Costs in the ecology and evolution of the vertebrate immune system

Abstract: A central assumption of theories of the ecology and evolution of immunological defence is that defence has not only benefits (in the form of resistance against parasites), but also costs. The aim of my studies was to investigate the nature and magnitude of costs of the vertebrate immune system, and to examine some of the consequences of these costs. First, I investigated the energetic cost of the adaptive immune system. To this end, I compared the basal metabolic rate (BMR) of transgenic mice lacking an adaptive immune system (i.e. mice with only innate defence) with that of normal mice. Surprisingly, mice with only innate defence had higher BMR than normal mice. This suggests that the combination of innate and adaptive immune defence has led to energetic benefits rather than costs. Second, I examined the role of costs of defence to understand the causes and consequences of variation in immune responsiveness (IR). To this end, I used the blue tit as model organism and measured IR as the strength of the ab-response to diphtheria-tetanus (DT) vaccine. A parent-offspring analysis showed that there is a substantial amount of genetic variation in IR to at least one of the antigens. However, experimental studies also showed that IR is reduced during stress in the form of low temperature and reproductive effort, i.e. that IR is phenotypically plastic. Could this be due to an energetic trade-off between the immune response to DT and other energetically costly activities? To investigate this, I compared the BMR of immunized and control blue tits. There was no statistically significant difference in BMR between the two groups, indicating that this response is rather cheap. This makes an energetic trade-off unlikely. Instead, I have proposed that stress in the form of for example a high reproductive effort increases the risk that the immune system will attack self (immunopathology), and that the immune system is suppressed during stress to counteract that. Irrespective of whether costs of defence are expressed in the currency of energy or immunopathology, these physiological costs must translate into fitness costs to have any ecological or evolutionary consequences. To investigate if that is the case, I immunized female blue tits with DT during the nestling-feeding period and compared their level of parental effort (nestling-feeding rate) with that of control birds. Immunized birds fed their nestlings at a lower rate, indicating a potential cost of the immune response in terms of reduced fecundity. Finally, to investigate the consequences of variation in IR, I measured ab-responsiveness to DT in blue tits during winter and investigated the relationship between IR and survival to the following breeding season. Primary IR to diphtheria was subject to stabilizing selection, indicating that this component o defence has both benefits and costs. On the other hand, secondary IR to tetanus was subject to positive directional selection, which suggests that this component of defence reflects an individual’s overall condition.