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Global change is reshaping Earth's biodiversity, but the changing distributions of nonpathogenic fungi remain largely undocumented, as do mechanisms enabling invasions. The ectomycorrhizalAmanita phalloidesis native to Europe and invasive in North America. Using population genetics and genomics, we sought to describe the life history traits of this successfully invading symbiotic fungus.

To test whether death caps spread underground using hyphae, or aboveground using sexual spores, we mapped and genotyped mushrooms from European and US sites. Larger genetic individuals (genets) would suggest spread mediated by vegetative growth, while many small genets would suggest dispersal mediated by spores. To test whether genets are ephemeral or persistent, we also sampled from populations over time.

At nearly every site and across all time points, mushrooms resolve into small genets. Individuals frequently establish from sexual spores. But at one Californian site, a single individual measuring nearly 10 m across dominated. At two Californian sites, the same genetic individuals were discovered in 2004, 2014, and 2015, suggesting single individuals (both large and small) can reproduce repeatedly over relatively long timescales.

A flexible life history strategy combining both mycelial growth and spore dispersal appears to underpin the invasion of this deadly perennial ectomycorrhizal fungus.

 

Abstract By introducing novel capacities and functions, new genes and gene families may play a crucial role in ecological transitions. Mechanisms generating new gene families include de novo gene birth, horizontal gene transfer, and neofunctionalization following a duplication event. The ectomycorrhizal (ECM) symbiosis is a ubiquitous mutualism and the association has evolved repeatedly and independently many times among the fungi, but the evolutionary dynamics enabling its emergence remain elusive. We developed a phylogenetic workflow to first understand if gene families unique to ECM Amanita fungi and absent from closely related asymbiotic species are functionally relevant to the symbiosis, and then to systematically infer their origins. We identified 109 gene families unique to ECM Amanita species. Genes belonging to unique gene families are under strong purifying selection and are upregulated during symbiosis, compared with genes of conserved or orphan gene families. The origins of seven of the unique gene families are strongly supported as either de novo gene birth (two gene families), horizontal gene transfer (four), or gene duplication (one). An additional 34 families appear new because of their selective retention within symbiotic species. Among the 109 unique gene families, the most upregulated gene in symbiotic cultures encodes a 1-aminocyclopropane-1-carboxylate deaminase, an enzyme capable of downregulating the synthesis of the plant hormone ethylene, a common negative regulator of plant-microbial mutualisms. 

Plant‐associated microbial communities can profoundly affect plant health and success, and research is still uncovering factors driving the assembly of these communities. Here, we examine how geography versus host species affects microbial community structure and differential abundances of individual taxa. We use metabarcoding to characterize the bacteria and eukaryotes associated with five, often co‐occurring species ofSarraceniapitcher plants (Sarraceniaceae) and three natural hybrids along the longitudinal gradient of the U.S. Gulf Coast, as well as samples fromS.purpureain Massachusetts. To tease apart the effects of geography versus host species, we focus first on sites with co‐occurring species and then on species located across different sites. Our analyses show that bacterial and eukaryotic community structures are clearly and consistently influenced by host species identity, with geographic factors also playing a role. Naturally occurring hybrids appear to also host unique communities, which are in some ways intermediate between their parent species. We see significant effects of geography (site and longitude), but these generally explain less of the variation among pitcher communities. Overall, inSarraceniapitchers, host plant phenotype significantly affects the pitcher microbiomes and other associated organisms.

 

Most plants engage in symbioses with mycorrhizal fungi in soils and net consequences for plants vary widely from mutualism to parasitism. However, we lack a synthetic understanding of the evolutionary and ecological forces driving such variation for this or any other nutritional symbiosis. We used meta-analysis across 646 combinations of plants and fungi to show that evolutionary history explains substantially more variation in plant responses to mycorrhizal fungi than the ecological factors included in this study, such as nutrient fertilization and additional microbes. Evolutionary history also has a different influence on outcomes of ectomycorrhizal versus arbuscular mycorrhizal symbioses; the former are best explained by the multiple evolutionary origins of ectomycorrhizal lifestyle in plants, while the latter are best explained by recent diversification in plants; both are also explained by evolution of specificity between plants and fungi. These results provide the foundation for a synthetic framework to predict the outcomes of nutritional mutualisms.

 

Despite host‐fungal symbiotic interactions being ubiquitous in all ecosystems, understanding how symbiosis has shaped the ecology and evolution of fungal spores that are involved in dispersal and colonization of their hosts has been ignored in life‐history studies. We assembled a spore morphology database covering over 26,000 species of free‐living to symbiotic fungi of plants, insects and humans and found more than eight orders of variation in spore size. Evolutionary transitions in symbiotic status correlated with shifts in spore size, but the strength of this effect varied widely among phyla. Symbiotic status explained more variation than climatic variables in the current distribution of spore sizes of plant‐associated fungi at a global scale while the dispersal potential of their spores is more restricted compared to free‐living fungi. Our work advances life‐history theory by highlighting how the interaction between symbiosis and offspring morphology shapes the reproductive and dispersal strategies among living forms.