Synchronized emergence under diatom sperm competition

Abstract

Appropriate timing of mating is crucial for the success of individuals. However, we know little about factors that explain variation in mating time in unicellular organisms. Unicellular eukaryotes often have facultative sexuality, that is, the less frequent sex is occasionally induced after long clonal reproduction. Thus, males originated from clonemates could be non-negligible mating rivals. Using a centric diatom whose clonal cells differentiate into either male or female, we analysed whether males (spermatogonium) compete or cooperate with each other. By analysing differentiation timing with hypotheses based on evolutionary game theory, we estimated that a substantial part of the variation in the mating timing of the diatom can be explained by results of optimization through interactions among selfish individuals rather than cooperation among clonemates. However, the competition is fiercer than expected owing to excessive synchronization, which was realized by adjustment of meiotic duration: cells completed mitotic division in the earlier mating phase took longer to enter into meiosis, whereas late-dividing cells entered into meiosis more quickly. Adjacent cells tended to synchronize, and model analyses suggest that cell–cell interaction can create a gap between the optimal and actual decisions. Our results provide insights into the evolution of cellular decision making and its restriction.