Theory predicts that virulence evolves as a consequence of selection to optimize transmission, generating a trade-off in which increased exploitation enhances transmission but shortens the infectious period. Despite its central role in evolutionary epidemiology, empirical support for this virulence-transmission trade-off remains limited, has focused largely on microparasites, and often overlooks variation in host immunity which can fundamentally alter links between virulence and transmission. Here, we provide a rare empirical test of virulence-transmission dynamics in a macroparasite with a complex life cycle. Using a field survey of the helminth parasite, Schistocephalus solidus, and its second intermediate host, threespine stickleback (Gasterosteus aculeatus), we quantify how host immune variation shapes relationships among parasite burden (a proxy for virulence) and transmission potential to definitive hosts, piscivorous birds. Importantly, host populations in the focal lakes span a gradient of evolved immune strategies, from low to high fibrosis, a strong anti-growth resistance mechanism. We find that variation in immune timing across host populations constrains the window in which parasites can reach transmissible stages. Subsequent changes in parasite burden scale up to alter transmission potential and reveal a nonlinear relationship consistent with a virulence-transmission trade-off. Transmission potential is highest at intermediate parasite burdens, which also corresponds to intermediate immune responses. Together, this work links within-host processes to population-level epidemiological outcomes and demonstrates how host immune variation can shape virulence-transmission relationships. Incorporating immune heterogeneity may therefore help reconcile the mixed empirical support for trade-off theory.
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