Variable opportunities for outcrossing result in hotspots of novel genetic variation in a pathogen metapopulation
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.
Data availability
All data and scripts used to perform the analyses presented in this paper are available in the git repository at https://github.com/ComputerBlue/FungalSex.git.
Article and author information
Author details
Funding
European Research Council (281517)
- Anna-Liisa Laine
European Research Council (724508)
- Anna-Liisa Laine
Academy of Finland (296686)
- Anna-Liisa Laine
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2019, Laine et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 1,638
- views
-
- 229
- downloads
-
- 11
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Ecology
- Evolutionary Biology
While host phenotypic manipulation by parasites is a widespread phenomenon, whether tumors, which can be likened to parasite entities, can also manipulate their hosts is not known. Theory predicts that this should nevertheless be the case, especially when tumors (neoplasms) are transmissible. We explored this hypothesis in a cnidarian Hydra model system, in which spontaneous tumors can occur in the lab, and lineages in which such neoplastic cells are vertically transmitted (through host budding) have been maintained for over 15 years. Remarkably, the hydras with long-term transmissible tumors show an unexpected increase in the number of their tentacles, allowing for the possibility that these neoplastic cells can manipulate the host. By experimentally transplanting healthy as well as neoplastic tissues derived from both recent and long-term transmissible tumors, we found that only the long-term transmissible tumors were able to trigger the growth of additional tentacles. Also, supernumerary tentacles, by permitting higher foraging efficiency for the host, were associated with an increased budding rate, thereby favoring the vertical transmission of tumors. To our knowledge, this is the first evidence that, like true parasites, transmissible tumors can evolve strategies to manipulate the phenotype of their host.
-
- Ecology
Environmental factors can influence ecological networks, but these effects are poorly understood in the realm of the phylogeny of host-parasitoid interactions. Especially, we lack a comprehensive understanding of the ways that biotic factors, including plant species richness, overall community phylogenetic and functional composition of consumers, and abiotic factors such as microclimate, determine host-parasitoid network structure and host-parasitoid community dynamics. To address this, we leveraged a 5-year dataset of trap-nesting bees and wasps and their parasitoids collected in a highly controlled, large-scale subtropical tree biodiversity experiment. We tested for effects of tree species richness, tree phylogenetic, and functional diversity, and species and phylogenetic composition on species and phylogenetic diversity of both host and parasitoid communities and the composition of their interaction networks. We show that multiple components of tree diversity and canopy cover impacted both, species and phylogenetic composition of hosts and parasitoids. Generally, phylogenetic associations between hosts and parasitoids reflected nonrandomly structured interactions between phylogenetic trees of hosts and parasitoids. Further, host-parasitoid network structure was influenced by tree species richness, tree phylogenetic diversity, and canopy cover. Our study indicates that the composition of higher trophic levels and corresponding interaction networks are determined by plant diversity and canopy cover, especially via trophic links in species-rich ecosystems.