Abstract
Symbiosis between insects and fungi arose multiple times during the evolution of both groups, and some of the most biologically diverse and economically important are mutualisms in which the insects cultivate and feed on fungi. Among these are bark beetles, whose ascomycetous cultivars are better known and studied than their frequently-overlooked and poorly understood basidiomycetous partners. In this study, we propose five new species of Entomocorticium, fungal mutualists in the Russulales (Basidiomycota) that are mutualistic symbionts of scolytine beetles. We have isolated these fungi from the beetle mycangia, which are structures adapted for the selective storage and transportation of fungal mutualists. Herein, we present the most complete phylogeny of the closely related genera Entomocorticium and Peniophora and provide insights into how an insect-associated taxon (Entomocorticium) evolved from within a wood-decaying, wind-dispersed lineage (Peniophora). Our results indicate that following a transition from angiosperms to gymnosperms, fungal domestication by beetles facilitated the evolution and diversification of Entomocorticium. We additionally propose four new species: Entomocorticium fibulatum Araújo, Li & Hulcr, sp. nov.; E. belizense Araújo, Li & Hulcr, sp. nov.; E. perryae Araújo, Li & Hulcr, sp. nov.; and E. macrovesiculatum Araújo, Li, Six & Hulcr, sp. nov. Our findings highlight the fact that insect-fungi associations remain an understudied field and that these associations harbor a large reservoir of novel fungal species.
Highlights
Several insect groups within ants, termites, wasps, and beetles have independently evolved mutualisms with a variety of fungal lineages that help them extract nutrients from wood, an otherwise intractable substrate [1,2,3]
To understand the species diversity and the evolutionary and ecological processes that led to the domestication of a wood-decaying fungal lineage by bark beetles, we built the most comprehensive phylogeny of the genera Peniophora (54 spp.) and Entomocorticium
Node A indicates the transition from angiosperms to gymnosperms and the origin of Entomocorticium, node B indicates fungal radiation following the association of Entomocorticium with bark beetles
Summary
Several insect groups within ants, termites, wasps, and beetles have independently evolved mutualisms with a variety of fungal lineages that help them extract nutrients from wood, an otherwise intractable substrate [1,2,3]. Insects are true fungus farmers, i.e., they inoculate their fungal symbionts into the substrate and cultivate them to feed their progeny, and the fungal symbionts have become domesticated crops [4,5] Many of these insect-cultivated fungi have evolved nutrient-provisioning adaptations and have become dependent on their partner insects for dispersal [4]. The most well-known fungi found living mutualistically with Scolytinae beetles are species within Ophiostomatales (Ascomycota) Because these are often targeted in surveys of bark beetle fungi, a dearth of knowledge exists on other potential fungal mutualists. Despite these previous investigations of symbiotic associations with D. frontalis, the diversity and evolutionary history of its most beneficial fungal associate—an Entomocorticium species (Russulaceae, Russulales, Basidiomycota)—remains obscure
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