Sexual conflict and correlated evolution between male persistence and female resistance traits in the seed beetle Callosobruchus maculatus

Abstract

Traumatic mating (or copulatory wounding) is an extreme form of sexual conflict whereby male genitalia physically harm females during mating. In such species females are expected to evolve counter-adaptations to reduce male-induced harm. Importantly, female counter-adaptations may include both genital and non-genital traits. In this study, we examine evolutionary associations between harmful male genital morphology and female reproductive tract morphology and immune function across 13 populations of the seed beetle We detected positive correlated evolution between the injuriousness of male genitalia and putative female resistance adaptations across populations. Moreover, we found evidence for a negative relationship between female immunity and population productivity, which suggests that investment in female resistance may be costly due to the resource trade-offs that are predicted between immunity and reproduction. Finally, the degree of female tract scarring (harm to females) was greater in those populations with both longer aedeagal spines and a thinner female tract lining. Our results are thus consistent with a sexual arms race, which is only apparent when both male and female traits are taken into account. Importantly, our study provides rare evidence for sexually antagonistic coevolution of male and female traits at the within-species level.

Demonstrating sexual selection by cryptic female choice on male genitalia: What is enough?

“…; Dougherty et al. ; Sloan and Simmons ). But the strong likelihood that the male genitalia of C. maculatus also stimulate the female and the possibility that females respond to this stimulation have not been tested (for instance, using local anesthetics).…”

“…CFC has generally not even been mentioned (e.g., Dougherty et al. ), and the possibility that it could be acting in conjunction with SAC has not been tested. Its possible importance is supported by the fact that CFC apparently favors spines on the genital jaws of males in the closely related beetle C. subinnotatus (van Haren et al.…”

“…The most common interpretation of SAC in genitalia concerns forceful manipulation of the female by the male (e.g., the genital damage discussed by Dougherty et al. ), but a second possibility is that males manipulate females in harmful ways by stimulating them (e.g., using sensory traps) (Chapman et al. ); we will consider these possibilities separately below.…”

The evolution of female genitalia

“…Male beetles possess spines on their genitalia that puncture the female reproductive tract (Figure ), thereby facilitating the movement of seminal fluid proteins into the female's bloodstream where they affect her subsequent use of the copulating male's sperm (Yamane, Goenaga, Rönn, & Arnqvist, ). Genital damage due to male spines is well known to have costly fitness consequences for females (Crudgington & Siva‐Jothy, ; Dougherty & Simmons, ; Edvardsson & Tregenza, ; Rönn, Katvala, & Arnqvist, ), and selection for increased length of genital spines appears to have driven the coevolution of thicker reproductive tracts in females in response to male harm, both among (Rönn et al., ) and within species (Dougherty et al., ).…”

Sexual selection on bushcricket genitalia operates in a mosaic pattern

“…Consequently, the compiled data for the bushcricket R. roeselii show that titillators in this species evolved under cryptic female choice (Eberhard & Lehmann, 2019), but sexually antagonistic coevolution might also act in bushcrickets. In the first case, titillators should be used as copulatory courtship devices to stimulate the females, while in the latter case, they could be used for grasping and position securing, allowing males to control the copulation duration, or even wound the females (Dougherty et al, 2017).…”