Abstract
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.
Highlights
Filamentous fungi are generally known to be common symbionts of bark and ambrosia beetles (Curculionidae: Scolytinae and Platypodinae)
In the Opiostomatales, the non-beetle-associated, endophyte Esteya vermicola (p = 0.008, Figure 2c) clearly showed pattern I while there was no significant increase in biomass but a general tolerance toward ethanol for the two nutritional mutualists of the ambrosia beetle Xyleborinus saxesenii, Raffaelea sulphurea (p = 0.65, Figure 2a) and R. canadensis (p = 0.35, Supplementary Figure 1B)
Our findings showed that the examined obligate and nutritional ambrosia beetle mutualists (A. hartigii, R. canadensis, R. sulphurea) as well as the obligate and nutritional bark beetle mutualist (E. dendroctoni) benefit or at least are not harmed (F. euwallaceae) by the presence of low (1–2%) concentrations of ethanol
Summary
Filamentous fungi are generally known to be common symbionts of bark and ambrosia beetles (Curculionidae: Scolytinae and Platypodinae). The most famous nutritional mutualisms are those between xylemcolonizing ambrosia beetles and various “ambrosia fungus” species in the ascomycete orders Hypocreales, Microascales and Ophiostomatales as well as phloem-colonizing Dendroctonus bark beetles and their basidiomycete and ascomycete mutualists in the orders Russulales and Ophiostomatales (Barras and Perry, 1972; Six and Paine, 1998; Six and Klepzig, 2004; Harrington, 2005; Kirkendall et al, 2015; Biedermann and Vega, 2020). These mutualisms are unique for beetles and comparable to the advanced fungi culturing systems of attine ants and fungusfarming termites (Farrell et al, 2001; Six, 2003; Müller et al, 2005; Biedermann and Vega, 2020)
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