Weak epistasis may drive adaptation in recombining bacteria

Brian J. Arnold, Michael U. Gutmann, Yonatan H. Grad, Samuel K. Sheppard, Jukka Corander, Marc Lipsitch, William P. Hanage

Research output: Contribution to journalArticlepeer-review

39 Citations (SciVal)

Abstract

The impact of epistasis on the evolution of multi-locus traits depends on recombination. While sexually reproducing eukaryotes recombine so frequently that epistasis between polymorphisms is not considered to play a large role in short-term adaptation, many bacteria also recombine, some to the degree that their populations are described as “panmictic” or “freely recombining.” However, whether this recombination is sufficient to limit the ability of selection to act on epistatic contributions to fitness is unknown. We quantify homologous recombination in five bacterial pathogens and use these parameter estimates in a multilocus model of bacterial evolution with additive and epistatic effects. We find that even for highly recombining species (e.g., Streptococcus pneumoniae or Helicobacter pylori), selection on weak interactions between distant mutations is nearly as efficient as for an asexual species, likely because homologous recombination typically transfers only short segments. However, for strong epistasis, bacterial recombination accelerates selection, with the dynamics dependent on the amount of recombination and the number of loci. Epistasis may thus play an important role in both the short- and long-term adaptive evolution of bacteria, and, unlike in eukaryotes, is not limited to strong effect sizes, closely linked loci, or other conditions that limit the impact of recombination.

Original languageEnglish
Pages (from-to)1247-1260
Number of pages14
JournalGenetics
Volume208
Issue number3
DOIs
Publication statusPublished - 1 Mar 2018

Bibliographical note

Copyright © 2018 by the Genetics Society of America.

Funding

All data used in this study came from previously published papers shown in Table S1 in File S1. B.J.A. was supported by a postdoctoral fellowship F32 GM120839-01, M.L. by research grant R01AI048935, and W.P.H. by R01AI106786 from the National Institutes of Health (www.nih.gov). These authors were additionally supported by the MIDAS program (U54GM088558). The computations in this paper were run on the Odyssey cluster supported by the Faculty of Arts and Sciences (FAS) Division of Science, Research Computing Group at Harvard University. The authors declare no competing financial interests.

Keywords

  • Approximate Bayesian computation
  • Bacteria
  • Epistasis
  • Homologous recombination
  • Multilocus selection

ASJC Scopus subject areas

  • Genetics

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