Plant Manipulation by Gall-Forming Social Aphids for Waste Management

Abstract

Many social aphids form spectacular galls on their host plants, in which hundreds to thousands of aphids thrive for several months or even for over a year. Here, in addition to colony defense against natural enemies, waste disposal is an important task for the gall dwellers to sustain their social life. In open galls, soldier nymphs actively clean colony wastes such as honeydew droplets, cast-off skins, and cadavers by pushing them with their head out of the gall opening. In the gall, the excreted honeydew is coated with aphid-derived powdery wax to form "honeydew balls," which prevents the aphids from wetting and drowning with their own excretion. How the aphids deal with the accumulated honeydew in closed galls has been a mystery. Here, we report a novel gall-cleaning mechanism: the gall inner surface absorbs and removes the liquid waste through the plant vascular system. Such a plant-mediated water-absorbing property is commonly found in aphids forming closed galls, which must have evolved at least three times independently. By contrast, the inner surface of open galls is wax-coated and water-repelling, and in some cases, the inner surface is covered with dense trichomes, which further enhance the water repellency. In conclusion, gall-forming aphids induce novel plant phenotypes to manage the waste problems by manipulating plant morphogenesis and physiology for their own sake. This review describes our recent studies on waste management strategies by gall-forming social aphids and discusses future directions of this research topic.

Keywords: gall; manipulation; plant cuticle; social aphid; trichome; waste management.

Figure 1

Open and closed galls of various aphids and water-absorbing property. (A–C) Closed galls of N. monzeni showing water-absorbing property. (A) A gall of N. monzeni on D. racemosum. (B) Safranin staining of the gall tissue, showing transported routes of absorbed water in red. (C) A histological section of the safranin-stained gall, in which the vascular bundle is conspicuously stained in red. Scale bar, 0.2 mm. (D) Waste management strategies in open and closed galls. Galls of C. japonica and C. nekoashi on S. japonicus, and C. clematis and P. morrisoni on Z. serrata are shown. A subgall of C. japonica with a slit opening and a subgall of C. nekoashi with no opening are also shown. Figures were modified from Kutsukake et al. (2012) and Uematsu et al. (2018). In, inner side of the gall; Out, outer side of the gall.

Figure 2

Evolution and plant surface structures of water-absorbing closed galls and water-repelling open galls. (A) A schematic phylogeny of the gall-forming social aphids and the evolution of water-absorbing/repelling properties. The occurrences of the water-absorbing closed galls are indicated in bold branches. The water-absorbing closed galls reported in Kutsukake et al. (2012) and Uematsu et al. (2018) are indicated in black, whereas others (potential water-absorbing galls) are indicated in gray. The evolution of dense trichomes on gall inner surface is indicated by black stars. High-density trichomes are indicated by a single star and very high-density trichomes are indicated by double stars. A white star indicates loss of trichomes. Closed (C) or open (O) galls are indicated in brackets. The phylogenetic relationship of gall-forming social aphids is based on Sano and Akimoto (2011) and Kutsukake et al. (2012). (B) Gall inside views and transmission electron micrographs of inner wall surface in galls of C. nekoashi and C. japonica. Hydrophobicity of the gall inner surface on which was placed a drop of food dye solution or water is also shown. (C) Gall inside views and scanning electron micrographs of the inner wall surface of galls of C. clematis and P. morrisoni. Note that aphid-derived wax was removed during the fixation procedure before the observation using a scanning electron microscope. Figures were modified from Kutsukake et al. (2012) and Uematsu et al. (2018). C, closed gall; CW, cell wall; CWL, cuticle wax layer; In, inner side of the gall; O, open gall; PC, plant cell.