Variable opportunities for outcrossing result in hotspots of novel genetic variation in a pathogen metapopulation

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This work examines the advantages to outcrossing via coinfection in a plant pathogen. It comprises a thorough and complete analysis of the opportunities for outcrossing due to coinfection using an extensive, multi-year field data set from 4000 plant host populations. This study advances our understanding of the benefits of sex in organisms with the most common life-style in nature, and across heterogeneous landscapes (and environmental conditions).

Summary:

The advantages of outcrossing in nature remain one of the biggest questions tackled by evolutionary biologists. Laine and colleagues address this question, in terms of overwintering success, using a phytopathogen which maintains mixed reproductive strategies (outcrossing and asexual reproduction/selfing) on its plant host. They use the powdery mildew fungus Podosphaera plantaginis, which is an obligate pathogen of Plantago lanceolate, to first test how coinfection varies across pathogen populations (coinfection is needed for outcrossing), they then examine whether novel pathogen multilocus genotypes are associated with coinfection (which would indicate outcrossing), and finally whether coinfection affects overwintering success. Using an impressively-sized and natural field study analysing almost 3000 pathogen populations over four sampling years, the authors use Spatial Bayesian models to assess disease dynamics and genotypic diversity data. They find that coinfection is common and spatially variable, that where there are high levels of coinfection there are more novel pathogen MLGs, and that there is a positive effect of coinfection on overwintering success. The authors provide evidence that a pathogen can ecologically benefit from outcrossing, and this result opens the door to more detailed experimental understanding of this phenomenon in the future.

Overall, this manuscript is interesting and timely, and contributes substantially to the debate on the evolution of sex. We have the following suggestions to improve the manuscript.

Essential revisions:

The Introduction would benefit from hypotheses and a mention on why the benefits of sex need exploration in pathogens/parasites. This study provides a very interesting and novel approach to questions surrounding the evolution of sex. What makes parasites similar/different from the free-living species in which the benefits of sex have already been examined? It may be valuable to integrate literature on non-parasite sexual recombination versus selfing and the fitness advantage of that in non-parasite individuals, e.g. in cyclical parthenogenetic invertebrates with resting stages.

Discussion of the results in the context of infections and evolution of sex would bolster the generality and significance of the study. At the moment, the authors undersell their findings in the final paragraph of the Discussion and fail to put them in a bigger context for infectious disease, epidemics, and evolution of sex.