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

mean fitness, in the sense that they must be locally adapted to different environmental niches. In contrast, our theory shows that multiple species with the same average fitness in the same environment (niche) can coexist indefinitely, as long as individuals within those species vary maximally in their competitive abilities. The theory predicts survival of the most variable and equally cumulatively fit individuals and thus predicts co-existence of such species. This find- ing implies that selection in generally adapted species favors maintenance of variability rather than the evolution of optimized trait values but also that the production of intra-specific or intra-genotype variation in trait values is adaptive. The genetic maintenance of intra-geno- mic variability has been reported [25]. The distribution of risk afforded by phenotypic het- erogeneity also points to a potential adaptive reservoir in physiological, behavioral and genetic diversity in light of large-scale changes occurring in ecosystems, including climate change [47, 48]. Intra-specific phenotypic variability thwarts invasion, promotes co- existence, and allows emergence of new species These mathematical proofs and supporting model results provide a fundamentally different mechanism for species co-existence than those previously advanced. There are several prior demonstrations that multiple species can coexist in the same niche or consuming the same resource, thus circumventing the competitive exclusion principle, such as two predators

existing on different life stages of the same prey species, or asynchronous introduction of two competitors into a system; see [44, 49] and references therein. These previously advanced solutions are similar in that they introduce some asynchrony in the competing species, thus essentially separating competitors and eliminating direct competition. This is equivalent to invoking environmental patchiness in either space or time to increase the number of avail- able niches. This type of asynchrony likely enhances species co-existence in numerous cases but is fundamentally an extension of the competitive exclusion principle; it expands the num- ber of niches but still relies on an assumption of one species per niche. Our results agree with the two species model in [34] but contradict their suggestion that in multi-species competi- tion, phenotypic heterogeneity depresses biodiversity. There is no mathematical contradic- tion because [34] considered a single trait with variations around a normal distribution whereas we mathematically analyze all traits and all distributions. The mechanism advanced here directly confronts competitors and is flexible in terms of the assumptions regarding population sizes and other specifics. We show that 100’s of species can coexist in the same niche despite direct cell-cell competitions simply by incorporating the high phenotypic het- erogeneity that is one of the empirically observed, fundamental characteristics of microbial populations. This study also identifies a novel adaptive advantage (persistence in the face of competitors)

and consequence (maintenance of diversity) of phenotypic heterogeneity. Phenotypic hetero- geneity has previously been suggested to be adaptive because it can increase survival in heter- ogenous or fluctuating environments by allowing genotypes to bet-hedge [24], but there are no studies addressing how phenotypic heterogeneity may be advantageous in a homogeneous environment, and why natural selection might favor a particular shape of phenotypic heteroge- neity. We demonstrate that because competitive interactions occur between individuals, the heterogenous condition can just as easily stem from the phenotypic heterogeneity in capabili- ties of competitors rather than features of the abiotic environment. Our findings explain how very high levels of genotype diversity [11, 50] can be maintained without invoking niche parti- tioning within species. 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 13 / 18