The evolution of parasite resistance has often been assumed to be governed by antagonistic selection pressures. Defense against pathogens, by mounting an immune response, confers evident benefits but may also incur costs, so that the optimal level of defense is expected to depend on the balance between benefits and costs. Although the benefits of immune surveillance are well known, estimates of costs are still equivocal. Here we studied the behavioral and physiological modifications associated with exposure to a nonreplicating antigen (lipopolysaccharide [LPS] of Escherichia coli) in a passerine species, the house sparrow (Passer domesticus). We further investigated whether the behavioral and physiological changes provoked by LPS induced measurable repercussions on life‐history traits, such as the breeding effort and reproductive success. Finally, we tested whether the trade‐off between immune activation and breeding effort was modulated by the workload required to feed the brood. Exposure to LPS reduced activity and increased body mass loss of captive individuals; similarly, LPS injection induced a dramatic drop in feeding rate and reproductive success of breeding females. However, this reduction depended on brood size, suggesting that the strength of the trade‐off between immune activation and reproduction was affected by the workload required to feed the brood. Overall, this study stresses the magnitude of costs associated with mounting immune responses and the ecological and evolutionary consequences for natural populations.
Nest-building behavior has been suggested to represent a postmating sexually selected signal in passerine birds, an hypothesis that has received both comparative and experimental support. Because selection pressure due to parasites and diseases should be particularly high during nest building, mainly due to energetic costs and depression of the immune system associated with this reproductive phase, we predicted a positive association between nest-building effort and immunity. Nest-building effort would reflect the ability to produce efficient immune responses of builders only if individuals with a superior immune system would display exaggerated nest-building effort. We tested this prediction by studying the relationship between volume of nest material used for nest construction and, at the intraspecific level, estimates of innate humoral immune response in barn swallows Hirundo rustica. At the interspecific level, we used responses to the mitogenic phytohemagglutinin as an indicator of adaptive immune response of European passerine species. As predicted, we found, after controlling for several potential confounding factors, that volume of nest material was positively related to immune response both at the intra- and at the interspecific level. Alternative hypotheses explaining the comparative results are discussed.
Melanin‐based coloration is widespread among vertebrates, but the adaptive function of this trait remains poorly known. Recently, it has been shown that differently coloured individuals have different abilities to cope with parasites. This correlation between melanin‐based coloration and immunity could be explained by the pleiotropic effects of genes coding for melanin pigmentation on the immune system (‘genetic link’ hypothesis) but also because differently coloured individuals may exploit alternative habitats varying in parasite exposure, which leads to different development of the immune function (‘exposure’ hypothesis). As feral pigeons Columba livia are genetically polymorphic with respect to melanic coloration, they constitute an ideal model system to address such hypotheses. In this study, we showed that darker melanic individuals had a lower endoparasite intensity (reflecting host susceptibility) and had a greater cellular immune response to PHA injection than paler ones, whereas parasite prevalence (reflecting exposure to vectors) was similar between colorations. These results provide a correlative support of the ‘genetic link’ hypothesis: differently coloured individuals might be similarly exposed to parasites but darker ones might have a better ability to control the infection. This suggests that parasitism could play a crucial role in the maintenance of colour polymorphism in natural populations, which opens the interesting possibility that differently coloured individuals could be adapted to alternative environments varying in parasite diversity and exposure.
The costs of parasitism to a host's reproductive success (RS) often increase with time since infection. For hosts experiencing this type of infection, it is predicted that they will maximize their RS by bringing forward their schedule of reproduction. This is because the costs associated with such a response can be discounted against a reduced future RS due to parasitism. The microsporidian Vavraia culicis is a natural parasite of mosquitoes and one whose costs increase over time as its spores accumulate and damage host tissues. As larvae, male and female Culex pipiens mosquitoes behaved differently towards infection with V. culicis. Infected females pupated earlier than uninfected females and tended to emerge as smaller adults, indicating a cost to their fecundity. However, the age and size at maturity of infected male mosquitoes was no different from uninfected males. The results of this study support theoretical predictions and highlight the potential roles that host gender and density–dependent interactions may have in determining the response of host life-history traits to parasitism.
Summary 1. Parental effects can have profound consequences on offspring phenotype. Still, little is known about the relative influence of prenatal versus postnatal parental effects of parasite exposure of parents on offspring traits. 2. In this study, we investigated the respective role of a prenatal and a postnatal immune challenge of parent feral pigeons ( Columba livia ) on offspring humoral immunity, growth and survival. We used a cross‐fostering design and antigen injections in biological and foster parents. Feral pigeons are particularly suitable for studying the effects of parental immune challenges because they can affect the phenotype of their young through the transmission of prenatal antibodies in the egg and postnatal antibodies in the ‘crop milk’, a substance produced in the crop of both parents. 3. Results show that a prenatal immune challenge of biological parents with keyhole limpet haemocyanin (KLH) antigen decreased the humoral response against KLH of nestlings injected at 14 days of age. In contrast, a postnatal immune challenge of foster parents with KLH enhanced the humoral response of 1‐year‐old juveniles exposed to a second KLH injection, but only when these juveniles had received their first injection at 3 days of age. 4. No effect on nestling and juvenile response to another antigen (NDV) was observed, indicating that the changes in humoral responses were specific to the KLH injected in parents. In addition to this, prenatal and postnatal parental immune challenges had an interaction effect on fledging body mass, but no effect on juvenile survival. 5. This study shows that pre‐ and postnatal exposure to antigens in parents has contrasted effects on offspring humoral response and growth. Moreover, it shows that the timing of an early exposure to antigens in nestlings has important effects on their specific humoral response. 6. This study thus suggests that pre‐ and postnatal parental effects have distinct roles in shaping the phenotype of the offspring on different time scales and calls for further investigations on the potential adaptive role of combined parental effects. Moreover, it suggests that pigeon milk has positive effects on offspring humoral immunity and thus could potentially have a similar immune role as mammalian milk.
Negative density feedbacks have been extensively described in animal species and involve both consumptive (i.e. trophic interactions) and non‐consumptive (i.e. social interactions) mechanisms. Glucocorticoids are a major component of the physiological stress response and homeostasis, and therefore make a good candidate for proximate determinants of negative density feedbacks. Here, we combined laboratory and field experiments with enclosed populations to investigate the relationship between density, social stress and plasma corticosterone levels in the common lizard Zootoca vivipara . This species exhibits strong negative density feedbacks that affect females more than males, and its life history is sensitive to experimentally‐induced chronic elevation of corticosterone plasma levels. We found that prolonged crowding in the laboratory can trigger a chronic secretion of corticosterone independent from food restriction. In the field experiments, corticosterone levels of females were not affected by population density. Corticosterone levels of males increased with population density but only during the late activity season in a first field experiment where we manipulated density. They also increased with density during the mating season but only in populations with a female‐biased sex ratio in a second field experiment where we crossed manipulated density and adult sex ratio. Altogether, our results provide limited evidence for a role of basal corticosterone secretion in density feedbacks in this species. Context and density‐dependent effects in males may arise from changes in behavior caused by competition for resources, male–male competition, and mating.
Summary 1. We tested the condition‐dependent hypothesis of sexual advertisement in house sparrows ( Passer domesticus ). Male house sparrows have a bib of black feathers which serves as both a badge of social status and as a cue for female choice. We manipulated environmental conditions during the premoult period of juvenile house sparrows kept in outdoor aviaries. Birds were assigned to two treatments differing in the amount of dietary proteins, which are known to affect the expression of immune response in birds. We tested whether birds in the protein‐rich group had better immune responses and developed larger bibs than birds reared on a protein‐poor diet. We also checked whether immune response was a predictor of survival and parasite resistance. 2. Individuals with higher cellular immune response at capture had greater probability to survive during the 3 months of the experiment, and they had a higher probability to recover from infection with Haemoproteus sp. (a blood parasite). Conversely, birds with high immunoglobulin concentrations at capture had a higher probability of mortality. 3. Birds on the protein‐rich diet had a higher cellular immune response compared to birds in the protein‐poor treatment. Humoral immune response showed the opposite pattern, being higher for birds in the protein‐poor treatment. We did not find any effect of food quality on the development of the badge, assessed as the size of the trait and its colour properties. 4. In conclusion, our results support the view that immune defences are important for survival and parasite resistance in natural populations, and that they might be costly to produce. On the other hand, we did not find support for the condition‐dependent hypothesis of sexual advertisement, suggesting that the badge may not be a costly trait to produce. However, badge size could reflect other aspects of condition. The kind of pigments involved in colour signals may be the key factor determining the production costs of such traits.
1. Integrative studies on ageing patterns in multiple traits of organisms are challenging and rare in free-living populations. However, developing integrative approaches could prove useful to understanding ageing patterns as causes of age variations are diverse, with conflicting or related actions. Accordingly, we investigated age variation of multiple aspects in the common lizard Lacerta (Zootoca) vivipara. 2. In a wild population of common lizards, we studied five fitness components, three physiological traits (cell-mediated immunity, corticosterone level, resting metabolic rate), and controlled for individual and environmental heterogeneities. To quantify ageing patterns in fitness, we used individual-based data collected over 14 years (18 684 captures, 892 reproductive events). 3. Ageing patterns were found in multiple aspects. They provided evidence for female maturation early in adulthood (access to reproduction, litter size), followed by senescence in female reproduction (litter success) and survival. In parallel to senescence, a pattern of terminal investment enhanced offspring quality (offspring body size, offspring corpulence, litter success). Ageing patterns involved physiology with higher metabolic rate and T cell-mediated immune response in old females. 4. Several ageing patterns were dependent on environmental and individual characteristics (habitat, year, sex, body size). Interestingly, senescence occurred only in females with a high reproductive effort early in life. Rarely showed, this trade-off between early and late-life performances is expected under the antagonistic pleiotropy and disposable soma theories of senescence. 5. Overall, this study emphasizes the interest of integrative studies to investigate the multifaceted process of ageing.
Melanin-based coloration is widespread among vertebrates, yet the adaptive significance of such pigments remains elusive, particularly with regard to the link between melanin and immune-mediated maternal effects. The aim of this study was to investigate whether melanin-based coloration could signal the ability of mothers to mount a humoral response and to transfer maternal antibodies (Ab) to their young. We injected differently coloured (pale and dark) female feral pigeons (Columba livia) with Chlamydiae (a natural antigen) and Keyhole Limpet Haemocyanin (KLH, an artificial antigen), and found no significant difference in humoral response between differently coloured females. However, darker females transferred more Ab against Chlamydiae into their eggs than paler ones, despite similar circulating levels of Ab. In addition to this, melanin-based coloration showed a high heritability value. This suggests that a genetically based coloured trait might be linked to the ability of females to transfer specific Ab against Chlamydiae (but not against KLH) to their offspring, independent of their ability to produce Ab. This suggests that transmission of maternal Ab is antigen dependent, and that melanin-based coloration might signal female ability to transmit specific Ab against natural pathogens.
