Atypical, ventro-ventral copulation position in aphids of the genus Stomaphis Walker, 1870 (Insecta, Hemiptera)

Abstract

Firm matching of genitals during copulation is of critical importance to effective insemination and thus, gene flow. During the evolution of insects, an effective position during copulation promoted higher fecundity through control over the act of mating or elimination of competitors. Usually during insect copulation, either twisting or flexing of the male abdomen occurs, and genitals remain symmetrically or asymmetrically disposed following changes in the mating position. However, it is always the dorsal side of the male genitalia that makes contact with the ventral side of female abdomen. Here we present the unusual case of a 'belly-to-belly' copulation, with symmetrically positioned male genitals and no twisting of the abdomen. During the mating of two species in the Stomaphis genus of large, tree dwelling aphids, the dwarfish male is attached to the underside of the female, with the ventral part of its genitals contacting the ventral part of female abdomen, and the aedeagus effectively inserted into the female genital organs. Interestingly, congeneric species do not exhibit this sort of mating, but differences in the genital plates of females, between species, may play an important role. These observations raise many questions concerning the possible dominant role of the female during mating and later, during mate guarding by male, which can lead to monandry in this generally polyandrous group of insects. It is possible that this sort of mating is either an adaptation to the competitive behaviour of other males or a consequence of the obligatory mutualistic relationship with ants, and the adaptation to specialised ecological niches enforced by this relationship. If ants do influence the mating habits of Stomaphis then it is possible that speciation in this group of insects, and phytophagous insects generally, is partially driven by their relationship with ants.