Many ways to stay in the game: individual variability maintains high biodiversity in planktonic microorganisms

Abstract

In apparent contradiction to competition theory, the number of known, coexisting plankton species far exceeds their explicable biodiversity-a discrepancy termed the Paradox of the Plankton. We introduce a new game-theoretic model for competing microorganisms in which one player consists of all organisms of one species. The stable points for the population dynamics in our model, known as strategic behaviour distributions (SBDs), are probability distributions of behaviours across all organisms which imply a stable population of the species as a whole. We find that intra-specific variability is the key characteristic that ultimately allows coexistence because the outcomes of competitions between individuals with variable competitive abilities are unpredictable. Our simulations based on the theoretical model show that up to 100 species can coexist for at least 10 000 generations, and that even small population sizes or species with inferior competitive ability can survive when there is intra-specific variability. In nature, this variability can be observed as niche differentiation, variability in environmental and ecological factors, and variability of individual behaviours or physiology. Therefore, previous specific explanations of the paradox are consistent with and provide specific examples of our suggestion that individual variability is the mechanism which solves the paradox.

Metatranscriptome analyses indicate resource partitioning between diatoms in the field

“…As was highlighted by Hutchinson (18), the phytoplankton violate Gause's law of competitive exclusion, which posits that two organisms competing for the same resources cannot coexist. Much thought has gone toward identifying the cause of the "paradox of the plankton," including explanations such as "contemporaneous disequilibrium" of patchy phytoplankton distributions (19), life history differences (20), species oscillations (21), environmental fluctuation (22), intraspecific variation (23), and differential niche partitioning (24). Of these potential factors, one of the most difficult to observe directly in the plankton is niche partitioning.…”

Co‐existence of distinct Ostreococcus ecotypes at an oceanic front

“…The exclusion timescale between two phenotypes depends on how close they are in relative fitness, and the bigger the difference in relative fitness, the faster the exclusion timescale (Barton et al ). Co‐existence may also be facilitated by the degree of individual variation within each population (Menden‐Deuer and Rowlett ), which could impact exclusion timescales by affecting the cumulative competitive ability between phenotypes. We do not have sufficient information on the physiologies or genetic diversity of Ostreococcus ecotypes to evaluate any measure of their relative fitness.…”

The theory of games and microbe ecology

“…Recent empirical data confirm that variations in motility at the strain level manifest themselves in different population distributions (Harvey et al 2015). Such intra-specific variability may enhance species survival and coexistence and has been suggested to be adaptive based on model simulations (Menden-Deuer and Rowlett 2014). Observations of intra-specific variability in marine microbes are not restricted to artificial laboratory settings.…”