Speedy speciation in a bacterial microcosm: new species can arise as frequently as adaptations within a species

Abstract

Microbiologists are challenged to explain the origins of enormous numbers of bacterial species worldwide. Contributing to this extreme diversity may be a simpler process of speciation in bacteria than in animals and plants, requiring neither sexual nor geographical isolation between nascent species. Here, we propose and test a novel hypothesis for the extreme diversity of bacterial species-that splitting of one population into multiple ecologically distinct populations (cladogenesis) may be as frequent as adaptive improvements within a single population's lineage (anagenesis). We employed a set of experimental microcosms to address the relative rates of adaptive cladogenesis and anagenesis among the descendants of a Bacillus subtilis clone, in the absence of competing species. Analysis of the evolutionary trajectories of genetic markers indicated that in at least 7 of 10 replicate microcosm communities, the original population founded one or more new, ecologically distinct populations (ecotypes) before a single anagenetic event occurred within the original population. We were able to support this inference by identifying putative ecotypes formed in these communities through differences in genetic marker association, colony morphology and microhabitat association; we then confirmed the ecological distinctness of these putative ecotypes in competition experiments. Adaptive mutations leading to new ecotypes appeared to be about as common as those improving fitness within an existing ecotype. These results suggest near parity of anagenesis and cladogenesis rates in natural populations that are depauperate of bacterial diversity.