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

Autor: Benoit Barrès, Jukka Sirén, Elina Numminen, Anna-Liisa Laine
Přispěvatelé: University of Zurich, Organismal and Evolutionary Biological Research Programme (OEB), Faculty of Biological and Environmental Sciences [Helsinki], University of Helsinki-University of Helsinki, Department of Evolutionary Biology and Environmental Studies, Universität Zürich [Zürich] = University of Zurich (UZH), CAractérisation et Suivi des Phénomènes d'Evolution de Résistance aux pesticides (CASPER), Institut National de la Recherche Agronomique (INRA)-Agence nationale de sécurité sanitaire de l'alimentation, de l'environnement et du travail (ANSES), Helsinki Institute for Information Technology (HIIT), Aalto University-University of Helsinki, European Research Council (ERC)281517Anna-Liisa Laine European Research Council 724508, University of Helsinki, Department of Computer Science, Aalto-yliopisto, Aalto University, Organismal and Evolutionary Biology Research Programme, Research Centre for Ecological Change, Viikki Plant Science Centre (ViPS), Environmental and Ecological Statistics Group
Jazyk: angličtina
Rok vydání: 2019
Předmět:
0106 biological sciences
0301 basic medicine
Evolution of sexual reproduction
Epidemiology
[SDV]Life Sciences [q-bio]
DIVERSITY
RECOMBINATION
Cost of sex
APPROXIMATE BAYESIAN COMPUTATION
01 natural sciences
2400 General Immunology and Microbiology
RED-QUEEN
Biology (General)
Organism
POPULATION
education.field_of_study
Ecology
General Neuroscience
Podosphaera plantaginis
2800 General Neuroscience
General Medicine
Overwintering
1181 Ecology
evolutionary biology

Host-Pathogen Interactions
590 Animals (Zoology)
Medicine
SEX
epidemiology
COINFECTION
Research Article
QH301-705.5
Neuroscience(all)
Science
Population
outcrossing
Metapopulation
Outcrossing
Genetics and Molecular Biology
Biology
010603 evolutionary biology
General Biochemistry
Genetics and Molecular Biology

03 medical and health sciences
10127 Institute of Evolutionary Biology and Environmental Studies
Ascomycota
1300 General Biochemistry
Genetics and Molecular Biology

Immunology and Microbiology(all)
Plantago lanceolata
Genetic variation
Animals
Parasites
education
Plantago
evolution of sex
Genetic diversity
Evolutionary Biology
General Immunology and Microbiology
Biochemistry
Genetics and Molecular Biology(all)

fungi
Genetic Variation
113 Computer and information sciences
coinfection
Sexual reproduction
030104 developmental biology
MAINTENANCE
Evolutionary biology
General Biochemistry
EVOLUTIONARY
570 Life sciences
biology
Other
RESISTANCE
Zdroj: eLife, Vol 8 (2019)
eLife
eLife, eLife Sciences Publication, 2019, 8, ⟨10.7554/eLife.47091⟩
ISSN: 2050-084X
Popis: 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.
eLife digest The existence of sex – broadly defined as the coming together of genes from different individuals – is one of the big evolutionary puzzles. Reproduction allows an organism to pass on its genes to future generations. However, while asexual and self-fertilizing individuals transmit all of their genes to their offspring, individuals that reproduce through sex transmit only half of their genome. This is considered the cost of sex. Many pathogens reproduce through sex, despite often also being able to reproduce asexually or by self-fertilization. Typically a pre-requisite of sex in pathogens is for at least two different strains to infect the same host. Aside from this limitation, little is known about when, where and why pathogens have sex. It has been tricky to study due to the microscopic size of pathogens and the difficulties of identifying different sexes. Moreover, sexual reproduction may be triggered by environmental cues that are difficult to mimic under controlled experimental conditions. Are there any benefits associated with pathogen sex? To find out, Laine et al. analyzed data collected over the course of four years from thousands of populations of a powdery mildew fungus that infected plants across the Åland islands. This revealed that the opportunities for pathogen sex vary in different locations. Areas where multiple strains of the fungus commonly infect the same plants result in hotspots of new genetic diversity. These mixed populations are also more likely to survive winter. This demonstrates the potential for pathogen sexual reproduction to provide an ecological benefit. Identifying areas and populations where pathogens have sex can help to identify when and where new strains are most likely to emerge. In the future, studies that use similar methods to Laine et al. could help to predict where infections and diseases are highly likely to arise.
Databáze: OpenAIRE