Purifying selection after episodes of recurrent adaptive diversification in fungal pathogens

Gladieux, Pierre; Devier, Benjamin; Aguileta, Gabriela; Cruaud, Corinne; Giraud, Tatiana

doi:10.1016/j.meegid.2013.03.012

Cited by 15 publications

(15 citation statements)

References 58 publications

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“…The admixed barplots observed in the microsatellite structure analyses must therefore have been due to low power of assignment rather than recent hybridization. This result was consistent with previous studies on several other anther‐smut fungi, in which no hybrids were detected in natural populations, even between very closely related species that can hybridize in the laboratory (Abbate et al, 2018; Badouin et al, 2017; Gladieux et al, 2013; Petit et al, 2017). The only case where hybrids were detected was among closely related anther‐smut fungi with overlapping host and geographical ranges, on Dianthus species (Petit et al, 2017).…”

Section: Discussionsupporting

confidence: 92%

Congruent population genetic structures and divergence histories in anther‐smut fungi and their host plants Silene italica and the Silene nutans species complex

et al. 2020

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Study of the congruence of population genetic structure between hosts and pathogens gives important insights into their shared phylogeographical and coevolutionary histories. We studied the population genetic structure of castrating anther‐smut fungi (genus Microbotryum) and of their host plants, the Silene nutans species complex, and the morphologically and genetically closely related Silene italica, which can be found in sympatry. Phylogeographical population genetic structure related to persistence in separate glacial refugia has been recently revealed in the S. nutans plant species complex across Western Europe, identifying several distinct lineages. We genotyped 171 associated plant–pathogen pairs of anther‐smut fungi and their host plant individuals using microsatellite markers and plant chloroplastic single nucleotide polymorphisms. We found clear differentiation between fungal populations parasitizing S. nutans and S. italica plants. The population genetic structure of fungal strains parasitizing the S. nutans plant species complex mirrored the host plant genetic structure, suggesting that the pathogen was isolated in glacial refugia together with its host and/or that it has specialized on the plant genetic lineages. Using random forest approximate Bayesian computation (ABC‐RF), we found that the divergence history of the fungal lineages on S. nutans was congruent with that previously inferred for the host plant and probably occurred with ancient but no recent gene flow. Genome sequences confirmed the genetic structure and the absence of recent gene flow between fungal genetic lineages. Our analyses of individual host–pathogen pairs contribute to a better understanding of co‐evolutionary histories between hosts and pathogens in natural ecosystems, in which such studies remain scarce.

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Section: Discussionsupporting

confidence: 92%

Congruent population genetic structures and divergence histories in anther‐smut fungi and their host plants Silene italica and the Silene nutans species complex

et al. 2020

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“…Interestingly, most of the genes that have been through episodes of adaptive diversification between Microbotryum species specialized on different hosts appeared to have subsequently evolved under strong functional constraints in the lineages remaining specialized on a given host plant (Gladieux et al . ), indicating they are not involved in the arms race against their host.…”

Section: Genetic Bases Of Adaptation: Within‐species Changesmentioning

confidence: 99%

Fungal evolutionary genomics provides insight into the mechanisms of adaptive divergence in eukaryotes

et al. 2014

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Fungi are ideal model organisms for dissecting the genomic bases of adaptive divergence in eukaryotes. They have simple morphologies and small genomes, occupy contrasting, well-identified ecological niches and tend to have short generation times, and many are amenable to experimental approaches. Fungi also display diverse lifestyles, from saprotrophs to pathogens or mutualists, and they play extremely important roles in both ecosystems and human activities, as wood decayers, mycorrhizal fungi, lichens, endophytes, plant and animal pathogens, and in fermentation or drug production. We review here recent insights into the patterns and mechanisms of adaptive divergence in fungi, including sources of divergence, genomic variation and, ultimately, speciation. We outline the various ecological sources of divergent selection and genomic changes, showing that gene loss and changes in gene expression and in genomic architecture are important adaptation processes, in addition to the more widely recognized processes of amino acid substitution and gene duplication. We also review recent findings regarding the interspecific acquisition of genomic variation and suggesting an important role for introgression, hybridization and horizontal gene transfers (HGTs). We show that transposable elements can mediate several of these genomic changes, thus constituting important factors for adaptation. Finally, we review the consequences of divergent selection in terms of speciation, arguing that genetic incompatibilities may not be as widespread as generally thought and that pleiotropy between adaptation and reproductive isolation is an important route of speciation in fungal pathogens.

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“…Previous studies on the population genetics of M. lychnidis‐dioicae provided one of the most clear‐cut examples of phylogeographic structure in pathogens (Vercken et al ., ; Gladieux et al ., , ; Fontaine et al ., ). Clustering analyses revealed the existence of three main genetically distinct groups within M. lychnidis‐dioicae , with distributions strikingly similar to the major intraspecific lineages identified in Europe for many temperate plant and animal species (Hewitt, ).…”

Section: Introductionmentioning

confidence: 99%

Strong phylogeographic co‐structure between the anther‐smut fungus and its white campion host

et al. 2016

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Although congruence between host and pathogen phylogenies has been extensively investigated, the congruence between host and pathogen genetic structures at the within-species level has received little attention. Using an unprecedented and comprehensive collection of associated plant-pathogen samples, we investigated the degree of congruence between the genetic structures across Europe of two evolutionary and ecological model organisms, the anther-smut pathogen Microbotryum lychnidis-dioicae and its host plant Silene latifolia. We demonstrated a significant and particularly strong level of host-pathogen co-structure, with three main genetic clusters displaying highly similar spatial ranges in Western Europe, Eastern Europe and Italy, respectively. Correcting for the geographical component of genetic variation, significant correlations were still found between the genetic distances of anther-smut and host populations. Inoculation experiments suggested plant local adaptation, at the cluster level, for resistance to pathogens. These findings indicate that the pathogen remained isolated in the same fragmented southern refugia as its host plant during the last glaciation, and that little long-distance dispersal has occurred since the recolonization of Europe for either the plant or the pathogen, despite their known ability to travel across continents. This, together with the inoculation results, suggests that coevolutionary and competitive processes may be drivers of host-pathogen co-structure.

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Purifying selection after episodes of recurrent adaptive diversification in fungal pathogens

Cited by 15 publications

References 58 publications

Congruent population genetic structures and divergence histories in anther‐smut fungi and their host plants Silene italica and the Silene nutans species complex

Congruent population genetic structures and divergence histories in anther‐smut fungi and their host plants Silene italica and the Silene nutans species complex

Fungal evolutionary genomics provides insight into the mechanisms of adaptive divergence in eukaryotes

Strong phylogeographic co‐structure between the anther‐smut fungus and its white campion host

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