Simple phenotypic sweeps hide complex genetic changes in populations

Ram P. Maharjan, Bin Liu, Lu Feng, Thomas Ferenci, Lei Wang

Research output: Contribution to journalArticle

10 Citations (Scopus)

Abstract

Changes in allele frequencies and the fixation of beneficial mutations are central to evolution. The precise relationship between mutational and phenotypic sweeps is poorly described however, especially when multiple alleles are involved. Here, we investigate these relationships in a bacterial population over 60 days in a glucose-limited chemostat in a large population. High coverage metagenomic analysis revealed a disconnection between smooth phenotypic sweeps and the complexity of genetic changes in the population. Phenotypic adaptation was due to convergent evolution and involved soft sweeps by 7-26 highly represented alleles of several genes in different combinations. Allele combinations spread from undetectably low baselines, indicating that minor subpopulations provide the basis of most innovations. A hard sweep was also observed, involving a single combination of rpoS, mglD, malE, sdhC, and malT mutations sweeping to greater than 95% of the population. Other mutant genes persisted but at lower abundance, including hfq, consistent with its demonstrated frequency-dependent fitness under glucose limitation. Other persistent, newly identified low-frequency mutations were in the aceF, galF, ribD and asm genes, in noncoding regulatory regions, three large indels and a tandem duplication; these were less affected by fluctuations involving more dominant mutations indicating separate evolutionary paths. Our results indicate a dynamic subpopulation structure with a minimum of 42 detectable mutations maintained over 60 days. We also conclude that the massive population-level mutation supply in combination with clonal interference leads to the soft sweeps observed, but not to the exclusion of an occasional hard sweep.

Original languageEnglish
Pages (from-to)531-544
Number of pages14
JournalGenome Biology and Evolution
Volume7
Issue number2
DOIs
Publication statusPublished - Feb 2015
Externally publishedYes

Bibliographical note

Copyright the Author(s) 2015. Version archived for private and non-commercial use with the permission of the author/s and according to publisher conditions. For further rights please contact the publisher.

Keywords

  • experimental evolution
  • mutational sweeps
  • Escherichia coli K12/cytology
  • metagenomics
  • Gene Frequency/genetics
  • Genes, Bacterial
  • Genotype
  • INDEL Mutation/genetics
  • Phenotype
  • Sequence Analysis, DNA
  • periodic selection
  • E. coli genome

Fingerprint Dive into the research topics of 'Simple phenotypic sweeps hide complex genetic changes in populations'. Together they form a unique fingerprint.

  • Cite this

    Maharjan, R. P., Liu, B., Feng, L., Ferenci, T., & Wang, L. (2015). Simple phenotypic sweeps hide complex genetic changes in populations. Genome Biology and Evolution, 7(2), 531-544. https://doi.org/10.1093/gbe/evv004