Biodiversity of marine microbes is safeguarded by phenotypic heterogeneity in ecological traits

Conclusion: A paradigm shift is needed to adequately conceptualize microbial populations Our theory implies that a shift in perspective is needed when conceptualizing microbial popu- lations. A microbe-centric perspective is necessitated by the fact that microbial ecology and evolution are subject to very different principles than the multi-cellular organisms upon which much biological theory was developed. The fundamental importance of microbes requires that the shape of the distribution of competitive strategies be investigated as a possible unifying and structuring principle governing the biodiversity of asexually reproducing microbes. We pre- dict that maximally variable trait distributions will be typical, because of their adaptive fea- tures. Our results also suggest that high phenotypic heterogeneity is expected in populations that persist through multiple rounds of competition even in the absence of environmental patchiness and that such heterogeneity may largely reflect inherent characteristics of species [51] rather than methodological limitations or differences [8]. Interestingly, the discovered equilibrium strategies display the very same features observed in microbes: (1) these strategies have maximal phenotypic heterogeneity and (2) there are an unlimited number of these strate- gies which are neutral towards each other, implying they cannot universally competitively exclude each other. The mathematics reflects the biological qualities of microbes. This funda- mental model for microbes can accommodate more complicated variations, which we have

not explored here in order to convey the fundaments of the theory. Disease dynamics, ecosystem function and evolutionary insights can be propelled forward by accounting for the direct linkage from individuals to communities to macroscopic pro- cesses such as the abundance and distribution of organisms without the loss of insight imparted by averaging out variability. We suggest that inherent phenotypic heterogeneity may be an essential determinant of microbe ecology. Remarkably, the role of phenotypic het- erogeneity is in direct contrast to diversity maintenance mechanisms that rely on ever- increasing numbers of niches because of spatial and temporal heterogeneity [46, 52], or more inclusive lists of traits that underlie fitness [53]. If true, our theory suggests a fundamentally different mechanism, one where trait selection favors variable distributions, rather than an optimum value with minimal variation. Furthermore, the distribution is at least as important as the average. There should be stabilizing selection on the generation of phenotypic hetero- geneity in an adapted population, rather than a minimization of that variation around an optimum value. A major implication of these findings is the prediction that entropy in the system always increases because equilibrium strategies have maximal entropy and promote unlimited coexis- tence and emergence of new species. Biological diversity continuously expands. It has not escaped our notice that we may have also discovered a mechanism to explain one of the funda-

mental laws in biology, that of ever-increasing complexity in evolving systems [54]. Our focus here was chiefly on marine microbes because we can support our arguments with empirical observations and constrain descriptions to specifics. Yet, there is no reason why the same rules should not apply to other, free-living microbes. Rather than habitat, phenotypic heterogeneity is a key factor in species persistence and diversity. Based on the mathematics, there is nothing to suggest that other free-living microbes would not be subject to similar principles. In fact, we believe that here we present a unifying theory that phenotypic heterogeneity enhances biodiversity. Supporting information S1 Fig. Reproducing competitive exclusion. Competition between uniform (blue) and an inferior competitor (orange) that has mean competitive ability < 0.5. In this case, our model PLOS ONE Biodiversity of marine microbes is safeguarded by phenotypic heterogeneity in ecological traits PLOS ONE | https://doi.org/10.1371/journal.pone.0254799 August 4, 2021 14 / 18