Variation in pre- and post-copulatory sexual selection on male genital size in two species of lygaeid bug

Abstract

Abstract: Sexual selection has been shown to be the driving force behind the evolution of the sometimes extreme and elaborate genitalia of many species. Sexual selection may arise before and/or after mating, or vary according to other factors such as the social environment. However, bouts of selection are typically considered in isolation. We measured the strength and pattern of selection acting on the length of the male intromittent organ (or processus) in two closely related species of lygaeid seed bug: Lygaeus equestris and Lygaeus simulans. In both species, we measured both pre- and post-copulatory selection. For L. equestris, we also varied the experimental choice design used in mating trials. We found contrasting pre- and post-copulatory selection on processus length in L. equestris. Furthermore, significant pre-copulatory selection was only seen in mating trials in which two males were present. This selection likely arises indirectly due to selection on a correlated trait, as the processus does not interact with the female prior to copulation. In contrast, we were unable to detect significant pre- or post-copulatory selection on processus length in L. simulans. However, a formal meta-analysis of previous estimates of post-copulatory selection on processus length in L. simulans suggests that there is significant stabilising selection across studies, but the strength of selection varies between experiments. Our results emphasise that the strength and direction of sexual selection on genital traits may be multifaceted and can vary across studies, social contexts and different stages of reproduction.

Significance statement: Animal genitalia vary greatly in size and complexity across species, and selection acting on genital size and shape can be complex. In this study, we show that the length of the penis in two species of seed bug is subject to complex patterns of selection, varying depending on the social context and whether selection is measured before or after mating. In one of the species, we show unexpectedly that penis length is correlated with male mating success, despite the fact that the penis does not interact with the female prior to mating. Our results highlight the fact that genitalia may be subject to both direct and indirect selection at different stages of mating and that to fully understand the evolution of such traits we should combine estimates of selection arising from these multiple episodes.

Keywords: Genital evolution; Lygaeinae; Meta-analysis; Post-copulatory; Pre-copulatory; Sexual selection; Social environment.

Fig. 1

Drawing of the basic anatomy of the intromittent organ of L. equestris and L. simulans. Th theca, V vesica, ER ejaculatory reservoir, Pr processus

Fig. 2

Fitness functions showing selection on male processus length in L. equestris for three measures of male reproductive success: a male mating success (mated or non-mated, N = 174), b male insemination success (production of offspring) for mated males (N = 64) and c male insemination success (production of offspring) for all males, including those that did not mate (N = 174). Dashed lines indicate 1 standard error above and below the predicted line

Fig. 3

Fitness functions showing pre-copulatory selection on male processus length in L. equestris for the four experimental choice designs: a no-choice (N = 39), b female choice (N = 54), c male choice (N = 26) and d mutual choice (N = 55). Dashed lines indicate 1 standard error above and below the predicted line

Fig. 4

Fitness function showing a pre-copulatory selection on male processus length for all males (N = 140), b post-copulatory selection on male processus length for mated males only (N = 101) and c post-copulatory selection on male processus length for all males (N = 140), in L. simulans. Dashed lines indicate 1 standard error above and below the predicted line

Fig. 5

Forest plot showing the quadratic selection gradient (γ) and associated 95 % CI of the effect sizes included in the meta-analysis. The sizes of the squares represent the relative weightings of each effect size in the model. The mean effect size estimate produced using a random-effects model is represented by the centre of the diamond, with the width of the diamond representing the 95 % CI of the estimate