Dynamic modulation of reproductive strategies in a simultaneous hermaphrodite and preference for the male role

Abstract

Reproductive traits are often tightly linked to variations in the social environment. In animals with separate sexes, producing male or female offspring results in different fitness gains depending on population structure. In simultaneous hermaphrodites, allocating a given proportion of resources to the two sexes results in fitness gains that depend on mating opportunities, and extremely plastic hermaphrodites may have a selective advantage. To test to what extent hermaphrodites have flexible and reversible sex allocation at the individual level, we exposed hermaphroditic Ophryotrocha diadema worms (an obligatorily nonselfing polychaete, with low numbers of aflagellate, immotile sperm and ‘pseudocopulation’) to weekly changes in actual or simulated mating opportunities and mate competition (controlling for density effects). We found that worms rapidly switched from high investment in the female function (eggs and courting) to high investment in the male function (aggressive behaviour) with increasing mating opportunities. Simulated mate competition and competition over the male role triggered similar variations in egg production (i.e. worms laid fewer eggs), indicating that these worms preferred to mate in the male role. These results highlight the key role of behaviour in the study of reproductive investment in hermaphrodites and the importance of plasticity in sex allocation (including precopulatory behaviours) in hermaphrodites as a way to compete for the male role and to keep hermaphroditism stable in fluctuating environments.