Journal
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
Volume 112, Issue 24, Pages 7530-7535Publisher
NATL ACAD SCIENCES
DOI: 10.1073/pnas.1410631112
Keywords
adaptive landscape; experimental evolution; NK model; landscape topography; spatial structure
Categories
Funding
- National Science Foundation (NSF) [DBI-0939454]
- NSF Graduate Research Fellowship
- NSF CAREER Award [DEB0952825]
- Direct For Biological Sciences
- Division Of Environmental Biology [0952825] Funding Source: National Science Foundation
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In the context of Wright's adaptive landscape, genetic epistasis can yield a multipeaked or rugged topography. In an unstructured population, a lineage with selective access to multiple peaks is expected to fix rapidly on one, which may not be the highest peak. In a spatially structured population, on the other hand, beneficial mutations take longer to spread. This slowdown allows distant parts of the population to explore the landscape semiindependently. Such a population can simultaneously discover multiple peaks, and the genotype at the highest discovered peak is expected to dominate eventually. Thus, structured populations sacrifice initial speed of adaptation for breadth of search. As in the fable of the tortoise and the hare, the structured population (tortoise) starts relatively slow but eventually surpasses the unstructured population (hare) in average fitness. In contrast, on single-peak landscapes that lack epistasis, all uphill paths converge. Given such smooth topography, breadth of search is devalued and a structured population only lags behind an unstructured population in average fitness (ultimately converging). Thus, the tortoise-hare pattern is an indicator of ruggedness. After verifying these predictions in simulated populations where ruggedness is manipulable, we explore average fitness in metapopulations of Escherichia coli. Consistent with a rugged landscape topography, we find a tortoise-hare pattern. Further, we find that structured populations accumulate more mutations, suggesting that distant peaks are higher. This approach can be used to unveil landscape topography in other systems, and we discuss its application for antibiotic resistance, engineering problems, and elements of Wright's shifting balance process.
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