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Cited by 41Evolution and Genetic DynamicsInsect symbiosis and bacterial influencesGenomics and Phylogenetic Studies

Reduced selective constraint in endosymbionts: elevation in radical amino acid replacements occurs genome-wide

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Wernegreen, Jennifer J.·2011·PLoS ONE
DOI 10.1371/journal.pone.0028905PMC PMC3237559
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Abstract

As predicted by the nearly neutral model of evolution, numerous studies have shown that reduced N(e) accelerates the accumulation of slightly deleterious changes under genetic drift. While such studies have mostly focused on eukaryotes, bacteria also offer excellent models to explore the effects of N(e). Most notably, the genomes of host-dependent bacteria with small N(e) show signatures of genetic drift, including elevated K(a)/K(s). Here, I explore the utility of an alternative measure of selective constraint: the per-site rate of radical and conservative amino acid substitutions (D(r)/D(c)). I test the hypothesis that purifying selection against radical amino acid changes is less effective in two insect endosymbiont groups (Blochmannia of ants and Buchnera of aphids), compared to related gamma-Proteobacteria. Genome comparisons demonstrate a significant elevation in D(r)/D(c) in endosymbionts that affects the majority (66-79%) of shared orthologs examined. The elevation of D(r)/D(c) in endosymbionts affects all functional categories examined. Simulations indicate that D(r)/D(c) estimates are sensitive to codon frequencies and mutational parameters; however, estimation biases occur in the opposite direction as the patterns observed in genome comparisons, thereby making the inference of elevated D(r)/D(c) more conservative. Increased D(r)/D(c) and other signatures of genome degradation in endosymbionts are consistent with strong effects of genetic drift in their small populations, as well as linkage to selected sites in these asexual bacteria. While relaxed selection against radical substitutions may contribute, genome-wide processes such as genetic drift and linkage best explain the pervasive elevation in D(r)/D(c) across diverse functional categories that include basic cellular processes. Although the current study focuses on a few bacterial lineages, it suggests D(r)/D(c) is a useful gauge of selective constraint and may provide a valuable alternative to K(a)/K(s) when high sequence divergences preclude estimates of K(s). Broader application of D(r)/D(c) will benefit from approaches less prone to estimation biases.

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  • Traces of relaxed selection have been documented in bacterial endosymbionts, including fixation of deleterious alleles and overall elevated rates of nonsynonymous and radical amino acid replacements.

    “Accordingly, traces of relaxed selection have been documented in bacterial endosymbionts, including fixation of deleterious alleles (e.g., loss of DNA replication proofreading enzymes) and overall elevated rates of nonsynonymous and radical amino acid replacements (Wernegreen 2011).”

    From RELAX: Detecting Relaxed Selection in a Phylogenetic Framework (2015) · cites this paper as Wernegreen 2011

    The Introduction (page unavailable) reports genome-wide rate acceleration concentrated at nonsynonymous sites, and the Discussion reports elevated radical replacements and evidence consistent with fixation of slightly deleterious mutations. The copy does not document the cited example of lost DNA-replication proofreading enzymes. The Discussion also says relaxed selection may contribute but is unlikely to explain the genome-wide pattern on its own; it favors genetic drift and linkage. (LLM, conf=0.84)

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Authors
Wernegreen, J. J.
Affiliations
Duke University (US)
Corresponding author
Wernegreen, Jennifer J.
ORCID
Wernegreen, Jennifer J.
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2011-12-14
Volume
6
Issue
12
Pages
e28905
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0028905
PMC
PMC3237559
OpenAlex
W2077622071
Cited by
41
References
1
Citations by year
2025: 1 · 2024: 3 · 2023: 2 · 2022: 1 · 2021: 1 · 2020: 4 · 2019: 3 · 2017: 4 · 2016: 3 · 2015: 2 · 2014: 10 · 2013: 5 · 2012: 2
FWCI
3.17
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
Funders
  • National Science Foundation (1103113)
  • National Institutes of Health
  • National Institute of General Medical Sciences (R01GM062626)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
  • Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect symbiosis and bacterial influences
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
Keywords
endosymbionts, purifying selection, genetic drift, effective population size, Buchnera, insect endosymbionts, genome degradation, linkage, codon frequency, estimation bias
MeSH terms
Amino Acids, Analysis of Variance, Animals, Ants, Aphids, Base Sequence, Codon, Computer Simulation, Phylogeny, Selection, Genetic, Species Specificity, Symbiosis, Genetic Variation, Genome, Bacterial, Buchnera, Databases, Genetic

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