Optimal ultra-short copulation duration in a sexually cannibalistic spider in which females want to be half-virgin

Optimal ultra-short copulation duration in a sexually cannibalistic spider. Braulio A. Assis, Matthias W. Foellmer. Behavioral Ecology and Sociobiology, September 2019, 73:117. August 3 2019. https://link.springer.com/article/10.1007/s00265-019-2733-5

Abstract: Sexual conflict has been shown to shape many behaviors in the reproductive context, such as the duration of copulation, across a broad taxonomic range. In spiders, copulation duration is one of the most variable reproductive traits, ranging from seconds to hours. Some species in the araneid genus Argiope exhibit very short copulations of a few seconds per pedipalp insertion. This has been hypothesized to be the result of cannibalistic females imposing selection on males to escape the attack by reducing insertion duration to a minimum. However, copulation duration is positively correlated with the number of sperm transferred and fertilization success in many species. Thus, given the tradeoff between sperm transfer and the risk of being cannibalized, males may optimize the duration of copulation to maximize lifetime reproductive success. Here we test whether males in the orb-weaver Argiope aurantia, which exhibits the shortest copulation in any spider and rivals the honey bee for shortest copulation reported for any arthropod with internal genital coupling, are optimizing the insertion duration of the first pedipalp to maximize the number of sperm transferred and eggs fertilized. We analyzed total sperm transferred to the female, and male fertilization success as a function of the first insertion’s duration, using data collected in previous staged-mating experiments and determined optimal copulations of 3–4 s, which is close to the averages of the source populations. Thus, we present evidence for sexual cannibalism as a driver of the extremely short copulations in A. aurantia.

Significance statement: Females and males often conflict over mating frequency. In spiders, both sexes have paired reproductive organs and can remain half virgin if only one of the two possible copulations are completed. In the orb-weaver Argiope aurantia, males place mating plugs and females almost always immediately attack males in copula, probably to prevent them from achieving both copulations and to be able to upgrade to a second mate. We find an optimal duration of 3–4 s for males to terminate copulation, which reduces the risk of being killed, while at the same time maximizing sperm transfer and fertilization success because copulation duration is positively related to the number of sperm transferred and allows males to achieve the second copulation. The optimal duration detected here is very close to average copulation durations in nature. Hence, we document the adaptive value of the shortest copulation known for any spider.

Keywords: Sexual cannibalism Copulation duration Sexual conflict Araneae Sexual size dimorphism Mating plug