Evidence for environmental and ecological selection in a microbe with no geographic limits to gene flow

Abstract

The ability for organisms to disperse throughout their environment is thought to strongly influence population structure and thus evolution of diversity within species. A decades-long debate surrounds processes that generate and support high microbial diversity, particularly in the ocean. The debate concerns whether diversification occurs primarily through geographic partitioning (where distance limits gene flow) or through environmental selection, and remains unresolved due to lack of empirical data. Here we show that gene flow in a diatom, an ecologically important eukaryotic microbe, is not limited by global-scale geographic distance. Instead, environmental and ecological selection likely play a more significant role than dispersal in generating and maintaining diversity. We detected significantly diverged populations (FST > 0.130) and discovered temporal genetic variability at a single site that was on par with spatial genetic variability observed over distances of 15,000 km. Relatedness among populations was decoupled from geographic distance across the global ocean and instead, correlated significantly with water temperature and whole-community chlorophyll a Correlations with temperature point to the importance of environmental selection in structuring populations. Correlations with whole-community chlorophyll a, a proxy for autotrophic biomass, suggest that ecological selection via interactions with other plankton may generate and maintain population genetic structure in marine microbes despite global-scale dispersal. Here, we provide empirical evidence for global gene flow in a marine eukaryotic microbe, suggesting that everything holds the potential to be everywhere, with environmental and ecological selection rather than geography or dispersal dictating the structure and evolution of diversity over space and time.