Reproduction of a marine planktonic protist: Individual success versus population survival

Abstract

Understanding the biology of reproduction is important for retracing key evolutionary processes in organisms, yet gaining detailed insights often poses major challenges. Planktonic Foraminifera are globally distributed marine microbial eukaryotes and important contributors to the global carbon cycle. Their extant biodiversity shows restricted distribution patterns of some species, whereas others are cosmopolitan in the world ocean. Planktonic Foraminifera cannot be bred under laboratory conditions, and thus details of their life cycle remain incomplete. Solely the production of flagellated gametes has been observed and taken as an indication for an exclusively sexual reproduction. Yet, sexual reproduction by spawning of gametes in the open ocean relies on sufficient gamete encounters to maintain viable populations, which represents a problem for organisms that lack the means of active propulsion and are marked by low population densities. To increase knowledge on the reproductive biology of planktonic Foraminifera, we applied a dynamic, individual-based modelling approach with parameters based on laboratory and field observations to test if random gamete encounters under commonly observed population densities are sufficient for maintaining viable populations. We show that temporal synchronization and potentially spatial concentration of gamete release seems inevitable for maintenance of the population. We 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. Our modelling approach helps to illuminate foraminiferal population dynamics and to predict the existence of necessary reproduction strategies, which may be detected in future field experiments. This study therefore contributes to our understanding of plankton ecology and evolution and their reproductive strategies in the open ocean.