Sociality in the aphid world

The existence of sterile individuals such as those find in social insects (e.g. termites, bees, ants) has long constituted an enigma for evolutionary biology. If natural selection retains the best fitted individuals, how to explain the maintenance of individuals whose reproductive value is zero. The answer to this enigma was provided by the famous British socio-biologist William Hamilton who introduced in 1964 the concept of kin selection: this theory states that individuals may transmit copies of their own genes not only by reproducing themselves but also by promoting the reproduction of related individuals (e.g. sisters, brothers or cousins) ​​by altruistic behavior (brood care, supply of food, defense), even by renouncing their own reproduction in the case of sterile individuals.

According to this principle, it is therefore not surprising to find in aphids, whose individuals can share the same genome when they live in a colony (they belong to the same clone), social species organized in castes. To date, more than 80 species belonging to the subfamilies Eriosomatinae and Hormaphidinae are known to be social, their colonies being made up of a caste of reproductive individuals and a caste of individuals with altruistic behaviors called "soldiers". The soldiers' caste has evolved several times in aphids.

Diversity in social lifestyles

The typical life cycle of the social aphids is complicated, in which they have both sexual and parthenogenetic generations and alternate their host plants seasonally. On the primary host plant, a stem mother (or fundatrix) hatched from a fertilized egg forms a gall and reproduces parthenogenetically in the gall. After migration to the secondary host plant, they spend several generations by parthenogenesis on the plant. Then, winged adults, called sexuparae, return to the primary host and produce sexual females and males, which mate and lay fertilized overwintering eggs that are to be stem mothers in next spring. Soldiers are found in many, if not all, of these species. They are commonly first or second instar nymphs. Note that it depends on the species that soldiers appear in the primary host generation or secondary host generation, or both. Another characteristic is that there are eusocial and presocial species in aphids. Soldiers of eusocial species are morphologically differentiated from normal nymphs and do not grow, whereas those of presocial species grow and reproduce, and no morphological differences are not detected between soldiers and non-soldiers.

Roles of soldiers

For soldiers, the primary social role is colony defense against natural enemies. They have specialized weapons for the attack. Second-instar soldiers in the primary host (galling) generation of Tuberaphis styraci and other Cerataphidini species attack predators with their stylet by penetrating and injecting soldier-specific venom into the body of victims (see the photo). The attacked predator is paralyzed and finally killed, or falls off the gall. First-instar soldiers in the secondary host generation of some Pseudoregma and Ceratovacuna aphids have enlarged forelegs and well-developed frontal horns. They clutch the opponent tightly with their legs and pierce it with the long and sharp horns. Besides, soldiers in some social aphids also perform nest labors, such as gall cleaning and repairing. Soldiers dispose garbage, such as honeydew droplets, cast-off skins and dead aphids, from the gall by pushing them with their heads or other body parts.

Tuberaphis styraci soldiers attacking a fruit fly larva by injecting venom through the stylet (photo Mayako Kutsukake):

The gall repair performed by soldiers of Nipponaphis monzeni is highly sophisticated. When the gall is attacked by a predator, soldiers repair the gall breach by discharging their body fluid and filling up the hole (movie: Mayako Kutsukake):