Adaptation of Biotrophic Leaf Pathogens to Fertilization-Mediated Changes in Plant Traits: A Comparison of the Optimization Principle to Invasion Fitness.

One of the conclusions of evolutionary ecology applied to agroecosystem management is that sustainable disease management strategies must be adaptive to overcome the immense adaptive potential of crop pathogens. In this context, knowledge of how pathogens adapt to changes in cultural practices is necessary. In this article we address the issue of the evolutionary response of biotrophic crop pathogens to changes in fertilization practices. For this purpose, we compare predictions of latent period evolution based on three empirical fitness measures (seasonal spore production, within-season exponential growth rate, and area under disease progress curves [AUDPCs]) with predictions based on the concept of invasion fitness from adaptive dynamics. We use pairwise invisibility plots to identify the evolutionarily stable strategies (ESSs) of the pathogen latent period. We find that the ESS latent period is in between the latent periods that maximize the seasonal spore production and the within-season exponential growth rate of the pathogen. The latent periods that maximize the AUDPC are similar to those of the ESS latent periods. The AUDPC may therefore be a critical variable to determine the issue of between-strain competition and shape pathogen evolution.

Does the Latent Period of Leaf Fungal Pathogens Reflect Their Trophic Type? A Meta-Analysis of Biotrophs, Hemibiotrophs, and Necrotrophs.

We performed a meta-analysis to search for a relation between the trophic type and latent period of fungal pathogens. The pathogen incubation period and the level of resistance of the hosts were also investigated. This ecological knowledge would help us to more efficiently regulate crop epidemics for different types of pathogens. We gathered latent period data from 103 studies dealing with 51 fungal pathogens of the three major trophic types (25 biotrophs, 15 hemibiotrophs, and 11 necrotrophs), representing 2,542 mean latent periods. We show that these three trophic types display significantly different latent periods. Necrotrophs exhibited the shortest latent periods (<100 degree-days [DD]), biotrophs had intermediate ones (between 100 and 200 DD), and hemibiotrophs had the longest latent periods (>200 DD). We argue that this relation between trophic type and latent period points to two opposing host exploitation strategies: necrotrophs mount a rapid destructive attack on the host tissue, whereas biotrophs and hemibiotrophs avoid or delay the damaging phase. We query the definition of hemibiotrophic pathogens and discuss whether the length of the latent period is determined by the physiological limits inherent to each trophic type or by the adaptation of pathogens of different trophic types to the contrasting conditions experienced in their interaction with the host.

Crop Fertilization Impacts Epidemics and Optimal Latent Period of Biotrophic Fungal Pathogens.

Crop pathogens are known to rapidly adapt to agricultural practices. Although cultivar resistance breakdown and resistance to pesticides have been broadly studied, little is known about the adaptation of crop pathogens to fertilization regimes and no epidemiological model has addressed that question. However, this is a critical issue for developing sustainable low-input agriculture. In this article, we use a model of life history evolution of biotrophic wheat fungal pathogens in order to understand how they could adapt to changes in fertilization practices. We focus on a single pathogen life history trait, the latent period, which directly determines the amount of resources allocated to growth and reproduction along with the speed of canopy colonization. We implemented three fertilization scenarios, corresponding to major effects of increased nitrogen fertilization on crops: (i) increase in nutrient concentration in leaves, (ii) increase of leaf lifespan, and (iii) increase of leaf number (tillering) and size that leads to a bigger canopy size. For every scenario, we used two different fitness measures to identify putative evolutionary responses of latent period to changes in fertilization level. We observed that annual spore production increases with fertilization, because it results in more resources available to the pathogens. Thus, diminishing the use of fertilizers could reduce biotrophic fungal epidemics. We found a positive relationship between the optimal latent period and fertilization when maximizing total spore production over an entire season. In contrast, we found a negative relationship between the optimal latent period and fertilization when maximizing the within-season exponential growth rate of the pathogen. These contrasting results were consistent over the three tested fertilization scenarios. They suggest that between-strain diversity in the latent period, as has been observed in the field, may be due to diversifying selection in different cultural environments.