Department of Forest Science, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Bunkyo, Tokyo, Japan.
PLoS One. 2012;7(7):e41893. doi: 10.1371/journal.pone.0041893. Epub 2012 Jul 27.
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.
微生物的培养用于食品生产，被称为培养共生，这在社会性和亚社会性昆虫中已有充分的记载，如蚂蚁、白蚁和粉蠹，而在非社会性昆虫中则描述得很少。在这里，我们报告了一种非社会性的龙虱科昆虫 Doubledaya bucculenta（鞘翅目：Erotylidae：Languriinae）的真菌养殖，它涉及到为真菌储存/接种而开发的一种特殊的雌性结构，即菌囊，以及昆虫对真菌共生体的绝对依赖。雌性成虫用其特化的下颚在最近死亡的竹茎上钻一个孔，将一个卵放入节间腔，并将孔用竹纤维堵塞。我们发现，幼虫寄生的竹节内的内壁总是覆盖着一层白色的真菌层。一种特定的酵母菌 Saccharomycetes，异常威克汉姆酵母（ = 假丝酵母），总是从竹节内的内壁和幼虫的体表分离出来。对成虫产卵器的组织学检查显示，第八腹节有一个外骨骼袋。推测的菌囊中含有酵母细胞，并且从共生器官中反复检测到异常威克汉姆酵母。当将初孵幼虫放在接种了异常威克汉姆酵母的培养基上时，它们正常生长发育到成虫。相比之下，放在无菌培养基或高压灭菌的竹节内壁上的初孵幼虫在第二龄期停止生长，而向培养基中添加异常威克汉姆酵母则恢复了幼虫的生长和发育。这些结果强烈表明 D. bucculenta-W. anomalus 之间存在共生关系，具有形态特化和生理依赖。基于这些结果，我们将 D. bucculenta 的真菌养殖与社会性和亚社会性昆虫的真菌养殖进行了比较，并讨论了与非社会性昆虫中真菌养殖进化相关的生态因素。
