Mechanisms regulating caste differentiation in an aphid social system

Abstract

For evolution and maintenance of the social systems of insect colonies, caste production should be controlled in response to external cues so that caste ratio in the colony is kept in an optimal range. Recent developments using artificial diet rearing techniques have revealed an underlying mechanism for adaptive control of caste production in a social aphid, Tuberaphis styraci, which has a sterile soldier caste in the 2nd instar. Aphid density was the proximate cue that acts on 1st instar nymphs and embryos to induce soldier differentiation. The final determination of soldier differentiation occurred postnatally, probably at a late 1st instar stage. Direct contact stimuli from live non-soldier aphids mediated the density effect. While coexisting non-soldiers facilitated soldier differentiation in 1st instar nymphs, coexisting soldiers acted to suppress such differentiation. These results suggest that caste production in aphid colonies is controlled by positive and negative feedback mechanisms consisting of density-dependent induction and suppression of soldier differentiation. Here, we demonstrate the mechanisms that coordinate aphid society, and provide a striking case of clonal superorganism system where simple responses of colony members to local extrinsic stimuli are integrated into a highly organized regulation of the whole colony.

Acknowledgements

This research was supported by a grant from the Kazato Research Foundation, a Grant-in-Aid (no. 18770012) for Scientific Research from the Japan Society for the Promotion of Science, and a 21^st COE (Centers of Excellence) Program of the Research Center of Integrated Sciences at the University of Tokyo financed by the Ministry of Education, Culture, Sports, Science and Technology, Japan.

Figures and Tables

Figure 1 Ecology and life cycle of Tuberaphis styraci. (A) A mature 2^nd-year-gall. (B) Two types of 2^nd instar nymphs. Left, soldier. Right, normal nymph. Soldiers are easily recognized by sclerotized cuticle and greenish color, in contrast to soft cuticle and yellowish color of normal 2^nd instar nymphs. Bar = 1 mm. (C) Soldiers attacking a lacewing larva. (D) Soldiers pushing honeydew globules with their heads. Here we summarize the ecology and life cycle of T. styraci. This aphid has a biennial life cycle on the host tree Styrax obassia.20,21 A fundatrix that hatched from an overwintered egg forms a small gall, and next year the incipient gall grows into a large gall, around 10 cm in diameter and coral-shaped. In the gall, adult females parthenogenetically produce monomorphic 1^st instar nymphs. When they molt into 2^nd instar, two distinct morphs, normal 2^nd instar nymphs and soldiers, appear. Normal 2^nd instar nymphs grow to adult and reproduce, whereas soldiers neither grow nor reproduce but are specialized for altruistic tasks, colony defense and housekeeping. Soldiers are gathering around small holes on the underside of the gall, guarding the openings, and cleaning the gall by pushing honeydew globules, shed skins and corpses out of the holes. Encountering intruders, soldiers aggressively attack them by stinging with their stylets and injecting toxic saliva. It was recently shown that the soldiers produce a venomous protease in their gut and inject it into predators for defense.57,58 Aphid predators such as syrphid maggots and lacewing larvae are tormented, paralyzed or killed by the attack, and usually drop off the gall surface with attacking soldiers attached to them. Therefore, the attacking behavior of soldiers is highly self-sacrificing. Mature large galls of T. styraci sometimes contain over 20,000 insects, more than a half of which may be soldier individuals. In late August to mid October, alate sexuparae, which migrate to another S. obassia trees and produce the sexual generation, emerge from the mature gall via the exit holes. Males and females produced by the sexuparae copulate and produce eggs, which hatch in the next year.

Figure 2 A model for the mechanism of caste differentiation and control in colonies of T. styraci. At the individual level, two factors are involved in soldier differentiation: normal aphids as an inducing cue and soldiers as a suppressing cue. At the colony level, positive and negative feedback is operating to control soldier production: higher density of normal aphids induces soldier production, whereas successive elevation of soldier proportion suppresses further soldier production, whereby investment to soldier production at the colony level is controlled within an appropriate range. In this way, simple responses of aphid individuals to local environmental cues can be integrated into a highly organized regulation of the whole colony.