Biogeographic patterns in ocean microbes emerge in a neutral agent-based model

Abstract

A key question in ecology and evolution is the relative role of natural selection and neutral evolution in producing biogeographic patterns. Here we quantify the role of neutral processes by simulating division, mutation and death of 100k individual marine bacteria cells with full 1 Mbp genomes in a global surface ocean circulation model. The model is run for up to 100k years and output is analyzed using BLAST alignment and metagenomics fragment recruitment. Simulations show the production and maintenance of biogeographic patterns, characterized by distinct provinces subject to mixing and periodic takeovers by neighbors (coalescence), after which neutral evolution re-establishes the province and the patterns reorganize. The emergent patterns are substantial (e.g., down to 99.5% DNA identity between North and Central Pacific provinces) and suggest that microbes evolve faster than ocean currents can disperse them. This approach can also be used to explore environmental selection. Main Text:An important ongoing endeavor in ecology and evolution is to understand the mechanisms underlying the geographic distribution patterns of organisms. Natural selection by contemporary environmental factors acting on adaptive mutations or a persistent seed bank of species is one mechanism that can create such patterns. Neutral evolution (selectively neutral mutations and genetic drift) coupled with dispersal limitation or isolation is another mechanism (1-6). These processes are not mutually exclusive and, for microbes in the global surface ocean, molecular observations (e.g., shotgun sequencing, (7)) provide support for the role of both mechanisms (8-11).Here we ask: How does neutral evolution influence the biogeographic distribution of surface ocean microbes? To what extent does dispersion allow for different operational taxonomic units (OTUs) to develop and persist? Are there emerging spatial patterns (e.g., provinces, (12)) and how do these change in time?Several approaches are available to quantify the contribution of the various processes in generating and maintaining biogeographic patterns among ocean microbes (2). A common empirical approach involves correlating observations (e.g., microbial composition) with environmental variables, subtracting out this environment effect and then correlating with geographic distance. In the ocean, hydrodynamic models coupled with tracers, either Eulerian concentration or Lagrangian particles, can be used as a measure of "connectivity" to supplement empirical relations (10,13). A problem with this approach is that one can never be sure that the distance effect is not actually caused by an unmeasured environmental variable. Mechanistic models constitute an alternative approach. Eulerian models with coupled phytoplankton ecology and biogeochemistry can simulate biogeographic patterns produced by environmental selection (14). However, the Eulerian approach generally assumes all species are present everywhere and does not consider dispersal limitation.An alternative approach is to u...

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

“…The physical connectivity of global surface seawater is estimated to be on the order of decades (19); this time frame aligns with the potential for gene flow in planktonic microbes. If microbes evolve more quickly than global circulation patterns can disperse them, we would expect biogeographic patterns to emerge; the potential for biogeographic patterns deriving from neutral evolution has been demonstrated in recent modeling efforts (18). Because we observed no correlation between geographic distance and population divergence on global scales, but still observed distinct populations in this species, it is likely that divergence observed in T. rotula populations is a product of ongoing selective forces that reduce gene flow among populations and allow them to persist over time frames greater than decadal-scale global surface seawater connectivity and perhaps even longer, given empirical evidence in the diatom S. marinoi, which exhibits stable F ST divergence on time scales of 100 y (54).…”

“…However, despite the evolutionary significance of environmental selection, its role in structuring populations within species occupying the high dispersal environment of the global ocean remains unclear. The additional role of dispersal and geography in structuring populations throughout the global ocean has added complexity to the debate (5,17,18).…”

Phytoplankton adapt to changing ocean environments

“…We do not know the constraints or timescales required for phytoplankton to adapt to changes in environmental conditions anticipated over the next century. Phytoplankton species have short generation times and large population sizes, so they may be particularly able to adapt to rapid climate change (20,21). In addition, temperature response curves measured in the laboratory show that phytoplankton usually have the fastest growth rates at or slightly below the mean temperature of the environment they were isolated from, suggesting that natural populations are adapted to their local environment (15,22), although some species have niches that do not reflect the environmental conditions from which they were isolated (23).…”

The 16S rRNA gene in the study of marine microbial communities

“…Además de abundantes, las comunidades microbianas marinas son altamente diversas debido a que los microorganismos se originaron en un mismo ambiente y han evolucionado adaptaciones fisiológicas exitosas (Hellweger et al 2014).…”

“…Having originated in a similar environment, marine microbial communities are highly abundant and diverse and have developed successful physiological adaptations (Hellweger et al 2014).…”