Courtship behavior as a war of attrition in a simultaneous hermaphrodite

Abstract

In outcrossing hermaphrodites with unilateral mating, where for each mating interaction one individual assumes the female role and the other the male role, each individual must take a sexual role opposite to that of its partner. In the polychaete worm Ophryotrocha diadema, the decision on sexual role is likely at stake during the day-long courtship. Here we describe, for the first time, courtship and pseudocopulation in this species, quantify their pre-copulatory behavior, and search for behavioral traits predicting the prospective sexual role (i.e., behavioral sexual dimorphism), by analyzing the courtship behavior of pairs of worms during the day preceding a mating event. We did not find any behavioral cue predicting the sexual role worms were to play; partners’ pre-copulatory behaviors were qualitatively and quantitatively symmetrical. We interpret this as the outcome of a war of attrition where partners share the preference for the same sexual role, and both hide their ‘willingness’ to play the less preferred one, until one individual reaches its cost threshold and accepts the less preferred sexual role.

Egg-trading worms start reciprocation with caution, respond with confidence and care about partners’ quality

“…Annelid body size is not fixed, and these worms can vary their body length and diameter because of their hydrostatic skeleton 82 . However, the prolonged and repeated bodily movements that worms exhibit while in physical contact prior to mating (e.g., rubbing 51 ) might allow them to gather chemical and mechanosensory information on their partner’s body size, egg maturation and willingness to donate eggs. The fact that these behavioral interactions were more frequent between more size-dissimilar worms suggests that reaching a deal is more complex between more dissimilar worms and requires prolonged reciprocal interactions.…”

“…For size assortment in particular, these include contingent conditions such as physical constraints on mating/copulation (e.g., 81 ) and spatial segregation (e.g., in hermaphroditic freshwater snails 86 ; and fish 33 ). In O. diadema worms, there is no physical limitation to mating between unmatched partners (fertilization is external although sperm are released inside the egg cocoon 39 , 51 ), and the rarity of the species 39 does not support spatial segregation in the wild. The current results suggest that size-assortative mating might enforce reciprocity and ensure matched benefits between partners, but the evolutionary link between assortative mating and egg trading deserves further theoretical investigation 66 .…”

“…We investigated whether newly paired partners interacted before starting egg exchanges and whether they regulated their interactions to suit their partner’s quality. Previous work showed that mating (pseudocopulation, i.e., external egg fertilization which occurs inside the egg cocoon while partners are in physical contact with each other 39 , 51 ) is preceded by partners following, being in contact and rubbing against each other’s bodies 51 . We hypothesized that worms in more size-dissimilar pairs would encounter broader conflicts over the start of reciprocal exchanges than those paired with size-matched partners and expected that they would interact more to solve the conflicts.…”

“…Once the mating pair has formed, worms engage in activities at and outside the nest (e.g., parental care of egg-cocoons, rubbing their partner and foraging, respectively) and regularly make their way back to the nest using the dense web of mucous trails they build 50 . While rubbing takes most of the time partners spend at the nest, mating (egg releasing by one worm and egg fertilizing by the other) is rapid and occurs every 2 days 51 . There is no evidence that worms recognize their mating partners, but they might use chemical cues in the mucous trails and around the nest to ensure that they encounter their partner again 52 .…”

New perspectives on meeting and mating

“…While the preceding two studies focus on species with unusual modes of sperm transfer, these organisms still have the conventional sexes, namely males and females. The paper by Lorenzi et al (2019) focusses on a situation where both sexes are present in the same individual, i.e., simultaneous hermaphrodites. Specifically, they used an experimental approach to investigate the long and complex precopulatory behaviour used by a polychaete worm to make its decision about the sexual role to adopt.…”