Recent studies have suggested that an extended postreproductive life span, such as life after menopause in human females, will evolve when the indirect (kin-selected) fitness benefits from altruistic behavior are greater than the direct fitness benefits from continuing reproduction. Under some conditions in which postreproductive altruism is more beneficial and/or continuing reproduction is more costly, the postreproductive life span can be shaped by natural selection. However, indirect fitness benefits during postreproductive survival have been documented mainly in intelligent mammals such as humans and cetaceans, in which elder females possess enhanced social knowledge through learning. Here we show that postreproductive females of the gall-forming aphid Quadrartus yoshinomiyai (Nipponaphidini) can gain indirect fitness benefits through their altruistic colony defense. These females cease reproduction around the time of gall opening and defend the colony by sticking themselves to intruding predators with a waxy secretion that is accumulated in their body with aging. Our results suggest that the presence of an age-related trait for altruistic behavior promotes the evolution of postreproductive altruism in this social insect via kin selection under natural selection imposed by predators.

In the social aphid Nipponaphis monzeni, a unique gall-repairing behaviour has been known: when a hole is made on the gall, many soldier nymphs discharge body fluid on the breach, which promptly solidifies and plugs the hole. Here, we experimentally investigated the subsequent fate of repaired galls and their inhabitants. Irrespective of natural repair by soldier nymphs or artificial repair with adhesive, repaired galls survived significantly better than non-repaired galls. Within a month after repair, the plant tissue around the hole proliferated and sealed up the hole. Many soldier nymphs were localized at the hole area and extermination of inhabiting aphids by insecticides aborted the gall regeneration, indicating that the gall regeneration requires inhabiting aphids, wherein soldier nymphs are likely to play a major role. This study provides an unprecedented case of scab formation and wound healing, which occurs at an animal-plant interface: scab derived from insect body fluid promptly plugs damaged plant tissue and subsequently the insects actively stimulate regeneration of the plant tissue, whereby the compromised plant tissue recovers. We suggest that the novel system may have evolved in the aphid lineage through enhancement and recruitment of the pre-existing capabilities of haemolymph coagulation and gall formation.

In colonies of social insects, non-random spatial positioning within the colonies may reflect division of labour and improve colony efficiency. Here, we describe a novel defence system in the colony of a gall-forming social aphid, Quadrartus yoshinomiyai (Nipponaphidini), where young and old defensive aphids move towards the dangerous area typically associated with a higher risk of predation, whereas the middle-aged reproductive individuals move away. Younger nymphs and post-reproductive adults of Q. yoshinomiyai concurrently defend against predators that intrude after their galls open. In natural open galls, both types of defenders were preferentially located around the open area vulnerable to invasion by predators, whereas reproductive individuals remained in the safer areas. In addition, when a hole was artificially made in closed galls, these morphs located themselves in similar spatial positions to the natural open galls within 12 hours. The defensive system led by oldest and youngest individuals may reflect the possibility of future reproduction for these insects, thereby optimizing colony efficiency in a seasonally changing environment, according to the reproductive values of colony members.

Many animals and plants have evolved elaborate water-repellent microstructures on their surface, which often play important roles in their ecological adaptation. Here, we report a unique type of water-repellent structure on a plant surface, which develops as an insect-induced plant morphology in a social context. Some social aphids form galls on their host plant, in which they produce large amounts of hydrophobic wax. Excreted honeydew is coated by the powdery wax to form ‘honeydew balls’, which are actively disposed by soldier nymphs through an opening on their gall. These activities are enabled by a highly water-repellent inner gall surface, and we discovered that this surface is covered with dense trichomes that are not found on normal plant surfaces. The trichomes are coated by fine particles of the insect-produced wax, thereby realizing a high water repellency with a cooperative interaction between aphids and plants. The plant leaves on which the gall is formed often exhibit patchy areas with dense trichomes, representing an ectopic expression of the insect-induced plant morphology. In the pouch-shaped closed galls of a related social aphid species, by contrast, the inner surface was not covered with trichomes. Our findings provide a convincing example of how the extended phenotype of an animal, expressed in a plant, plays a pivotal role in maintaining sociality.