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Many fungi have been domesticated for food production, with genetic differentiation between populations from food and wild environments, and food populations often acquiring beneficial traits through horizontal gene transfers. We studied the population structures and phenotypes of two distantly related Penicillium species used for dry-cured meat production, P. nalgiovense , the most common species in the dry-cured meat food industry, and P. salamii , used locally by farms. Both species displayed low genetic diversity, with no differentiation between strains isolated from dry-cured meat and those from other environments. Nevertheless, the strains collected from dry-cured meat within each species displayed slower proteolysis and lipolysis than their wild-type conspecifics, and those of P. nalgiovense were whiter. Phenotypically, the non-dry-cured meat strains were more similar to their sister species than to their conspecific dry-cured meat strains, indicating an evolution of specific phenotypes in dry-cured meat strains. A comparison of available Penicillium genomes from various environments revealed evidence of multiple horizontal gene transfers, particularly between P. nalgiovense and P. salamii . Some horizontal gene transfers involving P. biforme , also found in dry-cured meat products, were also detected. We also detected positive and purifying selection based on amino-acid changes. Our genetic and phenotypic findings suggest that human selection has shaped the P. salamii and P. nalgiovense populations used for dry-cured meat production, which constitutes domestication. Several genetic and phenotypic changes were similar in P. salamii , P. nalgiovense, and P. biforme , providing an interesting case of convergent adaptation to the same human-made environment.Many fungi have been domesticated for food production, with genetic differentiation between populations from food and wild environments, and food populations often acquiring beneficial traits through horizontal gene transfers. We studied the population structures and phenotypes of two distantly related Penicillium species used for dry-cured meat production, P. nalgiovense , the most common species in the dry-cured meat food industry, and P. salamii , used locally by farms. Both species displayed low genetic diversity, with no differentiation between strains isolated from dry-cured meat and those from other environments. Nevertheless, the strains collected from dry-cured meat within each species displayed slower proteolysis and lipolysis than their wild-type conspecifics, and those of P. nalgiovense were whiter. Phenotypically, the non-dry-cured meat strains were more similar to their sister species than to their conspecific dry-cured meat strains, indicating an evolution of specific phenotypes in dry-cured meat strains. A comparison of available Penicillium genomes from various environments revealed evidence of multiple horizontal gene transfers, particularly between P. nalgiovense and P. salamii . Some horizontal gene transfers involving P. biforme , also found in dry-cured meat products, were also detected. We also detected positive and purifying selection based on amino-acid changes. Our genetic and phenotypic findings suggest that human selection has shaped the P. salamii and P. nalgiovense populations used for dry-cured meat production, which constitutes domestication. Several genetic and phenotypic changes were similar in P. salamii , P. nalgiovense, and P. biforme , providing an interesting case of convergent adaptation to the same human-made environment.

Sex chromosomes often carry large nonrecombining regions that can extend progressively over time, generating evolutionary strata of sequence divergence. However, some sex chromosomes display an incomplete suppression of recombination. Large genomic regions without recombination and evolutionary strata have also been documented around fungal mating-type loci, but have been studied in only a few fungal systems. In the model fungus Podospora anserina (Ascomycota, Sordariomycetes), the reference S strain lacks recombination across a 0.8-Mb region around the mating-type locus. The lack of recombination in this region ensures that nuclei of opposite mating types are packaged into a single ascospore (pseudohomothallic lifecycle). We found evidence for a lack of recombination around the mating-type locus in the genomes of ten P. anserina strains and six closely related pseudohomothallic Podospora species. Importantly, the size of the nonrecombining region differed between strains and species, as indicated by the heterozygosity levels around the mating-type locus and experimental selfing. The nonrecombining region is probably labile and polymorphic, differing in size and precise location within and between species, resulting in occasional, but infrequent, recombination at a given base pair. This view is also supported by the low divergence between mating types, and the lack of strong linkage disequilibrium, chromosomal rearrangements, transspecific polymorphism and genomic degeneration. We found a pattern suggestive of evolutionary strata in P. pseudocomata. The observed heterozygosity levels indicate low but nonnull outcrossing rates in nature in these pseudohomothallic fungi. This study adds to our understanding of mating-type chromosome evolution and its relationship to mating systems.

The study of population genetic structure congruence between hosts and pathogens gives important insights into their shared phylogeographic and coevolutionary histories. We studied the population genetic structure of castrating anther-smut fungi (Microbotryumgenus) and of their host plants, theSilene nutansspecies complex, and the morphologically and genetically closeS. italica,which can be found in sympatry. Phylogeographic population genetic structure related to persistence in separate glacial refugia has been recently revealed in theS. nutansplant 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 SNPs. We found clear differentiation between fungal populations parasitizingS. nutansandS. italicaplants. The population genetic structure of fungal strains parasitizing theS. nutansplant 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 onS. nutanswas congruent with the one previously inferred for the host plant and likely 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 host-pathogen individual pairs contribute to a better understanding of co-evolutionary histories between hosts and pathogens in natural ecosystems, in which such studies are still scarce.

SummaryDomestication involves recent adaptation under strong human selection and rapid diversification, and therefore constitutes a good model for studies of these processes. We studied the domestication of the emblematic white moldPenicillium camemberti, used for the maturation of soft cheeses, such as Camembert and Brie, about which surprisingly little was known, despite its economic and cultural importance. Whole genome-based analyses of genetic relationships and diversity revealed that an ancient domestication event led to the emergence of the gray-greenP. biformemold used in cheese-making, by divergence from the blue-green wildP. fuscoglaucumfungus. Another much more recent domestication event led to the generation of theP. camemberticlonal lineage as a sister group toP. biforme. Penicillium biformedisplayed signs of phenotypic adaptation to cheese-making relative toP. fuscoglaucum, in terms of whiter color, faster growth on cheese medium under cave conditions, lower levels of toxin production and greater ability to prevent the growth of other fungi. TheP. camembertilineage displayed even stronger signs of domestication for all these phenotypic features. We also identified two differentiatedP. camembertivarieties, apparently associated with different kinds of cheeses, and with contrasted phenotypic features in terms of color, growth, toxin production and competitive ability. We have, thus, identified footprints of domestication in these fungi, with genetic differentiation between cheese and wild populations, bottlenecks and specific phenotypic traits beneficial for cheese-making. This study has not only fundamental implications for our understanding of domestication but can also have important impacts on cheese-making.

Domestication involves recent adaptation under strong human selection and rapid diversification, and therefore constitutes a good model for studies of these processes. We studied the domestication of the emblematic white mold Penicillium camemberti, used for the maturation of soft cheeses, such as Camembert and Brie, about which surprisingly little was known, despite its economic and cultural importance. Whole genome-based analyses of genetic relationships and diversity revealed that an ancient domestication event led to the emergence of the gray-green P. biforme mold used in cheese-making, from the blue-green wild P. fuscoglaucum fungus. Another much more recent domestication event led to the generation of the P. camemberti clonal lineage from P. biforme. Both these domestication events were associated with strong bottlenecks. Penicillium biforme displayed signs of phenotypic adaptation to cheese-making relative to P. fuscoglaucum, in terms of its whiter color, faster growth on cheese medium under cave conditions, lower levels of toxin production and greater ability to prevent the growth of other fungi. The P. camemberti lineage displayed even stronger signs of domestication for all these phenotypic features. We also identified two differentiated P. camemberti lineages linked to different kinds of cheeses with contrasted phenotypic features in terms of color, growth, toxin production and competitive ability. We have, thus, identified footprints of domestication in these fungi, with genetic differentiation between cheese and wild strains and specific phenotypic traits beneficial for cheese-making. This study has not only fundamental implications for our understanding of domestication but can also have important impacts on cheese-making.

Domestication provides an excellent framework for studying adaptive divergence. Using population genomics and phenotypic assays, we reconstructed the domestication history of the blue cheese mould Penicillium roqueforti. We showed that this fungus was domesticated twice independently. The population used in Roquefort originated from an old domestication event associated with weak bottlenecks and exhibited traits beneficial for pre‐industrial cheese production (slower growth in cheese and greater spore production on bread, the traditional multiplication medium). The other cheese population originated more recently from the selection of a single clonal lineage, was associated with all types of blue cheese worldwide except Roquefort, and displayed phenotypes more suited for industrial cheese production (high lipolytic activity, efficient cheese cavity colonization ability and salt tolerance). We detected genomic regions affected by recent positive selection and putative horizontal gene transfers. This study sheds light on the processes of rapid adaptation and raises questions about genetic resource conservation., see also the Perspective by Brigida Gallone, Jan Steensels and Kevin J. Verstrepen.

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.

Convergent adaptation provides unique insights into the predictability of evolution and ultimately into processes of biological diversification. Supergenes (beneficial gene linkage) are striking examples of adaptation, but little is known about their prevalence or evolution. A recent study on anther-smut fungi documented supergene formation by rearrangements linking two key mating-type loci, controlling pre- and post-mating compatibility. Here further high-quality genome assemblies reveal four additional independent cases of chromosomal rearrangements leading to regions of suppressed recombination linking these mating-type loci in closely related species. Such convergent transitions in genomic architecture of mating-type determination indicate strong selection favoring linkage of mating-type loci into cosegregating supergenes. We find independent evolutionary strata (stepwise recombination suppression) in several species, with extensive rearrangements, gene losses, and transposable element accumulation. We thus show remarkable convergence in mating-type chromosome evolution, recurrent supergene formation, and repeated evolution of similar phenotypes through different genomic changes., Supergenes result from beneficial linkage and recombination suppression between two or more genes. Giraud and colleagues use whole genome sequencing data to show convergent evolution of supergenes on mating-type chromosomes in multiple closely-related fungal lineages.

The family Ammotheidae is the most diversified group of the class Pycnogonida, with 297 species described in 20 genera. Its monophyly and intergeneric relationships have been highly debated in previous studies. Here, we investigated the phylogeny of Ammotheidae using specimens from poorly studied areas. We sequenced the mitochondrial gene encoding the first subunit of cytochrome c oxidase (CO1) from 104 specimens. The complete nuclear 18S rRNA gene was sequenced from a selection of 80 taxa to provide further phylogenetic signal. The base composition in CO1 shows a higher heterogeneity in Ammotheidae than in other families, which may explain their apparent polyphyly in the CO1 tree. Although deeper nodes of the tree receive no statistical support, Ammotheidae was found to be monophyletic and divided into two clades, here defined as distinct subfamilies: Achelinae comprises the genera Achelia Hodge, 1864, Ammothella Verrill, 1900, Nymphopsis Haswell, 1884 and Tanystylum Miers, 1879; and Ammotheinae includes the genera Ammothea Leach, 1814, Acheliana Arnaud, 1971, Cilunculus Loman, 1908, Sericosura Fry & Hedgpeth, 1969 and also Teratonotum gen. nov., including so far only the type species Ammothella stauromata Child, 1982. The species Cilunculus gracilis Nakamura & Child, 1991 is reassigned to Ammothella , forming the binomen Ammothella gracilis (Nakamura & Child, 1991) comb. nov. Additional taxonomic re-arrangements are suggested for the genera Achelia , Acheliana , Ammothella and Cilunculus .

International audience; Background: Anther-smut fungi belonging to the genus Microbotryum sterilize their host plants by aborting ovaries and replacing pollen by fungal spores. Sibling Microbotryum species are highly specialized on their host plants and they have been widely used as models for studies of ecology and evolution of plant pathogenic fungi. However, most studies have focused, so far, on M. lychnidis-dioicae that parasitizes the white campion Silene latifolia. Microbotryum saponariae, parasitizing mainly Saponaria officinalis, is an interesting anther-smut fungus, since it belongs to a tetrapolar lineage (i.e., with two independently segregating mating-type loci), while most of the anther-smut Microbotryum fungi are bipolar (i.e., with a single mating-type locus). Saponaria officinalis is a widespread long-lived perennial plant species with multiple flowering stems, which makes its anther-smut pathogen a good model for studying phylogeography and within-host multiple infections.Principal Findings: Here, based on a generated genome sequence of M. saponariae we developed 6 multiplexes with a total of 22 polymorphic microsatellite markers using an inexpensive and efficient method. We scored these markers in fungal individuals collected from 97 populations across Europe, and found that the number of their alleles ranged from 2 to 11, and their expected heterozygosity from 0.01 to 0.58. Cross-species amplification was examined using nine other Microbotryum species parasitizing hosts belonging to Silene, Dianthus and Knautia genera.All loci were successfully amplified in at least two other Microbotryum species.Significance: These newly developed markers will provide insights into the population genetic structure and the occurrence of within-host multiple infections of M. saponariae. In addition, the draft genome of M. saponariae, as well as one of the described markers will be useful resourcesfor studying the evolution of the breeding systems in the genus Microbotryum and the evolution of specialization onto different plant species.

International audience; Nuclear disasters at Chernobyl and Fukushima provide examples of effects of acute ionizing radiation on mutations that can affect the fitness and distribution of species. Here, we investigated the prevalence of Microbotryum lychnidis-dioicae, a pollinator-transmitted fungal pathogen of plants causing anther-smut disease in Chernobyl, its viability, fertility and karyotype variation, and the accumulation of nonsynonymous mutations in its genome. We collected diseased flowers of Silene latifolia from locations ranging by more than two orders of magnitude in background radiation, from 0.05 to 21.03 lGy/h. Disease prevalence decreased significantly with increasing radiation level, possibly due to lower pollinator abundance and altered pollinator behaviour. Viability and fertility, measured as the budding rate of haploid sporidia following meiosis from the diploid teliospores, did not vary with increasing radiation levels and neither did karyotype overall structure and level of chromosomal size heterozygosity. We sequenced the genomes of twelve samples from Chernobyl and of four samples collected from uncontaminated areas and analysed alignments of 6068 predicted genes, corresponding to 1.04 3 10 7 base pairs. We found no dose-dependent differences in substitution rates (neither dN, dS, nor dN/dS). Thus, we found no significant evidence of increased deleterious mutation rates at higher levels of background radiation in this plant pathogen. We even found lower levels of nonsynonymous substitution rates in contaminated areas compared to control regions, suggesting that purifying selection was stronger in contaminated than uncontaminated areas. We briefly discuss the possibilities for a mechanistic basis of radio resistance in this nonmelanized fungus.

Although most chitons (Mollusca: Polyplacophora) are shallow-water molluscs, diverse species also occur in deep-sea habitats. We investigated the feeding strategies of two species, Leptochiton boucheti and Nierstraszella lineata, recovered on sunken wood sampled in the western Pacific, close to the Vanuatu Islands. The two species display distinctly different associations with bacterial partners. Leptochiton boucheti harbours Mollicutes in regions of its gut epithelium and has no abundant bacterium associated with its gill. Nierstraszella lineata displays no dense gut-associated bacteria, but harbours bacterial filaments attached to its gill epithelium, related to the Deltaproteobacteria symbionts found in gills of the wood-eating limpet Pectinodonta sp. Stable carbon and nitrogen isotope signatures and an absence of cellulolytic activity give evidence against a direct wood-feeding diet; both species are secondary consumers within the wood food web. We suggest that the distinct associations with bacterial partners are linked to niche specialisations of the two species. Nierstraszella lineata is in a taxonomic family restricted to sunken wood and is possibly adapted to more anoxic conditions thanks to its gill-associated bacteria. Leptochiton boucheti is phylogenetically more proximate to an ancestral form not specialised on wood and may itself be more of a generalist; this observation is congruent with its association with Mollicutes, a bacterial clade comprising gut-associated bacteria occurring in several metazoan phyla.