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Proc Natl Acad Sci U S A. 2018 Apr 24;115(17):4447-4452. doi: 10.1073/pnas.1716852115. Epub 2018 Apr 9.

Symbiont selection via alcohol benefits fungus farming by ambrosia beetles.

Author information

1
Horticultural Insects Research Laboratory, US Department of Agriculture-Agricultural Research Service, Wooster, OH 44691; christopher.ranger@ars.usda.gov peter.biedermann@uni-wuerzburg.de.
2
Department of Entomology, Ohio Agricultural Research and Development Center, The Ohio State University, Wooster, OH 44691.
3
Department of Biochemistry, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany; christopher.ranger@ars.usda.gov peter.biedermann@uni-wuerzburg.de.
4
Department of Animal Ecology and Tropical Biology, Biozentrum, Julius Maximilian University Würzburg, 97074 Würzburg, Germany.
5
Department of Biological Sciences, Bowling Green State University, Bowling Green, OH 43403.
6
US Department of Agriculture-Agricultural Research Service Midwest Area, Peoria, IL 61604.
7
Department of Biochemistry, Max Planck Institute for Chemical Ecology, 07745 Jena, Germany.
8
Hawkesbury Institute for the Environment, Western Sydney University, Penrith, NSW 2751, Australia.
9
Horticultural Insects Research Laboratory, US Department of Agriculture-Agricultural Research Service, Wooster, OH 44691.
10
Hampton Roads Agricultural Research and Extension Center, Virginia Polytechnic Institute and State University, Virginia Beach, VA 23455.
11
School of Life Sciences Weihenstephan, Technical University of Munich, D-85354 Freising, Germany.

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 has long been known as the main attractant for many of these fungus-farming beetles as they select host trees in which they excavate tunnels and cultivate 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 fungal gardens or produced broods unless tree tissues contained in vivo ethanol resulting from irrigation 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. Selected Ambrosiella and Raffaelea fungal isolates from ethanol-responsive ambrosia beetles profited directly and indirectly by (i) a higher biomass on medium containing ethanol, (ii) strong alcohol dehydrogenase enzymatic activity, and (iii) a competitive advantage over weedy fungal garden competitors (Aspergillus, Penicillium) that are inhibited by ethanol. As ambrosia fungi both detoxify and produce ethanol, they may maintain the selectivity of their alcohol-rich habitat for their own purpose and that of other ethanol-resistant/producing microbes. This resembles biological screening of beneficial symbionts and a potentially widespread, unstudied benefit of alcohol-producing symbionts (e.g., yeasts) in other microbial symbioses.

KEYWORDS:

fungus-farming insects; host screening; insect–fungus mutualism; plant–insect–microbe interactions; symbiosis

PMID:
29632193
PMCID:
PMC5924889
DOI:
10.1073/pnas.1716852115
[Indexed for MEDLINE]
Free PMC Article

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