Predicting the evolution of organismal life history traits is a fundamental goal of evolutionary ecology. The evolution of parasites, in particular, poses a key challenge for both basic and applied ecology. For instance, parasite virulence and infectivity can strongly regulate the dynamics of host populations and structure ecological communities. Predicting the evolution of these traits remains challenging because parasite fitness depends on both within-host (e.g., immune function) and between-host (e.g., transmission) processes. To date, studies that account for these bidirectional feedbacks remain rare. Classical theoretical approaches to parasite evolution simplify within-host processes, using them primarily to justify life history trade-offs (e.g., virulence-transmission). Yet, ecological factors, such as host resources, can strongly alter the shape of life history trade-offs. Hence, current theory that overlooks these eco-evolutionary links may miss critical aspects of parasite evolution. We integrated data and theory centered on the zooplankton host Daphnia magna and the bacterial parasite Pasteuria ramosa to: develop and test a theoretical framework that helps clarify why, how, and when resources matter for parasite evolution. Specifically, we used a ‘nested’ modeling approach that explicitly includes both within-host and between-host processes.
Our results indicate that non-nested (classic, ‘trade-off’ models) and ‘nested’ models predict disparate outcomes for how resources influence the evolution of parasite life history. Classical approaches predict that resources will have no effect on parasite life history evolution, whereas models that include resource-dependent within-host interactions (i.e., ‘nested’ models) predict that virulence may increase or decrease as resource supply increases. The underlying mechanisms involve resource-dependent feedbacks between: (1) parasite-life history tradeoffs that modulate parasite fitness in different resource environments, (2) within-host processes; host immune function and energetic reserves either fuel or curtail parasite production, and (3) between-host processes; resource-driven changes in host density and stability regulate epidemiological dynamics. Together, these results illustrate how explicitly accounting for feedbacks between within-host and between-host processes can provide a mechanistic basis for key life-history trade-offs and facilitate a more predictive framework for studying parasite evolution.