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

Anna-Liisa Laine,Elina Numminen,Jukka P Siren,Benoit Barrès

doi:10.7554/elife.47091

Abstract

Many pathogens possess the capacity for sex through outcrossing, despite being able to reproduce also asexually and/or via selfing. Given that sex is assumed to come at a cost, these mixed reproductive strategies typical of pathogens have remained puzzling. While the ecological and evolutionary benefits of outcrossing are theoretically well-supported, support for such benefits in pathogen populations are still scarce. Here, we analyze the epidemiology and genetic structure of natural populations of an obligate fungal pathogen, Podosphaera plantaginis. We find that the opportunities for outcrossing vary spatially. Populations supporting high levels of coinfection -a prerequisite of sex - result in hotspots of novel genetic diversity. Pathogen populations supporting coinfection also have a higher probability of surviving winter. Jointly our results show that outcrossing has direct epidemiological consequences as well as a major impact on pathogen population genetic diversity, thereby providing evidence of ecological and evolutionary benefits of outcrossing in pathogens.

Highlights

Many pathogens possess the capacity for sex – here defined in its broadest sense as the coming together of genes from different individuals (Lehtonen and Kokko, 2014) – despite being able to reproduce asexually and/or via selfing
We used a SNP genotyping protocol to estimate the number of multilocus genotypes (MLGs) and prevalence of coinfection within pathogen populations (Tollenaere et al, 2012)
We found that coinfection was more likely to be found in larger and more diverse pathogen populations (Significant positive effect of number of MLGs and infection abundance; Table 1)

Summary

Introduction

Many pathogens possess the capacity for sex – here defined in its broadest sense as the coming together of genes from different individuals (Lehtonen and Kokko, 2014) – despite being able to reproduce asexually and/or via selfing. Individuals that undergo sexual reproduction transmit only half their genome per offspring produced in contrast to asexual and selfing individuals (Lehtonen et al, 2012) and understanding the maintenance of sex is one of the fundamental challenges in evolutionary biology. The Red Queen Hypothesis predicts sexual reproduction to be advantageous in the presence of coevolving parasites, as offspring that are genetically different from their parents should have higher fitness than non-sexual offspring (Bell, 1982; Hamilton, 1980; Lively, 2010) In support of this prediction, empirical studies have demonstrated parasite mediated selection to explain the observed distribution of outcrossing in hosts (King et al, 2011; Wilson and Sherman, 2013; Lively, 1987). The empirical evidence for such advantages of sex in parasite populations are still few and conflicting (Gouyon and de Vienne, 2015)

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