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Title: Inordinate fondness for alcohol benefits fungus-farming by ambrosia beetles

Author
item Ranger, Christopher
item BIEDERMANN, PETER - Max Planck Institute Of Chemical Ecology
item PHUNTUMART, VIPAPORN - Bowling Green State University
item BENZ, Y - Technical University Of Munich
item BELIGALA, GAYATHRI - Bowling Green State University
item GHOSH, SATYAKI - Bowling Green State University
item Palmquist, Debra
item MUELLER, ROBERT - Western Sydney University
item Barnett, Jenny
item SCHULTZ, PETER - Virginia Polytechnic Institution & State University
item Reding, Michael - Mike

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/14/2018
Publication Date: 4/24/2018
Citation: Ranger, C.M., Biedermann, P., Phuntumart, V., Benz, Y.P., Beligala, G.U., Ghosh, S., Palmquist, D.E., Mueller, R., Barnett, J.L., Schultz, P., Reding, M.E. 2018. Inordinate fondness for alcohol benefits fungus-farming by ambrosia beetles. Proceedings of the National Academy of Sciences. 115:4447-4452.

Interpretive Summary: Ambrosia beetles are among the true fungus farming insects, whereby they tunnel into trees to sow fungal gardens on which the adults and larvae must feed for nourishment. After invading new habitats, some aggressive species destructively attack living but weakened trees growing in horticultural, ornamental, and forested settings. Many species of ambrosia beetles are strongly attracted to ethanol, which is emitted from trees in response to a variety of physiological stressors. Adult female beetles typically tunnel into stem tissues containing ethanol to farm their symbiotic fungi, which seems counterproductive since ethanol is a potent antimicrobial agent that inhibits the growth of various fungi, yeasts, and bacteria. Our results are the first demonstration that ambrosia beetles rely on ethanol for reproduction because it benefits fungus farming by promoting growth of their fungal gardens while inhibiting growth of “weedy” fungal competitors. In particular, more than 300 attacks by Xylosandrus germanus and other species were triggered by baiting trees with ethanol lures, but none of the foundresses produced offspring unless tree tissues contained in vivo ethanol resulting from irrigating with ethanol solutions. More X. germanus brood were also produced in a rearing substrate containing ethanol. These benefits are a result of increased food supply via the positive effects of ethanol on food-fungus biomass combined with oviposition being delayed until fungal gardens are flourishing. Selected Ambrosiella and Raffaelea fungal isolates from ethanol-responsive ambrosia beetles also profited directly and indirectly by (i) increased growth on media containing ethanol and (ii) competitive advantage over “weedy” fungal garden competitors (Aspergillus, Penicillium) that are inhibited by ethanol. These findings suggest ambrosia beetle-fungus mutualism is based on a fondness for ethanol to specifically facilitate growth of the fungus symbionts. To our knowledge, this is the first example of a fungus benefitting from the presence of ethanol, presumably as a carbon source. Understanding the mechanism that promotes and inhibits establishment of ambrosia beetle fungal symbionts is important for novel management tactics since egg laying and brood production does not occur unless the fungal gardens are established within the trees.

Technical Abstract: Animal-microbe mutualisms are typically maintained by vertical symbiont transmission or partner choice. A third mechanism – screening of high-quality symbionts – has been predicted in theory, but empirical examples are rare. Here we demonstrate that ambrosia beetles rely on ethanol within host trees for promoting gardens of their fungal symbiont and producing offspring. Ethanol is long known as the main attractant for many of these fungus-farming beetles as they select host trees in which to excavate tunnels and sow fungal gardens. More than 300 attacks by Xylosandrus germanus and other species were triggered by baiting trees with ethanol lures, but none of the foundresses established broods unless tree tissues contained in vivo ethanol resulting from irrigating with ethanol solutions. More X. germanus brood were also produced in a rearing substrate containing ethanol. These benefits are a result of increased food supply via the positive effects of ethanol on food-fungus biomass combined with oviposition being delayed until fungal gardens are flourishing. Selected Ambrosiella and Raffaelea fungal isolates from ethanol-responsive ambrosia beetles also profited directly and indirectly by (i) increased growth on media containing ethanol and (ii) competitive advantage over “weedy” fungal garden competitors (Aspergillus, Penicillium) that are inhibited by ethanol. These findings suggest ambrosia beetle-fungus mutualism is based on a fondness for ethanol to specifically facilitate growth of the fungus symbionts. To our knowledge, this is the first example of biological screening in an animal-fungus mutualism by both beetles and their associated fungi.