Local demographic and epidemiological patterns in the Linum marginale–Melampsora lini association: a multi‐year study

Abstract

Summary Many theoretical and empirical studies operate from an assumption that pathogens have a significant influence on the fecundity and life span of their host species. However, there are surprisingly little data investigating the long‐term fitness impacts and genetic consequences that arise from pathogen infection in natural populations. Here, we address this gap through the analysis of a dataset investigating the local population dynamics of a native host plant (Linum marginale) and an associated rust pathogen (Melampsora lini) across 12 years. To investigate patterns of disease prevalence and severity and track effects on host fecundity and demography, we conducted censuses on an annual basis at a single site. Annual M. lini infection prevalence ranged from 0% to 99%. Severe epidemics occurred in 3‐ to 4‐year cycles causing high overwintering mortality and subsequent changes in the relative abundance of different host phenotypes. Host population size oscillated in response to epidemics and declined towards the end of the observation period. Changes in host numbers were found to affect disease severity but not infection prevalence. Melampsora lini infection increased L. marginale fecundity; the infected plants produced threefold more seed capsules on average than uninfected plants (13·3 vs. 4·3 seed capsules per plant). To investigate how variation in environmental conditions affects epidemiology and host demography, we identified climatic factors affecting host growth, overwintering and disease severity. Winter (June) rainfall increased host overwintering success and summer (December) rainfall favoured host growth. The progress of M. lini disease epidemics benefited from optimal temperatures in February and suffered from rainfall in January. We further examined links between the genetic structure of the pathogen population and disease dynamics. There was a positive correlation between mean pathogen infectivity (as measured across a host differential set) and the severity of disease epidemics. Synthesis. Our results provide new insights into local drivers and consequences of pathogen epidemiology in natural populations. Melampsora lini infection can have profound consequences on the phenotype, demography and population structure of Linum marginale by increasing host fecundity, overwinter mortality and disease resistance.