Natural female mating rate maximizes hatchling size in a marine invertebrate

Abstract

Summary 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.

Sexual Conflict in Hermaphrodites

“…A randomly sampled individual in the population will normally gain more from mating next as a male, because it likely has mated as a female already. The empirically observed Bateman gradients thus probably mean that these snails show a male sex-role preference (Anthes et al 2010;Pélissié et al 2012), and two studies on sea slugs, in which only the female function was examined, even suggested costs for high female mating rates (Sprenger et al 2008;Lange et al 2012).…”

Intra-locus sexual conflict and sexually antagonistic genetic variation in hermaphroditic animals

“…Choosing to invest in sexual conflict arms races over fecundity should be widespread among simultaneous hermaphrodites, according to recent theoretical work [36,37]. There is also empirical evidence suggesting that elevated mating rates may have opposite fitness effects via male and female sex functions [38,39]. (iv) Mediation of parasite-associated effects.…”

Sources of phenotypic variance in egg and larval traits in a marine invertebrate

“…Early larval survival (prop) 0.410 1.08 9 10 -2 (12.7) 2.85 9 10 -2 (33.4) 4.61 9 10 -2 (53.9) V A , additive genetic variance; V M?D , maternal and dominance variance; V E , environmental variance (Sprenger et al 2008a;Sprenger et al 2008b) is independent of a male's genetic quality and is not affected by the genes or the environment (e.g., accessory substances) provided by males. Recent suggestive evidence for the dependence of maternal allocation on the genetic compatibility (i.e., genetic quality) between parental genotypes derives from the live bearing pseudoscorpion Cordylochernes scorpioides.…”

“…Recent experimental work showed that polyandrous mothers (mated to four different partners) produce larger but not fewer eggs and larvae than repeatedly mated (four times to the same partner) and singly mated females (Sprenger et al 2008a). Moreover, per-offspring investment was maximized at an intermediate mating rate matching that accomplished in the field (Sprenger et al 2008b). Changes in mean offspring size did not affect the variance in offspring size between females (Sprenger et al 2008a;Sprenger et al 2008b), indicating non-selective sperm usage by females (García-González and Simmons 2005).…”

“…Moreover, per-offspring investment was maximized at an intermediate mating rate matching that accomplished in the field (Sprenger et al 2008b). Changes in mean offspring size did not affect the variance in offspring size between females (Sprenger et al 2008a;Sprenger et al 2008b), indicating non-selective sperm usage by females (García-González and Simmons 2005). Although we detected no direct link between offspring size and performance in these previous studies, a growing body of literature confirms that larger progeny generally perform better (reviewed in Marshall and Keough 2008).…”