Abstract
Culturing of microbes for food production, called cultivation mutualism, has been well-documented from eusocial and subsocial insects such as ants, termites and ambrosia beetles, but poorly described from solitary, non-social insects. Here we report a fungal farming in a non-social lizard beetle Doubledaya bucculenta (Coleoptera: Erotylidae: Languriinae), which entails development of a special female structure for fungal storage/inoculation, so-called mycangium, and also obligate dependence of the insect on the fungal associate. Adult females of D. bucculenta bore a hole on a recently-dead bamboo culm with their specialized mandibles, lay an egg into the internode cavity, and plug the hole with bamboo fibres. We found that the inner wall of the bamboo internode harboring a larva is always covered with a white fungal layer. A specific Saccharomycetes yeast, Wickerhamomyces anomalus ( = Pichia anomala), was consistently isolated from the inner wall of the bamboo internodes and also from the body surface of the larvae. Histological examination of the ovipositor of adult females revealed an exoskeletal pocket on the eighth abdominal segment. The putative mycangium contained yeast cells, and W. anomalus was repeatedly detected from the symbiotic organ. When first instar larvae were placed on culture media inoculated with W. anomalus, they grew and developed normally to adulthood. By contrast, first instar larvae placed on either sterile culture media or autoclaved strips of bamboo inner wall exhibited arrested growth at the second instar, and addition of W. anomalus to the media resumed growth and development of the larvae. These results strongly suggest a mutualistic nature of the D. bucculenta-W. anomalus association with morphological specialization and physiological dependence. Based on these results, we compare the fungal farming of D. bucculenta with those of social and subsocial insects, and discuss ecological factors relevant to the evolution of fungal farming in a non-social insect.
Highlights
IntroductionCultivation mutualism is a form of organism-organism symbiotic associations wherein an organism (normally called host) cultures another organism (often called symbiont or crop) as food source
Cultivation mutualism is a form of organism-organism symbiotic associations wherein an organism cultures another organism as food source
Eusocial insects like ants and termites and subsocial insects like ambrosia beetles exhibit sophisticated forms of cultivation mutualism, which may be comparable to human agriculture in many aspects [1,2]
Summary
Cultivation mutualism is a form of organism-organism symbiotic associations wherein an organism (normally called host) cultures another organism (often called symbiont or crop) as food source. Eusocial insects like ants and termites and subsocial insects like ambrosia beetles exhibit sophisticated forms of cultivation mutualism, which may be comparable to human agriculture in many aspects [1,2] These insects inoculate their specific fungal associates onto appropriate substrates, engineer the environmental conditions for their optimal growth, defend them against pests/ parasites/pathogens by monitoring, sequestration and/or antibiotic application, harvest and consume them as food, and are obligatorily dependent on them [1,2,3,4,5,6]. In these non-social insects, biological aspects of the mycangium-associated microbes, in particular their physiological roles for their hosts, have been poorly investigated
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