Abstract
Background: Most clinical and natural microbial communities live and evolve
in spatially structured environments. When changes in environmental conditions
trigger evolutionary responses, spatial structure can impact the types of
adaptive response and the extent to which they spread. In particular,
localized competition in a spatial landscape can lead to the emergence
of a larger number of different adaptive trajectories than would be found
in well-mixed populations. Our goal was to determine how two levels of
spatial structure affect genomic diversity in a population and how this
diversity is manifested spatially.
Methodology/Principal Findings: We serially transferred bacteriophage
populations growing at high temperatures (40ºC) on agar plates for 550
generations at two levels of spatial structure. The level of spatial
structure was determined by whether the physical locations of the phage
subsamples were preserved or disrupted at each passage to fresh bacterial
host populations. When spatial structure of the phage populations was
preserved, there was significantly greater diversity on a global scale
with restricted and patchy distribution. When spatial structure was
disrupted with passaging to fresh hosts, beneficial mutants were spread
across the entire plate. This resulted in reduced diversity, possibly due
to clonal interference as the most fit mutants entered into competition on
a global scale. Almost all substitutions present at the end of the adaptation
in the populations with disrupted spatial structure were also present in the
populations with structure preserved.
Conclusions/Significance: Our results are consistent with the patchy
nature of the spread of adaptive mutants in a spatial landscape. Spatial
structure enhances diversity and slows fixation of beneficial mutants. This
added diversity could be beneficial in fluctuating environments. We also
connect observed substitutions and their effects on fitness to aspects of
phage biology, and we provide evidence that some substitutions exclude each
other.