# Coevolution of host resistance and pathogen exploitation in a propagule-mediated infection model

## TL;DR

This study models how host resistance and pathogen strategies coevolve when transmission happens through environmental propagules, showing how survival costs and infection pressure shape evolutionary outcomes.

## Contribution

A novel population-level model using adaptive dynamics to explore coevolution of host resistance and pathogen exploitation in environmentally transmitted infections.

## Key findings

- Maximal host resistance evolves at intermediate infection pressures due to survival costs.
- Coevolution can lead to evolutionary branching, resulting in coexistence of host strains with different resistance levels.
- Coevolution affects free pathogen propagule density, either amplifying or suppressing infection depending on transmission and mortality parameters.

## Abstract

Host populations often face infection risk from pathogens that can persist in the environment as free-living propagules. We develop a population-level model to understand how host resistance - defined as reduced susceptibility to infection - evolves in response to the exploitation strategy of a pathogen where transmission occurs exclusively via environmental propagules. Using an adaptive dynamics framework, we analyze how the coevolution of host resistance and pathogen exploitation strategy unfolds under the following fitness costs: reduced survival associated with investment in resistance reflected by additional background mortality for the host; and reduced average lifespan represented by increased infected host mortality for the pathogen. Calculating individual host and pathogen invasion fitness expressions using standard invasion analysis, we track how stable levels of investment in host resistance vary across different infection scenarios. We found that costly resistance is disfavoured when pathogen encounters are excessively high, with maximal resistance selected at intermediate levels of transmission. Coevolutionary feedbacks between host resistance and pathogen exploitation can lead to diverse outcomes, including stable evolutionarily singular strategies and, under weakly accelerating costs, evolutionary branching that generates coexistence in the resistance trait. We further quantify how coevolution shapes the equilibrium density of free propagules, revealing conditions under which coevolution suppresses or amplifies pathogen prevalence in comparison to non-evolving scenarios. Overall, our model framework built on survival-based costs offers testable predictions for environmentally transmitted host-pathogen systems.

Hosts generally acquire infection in two primary ways: by coming into contact with their infected counterparts or by encountering free pathogen propagules in the environment. In this study, we developed a population-level model based on a host-pathogen system in which the pathogen can exist both within infected hosts and as free propagules, but transmission occurs exclusively through environmental propagules. We explore how hosts evolve resistance in response to exploitation strategies of the pathogen under the following trade-offs: resistant hosts experience reduced survival, while highly exploitative pathogens shorten the lifespan of their infected hosts. Our analysis reveals that maximal host resistance will evolve at intermediate infection pressures, reflecting a balance between the benefits of avoiding infection and the fitness costs paid as reduced survival. Furthermore, resistance is minimized at conditions reflecting lower population densities, i.e., when mortality rates of susceptible hosts, infected hosts, or free pathogen propagules are heightened. Under certain trade-off shapes, diversification in resistance traits can occur, leading to coexistence of host strains with distinct resistance levels. We also demonstrate the effect of coevolution on the density of free pathogens in the environment, leading to amplified or suppressed levels of infection depending upon varying transmission and mortality parameters. Overall, this work provides a general framework for understanding host-pathogen coevolution in environmentally transmitted systems such as Daphnia magna-Pasteuria ramosa and amphibian chytridiomycosis caused by fungal pathogen Batrachochytrium dendrobatidis, as well as other diseases involving free-living infectious stages, offering useful eco-evolutionary insights.