Asexual Reproduction Can Account for the High Diversity and Prevalence of Rare Taxa Observed in Microbial Communities.

Abstract

Recent studies evaluating the community structures of microorganisms and macroorganisms have found greater diversity and rarity within micro-scale communities, compared to macro-scale communities. However, reproductive method has been a confounding factor in these comparisons; the microbes considered generally reproduce asexually, while the macroorganisms considered generally reproduce sexually. Sexual reproduction imposes the constraint of mate finding, which can have significant demographic consequences by depressing birth rates at low population sizes. First, I construct an island biogeography model to study the organization of ecological communities under neutral stochastic processes. Then, I examine theoretically how the effects of mate finding in sexual populations translate to the emergent community properties of diversity, rarity, and dominance (size of the largest population). In mate-limited sexual populations, the decreased growth rates at low population densities translate to a higher extinction rate; this increased extinction rate had a disproportionately strong effect on taxa with low population densities. Thus, mate limitation decreased diversity, primarily by excluding small populations from communities. However, the most abundant taxa were minimally affected by mate limitation. Therefore, mate limitation affected the diversity and rarity of taxa in communities but did not alter the dominance of the largest population. The observed shifts in community structure mirror recent empirical studies of micro-scale versus macro-scale communities, which have shown that microbial communities have greater diversity and rarity than macrobial communities but are not different in dominance. Thus, reproductive method may contribute to observed differences in emergent properties between communities at these two scales.IMPORTANCE There have been numerous recent efforts to integrate microbes into broad-scale ecological theories. Microbial communities are often structurally distinct from macrobial communities, but it is unclear whether these differences are real or whether they are due to the different methodologies used to study communities at these two scales. One major difference between macroorganisms and microorganisms is that microbes are much more likely to reproduce asexually. Sexually reproducing taxa have diminished growth rates at low population size, because they must encounter another member of their species before reproducing. This study shows that communities of asexually reproducing taxa are expected to be more diverse, because taxa persist longer. Furthermore, asexually reproducing taxa can exist at much lower densities than sexually reproducing taxa. Thus, asexual reproduction by microbes can account for two major differences between microbial and macrobial communities, namely, greater diversity and greater prevalence of rare taxa for microbes.