Natural female mating rate maximizes hatchling size in a marine invertebrate.

1. Males and females often differ in their optimal mating rates, resulting potentially in conflicts over remating. In species with separate sexes, females typically have a lower optimal mating rate than males, and can regulate contacts with males accordingly. The realized mating rate may therefore be closer to the female's optimum. In simultaneous hermaphrodites, however, it has been suggested that the intraindividual optimization between 'male' and 'female' interests generates more 'male'-driven mating rates. 2. In order to assess the consequences of variation in mating rate on 'female' reproductive output, we exposed the simultaneously hermaphroditic sea slug Chelidonura sandrana to four mating rate regimes and recorded the effects on a variety of fitness components. 3. In focal 'females', we found (i) a slight but significant linear decrease in fecundity with mating rate, whereas (ii) maternal investment in egg capsule volume peaked at an intermediate mating rate. 4. Combining the observed fecundity cost with the apparent benefits of larger offspring size suggests that total female fitness is maximized at an intermediate mating rate. With the latter being close to the natural mating rate of C. sandrana in the field, our findings challenge the assumption of 'male'-driven mating systems in simultaneous hermaphrodites. 5. Our study provides experimental evidence for various mathematical models in which female fitness is maximized at intermediate mating rates.