Evidence for a sexually selected function of the attachment system in bedbugs Cimex lectularius (Heteroptera, Cimicidae)

Abstract

Attachment to surfaces is a major aspect of an animal's interaction with the environment. Consequently, mainly natural selection is considered to have shaped the attachment system in relation to weight load and substrate. However, sexual selection may also be important because many animals attach to the partner during mating. Both hypotheses generate opposing predictions in species where males are smaller than females. Natural selection predicts the attachment ability to scale positively with load, and hence body size, and so be larger in females than males. Sexual selection predicts attachment forces in males to be larger than females, despite the males’ smaller size because males benefit from uninterrupted copulation by stronger attachment to the female. We tested these predictions in the common bedbug Cimex lectularius, a species in which both sexes, as well as nymphs, regularly carry large loads, blood meals of up to three times the body weight. By measuring attachment forces to smooth surfaces and analysing in-situ fixed copulating pairs and the morphology of attachment devices, we show i) that males generate twice the attachment force of females, although weighing 15 % less, ii) that males adhere to females during copulation using hairy tibial adhesive pads, iii) more setae, and more setae per unit area, in the pads of males than females but no difference in shape of tarsal setae, and iv) the absence of hairy tibial attachment pads and low attachment force in nymphs. These results are consistent with a sexually selected function of attachment in bedbugs. Controlling sperm transfer and mate guarding by attaching to females during copulation may also shape the evolution of male attachment structures in other species. More generally, we hypothesise the existence of arms races of male attachment structures and female counterparts to impede attachment which may result in a similar evolutionary diversification as male genitalia.