The developmental dynamics of infection and immunity influence optimal resource allocation and immunological investment

Background/Question/Methods

The integration of molecular mechanism into life history theory provides a window into the genetic architecture that produces trade-offs between life history traits and the selective pressures that drive life history evolution. In larval insects, most pathways associated with immunological function also control aspects of larval growth and development, raising the possibility of antagonistic pleiotropy between development and immunity. Empirical evidence suggests that development may periodically commandeer pathway products and resources, producing an interference effect on the ability of a host to mount an immune response. However, this developmental interference effect is pegged to host developmental stage and depends on the specific genetic pathway, and may therefore exhibit a variety of transient dynamical patterns. We built a within-host model of energy allocation to development, immunity, and parasites that accounts for developmental interference on immunity for several pleiotropic pathways, while also incorporating the relationship between host stage and probability of exposure to specific parasites. We used this model to investigate the impact of developmental dynamics on optimal levels of resource mobilization rates and investment in constitutive immunity. We then simulated developmentally heterogeneous populations of insects to investigate the impact of developmental dynamics on patterns of susceptibility to infection.

Results/Conclusions

Developmental interference generally favors an increase in optimal constitutive immune investment and a decrease in energy mobilization rates compared to a scenario with no interference, although these patterns were sensitive to the stage at which the parasite attacks the host. Developmental interference also generally decreases resistance and increases fitness tolerance to infection. Finally, different patterns of interference, reflecting underlying differences in molecular mechanism, produce qualitatively different patterns of host population susceptibility depending on the age of parasite attack, which could confuse the interpretation of survival data in experimental settings. These model results suggest that the developmental dynamics of infection and immunity could bear responsibility for a substantial proportion of heterogeneity in host susceptibility to infection. Mechanism-specific developmental dynamics should therefore be considered in both experimental settings and models of disease dynamics.