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Immune responses evolve to balance the benefits of microbial killing against the costs of autoimmunity and energetic resource use. Models that explore the evolution of optimal immune responses generally include a term for constitutive immunity, or the level of immunological investment prior to microbial exposure, and for inducible immunity, or investment in immune function after microbial challenge. However, studies rarely consider the functional form of inducible immune responses with respect to microbial density, despite the theoretical dependence of immune system evolution on microbe‐ versus immune‐mediated damage to the host. In this study, we analyse antimicrobial peptide (AMP) gene expression from seven wild‐caught flour beetle populations (Triboliumspp.) during acute infection with the virulent bacteriaBacillus thuringiensis(Bt) andPhotorhabdus luminescens(P.lum) to demonstrate that inducible immune responses mediated by the humoral IMD pathway exhibit natural variation in both microbe density‐dependent and independent temporal dynamics. Beetle populations that exhibited greater AMP expression sensitivity to Bt density were also more likely to die from infection, while populations that exhibited higher microbe density‐independent AMP expression were more likely to surviveP. luminescensinfection. Reduction in pathway signalling efficiency through RNAi‐mediated knockdown of theimdgene reduced the magnitude of both microbe‐independent and dependent responses and reduced host resistance to Bt growth, but had no net effect on host survival. This study provides a framework for understanding natural variation in the flexibility of investment in inducible immune responses and should inform theory on the contribution of nonequilibrium host‐microbe dynamics to immune system evolution.

 

ABSTRACT A central challenge in the fields of evolutionary immunology and disease ecology is to understand the causes and consequences of natural variation in host susceptibility to infectious diseases. As hosts progress from birth to death in the wild, they are exposed to a wide variety of microorganisms that influence their physical condition, immune system maturation, and susceptibility to concurrent and future infection. Thus, multiple exposures to the same or different microbes can be important environmental drivers of host immunological variation and immune priming. In this perspective, I discuss parasite infracommunity interactions and their imprint on host immunity in space and time. I further consider feedbacks from parasite community dynamics within individual hosts on the transmission of disease at higher levels of biological organization and highlight the promise of systems biology approaches, using flour beetles as an example, for studying the role of multiple infections on immunological variation in wild populations.