Male mate guarding in a polyandrous and sexually cannibalistic praying mantid

Abstract

Sexually cannibalized males incur a significant fitness cost due to the loss of future mating opportunities and are expected to evolve behaviors to avoid or compensate for such costs. For example, partially cannibalized males may exhibit mate guarding, in which they accompany the female to prevent her from mating with another male. In some species, cannibalized males prolong the duration of copulation. However, little is known about the adaptive significance of the mating behavior of sexually cannibalized males. We hypothesized that mating itself serves a mate guarding function, and that behavioral change caused by cannibalism enhances the mate guarding function. We tested these hypotheses using the polyandrous and sexually cannibalistic praying mantid Tenodera angustipennis, with decapitation as a model of sexual cannibalism. We compared latencies to female mating with a rival male among three experimental treatments: unmated treatment, noncannibalistic mating treatment, and cannibalistic mating treatment. Mating itself delayed female remating, revealing its function in mate guarding. Decapitated males exhibited a higher guarding efficiency against rival males via firmer genital coupling. In addition, spermatophore attached to the female genital opening also delayed female remating, revealing an additional function in postmating mate guarding. Although copulation was prolonged due to decapitation, mating by a rival male was not delayed compared to noncannibalistic mating, probably because of weaker postcopulatory guarding. These findings suggest that greater mate guarding by decapitated males during copulation was offset by processes after copulation.

Significance statement

Sexually cannibalized males die and lose the chance for future mating. This means that males that can avoid or compensate for this fitness loss may be favored. We examined this possibility by focusing on the postmating behavior of sexually cannibalized male mantises. Experimental analysis revealed that cannibalized males grasped the female more firmly during copulation to avoid disruption by other males, and prolonged copulation duration compared with noncannibalized males. These behavioral changes by cannibalized males contributed to delaying female remating with other males to the same extent as noncannibalized males. This suggests that sexually cannibalized males did not fully compensate for the loss of future mating opportunities. Stronger mate guarding via firm genital coupling and prolonged copulation duration in cannibalized males may be offset by weaker postcopulatory guarding such as shorter duration of copulatory plug attachment.