Evolution of Pathogen Specialisation in a Host Metapopulation: Joint Effects of Host and Pathogen Dispersal

Abstract

Metapopulation processes are important determinants of epidemiological and evolutionary dynamics in host-pathogen systems, and are therefore central to explaining observed patterns of disease or genetic diversity. In particular, the spatial scale of interactions between pathogens and their hosts is of primary importance because migration rates of one species can affect both spatial and temporal heterogeneity of selection on the other. In this study we developed a stochastic and discrete time simulation model to specifically examine the joint effects of host and pathogen dispersal on the evolution of pathogen specialisation in a spatially explicit metapopulation. We consider a plant-pathogen system in which the host metapopulation is composed of two plant genotypes. The pathogen is dispersed by air-borne spores on the host metapopulation. The pathogen population is characterised by a single life-history trait under selection, the infection efficacy. We found that restricted host dispersal can lead to high amount of pathogen diversity and that the extent of pathogen specialisation varied according to the spatial scale of host-pathogen dispersal. We also discuss the role of population asynchrony in determining pathogen evolutionary outcomes.

A Multiscale Approach to Plant Disease Using the Metacommunity Concept

“…The ephemeral nature observed for many pathogens within host individuals and populations (27) is consistent with predictions of the metapopulation theory (52). This theoretical framework has proven useful for understanding the role of space in epidemiology and disease dynamics, e.g., in host-pathogen interactions (14,26), plant disease resistance (75), evolution of pathogen-host specialization (97), and implications for disease and host conservation (55). Host individuals also have been conceived of as patches, with pathogen transmission among hosts providing another scale at which metapopulation theory has led to novel insights into host-pathogen interactions (e.g., 48,73,84).…”

Mosaics often outperform pyramids: insights from a model comparing strategies for the deployment of plant resistance genes against viruses in agricultural landscapes

“…One of the main reasons for this is that most theoretical studies dealing with resistance durability consider only one susceptible and one resistant cultivar e.g . (van den Bosch & Gilligan, ; Skelsey et al ., ; Fabre et al ., , ; Lo Iacono et al ., ; Papaïx et al ., , ,b), making it impossible to compare strategies deploying more than one resistance gene. We extended the model proposed by Fabre et al .…”

Crop pathogen emergence and evolution in agro‐ecological landscapes

“…Conversely, as the host (respectively, the pathogen) dispersal ability increases severe boom and bust dynamics dominate due to a high level of synchrony among local populations, resulting in maladaptation of the pathogen (respectively, the host) population (Gandon ; Thrall and Burdon ; Papaïx et al. ). Such different patterns of disease and host–pathogen co‐evolutionary dynamics in wild patches are likely to have consequences for further pathogen evolution on the crop and need specific consideration to better predict the emergence of new crop pathogens.…”

“…For example, the ability of the wild host to disperse was fixed but the spatial scale of dispersal of both the host and the pathogen directly influence disease dynamics and plant pathogen co-evolution in the wild metapopulation. Low host and pathogen dispersal abilities imply a high level of asynchrony in disease dynamics among local populations with frequent local extinction and recolonization events and can result in a greater host and pathogen diversity (Thrall and Burdon 2002;Papa€ ıx et al 2014b). Conversely, as the host (respectively, the pathogen) dispersal ability increases severe boom and bust dynamics dominate due to a high level of synchrony among local populations, resulting in maladaptation of the pathogen (respectively, the host) population (Gandon 2002;Thrall and Burdon 2002;Papa€ ıx et al 2014b).…”

“…Low host and pathogen dispersal abilities imply a high level of asynchrony in disease dynamics among local populations with frequent local extinction and recolonization events and can result in a greater host and pathogen diversity (Thrall and Burdon 2002;Papa€ ıx et al 2014b). Conversely, as the host (respectively, the pathogen) dispersal ability increases severe boom and bust dynamics dominate due to a high level of synchrony among local populations, resulting in maladaptation of the pathogen (respectively, the host) population (Gandon 2002;Thrall and Burdon 2002;Papa€ ıx et al 2014b). Such different patterns of disease and host-pathogen co-evolutionary dynamics in wild patches are likely to have consequences for further pathogen evolution on the crop and need specific consideration to better predict the emergence of new crop pathogens.…”