Evolutionary consequences of gene flow in the absence or inhibition of dispersal in microbial communities

Abstract

Much of our understanding of the evolutionary dynamics of microbial populations is derived from population level studies which focus on the immediately present populations and ignore the contributions of nearby communities. Microbial ecology studies typically do not distinguish between gene flow, i.e., the movement of genetic material between populations, and dispersal, i.e., the movement of those populations themselves. These two processes are indeed linked, but not identical. We have known for centuries that genetic material can be transferred between physically distant and taxonomically disparate microbial populations; molecular biology tools like cloning are dependent on this capability. In other words, gene flow can occur even without dispersal. However, our ecological and evolutionary studies of microbial populations typically fail to acknowledge the evolutionary impact and genetic contributions of outside populations. Unique evolutionary scenarios arise when dispersal between two or more populations is prevented or limited, but gene flow can still occur between them. We hypothesized that this scenario would impact microbial populations by facilitating speciation, selection, and local adaptation. We aimed to test this hypothesis by studying endemic Meiothermus populations inhabiting serpentinite rocks in the subsurface of the Samail ophiolite in Oman. Samail Ophiolite microbial communities, of which Meiothermus populations are a component, are dispersed across the subsurface and separated by meters of solid rock and by chemical and pH gradients spanning orders of magnitude. Despite barriers to dispersal that are significant enough to shape community structure, we found that gene flow still occurred between nearly all observed populations of Meiothermus. This gene flow is contributing to disruptive selection amongst cohabiting populations, and may also be contributing to local adaptation, both at the genetic and genomic level. We also identified potential mechanisms for this gene flow, including abundant viral elements. The sequence similarity of mobile genetic elements in these Meiothermus populations implies that this gene flow occurred after colonization by a common Meiothermus ancestor and that diversification is likely ongoing. To our knowledge, this is the first demonstration of gene flow across barriers to dispersal in an environmental microbial system. In conclusion, these results suggest that the capacity for microbial populations to undergo gene flow even in the absence or inhibition of dispersal is a natural process, has substantial consequences for the evolution of the effected population, and may also have consequences for the microbial and surrounding environment.