One size fits all? Determinants of sperm transfer in a highly dimorphic orb-web spider

The evolutionary significance of widespread hypo-allometric scaling of genital traits in combination with rapid interspecific genital trait divergence has been of key interest to evolutionary biologists for many years and remains poorly understood. Here, we provide a detailed assessment of quantitative genital trait variation in males and females of the sexually highly dimorphic and cannibalistic orb-weaving spider Argiope aurantia. We then test how this trait variation relates to sperm transfer success. In particular, we test specific predictions of the one-size-fits-all and lock-and-key hypotheses for the evolution of genital characters. We use video-taped staged matings in a controlled environment with subsequent morphological microdissections and sperm count analyses. We find little support for the prediction of the one-size-fits-all hypothesis for the evolution of hypo-allometric scaling of genital traits, namely that intermediate trait dimensions confer highest sperm transfer success. Likewise, our findings do not support the prediction of the lock-and-key hypothesis that a tight fit of male and female genital traits mediates highest sperm transfer success. We do, however, detect directional effects of a number of male and female genital characters on sperm transfer, suggesting that genital trait dimensions are commonly under selection in nature. Importantly, even though females are much larger than males, spermatheca size limits the number of sperm transferred, contradicting a previous hypothesis about the evolutionary consequences of genital size dimorphism in extremely size-dimorphic taxa. We also find strong positive effects of male body size and copulation duration on the probability of sperm transfer and the number of sperm transferred, with implications for the evolution of extreme sexual size dimorphism and sexual cannibalism in orb weavers.