Disentangling Environmental and Within‐Host Drivers of Parasite Dynamics in Natural Populations

ABSTRACT

Understanding how parasite communities assemble and persist in the wild requires integrating both spatial and temporal dynamics, especially in systems involving multiple co‐circulating lineages. Using a unique 28‐year dataset of individually monitored great tits ( Parus major ) from five sites in western Switzerland, we investigated the eco‐evolutionary dynamics of haemosporidian parasites ( Plasmodium and Haemoproteus ). We examined (i) spatial and temporal variation in parasite prevalence and lineage composition, (ii) differences in host recovery across lineages, and (iii) within‐host transitions and evidence of competitive interactions. We found significant spatial patterns of prevalence and lineage dominance, not explained by a simple urban–rural gradient, with environmental filtering likely driving local parasite assemblages. While prevalence fluctuated across years, lineage composition remained temporally stable, suggesting long‐term coexistence shaped by site‐specific conditions. Recovery rates, based on whether birds cleared their infection between recaptures, varied across parasite lineages, suggesting lineage‐specific differences in infection persistence. In addition, Plasmodium homonucleophilum (SW2 lineage) frequently replaced other Plasmodium lineages within hosts but was never itself replaced, consistent with a pattern of competitive exclusion. Our results highlight the importance of spatial heterogeneity, local interactions, and lineage‐specific traits in shaping parasite communities over space and time. This study underscores the value of long‐term, individual‐based monitoring to understand natural parasite dynamics and the processes driving multi‐lineage coexistence.