Environmental proxies of antigen exposure explain variation in immune investment better than indices of pace of life
Horrocks, N.P.C. ; Hegemann, A. ; Ostrowski, S. ; Ndithia, H. ; Shobrak, M. ; Williams, J.B. ; Matson, K.D. ; Tieleman, B.I. - \ 2015
Oecologia 177 (2015)1. - ISSN 0029-8549 - p. 281 - 290.
female pied flycatchers - tropical birds - trade-offs - ecological immunology - microbial diversity - natural antibodies - aridity gradient - south-africa - history - patterns
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.
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
Hegemann, A. ; Matson, K.D. ; Versteegh, M.A. ; Villegas, A. ; Tieleman, B.I. - \ 2013
Journal of Experimental Biology 216 (2013)14. - ISSN 0022-0949 - p. 2573 - 2580.
sparrows passer-domesticus - physiological trade-offs - acute-phase response - heat-shock proteins - in-house sparrows - ecological immunology - humoral immunity - binding globulin - broiler-chickens - seasonal-changes
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.
Seasonal patterns in immune indices reflect microbial loads on birds but not microbes in the wider environment
Horrocks, N.P.C. ; Matson, K.D. ; Shobrak, M. ; Tinbergen, J.M. ; Tieleman, B.I. - \ 2012
Ecosphere 3 (2012)2. - ISSN 2150-8925 - 14 p.
feather-degrading bacteria - arabian desert - saudi-arabia - life-history - trade-offs - ecological immunology - evolutionary ecology - atmospheric bacteria - airborne particles - aridity gradient
Documenting patterns in immune function is a first step to understanding immune variation, but to comprehend causes and consequences, antigen and parasite exposure that may drive such variation must be determined. We measured host-independent microbial exposure in five species of larks (Alaudidae) in the Arabian Desert by sampling ambient air for culturable microbes during late spring and winter, two periods with contrasting environmental conditions. We developed a novel technique to assay densities of microbes shed from birds, and we quantified four indices of constitutive innate immunity. Birds shed significantly more microbes during spring than winter, and all immune indices except one were also significantly higher during spring. In contrast, concentrations of airborne environmental microbes were higher in winter. Among all birds in both seasons, lysis titers were positively correlated with total densities of microbes shed from birds, suggesting that immune defenses are directed towards the microbes that birds carry, rather than microbes in the wider environment. Our findings highlight the relevance of quantifying non-specific immune challenges in ecological immunology studies, and reinforce the importance of both host-dependent and host-independent measures of antigenic pressure for understanding immune variation. Read More: http://www.esajournals.org/doi/abs/10.1890/ES11-00287.1
Wild skylarks seasonally modulate energy budgets but maintain energetically costly inflammatory immune responses throughout the annual cycle
Hegemann, A. ; Matson, K.D. ; Versteegh, M.A. ; Tieleman, B.I. - \ 2012
PLoS ONE 7 (2012)5. - ISSN 1932-6203 - 8 p.
distance migrant shorebird - acute-phase response - basal metabolic-rate - trade-offs - life-history - ecological immunology - parental effort - house sparrows - zebra finches - wind-tunnel
A central hypothesis of ecological immunology is that immune defences are traded off against competing physiological and behavioural processes. During energetically demanding periods, birds are predicted to switch from expensive inflammatory responses to less costly immune responses. Acute phase responses (APRs) are a particularly costly form of immune defence, and, hence, seasonal modulations in APRs are expected. Yet, hypotheses about APR modulation remain untested in free-living organisms throughout a complete annual cycle. We studied seasonal modulations in the APRs and in the energy budgets of skylarks Alauda arvensis, a partial migrant bird from temperate zones that experiences substantial ecological changes during its annual cycle. We characterized throughout the annual cycle changes in their energy budgets by measuring basal metabolic rate (BMR) and body mass. We quantified APRs by measuring the effects of a lipopolysaccharide injection on metabolic rate, body mass, body temperature, and concentrations of glucose and ketone. Body mass and BMR were lowest during breeding, highest during winter and intermediate during spring migration, moult and autumn migration. Despite this variation in energy budgets, the magnitude of the APR, as measured by all variables, was similar in all annual cycle stages. Thus, while we find evidence that some annual cycle stages are relatively more energetically constrained, we find no support for the hypothesis that during these annual cycle stages birds compromise an immune defence that is itself energetically costly. We suggest that the ability to mount an APR may be so essential to survival in every annual cycle stage that skylarks do not trade off this costly form of defence with other annual cycle demands.
Immune function in a free-living bird varies over the annual cycle, but seasonal patterns differ between years
Hegemann, A. ; Matson, K.D. ; Both, C. ; Tieleman, B.I. - \ 2012
Oecologia 170 (2012)3. - ISSN 0029-8549 - p. 605 - 618.
in-house sparrows - trade-offs - ecological immunology - evolutionary ecology - passer-domesticus - alauda-arvensis - life-history - habitat use - blue tits - defense
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.
Immune indexes of larks from desert and temperate regions show weak associations with life history but stronger links to environmental variation in microbial abundance
Horrocks, N.P.C. ; Hegemann, A. ; Matson, K.D. ; Hine, K. ; Jaquier, S. ; Shobrak, M. ; Williams, J.B. ; Tinbergen, J.M. ; Tieleman, B.I. - \ 2012
Physiological and Biochemical Zoology 85 (2012)5. - ISSN 1522-2152 - p. 504 - 515.
tropical birds - trade-offs - ecological immunology - atmospheric bacteria - airborne particles - arabian desert - defense - haptoglobin - investment - diversity
Immune defense may vary as a result of trade-offs with other life-history traits or in parallel with variation in antigen levels in the environment. We studied lark species (Alaudidae) in the Arabian Desert and temperate Netherlands to test opposing predictions from these two hypotheses. Based on their slower pace of life, the trade-off hypothesis predicts relatively stronger immune defenses in desert larks compared with temperate larks. However, as predicted by the antigen exposure hypothesis, reduced microbial abundances in deserts should result in desert-living larks having relatively weaker immune defenses. We quantified host-independent and host-dependent microbial abundances of culturable microbes in ambient air and from the surfaces of birds. We measured components of immunity by quantifying concentrations of the acute-phase protein haptoglobin, natural antibody-mediated agglutination titers, complement-mediated lysis titers, and the microbicidal ability of whole blood. Desert-living larks were exposed to significantly lower concentrations of airborne microbes than temperate larks, and densities of some bird-associated microbes were also lower in desert species. Haptoglobin concentrations and lysis titers were also significantly lower in desert-living larks, but other immune indexes did not differ. Thus, contrary to the trade-off hypothesis, we found little evidence that a slow pace of life predicted increased immunological investment. In contrast, and in support of the antigen exposure hypothesis, associations between microbial exposure and some immune indexes were apparent. Measures of antigen exposure, including assessment of host-independent and host-dependent microbial assemblages, can provide novel insights into the mechanisms underlying immunological variation.
Trade-off between growth and immune function: a meta-analysis of selection experiments
Most, P.J. van der; Jong, B. de; Parmentier, H.K. ; Verhulst, S. - \ 2011
Functional Ecology 25 (2011)1. - ISSN 0269-8463 - p. 74 - 80.
newcastle-disease virus - increased body-weight - random-bred strain - sheep erythrocytes - antibody-response - pasteurella-multocida - life-history - physiological-responses - ecological immunology - evolutionary ecology
1. Evidence suggests that developing and maintaining an effective immune system may be costly and that an organism has to make a trade-off between immune function and other fitness-enhancing traits. To test for a trade-off between growth and immune function we carried out a meta-analysis of data from lines of poultry that had been divergently selected for either growth (body mass) or an aspect of immune function. This is relevant to our understanding of the evolution of immune function, but also because the increased prevalence of antibiotic-resistant bacteria and calls to restrict the use of antibiotics in the agricultural industry has made immune function of livestock an important theme. Has the selection of animals for rapid growth unintentionally resulted in reduced immune function? 2. The lines selected for increased growth all showed a strong and significant decrease in immune function (standard difference in means = 0·8; P <0·001). No difference was found between the effects on cellular or humoral immunity, although there were few data on cellular immunity, and hence this deserves more study. However, in the lines selected for immune function the effect on growth was heterogeneous and overall it was close to zero. 3. Testing for publication bias revealed that the effect of selection for body mass on immune function was robust. However, there was considerable heterogeneity in both body mass and immune function data. The heterogeneity in the growth-selected lines cannot be accounted for by gender or species: the only turkey line had an effect size between that of the two chicken lines. 4. In conclusion, we found that selection for growth does indeed compromise immune function, but selection for immune function did not consistently affect growth. This is in agreement with the supposition that the costs of growth are large relative to the costs of immune function, and on a practical level this suggests that it may be possible to breed animals for increased growth without loss of immune function.
Seasonal redistribution of immune function in migrant shorebird: annual cycle effects override adjustments to thermal regime
Buehler, D.M. ; Piersma, T. ; Matson, K.D. ; Tieleman, B.I. - \ 2008
American Naturalist 172 (2008)6. - ISSN 0003-0147 - p. 783 - 796.
long-distance migrant - trade-offs - ecological immunology - calidris-canutus - red knots - evolutionary ecology - natural antibodies - tropical birds - life-history - innate
Throughout the annual cycle, demands on competing physiological systems change, and animals must allocate resources to maximize fitness. Immune function is one such system and is important for survival. Yet detailed empirical data tracking immune function over the entire annual cycle are lacking for most wild animals. We measured constitutive immune indices once a month for a year on captive red knots (Calidris canutus). We also examined temperature as an environmental contributor to immune variation by manipulating ambient temperature to vary energy expenditure. To identify relationships among immune indices, we performed principal-component analysis. We found significant repeatability in immune indices over the annual cycle and covariation of immune indices within and among individuals. This covariation suggests immune strategies as individual traits among individuals and the use of different immune strategies during different annual-cycle stages within individuals. Over the annual cycle, both higher-cost phagocyte-based immunity and lower-cost lymphocyte-based immunity were high during mass change, but there was a clear shift toward lower-cost lymphocyte-based immunity during peak molt. Experimental manipulation of temperature had little effect on annual variation in immune function. This suggests that other environmental factors, such as food availability and disease, should also be examined in the future.
Rate of constitutive innate humoral immune development in Leach's storm petrel (Oceanodroma leucorhoa) chicks is negatively correlated with growth rate
Mauck, R.A. ; Matson, K.D. ; Philipsborn, J. ; Ricklefs, R.E. - \ 2005
Functional Ecology 19 (2005)6. - ISSN 0269-8463 - p. 1001 - 1007.
cell-mediated-immunity - trade-offs - ecological immunology - evolutionary ecology - natural antibodies - pied flycatchers - tit nestlings - immunocompetence - responses - costs
1 Using a simple technique for assessing constitutive innate immune function recently adapted for use in wild populations, we characterize changes in avian immune system development by repeated measurements of individuals over the period of nestling growth in a wild population of Leach's Storm-Petrels (Oceanodroma leucorhoa). 2 We measured levels of natural antibodies (NAb) during the early, middle and late phases of storm-petrel development and related these levels and NAb rate of change to mass and wing length growth. We used natural variation in nestling growth to assess the influence of nutritional status on the development of innate immunity. 3 NAb levels increased over the first 50 days of chick development; however, rate of increase was inversely proportional to wing growth. 4 Initial titre levels were inversely proportional to rate of change in NAb levels over the first 50 days of immune development. This suggests that individuals with low initial NAb levels accelerate immune development to reach adult levels, whereas individuals with high initial levels do not. 5 As in previous studies, our results demonstrate an inverse relationship between growth rate and development of components of the avian immune system. While such a relationship is consistent with the idea that immune function development involves trade-offs, the processes involved are more complex than simple energy allocation.