Abstract

Traumatic mating behaviors often bear signatures of sexual conflict and are then typically considered a male strategy to circumvent female choice mechanisms. In an extravagant mating ritual, the hermaphroditic sea slug Siphopteron quadrispinosum pierces the integument of their mating partners with a syringe-like penile stylet that injects prostate fluids. Traumatic injection is followed by the insertion of a spiny penis into the partner’s gonopore to transfer sperm. Despite traumatic mating, field mating rates exceed those required for female fertilization insurance, possibly because costs imposed on females are balanced by direct or indirect benefits of multiple sperm receipt. To test this idea, we exposed animals to a relevant range of mating opportunity regimes and assessed the effects on mating behavior and proxies of female fitness. We find penis intromission duration to decrease with mating rates, and a female fecundity maximum at intermediate mating rates. The latter finding indicates that benefits beyond fertilization insurance can make higher mating rates also beneficial from a female perspective in this traumatically mating species.

Highlights

  • Asymmetric reproductive economics between males and females can cause colliding evolutionary interests and drive sexual conflict [1,2]

  • As typically found in invertebrates with continuous growth and previously reported for Siphopteron sea slugs [25], female fecundity increased with size: Mean individual body weight significantly affected the number of spawn masses, average spawn size, and the total number of eggs per replicate mating group

  • As the average number of spawn masses per group did not vary significantly between mating treatment groups, this translated into a peak of the total number of eggs produced at moderate mating rates that was close to statistical significance

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Summary

Introduction

Asymmetric reproductive economics between males and females can cause colliding evolutionary interests and drive sexual conflict [1,2]. Behavioral observations suggest that these animals often avoid mating altogether by pushing away a putative mate, and otherwise preferentially move into the male rather than into the female mating position [10] This behavior implies that mating is costly in general and so in the female mating role where stylet injection and penile spines can result in tissue rupture and wounding [as found in nudibranchs, seed beetles, and bed bugs: 12–14]. Such an imbalance in sex-specific mating costs can be crucial to initiate sexual conflict [2], and can reinforce divergence in the degree to which reproductive success via male and female sex function increases or decreases with higher mating success as depicted in the analysis of sexual selection gradients (or Bateman gradients) [15,16]

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