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Abstract

Animal–microbe mutualisms are typically maintained by vertical symbiont
transmission or partner choice. A thirdmechanism, 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
themain attractant formany 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 foodfungus
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.