using piecewise structural equation modelling. We also accounted for relevant climatic and habitat-related factors and tested their correlations with the number of Lyme disease cases. We found that species assemblages with more related species (i.e., host species in the order Rodentia) were associated with more Lyme disease cases in humans. Host species richness correlated negatively with the number of Lyme disease cases at the state level (i.e., a dilution effect), a pattern that might be explained by the higher number of reservoir-incompetent species at high levels of species richness at this larger spatial scale. In contrast, a positive correlation was found between species richness and the number of Lyme disease cases at the county level, where a higher proportion of rodent species was associated with higher levels of species richness, potentially amplifying the disease risk. Our results highlight that analyse at a single spatial scale can miss some impacts of biodiversity on human health. Thus, multi-scale analyses with consideration of host phylogenetic diversity are critical for improving our understanding of diversity-disease relationships.

Intense flight and endotoxin injection elicit similar effects on leukocyte distributions but dissimilar effects on plasma-based immunological indices in pigeons.

Most birds rely on flight for survival. Yet as an energetically taxing and physiologically integrative process, flight has many repercussions. Studying pigeons (Columba livia) and employing physiological and immunological indices that are relevant to ecologists working with wild birds, we determined what, if any, acute immune-like responses result from bouts of intense, non-migratory flight. We compared the effects of flight with the effects of a simulated bacterial infection. We also investigated indices in terms of their post-flight changes within individuals and their relationship with flight speed among individuals. Compared to un-flown controls, flown birds exhibited significant elevations in numbers of heterophils relative to numbers of lymphocytes and significant reductions in numbers of eosinophils and monocytes. Furthermore, within-individual changes in concentrations of an acute phase protein were greater in flown birds than in controls. However, none of the flight-affected indices showed any evidence of being related to flight speed. While some of the effects of flight were comparable to the effects of the simulated bacterial infection, other effects were observed only after one of these two physiological challenges. Our study suggests that flight by pigeons yields immune-like responses, and these responses have the potential to complicate the conclusions drawn by ecologists regarding immune function in free-living birds. Still, a better understanding of the repercussions of flight can help clarify the ties between the physiology of exercise and the disease ecology of migration and will ultimately assist in the broader goal of accounting for immunological variation within and among species.

Immune function in a free-living bird varies over the annual cycle, but seasonal patterns differ between years.

A central hypothesis of eco-immunology proposes trade-offs between immune defences and competing physiological and behavioural processes, leading to immunological variation within and among annual-cycle stages, as has been revealed for some species. However, few studies have simultaneously investigated patterns of multiple immune indices over the entire annual cycle in free-living birds, and none has investigated the consistency of seasonal patterns across multiple years. We quantified lysis, agglutination, haptoglobin, leukocyte profiles, and body mass in free-living skylarks (Alauda arvensis) through two complete annual cycles and within and between four breeding seasons. The skylarks' annual cycle is characterised by annually repeated changes in energy and time budgets, social structure and diet. If trade-offs relating to these cyclic changes shape evolution, predictable intra-annual immune patterns may result. Alternatively, intra-annual immune patterns may vary among years if fluctuating environmental changes affect the cost-benefit balances of immune function. We found significant variation in immune indices and body mass across the annual cycle, and these patterns differed between years. Immune parameters differed between four breeding seasons, and in all years, lysis and agglutination increased as the season progressed independent of average levels. Population-level patterns (intra-annual, inter-annual, within breeding season) were consistent with within-individual patterns based on repeated measurements. We found little evidence for sex differences, and only haptoglobin was correlated (negatively) with body mass. We conclude that immune modulation is not simply a pre-programmed phenomenon that reflects predictable ecological changes. Instead, fluctuating environmental conditions that vary among years likely contribute to the immunological variation that we observed.

Baseline haptoglobin concentrations are repeatable and predictive of certain aspects of a subsequent experimentally-induced inflammatory response.

Ecologists sometimes assume immunological indices reflect fundamental attributes of individuals-an important assumption if an index is to be interpreted in an evolutionary context since among-individual variation drives natural selection. Yet the extent to which individuals vary over different timescales is poorly understood. Haptoglobin, an acute phase protein, is an interesting parameter for studying variability as it is easily quantified and concentrations vary widely due to the molecule's role in inflammation, infection and trauma. We quantified haptoglobin in pigeon plasma samples collected over fourteen months and calculated repeatability to evaluate if haptoglobin concentration is a distinctive trait of individuals. We also explored the capacity of baseline haptoglobin concentrations to predict an array of physiological changes associated with a subsequent experimentally-induced inflammatory response. Maximum repeatability, which occurred over a short mid-winter interval, equaled 0.57. Baseline haptoglobin concentrations predicted response haptoglobin concentrations better than any other endotoxin-induced change. Overall, we identified several strengths and limitations of baseline [Hp] quantification. Acknowledging these qualities should lead to more refined conclusions in studies of the ecology and evolution of immune function.

Digest: Great tits and their ticks: Life-history traits affect tick fitness.

Ectoparasites such as ticks face many challenges to reproduce. They must maximize the size of their blood meal while avoiding being removed by their host. In a new study, Fracasso and colleagues followed the fate of individual ticks to determine which life-history traits impact tick fitness. Their findings reveal a complex interplay between numerous parameters, including feeding time and engorgement weight. The situation is likely even more complicated when considering vector-borne pathogens.

The microbial environment modulates non-genetic maternal effects on egg immunity.

BACKGROUND: In a diverse microbial world immune function of animals is essential. Diverse microbial environments may contribute to extensive variation in immunological phenotypes of vertebrates, among and within species and individuals. As maternal effects benefit offspring development and survival, whether females use cues about their microbial environment to prime offspring immune function is unclear. To provide microbial environmental context to maternal effects, we asked if the bacterial diversity of the living environment of female zebra finches Taeniopygia guttata shapes maternal effects on egg immune function. We manipulated environmental bacterial diversity of birds and tested if females increased immunological investment in eggs in an environment with high bacterial diversity (untreated soil) versus low (gamma-sterilized soil). We quantified lysozyme and ovotransferrin in egg albumen and IgY in egg yolk and in female blood, and we used 16S rRNA gene sequencing to profile maternal cloacal and eggshell microbiotas. RESULTS: We found a maternal effect on egg IgY concentration that reflected environmental microbial diversity: females who experienced high diversity deposited more IgY in their eggs, but only if maternal plasma IgY levels were relatively high. We found no effects on lysozyme and ovotransferrin concentrations in albumen. Moreover, we uncovered that variation in egg immune traits could be significantly attributed to differences among females: for IgY concentration in yolk repeatability R = 0.80; for lysozyme concentration in albumen R = 0.27. Furthermore, a partial least squares path model (PLS-PM) linking immune parameters of females and eggs, which included maternal and eggshell microbiota structures and female body condition, recapitulated the treatment-dependent yolk IgY response. The PLS-PM additionally suggested that the microbiota and physical condition of females contributed to shaping maternal effects on egg immune function, and that (non-specific) innate egg immunity was prioritized in the environment with low bacterial diversity. CONCLUSIONS: The microbial environment of birds can shape maternal effects on egg immune function. Since immunological priming of eggs benefits offspring, we highlight that non-genetic maternal effects on yolk IgY levels based on cues from the parental microbial environment may prove important for offspring to thrive in the microbial environment that they are expected to face.