Mating Behaviour of the Sperm Trading Sea Slug Chelidonura hirundinina: Repeated Sex Role Alternation Balances Reciprocity

In animals with separate sexes, male fitness usually increases with the number of matings, whereas female fitness more directly depends on the amount of accessible reproductive resources. In simultaneous hermaphrodites, such differences in fitness pay‐offs between male and female sexual function can result in a preference to copulate in one particular sex role, generating conflicts over mating roles if mates share the same preference. Sperm trading, i.e. the conditional exchange of sperm between mates as found in some hermaphrodites, is often considered a possible solution for the conflict over mating roles. Conditional sperm exchange has recently been demonstrated in Chelidonura hirundinina (Opisthobranchia, Aglajidae), but its functional causes remain obscure. Based on a detailed characterization of mating in this species, we here assess two potential benefits of sperm trading, the balancing of sperm exchange between partners, and the acquisition of information about the partner’s fecundity. We found that the number of sperm droplets exchanged between partners varied more between than within pairs, supporting the first hypothesis. Moreover, larger individuals donated more sperm droplets and are known to produce more eggs. As body size is tightly linked to fecundity, a sperm recipient may use the number of received sperm droplets as an honest signal of the female quality of the sperm donor. Our findings thus help to elucidate how sperm trading may contribute to optimizing the investment of costly sperm in response to partner quality.