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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Variable opportunities for outcrossing result in hotspots of novel genetic variation in a pathogen metapopulation</title><author><name sortKey="Laine, Anna Liisa" sort="Laine, Anna Liisa" uniqKey="Laine A" first="Anna-Liisa" last="Laine">Anna-Liisa Laine</name><affiliation><nlm:aff id="aff1"><institution content-type="dept">Research Centre for Ecological Change, Organismal and Evolutionary Biology</institution><institution>University of Helsinki</institution><addr-line>Helsinki</addr-line><country>Finland</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff2"><institution content-type="dept">Department of Evolutionary Biology and Environmental Studies</institution><institution>University of Zurich</institution><addr-line>Winterthurerstrasse</addr-line><country>Switzerland</country></nlm:aff></affiliation></author><author><name sortKey="Barres, Benoit" sort="Barres, Benoit" uniqKey="Barres B" first="Benoit" last="Barrès">Benoit Barrès</name><affiliation><nlm:aff id="aff1"><institution content-type="dept">Research Centre for Ecological Change, Organismal and Evolutionary Biology</institution><institution>University of Helsinki</institution><addr-line>Helsinki</addr-line><country>Finland</country></nlm:aff></affiliation></author><author><name sortKey="Numminen, Elina" sort="Numminen, Elina" uniqKey="Numminen E" first="Elina" last="Numminen">Elina Numminen</name><affiliation><nlm:aff id="aff1"><institution content-type="dept">Research Centre for Ecological Change, Organismal and Evolutionary Biology</institution><institution>University of Helsinki</institution><addr-line>Helsinki</addr-line><country>Finland</country></nlm:aff></affiliation></author><author><name sortKey="Siren, Jukka P" sort="Siren, Jukka P" uniqKey="Siren J" first="Jukka P" last="Siren">Jukka P. Siren</name><affiliation><nlm:aff id="aff1"><institution content-type="dept">Research Centre for Ecological Change, Organismal and Evolutionary Biology</institution><institution>University of Helsinki</institution><addr-line>Helsinki</addr-line><country>Finland</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff3"><institution content-type="dept">Helsinki Institute for Information Technology, Department of Computer Science</institution><institution>Aalto University</institution><addr-line>Espoo</addr-line><country>Finland</country></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">31210640</idno><idno type="pmc">6667214</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6667214</idno><idno type="RBID">PMC:6667214</idno><idno type="doi">10.7554/eLife.47091</idno><date when="????">????</date><idno type="wicri:Area/Pmc/Corpus">000B53</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000B53</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Variable opportunities for outcrossing result in hotspots of novel genetic variation in a pathogen metapopulation</title><author><name sortKey="Laine, Anna Liisa" sort="Laine, Anna Liisa" uniqKey="Laine A" first="Anna-Liisa" last="Laine">Anna-Liisa Laine</name><affiliation><nlm:aff id="aff1"><institution content-type="dept">Research Centre for Ecological Change, Organismal and Evolutionary Biology</institution><institution>University of Helsinki</institution><addr-line>Helsinki</addr-line><country>Finland</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff2"><institution content-type="dept">Department of Evolutionary Biology and Environmental Studies</institution><institution>University of Zurich</institution><addr-line>Winterthurerstrasse</addr-line><country>Switzerland</country></nlm:aff></affiliation></author><author><name sortKey="Barres, Benoit" sort="Barres, Benoit" uniqKey="Barres B" first="Benoit" last="Barrès">Benoit Barrès</name><affiliation><nlm:aff id="aff1"><institution content-type="dept">Research Centre for Ecological Change, Organismal and Evolutionary Biology</institution><institution>University of Helsinki</institution><addr-line>Helsinki</addr-line><country>Finland</country></nlm:aff></affiliation></author><author><name sortKey="Numminen, Elina" sort="Numminen, Elina" uniqKey="Numminen E" first="Elina" last="Numminen">Elina Numminen</name><affiliation><nlm:aff id="aff1"><institution content-type="dept">Research Centre for Ecological Change, Organismal and Evolutionary Biology</institution><institution>University of Helsinki</institution><addr-line>Helsinki</addr-line><country>Finland</country></nlm:aff></affiliation></author><author><name sortKey="Siren, Jukka P" sort="Siren, Jukka P" uniqKey="Siren J" first="Jukka P" last="Siren">Jukka P. Siren</name><affiliation><nlm:aff id="aff1"><institution content-type="dept">Research Centre for Ecological Change, Organismal and Evolutionary Biology</institution><institution>University of Helsinki</institution><addr-line>Helsinki</addr-line><country>Finland</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff3"><institution content-type="dept">Helsinki Institute for Information Technology, Department of Computer Science</institution><institution>Aalto University</institution><addr-line>Espoo</addr-line><country>Finland</country></nlm:aff></affiliation></author></analytic><series><title level="j">eLife</title><idno type="eISSN">2050-084X</idno><imprint><date when="????">????</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>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, <italic>Podosphaera plantaginis</italic>. 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.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Barrett, Lg" uniqKey="Barrett L">LG Barrett</name></author><author><name sortKey="Thrall, Ph" uniqKey="Thrall P">PH Thrall</name></author><author><name sortKey="Burdon, Jj" uniqKey="Burdon J">JJ Burdon</name></author><author><name sortKey="Nicotra, Ab" uniqKey="Nicotra A">AB Nicotra</name></author><author><name sortKey="Linde, Cc" uniqKey="Linde C">CC Linde</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Beaumont, Ma" uniqKey="Beaumont M">MA Beaumont</name></author><author><name sortKey="Zhang, W" uniqKey="Zhang W">W Zhang</name></author><author><name sortKey="Balding, Dj" uniqKey="Balding D">DJ 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<front><journal-meta><journal-id journal-id-type="nlm-ta">eLife</journal-id><journal-id journal-id-type="iso-abbrev">Elife</journal-id><journal-id journal-id-type="publisher-id">eLife</journal-id><journal-title-group><journal-title>eLife</journal-title></journal-title-group><issn pub-type="epub">2050-084X</issn><publisher><publisher-name>eLife Sciences Publications, Ltd</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">31210640</article-id><article-id pub-id-type="pmc">6667214</article-id><article-id pub-id-type="publisher-id">47091</article-id><article-id pub-id-type="doi">10.7554/eLife.47091</article-id><article-categories><subj-group subj-group-type="display-channel"><subject>Research Article</subject></subj-group><subj-group subj-group-type="heading"><subject>Ecology</subject></subj-group><subj-group subj-group-type="heading"><subject>Evolutionary Biology</subject></subj-group></article-categories><title-group><article-title>Variable opportunities for outcrossing result in hotspots of novel genetic variation in a pathogen metapopulation</article-title></title-group><contrib-group><contrib id="author-135637" contrib-type="author" corresp="yes"><name><surname>Laine</surname><given-names>Anna-Liisa</given-names></name><contrib-id authenticated="true" contrib-id-type="orcid">https://orcid.org/0000-0002-0703-5850</contrib-id><email>anna-liisa.laine@ieu.uzh.ch</email><xref ref-type="aff" rid="aff1">1</xref><xref ref-type="aff" rid="aff2">2</xref><xref ref-type="other" rid="fund1"></xref><xref ref-type="other" rid="fund2"></xref><xref ref-type="other" rid="fund3"></xref><xref ref-type="fn" rid="con1"></xref><xref ref-type="fn" rid="conf1"></xref></contrib><contrib id="author-137252" contrib-type="author"><name><surname>Barrès</surname><given-names>Benoit</given-names></name><contrib-id authenticated="true" contrib-id-type="orcid">https://orcid.org/0000-0002-6777-0275</contrib-id><xref ref-type="aff" rid="aff1">1</xref><xref ref-type="fn" rid="con2"></xref><xref ref-type="fn" rid="conf1"></xref><xref ref-type="author-notes" rid="pa1">†</xref></contrib><contrib id="author-137251" contrib-type="author"><name><surname>Numminen</surname><given-names>Elina</given-names></name><xref ref-type="aff" rid="aff1">1</xref><xref ref-type="fn" rid="con3"></xref><xref ref-type="fn" rid="conf1"></xref></contrib><contrib id="author-137253" contrib-type="author"><name><surname>Siren</surname><given-names>Jukka P</given-names></name><xref ref-type="aff" rid="aff1">1</xref><xref ref-type="aff" rid="aff3">3</xref><xref ref-type="fn" rid="con4"></xref><xref ref-type="fn" rid="conf1"></xref></contrib><aff id="aff1"><label>1</label><institution content-type="dept">Research Centre for Ecological Change, Organismal and Evolutionary Biology</institution><institution>University of Helsinki</institution><addr-line>Helsinki</addr-line><country>Finland</country></aff><aff id="aff2"><label>2</label><institution content-type="dept">Department of Evolutionary Biology and Environmental Studies</institution><institution>University of Zurich</institution><addr-line>Winterthurerstrasse</addr-line><country>Switzerland</country></aff><aff id="aff3"><label>3</label><institution content-type="dept">Helsinki Institute for Information Technology, Department of Computer Science</institution><institution>Aalto University</institution><addr-line>Espoo</addr-line><country>Finland</country></aff></contrib-group><contrib-group><contrib contrib-type="editor"><name><surname>King</surname><given-names>Kayla</given-names></name><role>Reviewing Editor</role><aff><institution>University of Oxford</institution><country>United Kingdom</country></aff></contrib><contrib contrib-type="editor"><name><surname>Weigel</surname><given-names>Detlef</given-names></name><role>Senior Editor</role><aff><institution>Max Planck Institute for Developmental Biology</institution><country>Germany</country></aff></contrib></contrib-group><author-notes><fn fn-type="present-address" id="pa1"><label>†</label><p>Université de Lyon, Anses, INRA, USC CASPER, Lyon, France.</p></fn></author-notes><pub-date date-type="pub" publication-format="electronic"><day>18</day><month>6</month><year>2019</year></pub-date><pub-date pub-type="collection"><year>2019</year></pub-date><volume>8</volume><elocation-id>e47091</elocation-id><history><date date-type="received" iso-8601-date="2019-03-22"><day>22</day><month>3</month><year>2019</year></date><date date-type="accepted" iso-8601-date="2019-06-18"><day>18</day><month>6</month><year>2019</year></date></history><permissions><copyright-statement>© 2019, Laine et al</copyright-statement><copyright-year>2019</copyright-year><copyright-holder>Laine et al</copyright-holder><ali:free_to_read></ali:free_to_read><license xlink:href="http://creativecommons.org/licenses/by/4.0/"><ali:license_ref>http://creativecommons.org/licenses/by/4.0/</ali:license_ref><license-p>This article is distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>, which permits unrestricted use and redistribution provided that the original author and source are credited.</license-p></license></permissions><self-uri content-type="pdf" xlink:href="elife-47091.pdf"></self-uri><related-article related-article-type="commentary" id="d35e206" ext-link-type="doi" xlink:href="10.7554/eLife.49615"></related-article><abstract><p>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, <italic>Podosphaera plantaginis</italic>. 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.</p></abstract><abstract abstract-type="executive-summary"><title>eLife digest</title><p>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.</p><p>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.</p><p>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.</p><p>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.</p></abstract><kwd-group kwd-group-type="author-keywords"><kwd>evolution of sex</kwd><kwd>outcrossing</kwd><kwd>epidemiology</kwd><kwd><italic>Plantago lanceolata</italic></kwd><kwd><italic>Podosphaera plantaginis</italic></kwd><kwd>coinfection</kwd></kwd-group><kwd-group kwd-group-type="research-organism"><title>Research organism</title><kwd>Other</kwd></kwd-group><funding-group><award-group id="fund1"><funding-source><institution-wrap><institution-id institution-id-type="FundRef">http://dx.doi.org/10.13039/501100000781</institution-id><institution>European Research Council</institution></institution-wrap></funding-source><award-id>281517</award-id><principal-award-recipient><name><surname>Laine</surname><given-names>Anna-Liisa</given-names></name></principal-award-recipient></award-group><award-group id="fund2"><funding-source><institution-wrap><institution-id institution-id-type="FundRef">http://dx.doi.org/10.13039/501100000781</institution-id><institution>European Research Council</institution></institution-wrap></funding-source><award-id>724508</award-id><principal-award-recipient><name><surname>Laine</surname><given-names>Anna-Liisa</given-names></name></principal-award-recipient></award-group><award-group id="fund3"><funding-source><institution-wrap><institution-id institution-id-type="FundRef">http://dx.doi.org/10.13039/501100002341</institution-id><institution>Academy of Finland</institution></institution-wrap></funding-source><award-id>296686</award-id><principal-award-recipient><name><surname>Laine</surname><given-names>Anna-Liisa</given-names></name></principal-award-recipient></award-group><funding-statement>The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.</funding-statement></funding-group><custom-meta-group><custom-meta specific-use="meta-only"><meta-name>Author impact statement</meta-name><meta-value>In natural pathogen populations opportunities for sexual outcrossing vary, leading to spatial variation in genetic diversity and between-season survival.</meta-value></custom-meta></custom-meta-group></article-meta></front><body><sec sec-type="intro" id="s1"><title>Introduction</title><p>Many pathogens possess the capacity for sex – here defined in its broadest sense as the coming together of genes from different individuals (<xref rid="bib28" ref-type="bibr">Lehtonen and Kokko, 2014</xref>) – despite being able to reproduce also 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 (<xref rid="bib27" ref-type="bibr">Lehtonen et al., 2012</xref>) and hence, understanding the maintenance of sex is one of the fundamental challenges in evolutionary biology. To counteract this two-fold cost of sex, sexual outcrossing is assumed to provide both ecological and evolutionary advantages (<xref rid="bib34" ref-type="bibr">Otto, 2009</xref>). 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 (<xref rid="bib4" ref-type="bibr">Bell, 1982</xref>; <xref rid="bib16" ref-type="bibr">Hamilton, 1980</xref>; <xref rid="bib32" ref-type="bibr">Lively, 2010</xref>). In support of this prediction, empirical studies have demonstrated parasite mediated selection to explain the observed distribution of outcrossing in hosts (<xref rid="bib22" ref-type="bibr">King et al., 2011</xref>; <xref rid="bib53" ref-type="bibr">Wilson and Sherman, 2013</xref>; <xref rid="bib31" ref-type="bibr">Lively, 1987</xref>). Just as sexual reproduction is expected to be selected for in hosts to evade parasitism, parasites should equally be under selection to generate novel genetic variation to infect their ever-changing host populations. Indeed, theoretically it has been possible to identify a parameter space where coevolution with the host favors sexual reproduction in the parasite (<xref rid="bib18" ref-type="bibr">Howard and Lively, 2002</xref>; <xref rid="bib12" ref-type="bibr">Galvani et al., 2003</xref>; <xref rid="bib39" ref-type="bibr">Salathé et al., 2008</xref>). However, the empirical evidence for such advantages of sex in parasite populations are still few and conflicting (<xref rid="bib14" ref-type="bibr">Gouyon and de Vienne, 2015</xref>).</p><p>Sexual reproduction may also confer ecological advantages by bridging unfavorable seasons or habitats. In free-living facultatively sexual organisms that alternate between asexual and sexual reproduction, the sexual offspring are often the dormant or dispersing life stages (<xref rid="bib43" ref-type="bibr">Stelzer and Lehtonen, 2016</xref>; <xref rid="bib42" ref-type="bibr">Simon et al., 2002</xref>). Similarly, in some of the most devastating fungal pathogens of crops, the spores that are produced via outcrossing are also those that are suitable for long-distance dispersal (<xref rid="bib38" ref-type="bibr">Rieux et al., 2014</xref>), or provide means of surviving unfavorable environmental conditions (<xref rid="bib6" ref-type="bibr">Billiard et al., 2012</xref>; <xref rid="bib7" ref-type="bibr">Burt, 2000</xref>; <xref rid="bib40" ref-type="bibr">Saleh et al., 2012</xref>). While sexual offspring do not contribute to current local population growth, the ability to outcross may be a key determinant of both the numeric and genetic composition of the next season’s epidemic (<xref rid="bib36" ref-type="bibr">Penczykowski et al., 2015</xref>; <xref rid="bib47" ref-type="bibr">Tack and Laine, 2014</xref>). For such strategies where outscrossing is timed with low potential asexual growth, for example due to seasonality, the cost of sex is expected to be reduced (<xref rid="bib13" ref-type="bibr">Gerber et al., 2018</xref>). Homothallic species, where a haploid individual may mate with other haploid individuals of its species, as well as with itself, may be considered a special case of facultative outcrossing. Here, the maintenance of outcrossing is particularly puzzling given that the offspring produced via haploid selfing are expected to yield the same ecological functions as those produced by outcrossing. Nonetheless, there is evidence of high rates of outcrossing in homothallic species (<xref rid="bib6" ref-type="bibr">Billiard et al., 2012</xref>). To date the relevance of these short-term ecological processes in favoring selfing vs. outcrossing in pathogens populations has remained largely unknown.</p><p>Even when outcrossing is expected to provide short- or long-term advantages, maintenance of selfing may be favored when mate availability is spatially and/or temporally variable (<xref rid="bib19" ref-type="bibr">Jarne and Charlesworth, 1993</xref>). For many pathogens, coinfection is the ecological prerequisite of sexual recombination, as outcrossing and hybridization take place during active infection of the same host individual by different strains (<xref rid="bib11" ref-type="bibr">Froissart et al., 2005</xref>). With molecular tools becoming increasingly available for pathogens, we are beginning to unravel the spatio-temporal distribution of coinfection as well as the ecological outcomes, which may range from facilitation to competition (<xref rid="bib49" ref-type="bibr">Tollenaere et al., 2016</xref>). Although coinfections have been widely reported for different pathogens, remarkably little is understood of the determinants of coinfection (<xref rid="bib49" ref-type="bibr">Tollenaere et al., 2016</xref>). Identifying factors that increase the probability of coinfection also shed light on where we expect to see outcrossing in pathogens with mixed mating strategies.</p><p>Mixed reproductive strategies have been described for a wide range of pathogen species (<xref rid="bib6" ref-type="bibr">Billiard et al., 2012</xref>; <xref rid="bib5" ref-type="bibr">Billiard et al., 2011</xref>). However, the sexual stage is methodologically notoriously difficult to study in many pathogens given their microscopic size and the fact that mating types cannot be identified morphologically. Moreover, sexual reproduction may take place inside the host, and may be triggered by specific environmental cues that are difficult to mimic under controlled experimental conditions (<xref rid="bib6" ref-type="bibr">Billiard et al., 2012</xref>; <xref rid="bib47" ref-type="bibr">Tack and Laine, 2014</xref>). Hence, remarkably little is understood of this critical life-history stage. To understand why outcrossing is broadly maintained in pathogens despite the costs, here we investigate the ecological and genetic consequences of putative outcrossing in a large natural pathogen metapopulation. Our analysis is based on data collected from <italic>Podosphaera plantaginis</italic>, a specialist powdery mildew fungus naturally infecting <italic>Plantago lanceolata</italic>. The visually conspicuous symptoms caused by <italic>P. plantaginis</italic> enable accurate tracking of infection in the wild. Long-term epidemiological data across approximately 4000 local plant populations in the Åland Islands, southwest of Finland, have demonstrated this pathogen to persist as a highly dynamic metapopulation with frequent extinctions and (re)colonizations of local populations (<xref rid="bib21" ref-type="bibr">Jousimo et al., 2014</xref>). Overwinter survival of local pathogen populations has proven to be the vulnerable life-history stage of <italic>P. plantaginis</italic> in Åland with a high fraction of the local pathogen populations going extinct (<xref rid="bib21" ref-type="bibr">Jousimo et al., 2014</xref>). The pathogen survives the winter in resting structures, chasmothecia (<xref rid="bib47" ref-type="bibr">Tack and Laine, 2014</xref>). These resting structures are produced through sexual reproduction as the hyphal cells of one (selfing) or two strains (outcrossing) fuse when infecting the same host plant. The resulting diploid zygote undergoes meiotic division to yield haploid ascospores that develop inside the chasmothecium. At the onset of the growing season these chasmothecia rupture, releasing the ascopores that initiate new infections (<xref rid="bib50" ref-type="bibr">Tollenaere and Laine, 2013</xref>). Here, we (i) determine how coinfection - the pre-requisite for sexual outcrossing - varies in natural pathogen populations. We then measure whether (ii) putative outcrossing (<italic>i.e.</italic> coinfection) is associated with the generation of novel pathogen multilocus genotypes, and (iii) increased pathogen population overwintering success (<xref rid="bib21" ref-type="bibr">Jousimo et al., 2014</xref>). We’ve surveyed and sampled all found pathogen populations in the Åland Islands for four consecutive years, and we use Spatial Bayesian models (Integrated Nested Laplace Approximation; INLA; <xref rid="bib30" ref-type="bibr">Lindgren and Rue, 2015</xref>) to analyse data on disease dynamics and genotypic diversity from the natural metapopulation.</p></sec><sec sec-type="results" id="s2"><title>Results</title><p>We first quantify how the opportunities for sexual outcrossing – thta is coinfection - vary across hundreds of wild pathogen populations in four consecutive seasons. We sampled 619, 703, 693 and 833 populations in 2012–15 for subsequent genotyping (Table S1). We used a SNP genotyping protocol to estimate the number of multilocus genotypes (MLGs) and prevalence of coinfection within pathogen populations (<xref rid="bib48" ref-type="bibr">Tollenaere et al., 2012</xref>). Coinfection proved to be common yet spatially variable across the <italic>P. plantaginis</italic> metapopulation (<xref ref-type="fig" rid="fig1">Figure 1A</xref>) (<xref rid="bib44" ref-type="bibr">Susi et al., 2015</xref>). In all years approximately half of the pathogen populations supported at least one coinfected sample, (45–58%; <xref ref-type="supplementary-material" rid="supp1">Supplementary file 1</xref>). 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; <xref rid="table1" ref-type="table">Table 1</xref>). Connectivity of pathogen populations, which is considered a proxy for gene flow among populations as it is estimated from distances separating local pathogen populations (<xref rid="bib21" ref-type="bibr">Jousimo et al., 2014</xref>), had a positive, albeit not significant, effect on the probability of coinfection (<xref rid="table1" ref-type="table">Table 1</xref>). The INLA model we use here, controls for spatio-temporal autocorrelation characteristic of spatial ecological data due to unmeasured variables, thereby providing a conservative estimate of the model parameters as evidenced by model validation checks (<xref ref-type="fig" rid="fig1s1">Figure 1—figure supplements 1</xref>–<xref ref-type="fig" rid="fig1s5">5</xref>) (<xref rid="bib30" ref-type="bibr">Lindgren and Rue, 2015</xref>).</p><fig id="fig1" position="float" orientation="portrait"><object-id pub-id-type="doi">10.7554/eLife.47091.003</object-id><label>Figure 1.</label><caption><title>Hotspots for pathogen outcrossing - Novel pathogen genotypes emerge in populations with high prevalence of coinfection the previous year.</title><p>The heatplots for the spatial occurrence probability of coinfection in 2012–14 (A-C, respectively), and probability of a novel MLG emerging in pathogen populations in 2013–15 (D-F, respectively), were obtained by fitting spatial intercept-only models as presented in <xref rid="table1" ref-type="table">Table 1</xref>. The probabilities of events for each location were obtained from the linear predictor based on the estimated intercept and the spatial random field. Warmer tones correspond to areas of higher event occurrence probabilities. The number of genotyped samples supporting coinfection in a pathogen population correlated positively with the probability of detecting a MLG that had not been previously detected in that population using all data collected in 2012–15 (<bold>G</bold>). The fitted line corresponds to the 95% confidence level interval generated by the linear model in <xref rid="table1" ref-type="table">Table 1</xref>. Darker shades indicate higher data density.</p></caption><graphic xlink:href="elife-47091-fig1"></graphic><p content-type="supplemental-figure"><fig id="fig1s1" specific-use="child-fig" orientation="portrait" position="anchor"><object-id pub-id-type="doi">10.7554/eLife.47091.004</object-id><label>Figure 1—figure supplement 1.</label><caption><title>The estimated posterior distributions of the spatial ranges for the fitted spatio-temporal models described in <xref rid="table1" ref-type="table">Table 1</xref>.</title><p>Range corresponds to the distance at which the spatial autocorrelation becomes negligible (smaller than 0.1).</p></caption><graphic xlink:href="elife-47091-fig1-figsupp1"></graphic></fig></p><p content-type="supplemental-figure"><fig id="fig1s2" specific-use="child-fig" orientation="portrait" position="anchor"><object-id pub-id-type="doi">10.7554/eLife.47091.005</object-id><label>Figure 1—figure supplement 2.</label><caption><title>Mesh used for the spatio-temporal model.</title><p>The coastline of the study area is shown in blue. The spatial random field is approximated at the mesh nodes, and these values are then projected into the observation locations.</p></caption><graphic xlink:href="elife-47091-fig1-figsupp2"></graphic></fig></p><p content-type="supplemental-figure"><fig id="fig1s3" specific-use="child-fig" orientation="portrait" position="anchor"><object-id pub-id-type="doi">10.7554/eLife.47091.006</object-id><label>Figure 1—figure supplement 3.</label><caption><title>PIT-value distributions.</title><p>The close-to-uniform distributions of the corrected PIT-value for the coinfection (<bold>A</bold>), new strain emergence (<bold>B</bold>) and overwintering (<bold>C</bold>) indicate adequacy of the models.</p></caption><graphic xlink:href="elife-47091-fig1-figsupp3"></graphic></fig></p><p content-type="supplemental-figure"><fig id="fig1s4" specific-use="child-fig" orientation="portrait" position="anchor"><object-id pub-id-type="doi">10.7554/eLife.47091.007</object-id><label>Figure 1—figure supplement 4.</label><caption><title>CPO-values distributed in space.</title><p>The CPO-values for the three models exhibit no particular spatial patterns, providing a further model validation argument.</p></caption><graphic xlink:href="elife-47091-fig1-figsupp4"></graphic></fig></p><p content-type="supplemental-figure"><fig id="fig1s5" specific-use="child-fig" orientation="portrait" position="anchor"><object-id pub-id-type="doi">10.7554/eLife.47091.008</object-id><label>Figure 1—figure supplement 5.</label><caption><title>Distributions of the CPO-values for the four models for the different years.</title><p>No particular temporal structure is visible indicating the adequacy of the models.</p></caption><graphic xlink:href="elife-47091-fig1-figsupp5"></graphic></fig></p><p content-type="supplemental-figure"><fig id="fig1s6" specific-use="child-fig" orientation="portrait" position="anchor"><object-id pub-id-type="doi">10.7554/eLife.47091.009</object-id><label>Figure 1—figure supplement 6.</label><caption><title>Posterior distributions of the parameter values from the ABC inference on the infections and co-infections.</title><p>Each panel shows the posterior distribution for one parameter and separately for the two years. The posterior distributions for the two years are very similar for most parameters. The biggest difference is for the parameter <inline-formula><mml:math id="inf1"><mml:msub><mml:mrow><mml:mi>α</mml:mi></mml:mrow><mml:mrow><mml:mi>M</mml:mi><mml:mo>,</mml:mo><mml:mn>1</mml:mn></mml:mrow></mml:msub></mml:math></inline-formula>, which controls the average number of mildew strains infecting each patch. This is not unexpected, given the highly dynamic nature of the pathogen metapopulation. The posterior probability that <inline-formula><mml:math id="inf2"><mml:mstyle displaystyle="true" scriptlevel="0"><mml:mrow><mml:mi>γ</mml:mi><mml:mo>></mml:mo><mml:mo>;</mml:mo><mml:mn>0</mml:mn></mml:mrow></mml:mstyle></mml:math></inline-formula> was 0.98 for 2012 and 0.988 for 2013 indicating that coinfections are more common than expected by chance.</p></caption><graphic xlink:href="elife-47091-fig1-figsupp6"></graphic></fig></p><p content-type="supplemental-figure"><fig id="fig1s7" specific-use="child-fig" orientation="portrait" position="anchor"><object-id pub-id-type="doi">10.7554/eLife.47091.010</object-id><label>Figure 1—figure supplement 7.</label><caption><title>Accuracy of the parameter estimates from the ABC analysis of infections and co-infections.</title><p>Each boxplot shows the distribution of relative RMSE values for one parameter for year 2012 evaluated over 100 simulated test data sets with known parameter values. Relative RMSE 1 indicates no improvement over the prior distribution, while a value of 0 indicates perfect estimate. The parameter affecting the incidence of coinfections, <inline-formula><mml:math id="inf3"><mml:mi>γ</mml:mi></mml:math></inline-formula>, is among the best-estimated ones.</p></caption><graphic xlink:href="elife-47091-fig1-figsupp7"></graphic></fig></p><p content-type="supplemental-figure"><fig id="fig1s8" specific-use="child-fig" orientation="portrait" position="anchor"><object-id pub-id-type="doi">10.7554/eLife.47091.011</object-id><label>Figure 1—figure supplement 8.</label><caption><title>Posterior distributions of the parameter values from the ABC inference on the infections and co-infections under different modeling assumptions using data for 2012.</title><p>Each panel shows the posterior distribution for one parameter under four different modeling assumptions. Red line shows the results under the standard assumptions used in other analyses. For the parameter <inline-formula><mml:math id="inf4"><mml:mi>γ</mml:mi></mml:math></inline-formula>, the standard choices produce more conservative (closer to 0) distributions than the others and the probability that <inline-formula><mml:math id="inf5"><mml:mstyle displaystyle="true" scriptlevel="0"><mml:mrow><mml:mi>γ</mml:mi><mml:mo>></mml:mo><mml:mo>;</mml:mo><mml:mn>0</mml:mn></mml:mrow></mml:mstyle></mml:math></inline-formula> is lowest, suggesting that the modeling assumptions have not led to an overestimation of the incidence of coinfections.</p></caption><graphic xlink:href="elife-47091-fig1-figsupp8"></graphic></fig></p><p content-type="supplemental-figure"><fig id="fig1s9" specific-use="child-fig" orientation="portrait" position="anchor"><object-id pub-id-type="doi">10.7554/eLife.47091.012</object-id><label>Figure 1—figure supplement 9.</label><caption><title>The number of samples collected from <italic>Podosphaera plantaginis</italic> populations in 2013–15 depicted according to population size categories.</title><p>Population size categories are’3’ and ‘4’ are merged in this figure.</p></caption><graphic xlink:href="elife-47091-fig1-figsupp9"></graphic></fig></p><p content-type="supplemental-figure"><fig id="fig1s10" specific-use="child-fig" orientation="portrait" position="anchor"><object-id pub-id-type="doi">10.7554/eLife.47091.013</object-id><label>Figure 1—figure supplement 10.</label><caption><title>The global allele frequencies of the 19 SNP loci used for genotyping.</title></caption><graphic xlink:href="elife-47091-fig1-figsupp10"></graphic></fig></p><p content-type="supplemental-figure"><fig id="fig1s11" specific-use="child-fig" orientation="portrait" position="anchor"><object-id pub-id-type="doi">10.7554/eLife.47091.014</object-id><label>Figure 1—figure supplement 11.</label><caption><title>A schematic representation of the algorithm that identifies the unique multilocus genotypes that form the observed coinfections.</title></caption><graphic xlink:href="elife-47091-fig1-figsupp11"></graphic></fig></p></fig><table-wrap id="table1" orientation="portrait" position="float"><object-id pub-id-type="doi">10.7554/eLife.47091.015</object-id><label>Table 1.</label><caption><title>The estimated posterior means and 95% credibility intervals for the parameters of the fitted spatio-temporal models.</title><p>In each model, the abundance of infection category one is considered as the baseline factor level for every model. Whenever the credibility interval does not include zero (denoted with bold), the effect is considered significant. For temporal and spatial range, and the nominal variance, significance cannot be estimated as they can only get positive values. For more information about the predictors, please see the Model Variables-section in the Methods.</p></caption><table frame="hsides" rules="groups"><thead><tr><th valign="top" rowspan="1" colspan="1"></th><th align="center" colspan="3" valign="top" rowspan="1">Model</th></tr></thead><tbody><tr><td valign="top" rowspan="1" colspan="1">Parameter</td><td align="left" valign="top" rowspan="1" colspan="1">Coinfection presence in a pathogen population <break></break>(0/1)</td><td valign="top" rowspan="1" colspan="1">Number of new strains within a population</td><td valign="top" rowspan="1" colspan="1">Successful pathogen population overwintering <break></break>(0/1)</td></tr><tr><td rowspan="1" colspan="1">Intercept</td><td align="left" valign="top" rowspan="1" colspan="1"><bold>−1.04,(−1.16,–0.92)</bold></td><td valign="top" rowspan="1" colspan="1"><bold>−0.38,(−0.49,–0.27)</bold></td><td valign="top" rowspan="1" colspan="1"><bold>1.17, (0.93, 1.41)</bold></td></tr><tr><td rowspan="1" colspan="1">Number of coinfections</td><td align="left" valign="top" rowspan="1" colspan="1"><italic>not fitted</italic></td><td valign="top" rowspan="1" colspan="1"><bold>0.06,</bold><break></break><bold>(0.02, 0.11)</bold></td><td valign="top" rowspan="1" colspan="1"><bold>0.28,(0.11, 0.46)</bold></td></tr><tr><td rowspan="1" colspan="1">Number of strains</td><td align="left" valign="top" rowspan="1" colspan="1"><bold>1.07,</bold><break></break><bold>(0.93, 1.21)</bold></td><td valign="top" rowspan="1" colspan="1"><bold>0.08,</bold><break></break><bold>(0.04, 0.13)</bold></td><td valign="top" rowspan="1" colspan="1"><bold>0.34,(0.18, 0.5)</bold></td></tr><tr><td rowspan="1" colspan="1">Abundance of infection (category 2)</td><td align="left" valign="top" rowspan="1" colspan="1"><bold>0.37,</bold><break></break><bold>(0.22, 0.53)</bold></td><td valign="top" rowspan="1" colspan="1">−0.03, <break></break>(−0.08, 0.02)</td><td valign="top" rowspan="1" colspan="1"><bold>0.39,</bold><break></break><bold>(0.27, 0.51)</bold></td></tr><tr><td rowspan="1" colspan="1">Abundance of infection (category 3)</td><td align="left" valign="top" rowspan="1" colspan="1"><bold>0.61,</bold><break></break><bold>(0.46, 0.75)</bold></td><td valign="top" rowspan="1" colspan="1">−0.04, <break></break>(−0.1, 0.01)</td><td valign="top" rowspan="1" colspan="1"><bold>0.55,</bold><break></break><bold>(0.39, 0.72)</bold></td></tr><tr><td rowspan="1" colspan="1">Year 2013</td><td align="left" valign="top" rowspan="1" colspan="1"><italic>not fitted</italic></td><td valign="top" rowspan="1" colspan="1"><bold>0.17,</bold><break></break><bold>(0.03, 0.32)</bold></td><td valign="top" rowspan="1" colspan="1">0.05, <break></break>(−0.27, 0.37)</td></tr><tr><td rowspan="1" colspan="1">Year 2014</td><td align="left" valign="top" rowspan="1" colspan="1"><italic>not fitted</italic></td><td valign="top" rowspan="1" colspan="1"><bold>1.45,</bold><break></break><bold>(1.33, 1.58)</bold></td><td valign="top" rowspan="1" colspan="1"><bold>0.52,</bold><break></break><bold>(0.19, 0.85)</bold></td></tr><tr><td rowspan="1" colspan="1">Pathogen connectivity (<inline-formula><mml:math id="inf6"><mml:msubsup><mml:mrow><mml:mi>S</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow><mml:mrow><mml:mi>p</mml:mi></mml:mrow></mml:msubsup></mml:math></inline-formula>)</td><td align="left" valign="top" rowspan="1" colspan="1">0.05, <break></break>(−0.08, 0.19)</td><td valign="top" rowspan="1" colspan="1">0.02, <break></break>(−0.02, 0.07)</td><td valign="top" rowspan="1" colspan="1">−0.04, <break></break>(−0.19, 0.1)</td></tr><tr><td rowspan="1" colspan="1">Host population size (logm<sup>2</sup>)</td><td align="left" valign="top" rowspan="1" colspan="1">0.01, <break></break>(−0.12, 0.14)</td><td valign="top" rowspan="1" colspan="1"><bold>0.09,</bold><break></break><bold>(0.04, 0.14)</bold></td><td valign="top" rowspan="1" colspan="1">0.03, <break></break>(−0.1, 0.16)</td></tr><tr><td rowspan="1" colspan="1">Temporal autocorrelation (<inline-formula><mml:math id="inf7"><mml:mi>φ</mml:mi></mml:math></inline-formula>)</td><td align="left" valign="top" rowspan="1" colspan="1">0.03, <break></break>(−0.41, 0.43)</td><td valign="top" rowspan="1" colspan="1">0, <break></break>(−0.41, 0.41)</td><td valign="top" rowspan="1" colspan="1">−0.08, <break></break>(−0.43, 0.28)</td></tr><tr><td rowspan="1" colspan="1">Spatial range (meters)</td><td align="left" valign="top" rowspan="1" colspan="1">11410, <break></break>(460, 50811)</td><td valign="top" rowspan="1" colspan="1">14229, <break></break>(3266, 38058)</td><td valign="top" rowspan="1" colspan="1">8512, <break></break>(1775, 25860) <break></break></td></tr><tr><td rowspan="1" colspan="1"><inline-formula><mml:math id="inf8"><mml:msub><mml:mrow><mml:mi>σ</mml:mi></mml:mrow><mml:mrow><mml:mn>2</mml:mn></mml:mrow></mml:msub><mml:mi></mml:mi><mml:mo>(</mml:mo></mml:math></inline-formula>Nominal variance)</td><td align="left" valign="top" rowspan="1" colspan="1">0.2, <break></break>(0, 1.33)</td><td valign="top" rowspan="1" colspan="1">0.07, <break></break>(0.01, 0.22)</td><td valign="top" rowspan="1" colspan="1">0.45, <break></break>(0.1, 1.28) <break></break></td></tr></tbody></table></table-wrap><p>We then used an Approximate Bayesian Computation (ABC) approach to determine whether we detect more coinfection within populations than would be expected based on the number of parasite genotypes and host availability. Our results show that an already infected plant is more likely to be infected by another strain (<xref ref-type="fig" rid="fig1s6">Figure 1—figure supplement 6</xref>). In other words, coinfections were more common than expected by chance under the assumption that infections by different MLGs are statistically independent. The result was consistent in both years 2012 and 2013 (posterior probability 0.98 and 0.988, respectively; <xref ref-type="fig" rid="fig1s6">Figure 1—figure supplement 6</xref>), with the parameter controlling the prevalence of coinfections, <inline-formula><mml:math id="inf9"><mml:mi>γ</mml:mi><mml:mo>,</mml:mo></mml:math></inline-formula> being reliably estimated under different modeling assumptions (<xref ref-type="fig" rid="fig1s7">Figure 1—figure supplement 7</xref>–<xref ref-type="fig" rid="fig1s8">8</xref>).</p><p>The detection of novel MLGs in the pathogen metapopulation from one year to another suggests that sexual outcrossing is common for this pathogen. When all located pathogen populations were genotyped, we identified 182, 189, and 235 novel MLGs in 2013–2015, respectively, when compared to MLGs detected the previous year (<xref ref-type="supplementary-material" rid="supp1">Supplementary file 1</xref>; <xref ref-type="fig" rid="fig1">Figure 1B</xref>). The number of new MLGs at the population level increased with the prevalence of coinfection at the end of the previous epidemic season which is the time when outcrossing takes place (<xref ref-type="fig" rid="fig1">Figure 1C</xref>; <xref rid="table1" ref-type="table">Table 1</xref>). The prevalence of coinfection was a strong predictor of novel MLGs the following year even after controlling for the effects of local pathogen population size, diversity (number of MLGs), pathogen population connectivity (proxy for gene flow) as well as spatial and temporal autocorrelation (<xref rid="table1" ref-type="table">Table 1</xref>).</p><p>Using data from the natural pathogen metapopulation, we also found that in those pathogen populations where the prevalence of coinfection is high – and hence where sexual reproduction can take place – the pathogen has a higher survival probability (<xref rid="table1" ref-type="table">Table 1</xref>; <xref ref-type="fig" rid="fig2">Figure 2A and B</xref>). The effect of coinfection on successful overwintering is positive even after controlling for the effects of pathogen population size and diversity, which both increase survival probability. The INLA model also controls for spatial and temporal autocorrelation in these data that may be generated by abiotic variation known to be important for overwintering ecology of this pathogen (<xref rid="bib36" ref-type="bibr">Penczykowski et al., 2015</xref>). Hence, we view this as a conservative estimate of the effect of coinfection on overwintering. Resting spores, which were visually scored in the field (<xref rid="bib47" ref-type="bibr">Tack and Laine, 2014</xref>), were produced in nearly all pathogen populations regardless of whether they supported coinfection or not (96% <italic>vs.</italic> 93%, respectively).</p><fig id="fig2" orientation="portrait" position="float"><object-id pub-id-type="doi">10.7554/eLife.47091.016</object-id><label>Figure 2.</label><caption><title>Pathogen overwinter survival was highest in populations that supported higher levels of coinfection.</title><p>The heatplot for the spatial occurrence probabilities of overwinter survival were obtained by merging the corresponding event data from corresponding years and fitting spatial intercept-only models as presented in <xref rid="table1" ref-type="table">Table 1</xref>. The probabilities of events for each location were obtained from the linear predictor based on the estimated intercept and the spatial random field. The maps shows spatial variation in overwinter survival for 2012–13 (<bold>A</bold>), 2013–14 (<bold>B</bold>) and 2014–15 (<bold>C</bold>) with warmer tones corresponding to areas of higher event occurrence probabilities. (<bold>B</bold>) The average probability of successful pathogen population overwintering was higher in populations with coinfection than in populations without coinfection in all three years in 2012–15.</p></caption><graphic xlink:href="elife-47091-fig2"></graphic></fig></sec><sec sec-type="discussion" id="s3"><title>Discussion</title><p>Here, we report compelling evidence of outcrossing that generates novel genetic diversity in the pathogen metapopulation. Our results demonstrate variation in how opportunities for outcrossing are distributed across space. Finding more coinfection than would be expected by chance is in line with previous fine-scale field sampling of infections and experimental work, which show that hosts already infected with one strain of the pathogen are more likely to become infected by another strain of the same pathogen than uninfected hosts (<xref rid="bib24" ref-type="bibr">Laine, 2011</xref>; <xref rid="bib45" ref-type="bibr">Susi and Laine, 2017</xref>). This may be due to already infected individuals becoming more susceptible to subsequent infection, or due to strains aggregating on those hosts that are the most susceptible genotypes (<xref rid="bib45" ref-type="bibr">Susi and Laine, 2017</xref>). Moreover, variation in host density and (micro)climatic conditions may be an important driver of infection patters in the wild (<xref rid="bib37" ref-type="bibr">Penczykowski et al., 2018</xref>). Our results do not support the priming hypothesis (<xref rid="bib17" ref-type="bibr">Hilker et al., 2016</xref>), whereby prior attack provides increased protection against later attack.</p><p>We find that spatial variation in coinfection results in spatially delineated hotspots of novel genetic diversity. The high number of new MLGs detected every year is indicative of outcrossing taking place in this pathogen metapopulation. Although our sampling is likely to miss some rare strains, and novel MLGs may be generated through mutations, these are unlikely to explain the high turnover of MLGs between years we report here. Mainland populations, which are separated by at least 38 km of open water, are also expected to play a negligible role as sources of gene flow given that experimental and field data have confirmed this pathogen to typically disperse short distances (<xref rid="bib21" ref-type="bibr">Jousimo et al., 2014</xref>; <xref rid="bib46" ref-type="bibr">Tack et al., 2014</xref>). Our results suggest that sexual outcrossing takes place where there is the opportunity for it, that is in populations where levels of coinfection are high. To date, this phenomenon has only received limited experimentally derived support in pathogens (<xref rid="bib41" ref-type="bibr">Schelkle et al., 2012</xref>). Spatio-temporal variation in outcrossing is expected to have both evolutionary and epidemiological consequences for the pathogen. In the short term, generation of novel genetic diversity may increase transmission across host populations that support considerable resistance diversity both within and among populations (<xref rid="bib21" ref-type="bibr">Jousimo et al., 2014</xref>; <xref rid="bib25" ref-type="bibr">Laine et al., 2011</xref>). Novel genetic diversity may also increase the evolutionary potential of pathogens that need to adapt to both biotic and abiotic variation in their environment (<xref rid="bib15" ref-type="bibr">Greischar and Koskella, 2007</xref>; <xref rid="bib54" ref-type="bibr">Wolinska and King, 2009</xref>).</p><p>Our multi-year census data further revealed the putative outcrossing to yield a benefit that is realized in an ecologically important function – higher overwintering success. Overwintering determines both the genetic and numeric structure of the next epidemic (<xref rid="bib47" ref-type="bibr">Tack and Laine, 2014</xref>; <xref rid="bib36" ref-type="bibr">Penczykowski et al., 2015</xref>), and hence may be a sufficiently important trait to promote the maintenance of outcrossing in a pathogen that is able to complete its life-cycle also through haploid selfing. Our results suggest that successful overwintering is not due to higher production of resting spores. Hence, there may be a difference in the quality of progeny produced via selfing <italic>vs</italic>. outcrossing. Prior experimental work has demonstrated significant variation in spore viability in the resting structures of <italic>P. plantaginis</italic>. There is evidence of higher viability of progeny from coinfections than from single infections, but the strength and direction of this trend is affected by the genotypes of the interacting strains, as well as by temperature (<xref rid="bib51" ref-type="bibr">Vaumourin and Laine, 2018</xref>). Despite the higher overwintering success of outcrossed progeny, haploid selfing may be preserved due to the low probability of encountering a suitable mating partner infecting the same host. Moreover, there may be a cost to outcrossing as it breaks up locally adapted pathogen populations by producing novel – and potentially maladapted – genetic variation.</p><p>Overall, the selection pressures and opportunities to mate vary considerably across space and time, and hence, it is not surprising that many pathogens have evolved highly complex mating strategies (<xref rid="bib5" ref-type="bibr">Billiard et al., 2011</xref>). A loss of sexual reproduction in pathogens has been linked to homogenous habitat (<xref rid="bib40" ref-type="bibr">Saleh et al., 2012</xref>) or stable environmental conditions (<xref rid="bib1" ref-type="bibr">Barrett et al., 2008</xref>). Maintaining a mixed mating system may provide a bet-hedging strategy for this pathogen to survive in a fragmented landscape, with a high probability of population extinction during the off-season. It is noteworthy that here we succeeded in identifying predictors of how coinfection is spatially distributed - and hence where hotspots of outcrossing are formed - despite the considerable environmental ‘noise’ this natural system supports. The correlations in field collected data we have observed here are a promising start to uncovering the variable selective pressures and advantages of outcrossing in pathogens. Establishing direct links between variation in reproductive strategies and epidemiological dynamics offers an exciting venue of research, and is needed to truly predict where risks of infection and disease emergence are the highest.</p></sec><sec sec-type="materials|methods" id="s4"><title>Materials and methods</title><sec id="s4-1"><title>Survey of natural pathogen metapopulation</title><p><italic>Plantago lanceolata</italic> is a perennial rosette-forming herb that is naturally infected by <italic>Podosphaera plantaginis</italic> (Castagne; U. Braun and S. Takamatsu), a powdery mildew fungus in the order Erysiphales within the Ascomycota. This pathogen is a host-specific obligate biotroph that completes its entire life cycle on the surface of the host plant where it is visible as localized (nonsystemic) white powdery lesions. The interaction between <italic>P. lanceolata</italic> and <italic>P. plantaginis</italic> functions in a two-step manner typical of many plant–pathogen associations. First, as the pathogen attempts to infect a new host, the interaction is strain specific as a given host genotype expresses resistance against some strains (recognition) of the pathogen while being susceptible to others (nonrecognition) (<xref rid="bib20" ref-type="bibr">Jones and Dangl, 2006</xref>). Once a <italic>P. plantaginis</italic> strain has successfully established there is still considerable variation in its development that is affected by both pathogen and host genotype (<xref rid="bib23" ref-type="bibr">Laine, 2007</xref>). The pathogen is a significant stress factor for its host and may cause host mortality (<xref rid="bib36" ref-type="bibr">Penczykowski et al., 2015</xref>).</p><p>The locations of <italic>P. lanceolata</italic> populations have been systematically mapped in the Åland Islands, southwest of Finland, since the 1990s. There are currently <italic>c</italic>. 4000 known host populations that range in size from a few square meters to several hectares, with a median size of 300 m<sup>2</sup> (<xref rid="bib21" ref-type="bibr">Jousimo et al., 2014</xref>). Within host populations, initial pathogen foci are established from resting spores (chasmothecia), or from a spore immigrating into the local population from another population. The first visible signs of infection appear in late June as white-greyish lesions consisting of mycelium supporting spores (conidia) are formed. The spores are dispersed by wind to the same or new host individuals. Some six to eight clonally produced generations (estimated from spore germination-production times observed in the laboratory) follow one another in quick succession, often leading to a substantial proportion of the host individuals within a population being infected by late summer (<xref rid="bib35" ref-type="bibr">Ovaskainen and Laine, 2006</xref>). Resting spores (chasmothecia) appear towards the end of the growing season in August–September. Each chasmothecia contains eight ascospores that can each cause a new infection in the spring upon their release. Infected leaves may support hundreds of chasmothecia. In <italic>P. plantaginis</italic>, chasmothecia production is achieved via both haploid selfing as well as outcrossing between two strains simultaneously infecting the same host plant. Pure strains of <italic>P. plantaginis</italic> have been shown to carry both MAT1-1-1 and MAT1-2-1 that determine compatibility in several other powdery mildew species (<xref rid="bib50" ref-type="bibr">Tollenaere and Laine, 2013</xref>).</p><p>In early September every year since 2001, all known <italic>P. lanceolata</italic> populations have been surveyed for the presence/absence of the powdery mildew (for details on the survey, please see <xref rid="bib21" ref-type="bibr">Jousimo et al., 2014</xref>). These data can be used to identify pathogen populations, which have persisted from one year to the next, newly colonized populations, and populations that have gone extinct. These data have demonstrated that <italic>P. plantaginis</italic> persists as a highly dynamic metapopulation through extinction and (re)colonization of local host populations (<xref rid="bib21" ref-type="bibr">Jousimo et al., 2014</xref>).</p></sec><sec id="s4-2"><title>Genotyping of field collected pathogen samples</title><p>In 2012–15 nearly all located pathogen populations were sampled for genotyping (N = 619, 703, 693, and 833 populations, respectively, which represented 96–97% of all located pathogen populations each year; <xref ref-type="supplementary-material" rid="supp1">Supplementary file 1</xref>). A sample consists of one infected leaf collected from an infected plant, and infected plants were sampled at a minimum distance of five meters between infected plants. The aim was to collect ten samples from each population but in smaller pathogen populations sampling effort needed to be scaled to how much infection was available for sampling (Please see ‘Pathogen population size’ below in Model variables -section below for a description, and for numbers of samples in each pathogen population size category, please see <xref ref-type="fig" rid="fig1s9">Figure 1—figure supplement 9</xref>). The infected leaves were placed in separate falcon tubes and brought back to the laboratory where fungal material for each sample was collected by scraping off the surface of the infected leaf. This material and a 1 cm<sup>2</sup> piece of the same infected leaf were placed in an individual well of a 96-well plate. Samples were stored at −20°C until DNA extraction.</p><p>DNA extraction was performed using E.Z.N.A. Plant DNA kit (Omega Bio Tek Inc, Norcross, GA, USA) at The Institute of Biotechnology (BI, Helsinki, Finland). Samples were genotyped with 27 SNP markers using Sequenom MassARRAY iPLEX platform as described in <xref rid="bib48" ref-type="bibr">Tollenaere et al. (2012)</xref> at the Finnish Institute for Molecular Medicine (FIMM, Helsinki, Finland). Automatic calling of the genotypes was performed using MassARRAY Typer four software (Sequenom, San Diego, CA). Because of the presence of null alleles in the studied populations, eight SNP were discarded from the analysis. Allele frequencies are shown in <xref ref-type="fig" rid="fig1s10">Figure 1—figure supplement 10</xref>. The genotyping results were used to identify the multilocus genotypes (MLGs) of each sample and to detect coinfection in the collected samples. <italic>Podosphaera plantaginis</italic> is haploid, and therefore the detection of a heterozygote genotype for one or more SNP markers is a clear highly repeatable method for calling coinfections (<xref rid="bib48" ref-type="bibr">Tollenaere et al., 2012</xref>; <xref rid="bib44" ref-type="bibr">Susi et al., 2015</xref>).</p></sec><sec id="s4-3"><title>Model variables</title><p>The survey data from the natural populations and the genotyping data from years 2012–15 were used to generate the following variables used in the analyses (See Statistical modeling below):</p><sec id="s4-3-1"><title>Pathogen population size</title><p>The abundance of pathogen was scored on a categorical scale with five levels, defined as: 0 = no infection, 1 = 1–9 infected plants, 2 = 10–99 infected plants, 3 = 100–999 and 4 = 1000 or more. Due to the small number of category four infections, the categories 3 and 4 were merged for the analyses.</p></sec><sec id="s4-3-2"><title>Number of MultiLocus genotypes (MLG) in local pathogen populations and identification of MLGs from coinfected samples</title><p>For each population and year we estimated the number of unique multilocus genotypes (MLG) observed using the SNP genotyping protocol described above. This number was obscured by samples supporting coinfection, for which the MLGs could not be directly identified. To solve this, we developed an algorithm that gives as an output a lower limit for the number of strains in the population, that would correspond to all the observed MLG profiles, both those observed for single and coinfected samples (<xref ref-type="fig" rid="fig1s11">Figure 1—figure supplement 11</xref>). The algorithm was designed to be conservative to avoid overestimating the number of MLGs. To this end, we assumed that in a coinfected sample, the detection of multiple alleles in a locus could have failed, and only one allele observed. The five stages of the algorithm are as follows: First, we identified the unique MLGs from the single infections. Second, we identified coinfections, whose alleles could not be obtained as a combination of two unique MLGs from the first stage. Third, we removed duplicate coinfections, whose alleles were subsets of another coinfection in the loci that the samples shared. We considered subsets to accommodate possible genotyping errors for the coinfections, where only one allele is detected for a loci. Fourth, for each remaining coinfection, we constructed a new minimal candidate MLG, which was needed in addition to a unique MLG identified from single infections to generate the alleles in the coinfection. Only those loci where an allele not present in the single infection was observed in the coinfection were defined for the candidate MLG, and the remaining alleles were defined as unknown, because they could have been unobserved due to genotyping error. Fifth, we merged candidate MLGs that had same alleles in all the loci that were defined. The unique MLGs from single infections and the constructed candidate MLGs were now considered the unique strains for the population. The number of new MLGs in a population for a given year was estimated using the same algorithm. First, we applied the algorithm to samples from current and previous year, and then to samples from current year only. The number of new MLGs was then estimated as the difference between the number of MLGs from the two runs.</p></sec><sec id="s4-3-3"><title>Prevalence of coinfection in a population</title><p>Number of samples supporting coinfection in local pathogen populations identified using the SNP genotyping protocol described above.</p></sec><sec id="s4-3-4"><title>Abundance of pathogen resting structures</title><p>The powdery mildew survives the winter in resting structures (chasmothecia). These are visually conspicuous and their abundance has been systematically surveyed on the infected plants located during the field survey (<xref rid="bib47" ref-type="bibr">Tack and Laine, 2014</xref>). The abundance of chasmothecia in local populations has been recorded on a categorical scale: 0 = no infected plants with chasmothecia; 1 =<10% of infected plants with chasmothecia; 2 = 10–25% of infected plants with chasmothecia; 3 = 25–50% of infected plants with chasmothecia, and 4 = 50–100% of infected plants with chasmothecia.</p></sec><sec id="s4-3-5"><title>Successful overwintering of pathogen populations</title><p>Pathogen populations that were located in two successive autumn surveys were considered to have successfully overwintered.</p></sec><sec id="s4-3-6"><title>Pathogen connectivity</title><p>Connectivity, denoted with <inline-formula><mml:math id="inf10"><mml:msubsup><mml:mrow><mml:mi>S</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow><mml:mrow><mml:mi>p</mml:mi></mml:mrow></mml:msubsup></mml:math></inline-formula><sup>37</sup> of each pathogen population, <italic>i</italic>, was computed as:<disp-formula id="equ1"><mml:math id="m1"><mml:msubsup><mml:mrow><mml:mi>S</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow><mml:mrow><mml:mi>p</mml:mi></mml:mrow></mml:msubsup><mml:mo>(</mml:mo><mml:mi>t</mml:mi><mml:mo>)</mml:mo><mml:mo>=</mml:mo><mml:mi></mml:mi><mml:mrow><mml:munder><mml:mo>∑</mml:mo><mml:mrow><mml:mi>i</mml:mi><mml:mi></mml:mi><mml:mo>≠</mml:mo><mml:mi>j</mml:mi></mml:mrow></mml:munder><mml:mrow><mml:msup><mml:mrow><mml:mi>e</mml:mi></mml:mrow><mml:mrow><mml:mo>-</mml:mo><mml:mfrac><mml:mrow><mml:msub><mml:mrow><mml:mi>d</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi></mml:mrow></mml:msub></mml:mrow><mml:mrow><mml:mi>α</mml:mi></mml:mrow></mml:mfrac></mml:mrow></mml:msup></mml:mrow></mml:mrow><mml:msub><mml:mrow><mml:mi>O</mml:mi></mml:mrow><mml:mrow><mml:mi>j</mml:mi></mml:mrow></mml:msub></mml:math></disp-formula>where <inline-formula><mml:math id="inf11"><mml:msub><mml:mrow><mml:mi>O</mml:mi></mml:mrow><mml:mrow><mml:mi>j</mml:mi></mml:mrow></mml:msub><mml:mo>=</mml:mo><mml:mn>1</mml:mn></mml:math></inline-formula>, if population <italic>j</italic> was infected and <inline-formula><mml:math id="inf12"><mml:msub><mml:mrow><mml:mi>O</mml:mi></mml:mrow><mml:mrow><mml:mi>j</mml:mi></mml:mrow></mml:msub><mml:mo>=</mml:mo><mml:mn>0</mml:mn><mml:mo>,</mml:mo></mml:math></inline-formula> if population j was not infected in the current year t, and <inline-formula><mml:math id="inf13"><mml:msub><mml:mrow><mml:mi>d</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula> corresponds to the distance between populations i and j. The parameter <inline-formula><mml:math id="inf14"><mml:mi>α</mml:mi></mml:math></inline-formula>, describing the mean dispersal distance at the metapopulation level, was set <inline-formula><mml:math id="inf15"><mml:mi>α</mml:mi><mml:mo>=</mml:mo><mml:mn>1000</mml:mn></mml:math></inline-formula> (meters) following results of <xref rid="bib21" ref-type="bibr">Jousimo et al. (2014)</xref>. <italic>Si</italic> is thus assumed to be a rough proxy for the expected number of pathogen transmission coming to population <italic>i</italic> from all the infected populations, under the assumption of exponentially distributed dispersal distance.</p></sec><sec id="s4-3-7"><title>Host population size</title><p>The total coverage (in m<sup>2</sup>) of the host in the local population has been visually assessed each year simultaneously when the pathogen infection data were collected. The criteria for describing host populations is provided in detail in <xref rid="bib33" ref-type="bibr">Ojanen et al. (2013)</xref>. In brief, suitable host populations have been identified by the presence of dense clusters of <italic>P. lanceolata</italic>, which in Åland occur on dry meadows and pastures. These occur as well-defined, discrete patches across the landscape.</p></sec></sec><sec id="s4-4"><title>Spatial bayesian modelling of the effect of coinfection on pathogen overwintering and strain diversity</title><p>We modeled the following events of interest: the effect of the number of coinfections on persistence of infection from one year to the next, and the number of new, previously unidentified, MLGs in a pathogen population that survived from one year to the next. In addition, we assessed the drivers of the presence/absence of resting spores and coinfections among the infected populations. Our models were fitted to data from years 2012-2015. To control for the possible effect that population size, connectivity and diversity could have on the results, our models included the following predictors (described above in detail): Pathogen population size, host population size, number of distinct pathogen strains, and pathogen connectivity <inline-formula><mml:math id="inf16"><mml:msubsup><mml:mrow><mml:mi>S</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow><mml:mrow><mml:mi>p</mml:mi></mml:mrow></mml:msubsup></mml:math></inline-formula>. Predictors with continuous support and the number of observed coinfections, were scaled and centered around zero, and factors transformed into binary 0/1-variables.</p><sec id="s4-4-1"><title>Spatio-temporal logistic regression model</title><p>The statistical modeling of the phenomena of interest (coinfection presence, the emergence of new strains in a population and survival of pathogen population) was done by considering a logistic regression modeling framework, where the observation at location <italic>s</italic> at time <italic>t</italic> was assumed to be Bernoulli distributed with the event probability <inline-formula><mml:math id="inf17"><mml:msub><mml:mrow><mml:mi mathvariant="normal">μ</mml:mi></mml:mrow><mml:mrow><mml:mi mathvariant="normal">s</mml:mi><mml:mi mathvariant="normal">t</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula>. The spatial- and temporal autocorrelation was taken into account by assuming that <inline-formula><mml:math id="inf18"><mml:msub><mml:mrow><mml:mi mathvariant="normal">μ</mml:mi></mml:mrow><mml:mrow><mml:mi mathvariant="normal">s</mml:mi><mml:mi mathvariant="normal">t</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula> has an explicit spatio-temporal correlation structure, defined as follows:<disp-formula id="equ2"><mml:math id="m2"><mml:mstyle displaystyle="true" scriptlevel="0"><mml:mrow><mml:mrow><mml:mi mathvariant="normal">l</mml:mi></mml:mrow><mml:mrow><mml:mi mathvariant="normal">o</mml:mi></mml:mrow><mml:mrow><mml:mi mathvariant="normal">g</mml:mi></mml:mrow><mml:mrow><mml:mi mathvariant="normal">i</mml:mi></mml:mrow><mml:mrow><mml:mi mathvariant="normal">t</mml:mi></mml:mrow><mml:mrow><mml:mo>(</mml:mo><mml:msub><mml:mi>μ</mml:mi><mml:mrow><mml:mi>s</mml:mi><mml:mi>t</mml:mi></mml:mrow></mml:msub><mml:mo>)</mml:mo></mml:mrow><mml:mo>=</mml:mo><mml:mi>z</mml:mi><mml:mrow><mml:mo>(</mml:mo><mml:mrow><mml:mi>s</mml:mi><mml:mo>,</mml:mo><mml:mi>t</mml:mi></mml:mrow><mml:mo>)</mml:mo></mml:mrow><mml:mi>β</mml:mi><mml:mo>+</mml:mo><mml:mi>δ</mml:mi><mml:mrow><mml:mo>(</mml:mo><mml:mrow><mml:mi>s</mml:mi><mml:mo>,</mml:mo><mml:mi>t</mml:mi></mml:mrow><mml:mo>)</mml:mo></mml:mrow><mml:mo>+</mml:mo><mml:mi>ε</mml:mi><mml:mrow><mml:mo>(</mml:mo><mml:mrow><mml:mi>s</mml:mi><mml:mo>,</mml:mo><mml:mi>t</mml:mi></mml:mrow><mml:mo>)</mml:mo></mml:mrow></mml:mrow></mml:mstyle></mml:math></disp-formula><disp-formula id="equ3"><mml:math id="m3"><mml:mstyle displaystyle="true" scriptlevel="0"><mml:mrow><mml:mi>δ</mml:mi><mml:mrow><mml:mo>(</mml:mo><mml:mrow><mml:mi>s</mml:mi><mml:mo>,</mml:mo><mml:mi>t</mml:mi></mml:mrow><mml:mo>)</mml:mo></mml:mrow><mml:mo>=</mml:mo><mml:mi>φ</mml:mi><mml:mo>⋅</mml:mo><mml:mi>δ</mml:mi><mml:mrow><mml:mo>(</mml:mo><mml:mrow><mml:mi>s</mml:mi><mml:mo>,</mml:mo><mml:mi>t</mml:mi><mml:mo>−</mml:mo><mml:mn>1</mml:mn></mml:mrow><mml:mo>)</mml:mo></mml:mrow><mml:mo>+</mml:mo><mml:mi>w</mml:mi><mml:mrow><mml:mo>(</mml:mo><mml:mrow><mml:mi>s</mml:mi><mml:mo>,</mml:mo><mml:mi>t</mml:mi></mml:mrow><mml:mo>)</mml:mo></mml:mrow></mml:mrow></mml:mstyle></mml:math></disp-formula></p><p>Here <italic>z(s,t)</italic> corresponds to the covariate information and <inline-formula><mml:math id="inf19"><mml:mi>ε</mml:mi><mml:mfenced separators="|"><mml:mrow><mml:mi>s</mml:mi><mml:mo>,</mml:mo><mml:mi>t</mml:mi></mml:mrow></mml:mfenced></mml:math></inline-formula> is the measurement error. Further, <inline-formula><mml:math id="inf20"><mml:mi>δ</mml:mi><mml:mfenced separators="|"><mml:mrow><mml:mi>s</mml:mi><mml:mo>,</mml:mo><mml:mi>t</mml:mi></mml:mrow></mml:mfenced></mml:math></inline-formula> is a spatio-temporal latent process with first-order temporal autocorrelation, described by parameter <inline-formula><mml:math id="inf21"><mml:mi>φ</mml:mi></mml:math></inline-formula>(<inline-formula><mml:math id="inf22"><mml:mstyle displaystyle="true" scriptlevel="0"><mml:mrow><mml:mrow><mml:mo>|</mml:mo><mml:mi>φ</mml:mi><mml:mo>|</mml:mo></mml:mrow><mml:mo><</mml:mo><mml:mo>;</mml:mo><mml:mn>1</mml:mn><mml:mo stretchy="false">)</mml:mo></mml:mrow></mml:mstyle></mml:math></inline-formula>, and spatially correlated outcomes described by zero-mean Gaussian distribution <inline-formula><mml:math id="inf23"><mml:mi>w</mml:mi><mml:mfenced separators="|"><mml:mrow><mml:mi>s</mml:mi><mml:mo>,</mml:mo><mml:mi>t</mml:mi></mml:mrow></mml:mfenced></mml:math></inline-formula>. The spatial correlation is included by assuming that <inline-formula><mml:math id="inf24"><mml:mi>w</mml:mi><mml:mfenced separators="|"><mml:mrow><mml:mi>s</mml:mi><mml:mo>,</mml:mo><mml:mi>t</mml:mi></mml:mrow></mml:mfenced></mml:math></inline-formula> has the following covariance structure:<disp-formula id="equ4"><mml:math id="m4"><mml:mstyle displaystyle="true" scriptlevel="0"><mml:mrow><mml:mi>C</mml:mi><mml:mi>o</mml:mi><mml:mi>v</mml:mi><mml:mrow><mml:mo>(</mml:mo><mml:mrow><mml:mi>w</mml:mi><mml:mrow><mml:mo>(</mml:mo><mml:mrow><mml:mi>s</mml:mi><mml:mo>,</mml:mo><mml:mi>t</mml:mi></mml:mrow><mml:mo>)</mml:mo></mml:mrow><mml:mo>,</mml:mo><mml:mtext> </mml:mtext><mml:mi>C</mml:mi><mml:mi>o</mml:mi><mml:mi>v</mml:mi><mml:mrow><mml:mo>(</mml:mo><mml:mrow><mml:msup><mml:mi>s</mml:mi><mml:mrow><mml:mo>′</mml:mo></mml:mrow></mml:msup><mml:mo>,</mml:mo><mml:msup><mml:mi>t</mml:mi><mml:mrow><mml:mo>′</mml:mo></mml:mrow></mml:msup></mml:mrow><mml:mo>)</mml:mo></mml:mrow></mml:mrow><mml:mo>)</mml:mo></mml:mrow><mml:mo>=</mml:mo><mml:mrow><mml:mo>{</mml:mo><mml:mtable columnalign="left left" columnspacing="1em" displaystyle="false" rowspacing=".2em"><mml:mtr><mml:mtd><mml:msub><mml:mi>σ</mml:mi><mml:mrow><mml:mn>2</mml:mn></mml:mrow></mml:msub><mml:mi>C</mml:mi><mml:mrow><mml:mo>(</mml:mo><mml:mi>h</mml:mi><mml:mo>)</mml:mo></mml:mrow><mml:mtext> </mml:mtext></mml:mtd></mml:mtr><mml:mtr><mml:mtd><mml:mn>0</mml:mn><mml:mo>,</mml:mo><mml:mtext> </mml:mtext><mml:mi>i</mml:mi><mml:mi>f</mml:mi><mml:mtext> </mml:mtext><mml:mi>t</mml:mi><mml:mo>≠</mml:mo><mml:msup><mml:mi>t</mml:mi><mml:mo>′</mml:mo></mml:msup></mml:mtd></mml:mtr></mml:mtable><mml:mo fence="true" stretchy="true" symmetric="true"></mml:mo></mml:mrow></mml:mrow></mml:mstyle></mml:math></disp-formula></p><p>Here <inline-formula><mml:math id="inf25"><mml:msub><mml:mrow><mml:mi>σ</mml:mi></mml:mrow><mml:mrow><mml:mn>2</mml:mn></mml:mrow></mml:msub></mml:math></inline-formula> is the overall variance of the random field, and <inline-formula><mml:math id="inf26"><mml:mi>C</mml:mi><mml:mo>(</mml:mo><mml:mi>h</mml:mi><mml:mo>)</mml:mo></mml:math></inline-formula> is the Matern covariance function, that only depends on the Euclidean distance <italic>h</italic> between the latent locations <italic>s</italic> and <italic>s’</italic>, and hyperparameters <inline-formula><mml:math id="inf27"><mml:mi>κ</mml:mi></mml:math></inline-formula> and <inline-formula><mml:math id="inf28"><mml:mi>ϑ</mml:mi></mml:math></inline-formula>. Details on the covariance function, and an in-depth description of the modeling framework is given in <xref rid="bib8" ref-type="bibr">Cameletti et al. (2013)</xref>. The aim of our analysis was to infer the joint posterior distribution of <inline-formula><mml:math id="inf29"><mml:mi>θ</mml:mi></mml:math></inline-formula>:<disp-formula id="equ5"><mml:math id="m5"><mml:mstyle displaystyle="true" scriptlevel="0"><mml:mrow><mml:mi>θ</mml:mi><mml:mo>=</mml:mo><mml:mrow><mml:mo>{</mml:mo><mml:mrow><mml:mi>β</mml:mi><mml:mo>,</mml:mo><mml:mtext> </mml:mtext><mml:mi>φ</mml:mi><mml:mo>,</mml:mo><mml:mtext> </mml:mtext><mml:msub><mml:mi>σ</mml:mi><mml:mrow><mml:mn>2</mml:mn></mml:mrow></mml:msub><mml:mo>,</mml:mo><mml:mtext> </mml:mtext><mml:mi>κ</mml:mi><mml:mo>,</mml:mo><mml:mtext> </mml:mtext><mml:mrow><mml:mtext> </mml:mtext></mml:mrow><mml:mi>ϑ</mml:mi><mml:mo>,</mml:mo></mml:mrow><mml:mo fence="true" stretchy="true" symmetric="true"></mml:mo></mml:mrow></mml:mrow></mml:mstyle></mml:math></disp-formula>the main interest being in <inline-formula><mml:math id="inf30"><mml:mi>β</mml:mi></mml:math></inline-formula>, which describes the effects of the covariates listed and described in the Model variables section.</p><p>Efficient implementation of such inference is provided by the R-INLA package, which provides posterior distribution of <inline-formula><mml:math id="inf31"><mml:mi>θ</mml:mi></mml:math></inline-formula> by marginalizing <inline-formula><mml:math id="inf32"><mml:msub><mml:mrow><mml:mi>μ</mml:mi></mml:mrow><mml:mrow><mml:mi>s</mml:mi><mml:mi>t</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula> with Laplace approximation. When setting the prior distributions for hyperparametersand <inline-formula><mml:math id="inf33"><mml:mi>ϑ</mml:mi></mml:math></inline-formula>, we followed the heuristics proposed by the INLA developers (<xref rid="bib30" ref-type="bibr">Lindgren and Rue, 2015</xref>), ensuring that a 95% prior probability is set to the range being smaller than the size of the spatial domain considered. Here the range is defined as the distance at which the spatial autocorrelation becomes negligible (smaller than 0.1 under the Matern covariance). The other prior distributions were set to default uninformative prior distributions (<xref rid="bib29" ref-type="bibr">Lindgren, 2012</xref>), Finally, another computational gain is obtained by approximating the spatial random field <inline-formula><mml:math id="inf34"><mml:mi>w</mml:mi><mml:mfenced separators="|"><mml:mrow><mml:mi>s</mml:mi><mml:mo>,</mml:mo><mml:mi>t</mml:mi></mml:mrow></mml:mfenced></mml:math></inline-formula> with the help of a mesh, visualized in <xref ref-type="fig" rid="fig1s1">Figure 1—figure supplement 1</xref>.</p></sec><sec id="s4-4-2"><title>Model validation</title><p>As a model validation argument, we inspected the distribution of the CPO-values, <italic>Conditional Predictive Ordinates</italic>, defined as:<disp-formula id="equ6"><mml:math id="m6"><mml:mi>C</mml:mi><mml:mi>P</mml:mi><mml:msub><mml:mrow><mml:mi>O</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub><mml:mo>=</mml:mo><mml:mi></mml:mi><mml:mi>P</mml:mi><mml:mfenced close="|" separators="|"><mml:mrow><mml:msubsup><mml:mrow><mml:mi>d</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow><mml:mrow><mml:mi>n</mml:mi><mml:mi>e</mml:mi><mml:mi>w</mml:mi></mml:mrow></mml:msubsup><mml:mo>=</mml:mo><mml:msub><mml:mrow><mml:mi>d</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub><mml:mi></mml:mi></mml:mrow></mml:mfenced><mml:mi></mml:mi><mml:msub><mml:mrow><mml:mi>D</mml:mi></mml:mrow><mml:mrow><mml:mo>-</mml:mo><mml:mi>i</mml:mi></mml:mrow></mml:msub><mml:mo>)</mml:mo><mml:mo>.</mml:mo></mml:math></disp-formula></p><p><inline-formula><mml:math id="inf35"><mml:mi>C</mml:mi><mml:mi>P</mml:mi><mml:msub><mml:mrow><mml:mi>O</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula> `corresponds to the probability of predicting the observation <inline-formula><mml:math id="inf36"><mml:msub><mml:mrow><mml:mi>d</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula>, when <inline-formula><mml:math id="inf37"><mml:msub><mml:mrow><mml:mi>d</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula> is excluded from the model fitting. Briefly, high CPO-values indicate high predictive power of the fitted model, while very low CPO values would indicate outlier observations, or a poor fit of the model, and patterns in CPO values (such as spatial or temporal) suggest inappropriate model structure.</p><p>To ensure the adequacy of the fitted models, we considered leave-one-out predictive measures of fit, assessing how well the model is able to predict the observed dynamics. In particular, we considered the so-called <italic>probability integral transform</italic> (<xref rid="bib10" ref-type="bibr">Dawid, 1984</xref>), defined as:<disp-formula id="equ7"><mml:math id="m7"><mml:mi>P</mml:mi><mml:mi>I</mml:mi><mml:msub><mml:mrow><mml:mi>T</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub><mml:mo>=</mml:mo><mml:mi>P</mml:mi><mml:mfenced close="|" separators="|"><mml:mrow><mml:msubsup><mml:mrow><mml:mi>d</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow><mml:mrow><mml:mi>n</mml:mi><mml:mi>e</mml:mi><mml:mi>w</mml:mi></mml:mrow></mml:msubsup><mml:mo>≤</mml:mo><mml:msubsup><mml:mrow><mml:mi>d</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow><mml:mrow><mml:mi>n</mml:mi><mml:mi>e</mml:mi><mml:mi>w</mml:mi></mml:mrow></mml:msubsup><mml:mi></mml:mi></mml:mrow></mml:mfenced><mml:mi></mml:mi><mml:msub><mml:mrow><mml:mi>D</mml:mi></mml:mrow><mml:mrow><mml:mo>-</mml:mo><mml:mi>i</mml:mi></mml:mrow></mml:msub><mml:mo>)</mml:mo><mml:mo>,</mml:mo></mml:math></disp-formula></p><p>Here <inline-formula><mml:math id="inf38"><mml:msubsup><mml:mrow><mml:mi>d</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow><mml:mrow></mml:mrow></mml:msubsup></mml:math></inline-formula> denotes for the i’th observed outcome in the data, and <inline-formula><mml:math id="inf39"><mml:msub><mml:mrow><mml:mi>D</mml:mi></mml:mrow><mml:mrow><mml:mo>-</mml:mo><mml:mi>i</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula> for the data with this observation excluded, and <inline-formula><mml:math id="inf40"><mml:mi>P</mml:mi><mml:mi>I</mml:mi><mml:msub><mml:mrow><mml:mi>T</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula> corresponds to the cumulative predictive distribution for the outcome i, given all the other observations. We adjust this to take into account the discrete nature of the modeled outcomes, as follows (<xref rid="bib9" ref-type="bibr">Czado et al., 2009</xref>):<disp-formula id="equ8"><mml:math id="m8"><mml:mstyle displaystyle="true" scriptlevel="0"><mml:mrow><mml:mi>P</mml:mi><mml:mi>I</mml:mi><mml:msub><mml:mi>T</mml:mi><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub><mml:mo>=</mml:mo><mml:mi>P</mml:mi><mml:mrow><mml:mo>(</mml:mo><mml:mrow><mml:msubsup><mml:mi>d</mml:mi><mml:mrow><mml:mi>i</mml:mi></mml:mrow><mml:mrow><mml:mi>n</mml:mi><mml:mi>e</mml:mi><mml:mi>w</mml:mi></mml:mrow></mml:msubsup><mml:mo><</mml:mo><mml:mo>;</mml:mo><mml:msub><mml:mi>d</mml:mi><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub><mml:mtext> </mml:mtext></mml:mrow><mml:mo>|</mml:mo></mml:mrow><mml:mtext> </mml:mtext><mml:msub><mml:mi>D</mml:mi><mml:mrow><mml:mo>−</mml:mo><mml:mi>i</mml:mi></mml:mrow></mml:msub><mml:mo stretchy="false">)</mml:mo><mml:mo>+</mml:mo><mml:mfrac><mml:mn>1</mml:mn><mml:mn>2</mml:mn></mml:mfrac><mml:mo>∗</mml:mo><mml:mi>P</mml:mi><mml:mrow><mml:mo>(</mml:mo><mml:mrow><mml:msubsup><mml:mi>d</mml:mi><mml:mrow><mml:mi>i</mml:mi></mml:mrow><mml:mrow><mml:mi>n</mml:mi><mml:mi>e</mml:mi><mml:mi>w</mml:mi></mml:mrow></mml:msubsup><mml:mo>=</mml:mo><mml:msub><mml:mi>d</mml:mi><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub><mml:mtext> </mml:mtext></mml:mrow><mml:mo>|</mml:mo></mml:mrow><mml:mtext> </mml:mtext><mml:msub><mml:mi>D</mml:mi><mml:mrow><mml:mo>−</mml:mo><mml:mi>i</mml:mi></mml:mrow></mml:msub><mml:mo stretchy="false">)</mml:mo><mml:mo>.</mml:mo></mml:mrow></mml:mstyle></mml:math></disp-formula></p><p>In brief, skewedness of the distribution of PIT-values indicates biases, U- and inverse-U-shaped distributions indicate under- and over-dispersion, respectively, while a uniform distribution indicates good model fit.</p></sec><sec id="s4-4-3"><title>Parameter estimates</title><p>We considered a covariate to have a significant effect on the outcome, whenever its 95% credibility interval did not contain zero.</p></sec></sec><sec id="s4-5"><title>Analysis of occurrence of co-infections with approximate bayesian computation</title><p>We take an Approximate Bayesian Computation approach to determine whether there is more co-infection in the pathogen metapopulation than expected by chance. The model does not take into account the spatial structure of the patches, but considers them independent conditional on the model parameters.</p><sec id="s4-5-1"><title>Process model</title><p>First, consider a single patch <italic>i</italic>. Let <inline-formula><mml:math id="inf41"><mml:msub><mml:mrow><mml:mi>x</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula> denote a vector of environmental covariates of the patch <italic>i</italic> and including a constant. The number of plant individuals in patch <italic>i</italic>, <inline-formula><mml:math id="inf42"><mml:msub><mml:mrow><mml:mi>N</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula>, is modeled as<disp-formula id="equ9"><mml:math id="m9"><mml:msub><mml:mrow><mml:mi>N</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub><mml:mo>~</mml:mo><mml:mi>P</mml:mi><mml:mi>o</mml:mi><mml:mi>i</mml:mi><mml:mi>s</mml:mi><mml:mi>s</mml:mi><mml:mi>o</mml:mi><mml:mi>n</mml:mi><mml:mfenced separators="|"><mml:mrow><mml:msub><mml:mrow><mml:mi>x</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub><mml:msub><mml:mrow><mml:mi>α</mml:mi></mml:mrow><mml:mrow><mml:mi>N</mml:mi></mml:mrow></mml:msub></mml:mrow></mml:mfenced><mml:mo>,</mml:mo></mml:math></disp-formula>where <inline-formula><mml:math id="inf43"><mml:msub><mml:mrow><mml:mi>α</mml:mi></mml:mrow><mml:mrow><mml:mi>N</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula> are the parameters relating covariates <inline-formula><mml:math id="inf44"><mml:msub><mml:mrow><mml:mi>x</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula> to the expectation of <inline-formula><mml:math id="inf45"><mml:msub><mml:mrow><mml:mi>N</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula>. The number of MLGs in patch <italic>i</italic>, <inline-formula><mml:math id="inf46"><mml:msub><mml:mrow><mml:mi>M</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula>, is modeled similarly<disp-formula id="equ10"><mml:math id="m10"><mml:msub><mml:mrow><mml:mi>M</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub><mml:mo>~</mml:mo><mml:mi>P</mml:mi><mml:mi>o</mml:mi><mml:mi>i</mml:mi><mml:mi>s</mml:mi><mml:mi>s</mml:mi><mml:mi>o</mml:mi><mml:mi>n</mml:mi><mml:mfenced separators="|"><mml:mrow><mml:msub><mml:mrow><mml:mi>x</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub><mml:msub><mml:mrow><mml:mi>α</mml:mi></mml:mrow><mml:mrow><mml:mi>M</mml:mi></mml:mrow></mml:msub></mml:mrow></mml:mfenced><mml:mo>,</mml:mo></mml:math></disp-formula>where <inline-formula><mml:math id="inf47"><mml:msub><mml:mrow><mml:mi>α</mml:mi></mml:mrow><mml:mrow><mml:mi>M</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula> are the parameters. The number <inline-formula><mml:math id="inf48"><mml:msub><mml:mrow><mml:mi>M</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula> might be restricted with an upper limit <inline-formula><mml:math id="inf49"><mml:msub><mml:mrow><mml:mi>M</mml:mi></mml:mrow><mml:mrow><mml:mi>m</mml:mi><mml:mi>a</mml:mi><mml:mi>x</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula>, so that <inline-formula><mml:math id="inf50"><mml:msub><mml:mrow><mml:mi>M</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub><mml:mo>≤</mml:mo><mml:mo>~</mml:mo><mml:msub><mml:mrow><mml:mi>M</mml:mi></mml:mrow><mml:mrow><mml:mi>m</mml:mi><mml:mi>a</mml:mi><mml:mi>x</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula>.</p><p>Let <inline-formula><mml:math id="inf51"><mml:msub><mml:mrow><mml:mi>μ</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub><mml:mo>=</mml:mo><mml:mfenced separators="|"><mml:mrow><mml:msub><mml:mrow><mml:mi>μ</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mn>1</mml:mn></mml:mrow></mml:msub><mml:mo>,</mml:mo><mml:mo>…</mml:mo><mml:mo>,</mml:mo><mml:msub><mml:mrow><mml:mi>μ</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:msub><mml:mrow><mml:mi>M</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub></mml:mrow></mml:msub></mml:mrow></mml:mfenced></mml:math></inline-formula> be a vector of transformed prevalences of the different MLGs in patch <italic>i</italic>. We assume a normal distribution for <inline-formula><mml:math id="inf52"><mml:msub><mml:mrow><mml:mi>μ</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>k</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula>, <italic>k=1,…,</italic><inline-formula><mml:math id="inf53"><mml:msub><mml:mrow><mml:mi>M</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula>,<disp-formula id="equ11"><mml:math id="m11"><mml:msub><mml:mrow><mml:mi>μ</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>k</mml:mi></mml:mrow></mml:msub><mml:mo>~</mml:mo><mml:mi>N</mml:mi><mml:mi>o</mml:mi><mml:mi>r</mml:mi><mml:mi>m</mml:mi><mml:mi>a</mml:mi><mml:mi>l</mml:mi><mml:mfenced separators="|"><mml:mrow><mml:msub><mml:mrow><mml:mi>x</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub><mml:mi>β</mml:mi><mml:mo>,</mml:mo><mml:mn>1</mml:mn></mml:mrow></mml:mfenced><mml:mo>,</mml:mo></mml:math></disp-formula>where <inline-formula><mml:math id="inf54"><mml:mi>β</mml:mi></mml:math></inline-formula> is a vector of linear predictors.</p><p>For the <italic>j</italic><sup>th</sup> plant in patch <italic>i</italic> the infection status is represented by a vector <inline-formula><mml:math id="inf55"><mml:msub><mml:mrow><mml:mi>Z</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi></mml:mrow></mml:msub><mml:mo>=</mml:mo><mml:mfenced separators="|"><mml:mrow><mml:msub><mml:mrow><mml:mi>Z</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi><mml:mo>,</mml:mo><mml:mn>1</mml:mn></mml:mrow></mml:msub><mml:mo>,</mml:mo><mml:mo>…</mml:mo><mml:mo>,</mml:mo><mml:msub><mml:mrow><mml:mi>Z</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi><mml:mo>,</mml:mo><mml:msub><mml:mrow><mml:mi>M</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub></mml:mrow></mml:msub></mml:mrow></mml:mfenced></mml:math></inline-formula>. If <inline-formula><mml:math id="inf56"><mml:mstyle displaystyle="true" scriptlevel="0"><mml:mrow><mml:msub><mml:mi>Z</mml:mi><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi><mml:mo>,</mml:mo><mml:mi>k</mml:mi></mml:mrow></mml:msub><mml:mo>></mml:mo><mml:mo>;</mml:mo><mml:mn>0</mml:mn></mml:mrow></mml:mstyle></mml:math></inline-formula>, then the plant if infected by MLG <italic>k</italic>, and otherwise it is not infected by the strain <italic>k</italic>. We assume that the plant is exposed to the MLGs <italic>1,…,</italic><inline-formula><mml:math id="inf57"><mml:msub><mml:mrow><mml:mi>M</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi><mml:mi></mml:mi></mml:mrow></mml:msub></mml:math></inline-formula> in order <inline-formula><mml:math id="inf58"><mml:msub><mml:mrow><mml:mi>σ</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula>, which is a permutation of the MLG indices. The distribution for <inline-formula><mml:math id="inf59"><mml:msub><mml:mrow><mml:mi>Z</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi><mml:mo>,</mml:mo><mml:mi>k</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula> is<disp-formula id="equ12"><mml:math id="m12"><mml:mstyle displaystyle="true" scriptlevel="0"><mml:mrow><mml:msub><mml:mi>Z</mml:mi><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi><mml:mo>,</mml:mo><mml:mi>k</mml:mi></mml:mrow></mml:msub><mml:mo>∼</mml:mo><mml:mspace width="thinmathspace"></mml:mspace><mml:mspace width="thinmathspace"></mml:mspace><mml:mi>N</mml:mi><mml:mi>o</mml:mi><mml:mi>r</mml:mi><mml:mi>m</mml:mi><mml:mi>a</mml:mi><mml:mi>l</mml:mi><mml:mo stretchy="false">(</mml:mo><mml:mi>η</mml:mi><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi><mml:mo>,</mml:mo><mml:mi>k</mml:mi><mml:mo>,</mml:mo><mml:msup><mml:mi>τ</mml:mi><mml:mrow><mml:mn>2</mml:mn></mml:mrow></mml:msup><mml:mo stretchy="false">)</mml:mo><mml:mo>,</mml:mo></mml:mrow></mml:mstyle></mml:math></disp-formula>where <inline-formula><mml:math id="inf60"><mml:msup><mml:mrow><mml:mi>τ</mml:mi></mml:mrow><mml:mrow><mml:mn>2</mml:mn></mml:mrow></mml:msup></mml:math></inline-formula> is the variance parameter and the mean <inline-formula><mml:math id="inf61"><mml:msub><mml:mrow><mml:mi>η</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi><mml:mo>,</mml:mo><mml:mi>k</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula> depends on the values of <inline-formula><mml:math id="inf62"><mml:msub><mml:mrow><mml:mi>Z</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi><mml:mo>,</mml:mo><mml:mi>k</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula> for MLGs l that are before MLG k in the order <inline-formula><mml:math id="inf63"><mml:msub><mml:mrow><mml:mi>σ</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula> . Specifically,<disp-formula id="equ13"><mml:math id="m13"><mml:mstyle displaystyle="true" scriptlevel="0"><mml:mrow><mml:msub><mml:mi>η</mml:mi><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi><mml:mo>,</mml:mo><mml:mi>k</mml:mi></mml:mrow></mml:msub><mml:mo>=</mml:mo><mml:mrow><mml:mo>{</mml:mo><mml:mtable columnalign="left left" columnspacing="1em" displaystyle="false" rowspacing=".2em"><mml:mtr><mml:mtd><mml:msub><mml:mi>μ</mml:mi><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>k</mml:mi></mml:mrow></mml:msub><mml:mo>+</mml:mo><mml:mi>γ</mml:mi></mml:mtd><mml:mtd><mml:mi>i</mml:mi><mml:mi>f</mml:mi><mml:mtext> </mml:mtext><mml:msub><mml:mi>Z</mml:mi><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi><mml:mo>,</mml:mo><mml:msub><mml:mi>σ</mml:mi><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi></mml:mrow></mml:msub><mml:mrow><mml:mo>(</mml:mo><mml:mi>l</mml:mi><mml:mo>)</mml:mo></mml:mrow></mml:mrow></mml:msub><mml:mo>></mml:mo><mml:mo>;</mml:mo><mml:mn>0</mml:mn><mml:mtext> </mml:mtext><mml:mi>f</mml:mi><mml:mi>o</mml:mi><mml:mi>r</mml:mi><mml:mtext> </mml:mtext><mml:mi>a</mml:mi><mml:mi>n</mml:mi><mml:mi>y</mml:mi><mml:mtext> </mml:mtext><mml:msub><mml:mi>σ</mml:mi><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi></mml:mrow></mml:msub><mml:mrow><mml:mo>(</mml:mo><mml:mi>l</mml:mi><mml:mo>)</mml:mo></mml:mrow><mml:mtext> </mml:mtext><mml:mi>l</mml:mi><mml:mi>t</mml:mi><mml:mo>;</mml:mo><mml:mi>k</mml:mi></mml:mtd></mml:mtr><mml:mtr><mml:mtd><mml:msub><mml:mi>μ</mml:mi><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>k</mml:mi></mml:mrow></mml:msub></mml:mtd><mml:mtd><mml:mi>o</mml:mi><mml:mi>t</mml:mi><mml:mi>h</mml:mi><mml:mi>e</mml:mi><mml:mi>r</mml:mi><mml:mi>w</mml:mi><mml:mi>i</mml:mi><mml:mi>s</mml:mi><mml:mi>e</mml:mi></mml:mtd></mml:mtr></mml:mtable><mml:mo fence="true" stretchy="true" symmetric="true"></mml:mo></mml:mrow></mml:mrow></mml:mstyle></mml:math></disp-formula></p><p>In other words, if MLG <italic>k</italic> infects the plant (i.e. <inline-formula><mml:math id="inf64"><mml:mstyle displaystyle="true" scriptlevel="0"><mml:mrow><mml:msub><mml:mi>Z</mml:mi><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi><mml:mo>,</mml:mo><mml:mi>k</mml:mi></mml:mrow></mml:msub><mml:mo>></mml:mo><mml:mo>;</mml:mo><mml:mn>0</mml:mn></mml:mrow></mml:mstyle></mml:math></inline-formula>), then the mean <inline-formula><mml:math id="inf65"><mml:msub><mml:mrow><mml:mi>η</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi><mml:mo>,</mml:mo><mml:mi>k</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula> is increased by <inline-formula><mml:math id="inf66"><mml:mi>γ</mml:mi></mml:math></inline-formula> for the MLG that the plant is exposed afterwards according to the order <inline-formula><mml:math id="inf67"><mml:msub><mml:mrow><mml:mi>σ</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula>. If <inline-formula><mml:math id="inf68"><mml:mstyle displaystyle="true" scriptlevel="0"><mml:mrow><mml:mi>γ</mml:mi><mml:mo>></mml:mo><mml:mo>;</mml:mo><mml:mn>0</mml:mn></mml:mrow></mml:mstyle></mml:math></inline-formula>, then it is easier for the subsequent strains to infect the plant, while if <inline-formula><mml:math id="inf69"><mml:mstyle displaystyle="true" scriptlevel="0"><mml:mrow><mml:mi>γ</mml:mi><mml:mo>></mml:mo><mml:mo>;</mml:mo><mml:mn>0</mml:mn></mml:mrow></mml:mstyle></mml:math></inline-formula>, then it is more difficult for the subsequent strains to infect the plant.</p><p>The order <inline-formula><mml:math id="inf70"><mml:msub><mml:mrow><mml:mi>σ</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula> may be same for all plants in the patch, so that <inline-formula><mml:math id="inf71"><mml:msub><mml:mrow><mml:mi>σ</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi></mml:mrow></mml:msub><mml:mo>=</mml:mo><mml:msub><mml:mrow><mml:mi>σ</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula> for all plants <italic>j</italic> in patch <italic>i</italic>. The order <inline-formula><mml:math id="inf72"><mml:msub><mml:mrow><mml:mi>σ</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula> may be given a uniform distribution in the set of all permutations, or it may depend on the strain prevalences <inline-formula><mml:math id="inf73"><mml:msub><mml:mrow><mml:mi>μ</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula>.</p></sec><sec id="s4-5-2"><title>Sampling model</title><p>The data considered here are the genotypes of sampled individuals. For a single patch <italic>i</italic>, if the mildew is present in the patch, up to 10 infected plants are sampled and the MLGs infecting them determined. The exact number of sampled plants depends on the number available in the patch; as many infected plants are sampled as possible until 10 is reached. The observed genotype for the <italic>j </italic>th sampled plant (note that here <italic>j</italic> goes from 1 to 10, not from 1 to <inline-formula><mml:math id="inf74"><mml:msub><mml:mrow><mml:mi>N</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula>) in patch <italic>i</italic> is<disp-formula id="equ14"><mml:math id="m14"><mml:mstyle displaystyle="true" scriptlevel="0"><mml:mrow><mml:msub><mml:mi>G</mml:mi><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi></mml:mrow></mml:msub><mml:mo>=</mml:mo><mml:mrow><mml:mo>{</mml:mo><mml:mtable columnalign="left left" columnspacing="1em" rowspacing="4pt"><mml:mtr><mml:mtd><mml:mi>k</mml:mi><mml:mspace width="thinmathspace"></mml:mspace><mml:mspace width="thinmathspace"></mml:mspace><mml:mi>i</mml:mi><mml:mi>f</mml:mi><mml:mspace width="thinmathspace"></mml:mspace><mml:msub><mml:mi>Z</mml:mi><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi><mml:mo>,</mml:mo><mml:mi>k</mml:mi></mml:mrow></mml:msub><mml:mo>></mml:mo><mml:mn>0</mml:mn><mml:mspace width="thinmathspace"></mml:mspace><mml:mspace width="thinmathspace"></mml:mspace><mml:mi>a</mml:mi><mml:mi>n</mml:mi><mml:mi>d</mml:mi><mml:mspace width="thinmathspace"></mml:mspace><mml:mspace width="thinmathspace"></mml:mspace><mml:msub><mml:mi>Z</mml:mi><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi><mml:mo>,</mml:mo><mml:mi>l</mml:mi></mml:mrow></mml:msub><mml:mo><</mml:mo><mml:mn>0</mml:mn><mml:mspace width="thinmathspace"></mml:mspace><mml:mspace width="thinmathspace"></mml:mspace><mml:mi>f</mml:mi><mml:mi>o</mml:mi><mml:mi>r</mml:mi><mml:mspace width="thinmathspace"></mml:mspace><mml:mspace width="thinmathspace"></mml:mspace><mml:mi>a</mml:mi><mml:mi>l</mml:mi><mml:mi>l</mml:mi><mml:mspace width="thinmathspace"></mml:mspace><mml:mi>l</mml:mi><mml:mspace width="thinmathspace"></mml:mspace><mml:mo>≠</mml:mo><mml:mi>k</mml:mi></mml:mtd></mml:mtr><mml:mtr><mml:mtd><mml:mn>0</mml:mn><mml:mspace width="thinmathspace"></mml:mspace><mml:mspace width="thinmathspace"></mml:mspace><mml:msub><mml:mi>Z</mml:mi><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi><mml:mo>,</mml:mo><mml:mi>l</mml:mi></mml:mrow></mml:msub><mml:mo>></mml:mo><mml:mn>0</mml:mn><mml:mspace width="thinmathspace"></mml:mspace><mml:mspace width="thinmathspace"></mml:mspace><mml:mi>f</mml:mi><mml:mi>o</mml:mi><mml:mi>r</mml:mi><mml:mspace width="thinmathspace"></mml:mspace><mml:mspace width="thinmathspace"></mml:mspace><mml:mi>m</mml:mi><mml:mi>u</mml:mi><mml:mi>l</mml:mi><mml:mi>t</mml:mi><mml:mi>i</mml:mi><mml:mi>p</mml:mi><mml:mi>l</mml:mi><mml:mi>e</mml:mi><mml:mspace width="thinmathspace"></mml:mspace><mml:mspace width="thinmathspace"></mml:mspace><mml:mi>l</mml:mi></mml:mtd></mml:mtr></mml:mtable><mml:mo fence="true" stretchy="true" symmetric="true"></mml:mo></mml:mrow></mml:mrow></mml:mstyle></mml:math></disp-formula></p><p>In words, genotype <inline-formula><mml:math id="inf75"><mml:msub><mml:mrow><mml:mi>G</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula> is the MLG index, if only one MLG is infecting the plant, and 0 if there is co-infection by multiple MLGs. Note that the genotypes of the MLGs in a co-infection are not observed.</p><p>We also use data on pathogen population size for patch <italic>i</italic>, <inline-formula><mml:math id="inf76"><mml:msub><mml:mrow><mml:mi>A</mml:mi><mml:mi>A</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula>, measured as a categorical variable (1 = less than 10 plants infected, 2 = 10-99 plants infected, 3 = 100-999 or 4 = 1000 or more) and infection prevalence for patch <italic>i</italic>, <inline-formula><mml:math id="inf77"><mml:msub><mml:mrow><mml:mi>R</mml:mi><mml:mi>A</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula>, (categories of the proportion of plants infected: 1 = 0-0.25, 2 = 0.25-0.5, 3 = 0.5-0.75 and 4 = 0.75-1).</p></sec><sec id="s4-5-3"><title>Prior distributions</title><p>The model includes <inline-formula><mml:math id="inf78"><mml:mn>2</mml:mn><mml:mo>+</mml:mo><mml:mn>3</mml:mn><mml:msub><mml:mrow><mml:mi>n</mml:mi></mml:mrow><mml:mrow><mml:mi>x</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula> parameters, where <inline-formula><mml:math id="inf79"><mml:msub><mml:mrow><mml:mi>n</mml:mi></mml:mrow><mml:mrow><mml:mi>x</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula> is the number of covariates <inline-formula><mml:math id="inf80"><mml:msub><mml:mrow><mml:mi>x</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula> for patch <italic>i,</italic> including constant. All of the parameters, or alternatively their logarithms, are given uniform prior distributions on bounded intervals. For example, the variance parameter <inline-formula><mml:math id="inf81"><mml:msup><mml:mrow><mml:mi>τ</mml:mi></mml:mrow><mml:mrow><mml:mn>2</mml:mn></mml:mrow></mml:msup></mml:math></inline-formula> has to be positive, so the uniform distribution is put on its logarithm. Additionally, some covariates might be restricted to have a positive (negative) effect on some feature, in which case the uniform distribution is put on the logarithm of the parameter (negative of the parameter).</p></sec><sec id="s4-5-4"><title>Posterior distribution</title><p>The goal of the inference is to compute and sample from the posterior distribution of the parameters given the observed data,<disp-formula id="equ15"><mml:math id="m15"><mml:mi>p</mml:mi><mml:mfenced separators="|"><mml:mrow><mml:mi>γ</mml:mi><mml:mo>,</mml:mo><mml:msup><mml:mrow><mml:mi>τ</mml:mi></mml:mrow><mml:mrow><mml:mn>2</mml:mn></mml:mrow></mml:msup><mml:mo>,</mml:mo><mml:msub><mml:mrow><mml:mi>α</mml:mi></mml:mrow><mml:mrow><mml:mi>N</mml:mi></mml:mrow></mml:msub><mml:mo>,</mml:mo><mml:msub><mml:mrow><mml:mi>α</mml:mi></mml:mrow><mml:mrow><mml:mi>M</mml:mi></mml:mrow></mml:msub><mml:mo>,</mml:mo><mml:mi>β</mml:mi><mml:mo>|</mml:mo><mml:mi>G</mml:mi><mml:mo>,</mml:mo><mml:mi>A</mml:mi><mml:mi>A</mml:mi><mml:mo>,</mml:mo><mml:mi>R</mml:mi><mml:mi>A</mml:mi></mml:mrow></mml:mfenced></mml:math></disp-formula></p><p>As data is available for multiple years, we considered each of them separately. As covariates in <inline-formula><mml:math id="inf82"><mml:msub><mml:mrow><mml:mi>x</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula> for patch <italic>i</italic> we included the area of the patch and <italic>P. lanceolata</italic> coverage. We included in the data only patches, where these covariates are available, resulting in 3817 and 3615 patches for years 2012 and 2013, respectively. The covariates (constant excluded) were standardized to have zero mean and unit variance across the patches. The total number of parameters in the model is 11.</p><p>Unless otherwise stated, the maximum number of MLGs in each patch was set to <inline-formula><mml:math id="inf83"><mml:msub><mml:mrow><mml:mi>M</mml:mi></mml:mrow><mml:mrow><mml:mi>m</mml:mi><mml:mi>a</mml:mi><mml:mi>x</mml:mi></mml:mrow></mml:msub><mml:mo>=</mml:mo><mml:mn>30</mml:mn></mml:math></inline-formula>. Similarly, the order <inline-formula><mml:math id="inf84"><mml:msub><mml:mrow><mml:mi>σ</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula> was given a uniform distribution in the set of all permutations independently for each <italic>i</italic> and <italic>j</italic>.</p></sec><sec id="s4-5-5"><title>Approximate bayesian computation</title><p>We use an Approximate Bayesian computation (ABC) approach (<xref rid="bib3" ref-type="bibr">Beaumont, 2010</xref>) to make inference on the posterior distribution of the parameters. ABC refers to a class of computational methods for Bayesian statistics, where the computation of likelihood is replaced by simulations from the model, and it is ideal for our purpose given that the dimension of the model is not fixed, because the number of plants <inline-formula><mml:math id="inf85"><mml:msub><mml:mrow><mml:mi>N</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula> and the number of MLGs <inline-formula><mml:math id="inf86"><mml:msub><mml:mrow><mml:mi>M</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula> in patch <italic>i</italic> is allowed to vary. Moreover, as our aim is to infer general patterns from the data in using information on for example the number of MLGs in a particular patch, an ABC approach is an efficient strategy.</p><p>Parameter estimation is carried out using standard ABC techniques (<xref rid="bib3" ref-type="bibr">Beaumont, 2010</xref>). Candidate parameters are simulated from the prior, pseudo-datasets simulated for each parameter value and summary statistics are computed from the datasets. The number of simulations in each analysis is 100,000. The threshold of accepting simulations is based on obtaining a fixed size set of accepted values, that is the acceptance threshold is a quantile of the distances. We use 500 closest values in the analysis.</p><p>Raw summary statistics are transformed using two transformations. First, the raw summary statistics are brought closer to normality with one parameter (without shift) Box-Cox transformation applied independently to each statistic. Many of the proposed summary statistics are zero-inflated, which would make estimation of the parameter <inline-formula><mml:math id="inf87"><mml:mi>λ</mml:mi></mml:math></inline-formula> of the Box-Cox transformation unreliable. Because of this, fixed value <inline-formula><mml:math id="inf88"><mml:mi>λ</mml:mi><mml:mo>=</mml:mo><mml:mn>0.5</mml:mn></mml:math></inline-formula> is used. After the Box-Cox transformation, the summary statistics are centered and standardized to have unit variance. Second, the summary statistics are transformed with partial least squares (PLS) to produce orthogonal summary statistics while maximizing covariance with the parameters (<xref rid="bib52" ref-type="bibr">Wegmann et al., 2009</xref>). The PLS is applied to all of the simulated parameter values and datasets. If applied to a set of summary statistics of dimension <italic>k</italic>, the maximum number of transformed statistics is <italic>k-1</italic>. In the analyses we use dimensionality of 20, which is larger than the number of parameters, but still substantially lower than the number of original summary statistics. Finally, local linear regression adjustment is utilized for the parameters in the set of accepted values (<xref rid="bib2" ref-type="bibr">Beaumont et al., 2002</xref>). The parameter values are transformed based on the distances of the summary statistics to the summaries of the observed data.</p></sec><sec id="s4-5-6"><title>Summary statistics</title><p>We use the following raw summary statistics (36 in total):</p><list list-type="bullet"><list-item><p>Number of patches with infected plants.</p></list-item><list-item><p>Number of patches with coinfected plants.</p></list-item><list-item><p>Mean and standard deviation of pathogen population size categories.</p></list-item><list-item><p>Parameter estimates and standard deviation of residuals from linear regression of covariates against the pathogen population size category.</p></list-item><list-item><p>Mean and standard deviation of the disease prevalence categories.</p></list-item><list-item><p>Parameter estimates and standard deviation of residuals from linear regression of covariates against the disease prevalence category.</p></list-item><list-item><p>Parameter estimates and standard deviation of residuals from binomial regression of covariates against the number of infected plants in a patch.</p></list-item><list-item><p>Parameter estimates and standard deviation of residuals from binomial regression of covariates against the number of coinfected plants in a patch.</p></list-item><list-item><p>Parameter estimates and standard deviation of residuals from Poisson regression of covariates against the number of observed MLGs in a patch.</p></list-item></list></sec><sec id="s4-5-7"><title>Effect of the modeling assumptions</title><p>To assess the robustness of the results, we tested the effect that the modeling assumptions have on the posterior distributions of the parameters. Studying all aspects of the model is obviously not possible, but we chose two assumptions, namely the order <inline-formula><mml:math id="inf89"><mml:msub><mml:mrow><mml:mi>σ</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula> in which the mildew strains try to infect the plant, and the maximum number of strains in a patch <inline-formula><mml:math id="inf90"><mml:msub><mml:mrow><mml:mi>M</mml:mi></mml:mrow><mml:mrow><mml:mi>m</mml:mi><mml:mi>a</mml:mi><mml:mi>x</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula>.</p><p>We used three different distributions for the order <inline-formula><mml:math id="inf91"><mml:msub><mml:mrow><mml:mi>σ</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula>:</p><list list-type="order"><list-item><p>Uniform distribution among all permutations of <inline-formula><mml:math id="inf92"><mml:msub><mml:mrow><mml:mi>M</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula> items.</p></list-item><list-item><p>Fixed order based on decreasing <inline-formula><mml:math id="inf93"><mml:msub><mml:mrow><mml:mi>μ</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>k</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula>s, i.e. MLGs with highest prevalences being first to infect.</p></list-item><list-item><p>Simulate first <inline-formula><mml:math id="inf94"><mml:msub><mml:mrow><mml:mi>δ</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi></mml:mrow></mml:msub><mml:mo>=</mml:mo><mml:mfenced separators="|"><mml:mrow><mml:msub><mml:mrow><mml:mi>δ</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi><mml:mo>,</mml:mo><mml:mn>1</mml:mn></mml:mrow></mml:msub><mml:mo>,</mml:mo><mml:mo>…</mml:mo><mml:mo>,</mml:mo><mml:msub><mml:mrow><mml:mi>δ</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi><mml:mo>,</mml:mo><mml:msub><mml:mrow><mml:mi>M</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi></mml:mrow></mml:msub></mml:mrow></mml:msub></mml:mrow></mml:mfenced></mml:math></inline-formula> from Dirichlet distribution with parameters <inline-formula><mml:math id="inf95"><mml:mi>κ</mml:mi><mml:msup><mml:mrow><mml:mi mathvariant="normal">l</mml:mi><mml:mi mathvariant="normal">o</mml:mi><mml:mi mathvariant="normal">g</mml:mi><mml:mi mathvariant="normal">i</mml:mi><mml:mi mathvariant="normal">t</mml:mi></mml:mrow><mml:mrow><mml:mo>-</mml:mo><mml:mn>1</mml:mn></mml:mrow></mml:msup><mml:mfenced separators="|"><mml:mrow><mml:msub><mml:mrow><mml:mi>μ</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>k</mml:mi></mml:mrow></mml:msub></mml:mrow></mml:mfenced></mml:math></inline-formula> and choose the order based on decreasing values of <inline-formula><mml:math id="inf96"><mml:msub><mml:mrow><mml:mi>δ</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi><mml:mo>,</mml:mo><mml:mi>k</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula>.</p></list-item></list><p>The last distribution is intermediate between the first two, and the value of <inline-formula><mml:math id="inf97"><mml:mi>κ</mml:mi></mml:math></inline-formula> dictates how much the prevalences of individual MLGs affect the order. If <inline-formula><mml:math id="inf98"><mml:mi>κ</mml:mi></mml:math></inline-formula> is close to 0 then the distribution is close to uniform, and if <inline-formula><mml:math id="inf99"><mml:mi>κ</mml:mi></mml:math></inline-formula> goes to infinity the order is the same as second choice above. We use a value <inline-formula><mml:math id="inf100"><mml:mi>κ</mml:mi><mml:mo>=</mml:mo><mml:mn>5</mml:mn></mml:math></inline-formula> in the analyses.</p><p>We analyzed the year 2012 data four times with different assumptions. For the first three we used <inline-formula><mml:math id="inf101"><mml:msub><mml:mrow><mml:mi>M</mml:mi></mml:mrow><mml:mrow><mml:mi>m</mml:mi><mml:mi>a</mml:mi><mml:mi>x</mml:mi></mml:mrow></mml:msub><mml:mo>=</mml:mo><mml:mn>30</mml:mn></mml:math></inline-formula> and each of the distributions shown above for <inline-formula><mml:math id="inf102"><mml:msub><mml:mrow><mml:mi>σ</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula>. For the last one we set <inline-formula><mml:math id="inf103"><mml:msub><mml:mrow><mml:mi>M</mml:mi></mml:mrow><mml:mrow><mml:mi>m</mml:mi><mml:mi>a</mml:mi><mml:mi>x</mml:mi></mml:mrow></mml:msub><mml:mo>=</mml:mo><mml:mn>100</mml:mn></mml:math></inline-formula> and the uniform distribution for <inline-formula><mml:math id="inf104"><mml:msub><mml:mrow><mml:mi>σ</mml:mi></mml:mrow><mml:mrow><mml:mi>i</mml:mi><mml:mo>,</mml:mo><mml:mi>j</mml:mi></mml:mrow></mml:msub></mml:math></inline-formula>. In each analysis we performed 50,000 simulations and used 500 closest for the posterior.</p></sec><sec id="s4-5-8"><title>Accuracy of inference</title><p>As a measure of goodness of fit the root mean squared error (RMSE) was computed independently for each parameter. RMSE for a parameter <inline-formula><mml:math id="inf105"><mml:mi>θ</mml:mi></mml:math></inline-formula> is computed as<disp-formula id="equ16"><mml:math id="m16"><mml:mi>R</mml:mi><mml:mi>M</mml:mi><mml:mi>S</mml:mi><mml:mi>E</mml:mi><mml:mfenced separators="|"><mml:mrow><mml:mi>θ</mml:mi></mml:mrow><mml:mrow><mml:mi>A</mml:mi></mml:mrow></mml:mfenced><mml:mo>=</mml:mo><mml:msqrt><mml:mfrac><mml:mrow><mml:mn>1</mml:mn></mml:mrow><mml:mrow><mml:mi>N</mml:mi></mml:mrow></mml:mfrac><mml:mrow><mml:munder><mml:mo>∑</mml:mo><mml:mrow><mml:mi>j</mml:mi><mml:mo>∈</mml:mo><mml:mi>A</mml:mi></mml:mrow></mml:munder><mml:mrow><mml:msup><mml:mrow><mml:mfenced separators="|"><mml:mrow><mml:msub><mml:mrow><mml:mi>θ</mml:mi></mml:mrow><mml:mrow><mml:mi>j</mml:mi></mml:mrow></mml:msub><mml:mo>-</mml:mo><mml:msub><mml:mrow><mml:mi>θ</mml:mi></mml:mrow><mml:mrow><mml:mi>t</mml:mi></mml:mrow></mml:msub></mml:mrow></mml:mfenced></mml:mrow><mml:mrow><mml:mn>2</mml:mn></mml:mrow></mml:msup></mml:mrow></mml:mrow></mml:msqrt><mml:mo>,</mml:mo></mml:math></disp-formula></p></sec></sec><sec id="s4-6"><title>Data availability and repeatability of analysis</title><p>All data and scripts used to perform the analyses presented in this paper are available in the git repository at <ext-link ext-link-type="uri" xlink:href="https://github.com/ComputerBlue/FungalSex">https://github.com/ComputerBlue/FungalSex</ext-link> (<xref rid="bib26" ref-type="bibr">Laine, 2019</xref>; copy archived at <ext-link ext-link-type="uri" xlink:href="https://github.com/elifesciences-publications/FungalSex">https://github.com/elifesciences-publications/FungalSex</ext-link>).</p></sec></sec></body><back><sec sec-type="funding-information"><title>Funding Information</title><p>This paper was supported by the following grants:</p><list list-type="bullet"><list-item><p><funding-source><institution-wrap><institution-id institution-id-type="FundRef">http://dx.doi.org/10.13039/501100000781</institution-id><institution>European Research Council</institution></institution-wrap></funding-source><award-id>281517</award-id> to Anna-Liisa Laine.</p></list-item><list-item><p><funding-source><institution-wrap><institution-id institution-id-type="FundRef">http://dx.doi.org/10.13039/501100000781</institution-id><institution>European Research Council</institution></institution-wrap></funding-source><award-id>724508</award-id> to Anna-Liisa Laine.</p></list-item><list-item><p><funding-source><institution-wrap><institution-id institution-id-type="FundRef">http://dx.doi.org/10.13039/501100002341</institution-id><institution>Academy of Finland</institution></institution-wrap></funding-source><award-id>296686</award-id> to Anna-Liisa Laine.</p></list-item></list></sec><ack id="ack"><title>Acknowledgements</title><p>We would like to acknowledge the numerous students who have been involved in the survey and sampling of powdery mildew populations in the Åland Islands in 2012–15. K Raveala supervised the field surveys. B McDonald and T Giraud provided comments on an earlier version of the manuscript. Comments from K King, D Weigel, E Decaestecker and an anonymous reviewer during the review process helped significantly improve the manuscript. The DNA extractions and SNP genotyping were carried out at Institute of Biotechnology and Finnish Institute of Molecular Medicine at University of Helsinki, respectively. This work was funded by grants from the Academy of Finland (296686), Jane and Aatos Erkko Foundation, and the European Research Council (Starting Grant PATHEVOL 281517 and Consolidator Grant RESISTANCE 724508) to A-LL.</p></ack><sec id="s5" sec-type="additional-information"><title>Additional information</title><fn-group content-type="competing-interest"><title><bold>Competing interests</bold></title><fn fn-type="COI-statement" id="conf1"><p>No competing interests declared.</p></fn></fn-group><fn-group content-type="author-contribution"><title><bold>Author contributions</bold></title><fn fn-type="con" id="con1"><p>Conceptualization, Resources, Supervision, Funding acquisition, Writing—original draft.</p></fn><fn fn-type="con" id="con2"><p>Data curation, Methodology, BB oversaw the large-scale genotyping study.</p></fn><fn fn-type="con" id="con3"><p>Data curation, Formal analysis, Visualization, Methodology, Writing—original draft, EN carried out the spatial statistical analyses.</p></fn><fn fn-type="con" id="con4"><p>Software, Validation, Visualization, Methodology, Writing—original draft, JS implemented the Approximate Bayesian Computation model.</p></fn></fn-group></sec><sec id="s6" sec-type="supplementary-material"><title>Additional files</title><supplementary-material content-type="local-data" id="supp1"><object-id pub-id-type="doi">10.7554/eLife.47091.017</object-id><label>Supplementary file 1.</label><caption><title>Characteristics of the pathogen metapopulation for each year.</title><p>MLG: MultiLocus Genotype.</p></caption><media mime-subtype="docx" mimetype="application" xlink:href="elife-47091-supp1.docx" orientation="portrait" id="d35e4184" position="anchor"></media></supplementary-material><supplementary-material content-type="local-data" id="transrepform"><object-id pub-id-type="doi">10.7554/eLife.47091.018</object-id><label>Transparent reporting form</label><media mime-subtype="pdf" mimetype="application" xlink:href="elife-47091-transrepform.pdf" orientation="portrait" id="d35e4190" position="anchor"></media></supplementary-material></sec><sec id="s7" sec-type="data-availability"><title>Data availability</title><p>All data and scripts used to perform the analyses presented in this paper are available in the git repository at <ext-link ext-link-type="uri" xlink:href="https://github.com/ComputerBlue/FungalSex">https://github.com/ComputerBlue/FungalSex</ext-link> (copy archived at <ext-link ext-link-type="uri" xlink:href="https://github.com/elifesciences-publications/FungalSex">https://github.com/elifesciences-publications/FungalSex</ext-link>).</p><p>The following datasets were generated:</p></sec><ref-list><title>References</title><ref id="bib1"><element-citation publication-type="journal"><person-group 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Parasitology</source><volume>25</volume><fpage>236</fpage><lpage>244</lpage><pub-id pub-id-type="doi">10.1016/j.pt.2009.02.004</pub-id><pub-id pub-id-type="pmid">19356982</pub-id></element-citation></ref></ref-list></back><sub-article id="SA1" article-type="decision-letter"><front-stub><article-id pub-id-type="doi">10.7554/eLife.47091.020</article-id><title-group><article-title>Decision letter</article-title></title-group><contrib-group><contrib contrib-type="editor"><name><surname>King</surname><given-names>Kayla</given-names></name><role>Reviewing Editor</role><aff><institution>University of Oxford</institution><country>United Kingdom</country></aff></contrib><contrib contrib-type="reviewer"><name><surname>Decaestecker</surname><given-names>Ellen</given-names></name><role>Reviewer</role><aff><institution></institution></aff></contrib></contrib-group></front-stub><body><boxed-text position="float" orientation="portrait"><p>In the interests of transparency, eLife includes the editorial decision letter and accompanying author responses. A lightly edited version of the letter sent to the authors after peer review is shown, indicating the most substantive concerns; minor comments are not usually included.</p></boxed-text><p>Thank you for submitting your article "A direct ecological benefit of outcrossing in an obligate pathogen" for consideration by <italic>eLife</italic>. Your article has been reviewed by three peer reviewers, including Kayla King as guest Reviewing Editor, and the evaluation has been overseen by Detlef Weigel as the Senior Editor. The following individual involved in review of your submission has agreed to reveal their identity: Ellen Decaestecker (Reviewer #3).</p><p>The reviewers have discussed the reviews with one another and the Reviewing Editor has drafted this decision to help you prepare a revised submission.</p><p>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).</p><p>Summary:</p><p>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 <italic>Podosphaera plantaginis</italic>, which is an obligate pathogen of <italic>Plantago lanceolate</italic>, 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.</p><p>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.</p><p>Essential revisions:</p><p>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.</p><p>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.</p></body></sub-article><sub-article id="SA2" article-type="reply"><front-stub><article-id pub-id-type="doi">10.7554/eLife.47091.021</article-id><title-group><article-title>Author response</article-title></title-group></front-stub><body><disp-quote content-type="editor-comment"><p>Essential revisions:</p><p>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.</p></disp-quote><p>We thank the editors for this suggestions, and we have now completely re-written the first two paragraphs to provide a more concise theoretical framework for our study. We first outline the predictions and empirical support for the Red Queen Hypothesis in explaining the maintenance of sex in free-living hosts. We then clarify that coevolution should in fact be even more critical for maintaining outcrossing in parasite populations that need to adapt to their ever-changing host populations. We now cover the limited theoretical literature on the role of coevolution in maintaining sex in parasite populations (Introduction).</p><p>We also consider in more depth the fitness advantages of asexual vs. sexual strategies especially in facultatively sexual organisms where sexual offspring provide ecological functions such as dormancy and dispersal. We relate this to homothallic species where the same functions may be achieved via selfing or outcrossing but still outcrossing is frequently found (Introduction).</p><disp-quote content-type="editor-comment"><p>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.</p></disp-quote><p>We thank to the editors for this suggestion and agree that we had not provided an in depth consideration of the broader relevance of our findings. We’ve now added a new paragraph in the Discussion where we consider both the evolutionary and epidemiological implications of our findings for pathogens more generally.</p></body></sub-article></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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