Female Genitalia Concealment Promotes Intimate Male Courtship in a Water Strider

Abstract

Violent coercive mating initiation is typical for animals with sexual conflict over mating. In these species, the coevolutionary arms-race between female defenses against coercive mating and male counter-adaptations for increased mating success leads to coevolutionary chases of male and female traits that influence the mating. It has been controversial whether one of the sexes can evolve traits that allow them to “win” this arms race. Here, we use morphological analysis (traditional and scanning electron micrographs), laboratory experiments and comparative methods to show how females of a species characterized by typical coercive mating initiation appear to “win” a particular stage of the sexual conflict by evolving morphology to hide their genitalia from direct, forceful access by males. In an apparent response to the female morphological adaptation, males of this species added to their typically violent coercive mounting of the female new post-mounting, pre-copulatory courtship signals produced by tapping the water's surface with the mid-legs. These courtship signals are intimate in the sense that they are aimed at the female, on whom the male is already mounted. Females respond to the signals by exposing their hidden genitalia for copulatory intromission. Our results indicate that the apparent victory of coevolutionary arms race by one sex in terms of morphology may trigger evolution of a behavioral phenotype in the opposite sex.

Male water striders attract predators to intimidate females into copulation

“…Furthermore, the log-transformed number of leg movements per bout (Fig. 3c; see Han and Jablonski9 for signal structure description) increased in response to predator treatment for large ( t 26 =−2.508, P =0.019), but not for small ( t 16 =1.209, P =0.244), males (interaction term: F 1,42 =6.263, P =0.016). Hence, it seems that, in response to predators, males did not decrease, with large males even increasing, their leg tapping movements that produce the predator-attracting signals.…”

“…We recently described morphological and behavioural adaptations to this evolutionary conflict in Gerris gracilicornis 910. Females of this species evolved a morphological shield over their vulvar opening, preventing mounted males from coercive intromission.…”

Water striders adjust leg movement speed to optimize takeoff velocity for their morphology

“…our results prove that water striders are able to exploit water surface properties to optimally perform their predation avoidance jumps using elongated legs that are developmentally shaped by recently discovered genetic mechanism16, which is an apparent outcome of natural selection to avoid predator attacks. This work adds to the documented or suggested repertoire of water striders' behaviours that evolved to exploit the water surface properties: defence of territories1718192021, courtship212223, establishing dominance in agonistic interactions2024, defence of mates against harassment from other males during mate guarding25, sex recognition202126 and sensing distribution of food in environment27 or possibly also sensing local sex ratio in a population28.…”

The Evolution of Sexually Antagonistic Phenotypes

“…2), both of which vary among populations and species and affect mating outcomes (Arnqvist and Rowe 2005;Ronkainen et al 2005;Perry and Rowe 2012b). Han and Jablonski (2009) have identified a new trait in females that may have a substantial effect on SAC. The basal state in Gerris spp.…”

“…In contrast, the pregenital segment 7 of G. gracilicornis largely covers the vulvar opening. Han and Jablonski (2009) have suggested that this precludes so-called forced copulation because females must inflate their genitalia to allow male access. An interesting hypothesis is that males have responded by making resistance (delay in inflating genitalia) costly to females, potentially through a "war of attrition"-type process.…”