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A selective fungal transport organ (mycangium) maintains coarse phylogenetic congruence between fungus-farming ambrosia beetles and their symbionts.

ABSTRACT: Thousands of species of ambrosia beetles excavate tunnels in wood to farm fungi. They maintain associations with particular lineages of fungi, but the phylogenetic extent and mechanisms of fidelity are unknown. We test the hypothesis that selectivity of their mycangium enforces fidelity at coarse phylogenetic scales, while permitting promiscuity among closely related fungal mutualists. We confirm a single evolutionary origin of the Xylosandrus complex-a group of several xyleborine genera that farm fungi in the genus Ambrosiella. Multi-level co-phylogenetic analysis revealed frequent symbiont switching within major Ambrosiella clades, but not between clades. The loss of the mycangium in Diuncus, a genus of evolutionary cheaters, was commensurate with the loss of fidelity to fungal clades, supporting the hypothesis that the mycangium reinforces fidelity. Finally, in vivo experiments tracked symbiotic compatibility throughout the symbiotic life cycle of Xylosandrus compactus and demonstrated that closely related Ambrosiella symbionts are interchangeable, but the probability of fungal uptake in the mycangium was significantly lower in more phylogenetically distant species of symbionts. Symbiont loads in experimental subjects were similar to wild-caught beetles. We conclude that partner choice in ambrosia beetles is achieved in the mycangium, and co-phylogenetic inferences can be used to predict the likelihood of specific symbiont switches.

SUBMITTER: Skelton J

PROVIDER: S-EPMC6367168 | biostudies-literature | 2019 Jan

REPOSITORIES: biostudies-literature

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A selective fungal transport organ (mycangium) maintains coarse phylogenetic congruence between fungus-farming ambrosia beetles and their symbionts.

Skelton James J Johnson Andrew J AJ Jusino Michelle A MA Bateman Craig C CC Li You Y Hulcr Jiri J

Proceedings. Biological sciences 20190101 1894

Thousands of species of ambrosia beetles excavate tunnels in wood to farm fungi. They maintain associations with particular lineages of fungi, but the phylogenetic extent and mechanisms of fidelity are unknown. We test the hypothesis that selectivity of their mycangium enforces fidelity at coarse phylogenetic scales, while permitting promiscuity among closely related fungal mutualists. We confirm a single evolutionary origin of the Xylosandrus complex-a group of several xyleborine genera that fa ...[more]

PMID: 30963860

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Project description:UNLABELLED: INTRODUCTION:In wood-dwelling fungus-farming weevils, the so-called ambrosia beetles (Curculionidae: Scolytinae and Platypodinae), wood in the excavated tunnels is used as a medium for cultivating fungi by the combined action of digging larvae (which create more space for the fungi to grow) and of adults sowing and pruning the fungus. The beetles are obligately dependent on the fungus that provides essential vitamins, amino acids and sterols. However, to what extent microbial enzymes support fungus farming in ambrosia beetles is unknown. Here we measure (i) 13 plant cell-wall degrading enzymes in the fungus garden microbial consortium of the ambrosia beetle Xyleborinus saxesenii, including its primary fungal symbionts, in three compartments of laboratory maintained nests, at different time points after gallery foundation and (ii) four specific enzymes that may be either insect or microbially derived in X. saxesenii adult and larval individuals. RESULTS:We discovered that the activity of cellulases in ambrosia fungus gardens is relatively small compared to the activities of other cellulolytic enzymes. Enzyme activity in all compartments of the garden was mainly directed towards hemicellulose carbohydrates such as xylan, glucomannan and callose. Hemicellulolytic enzyme activity within the brood chamber increased with gallery age, whereas irrespective of the age of the gallery, the highest overall enzyme activity were detected in the gallery dump material expelled by the beetles. Interestingly endo-?-1,3(4)-glucanase activity capable of callose degradation was identified in whole-body extracts of both larvae and adult X. saxesenii, whereas endo-?-1,4-xylanase activity was exclusively detected in larvae. CONCLUSION:Similar to closely related fungi associated with bark beetles in phloem, the microbial symbionts of ambrosia beetles hardly degrade cellulose. Instead, their enzyme activity is directed mainly towards comparatively more easily accessible hemicellulose components of the ray-parenchyma cells in the wood xylem. Furthermore, the detection of xylanolytic enzymes exclusively in larvae (which feed on fungus colonized wood) and not in adults (which feed only on fungi) indicates that only larvae (pre-) digest plant cell wall structures. This implies that in X. saxesenii and likely also in many other ambrosia beetles, adults and larvae do not compete for the same food within their nests - in contrast, larvae increase colony fitness by facilitating enzymatic wood degradation and fungus cultivation.

Project description:Bark beetles (sensu lato) colonize woody tissues like phloem or xylem and are associated with a broad range of micro-organisms. Specific fungi in the ascomycete orders Hypocreales, Microascales and Ophistomatales as well as the basidiomycete Russulales have been found to be of high importance for successful tree colonization and reproduction in many species. While fungal mutualisms are facultative for most phloem-colonizing bark beetles (sensu stricto), xylem-colonizing ambrosia beetles are long known to obligatorily depend on mutualistic fungi for nutrition of adults and larvae. Recently, a defensive role of fungal mutualists for their ambrosia beetle hosts was revealed: Few tested mutualists outcompeted other beetle-antagonistic fungi by their ability to produce, detoxify and metabolize ethanol, which is naturally occurring in stressed and/or dying trees that many ambrosia beetle species preferentially colonize. Here, we aim to test (i) how widespread beneficial effects of ethanol are among the independently evolved lineages of ambrosia beetle fungal mutualists and (ii) whether it is also present in common fungal symbionts of two bark beetle species (Ips typographus, Dendroctonus ponderosae) and some general fungal antagonists of bark and ambrosia beetle species. The majority of mutualistic ambrosia beetle fungi tested benefited (or at least were not harmed) by the presence of ethanol in terms of growth parameters (e.g., biomass), whereas fungal antagonists were inhibited. This confirms the competitive advantage of nutritional mutualists in the beetle's preferred, ethanol-containing host material. Even though most bark beetle fungi are found in the same phylogenetic lineages and ancestral to the ambrosia beetle (sensu stricto) fungi, most of them were highly negatively affected by ethanol and only a nutritional mutualist of Dendroctonus ponderosae benefited, however. This suggests that ethanol tolerance is a derived trait in nutritional fungal mutualists, particularly in ambrosia beetles that show cooperative farming of their fungi.

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A selective fungal transport organ (mycangium) maintains coarse phylogenetic congruence between fungus-farming ambrosia beetles and their symbionts.

Publications

A selective fungal transport organ (mycangium) maintains coarse phylogenetic congruence between fungus-farming ambrosia beetles and their symbionts.

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