Highway to the danger zone: exposure‐dependent costs of immunity in a vertebrate ectotherm

Abstract

Summary Parasite exposure often causes innate immune activation, resulting in trade‐offs among physiological processes and strong selection on the parasite. Costs of immune activation vary widely among and within host populations though, likely dependent on the evolutionary history of host–parasite interactions and the environments in which they occur. For hosts, degree of exposure may drive the magnitude of costs incurred and subsequently whether hosts resist or tolerate infections. If costs increase concomitantly with exposure, a threshold may exist where the expense of parasite resistance becomes prohibitive and parasite tolerance becomes favourable. Here, we characterized exposure‐dependent costs of an innate immune response in brown anoles (Anolis sagrei) by tracking allocation of an isotopically labelled essential amino acid (13C‐leucine), to the liver and gonads. To elicit immune responses, we used lipopolysaccharide (LPS), a strongly immunogenic molecule from Salmonella spp. We found that both sexes paid dose‐dependent costs of SalmonellaLPS‐induced immune activation, but costs were experienced differently by the sexes, likely due to differences in life history. Males allocated more leucine to their livers in response to higher LPS doses. In females, a tendency for increased costs in response to dose was only revealed when leucine allocation ratios between lymphoid and reproductive organs were considered. We also found that regardless of dose, males always allocated more leucine to their gonads than females. Lastly, and perhaps most interestingly, cost functions in both sexes were linear, but with shallow slopes, indicating modest costs of immune activation in response to SalmonellaLPS in this species. Altogether, our results demonstrate that costs of immunity are dose dependent in this introduced lizard species, sexes experience costs differently. Characterization of relationships between host exposure and costs of immune activation such as these can facilitate predictions about how parasites might circulate through communities.