Reproduction strategies in a marine protist: A digital experiment

Understanding the biology of reproduction is important for retracing key evolutionary processes (e.g. speciation and adaptation) in any group of organisms, yet gaining detailed insights often poses a major challenge. Planktonic Foraminifera are a group of globally distributed marine microbial eukaryotes that are important contributors to the global carbon cycle and, due to their fossil record, are widely used as model organisms to investigate the responses of plankton to past environmental changes. The extant biodiversity of planktonic Foraminifera shows restricted distribution patterns and local adaptations of some species, whereas others are cosmopolitan in the world ocean. Hypotheses on their diversification and population dynamics so far entirely rely on the assumption of a nearly exclusively sexual reproduction.

So far, reproduction in culture has not been successful under laboratory conditions, and thus details on their life cycle and its influence on the evolution of the group remain unknown. Only the production of flagellated gametes has been observed and is taken as an indication for sexual reproduction. Yet, sexual reproduction by spawning of gametes in the open ocean relies on sufficient gamete encounters to maintain viable populations. This represents a problem especially for unflagellated protists like planktonic Foraminifera, which lack the means of active propulsion and are characterized by low population densities in large areas of the world ocean.

To increase the sparse knowledge on the reproductive biology of planktonic Foraminifera, we applied a dynamic, individual-based modelling approach with parameters based on laboratory and field observations. We tested if random gamete encounters under commonly observed population densities are sufficient for maintaining viable populations or if alternative strategies, such as asexual reproduction or synchronization in depth and time, are indispensable to achieve reproduction success. Our results show that a strict synchronization of gamete release in time and/or space seems inevitable for a successful maintenance of populations. We further argue that planktonic Foraminifera optimized their individual reproductive success at the expense of community-wide gene flow, which may explain their high degree of diversity as well as hampered evolvability. Our modelling approach helps to illuminate the ecology and evolution of this important marine calcifier and to predict the existence of necessary reproduction strategies, which may be detectable in future field and laboratory experiments.