No evidence of metabolic costs following adaptive immune activation or reactivation in house sparrows

Abstract

The energy cost of adaptive immune activation in endotherms is typically quantified from changes in resting metabolic rate following exposure to a novel antigen. An implicit assumption of this technique is that all variation in energy costs following antigenic challenge is due solely to adaptive immunity, while ignoring potential changes in the energy demands of ongoing bodily functions. We critically assess this assumption by measuring both basal metabolic rate (BMR) and exercise-induced maximal metabolic rate (MMR) in house sparrows before and after the primary and two subsequent vaccinations with either saline (sham) or two novel antigens (keyhole limpet haemocyanin and sheep red blood cells; KLH and SRBC, respectively). We also examined the effect of inducing male breeding levels of testosterone (T) on immune responses and their metabolic costs in both males and females. Although there was a moderate decrease in KLH antibody formation in T-treated birds, there was no effect of T on BMR, MMR or immunity to SRBC. There was no effect of vaccination on BMR but, surprisingly, all vaccinated birds maintained MMR better than sham-treated birds as the experiment progressed. Our findings caution against emphasizing energy costs or nutrient diversion as being responsible for reported fitness reductions following activation of adaptive immunity.

Keywords: adaptive immune costs; basal metabolic rate; hypervaccination; immunocompetence handicap hypothesis; maximum metabolic rate; testosterone.

Figure 1.

Change in immune responses of antigen-injected (immune-challenged) (n = 32) and sham-injected (n = 30) birds following serial injections, in relation to pre-injection ‘baseline’ scores, where immune responses were measured as the highest twofold dilution of plasma producing lysis (a) or agglutination (b) to SRBC, and the optical density (at 450 nm) of plasma in an ELISA to KLH as a percentage of positive control (c). Immune responses of birds given a sham injection did not deviate from pre-injection values, whereas immune responses of vaccinated birds increased significantly after each injection.

Figure 2.

Change in body mass (a) and metabolic rates ((b) BMR; (c) MMR) of antigen-injected (immune-challenged) (n = 32) and sham-injected (n = 30) birds following serial injections, in relation to pre-injection ‘baseline’ scores. Body mass and BMR were unaffected by injection type and did not vary over time. By contrast, MMR declined in all treatment groups over the experimental period, but to a lesser extent in immune-challenged birds compared to sham-injected birds.