An insect-induced novel plant phenotype for sustaining social life in a closed system

Abstract

Foraging, defense and waste disposal are essential for sustaining social insect colonies. Hence, their nest generally has an open structure, wherein specialized castes called workers and soldiers perform these tasks. However, some social aphids form completely closed galls, wherein hundreds to thousands of insects grow and reproduce for several months in isolation. Why these social aphids are not drowned by accumulated honeydew has been an enigma. Here we report a sophisticated biological solution to the waste problem in the closed system: the gall inner surface is specialized for absorbing water, whereby honeydew is promptly removed via the plant vascular system. The water-absorbing closed galls have evolved at least twice independently among social aphids. The plant-mediated waste removal, which entails insect's manipulation of plant morphogenesis and physiology, comprises a previously unknown mechanism of nest cleaning, which can be regarded as ‘extended phenotype' and ‘indirect social behavior' of the social aphids.

Comparative phenotyping across a social transition in aphids

“…There is some evidence that aphid galls are resource sinks, and there may be interspecific differences in the degree to which galls concentrate plant metabolites (Larson, 1991). Finally, unusual adaptations have been described in some aphid species whose galls are closed, preventing the removal of honeydew (Kutsukake, Meng, Katayama, Shibao, & Fukatsu, 2012). Possibly, P. populitransversus expresses behaviours for managing honeydew that we did not account for.…”

The histo structure of galls induced by aphids as a useful taxonomic character: the case of Rectinasus (Hemiptera, Aphididae, Eriosomatinae)

“…In the first group, the inner surface of the gall shows cavities (Álvarez 2012), while in the second group this surface has a dimpled appearance without any cavities (Álvarez et al 2009). The presence of these cavities can be interpreted along the lines of Kutsukake et al (2012) as an adaptation of the species that induce closed galls, and which allows them to totally or partially remove honeydew from the inside of the galls to the vascular tissues of the plant.…”

Formation of long‐lasting galls by overwintered nymphs in the Japanese aphid Quadrartus yoshinomiyai (Hemiptera: Aphididae: Hormaphidinae)

“…Water absorption through the gall inner surface facilitates such a long life in such completely enclosed galls (Kutsukake et al . ).…”

“…Galls of N. monzeni, in particular, can survive for four and a half years (Kurosu & Aoki 2009). Water absorption through the gall inner surface facilitates such a long life in such completely enclosed galls (Kutsukake et al 2012).…”