Accelerated evolution and Muller’s Rachet in endosymbiotic bacteria
Open accessAbstract
Many bacteria live only within animal cells and infect hosts through cytoplasmic inheritance. These endosymbiotic lineages show distinctive population structure, with small population size and effectively no recombination. As a result, endosymbionts are expected to accumulate mildly deleterious mutations. If these constitute a substantial proportion of new mutations, endosymbionts will show (i) faster sequence evolution and (ii) a possible shift in base composition reflecting mutational bias. Analyses of 16S rDNA of five independently derived endosymbiont clades show, in every case, faster evolution in endosymbionts than in free-living relatives. For aphid endosymbionts (genus Buchnera), coding genes exhibit accelerated evolution and unusually low ratios of synonymous to nonsynonymous substitutions compared to ratios for the same genes for enterics. This concentration of the rate increase in nonsynonymous substitutions is expected under the hypothesis of increased fixation of deleterious mutations. Polypeptides for all Buchnera genes analyzed have accumulated amino acids with codon families rich in A+T, supporting the hypothesis that substitutions are deleterious in terms of polypeptide function. These observations are best explained as the result of Muller's ratchet within small asexual populations, combined with mutational bias. In light of this explanation, two observations reported earlier for Buchnera, the apparent loss of a repair gene and the overproduction of a chaperonin, may reflect compensatory evolution. An alternative hypothesis, involving selection on genomic base composition, is contradicted by the observation that the speedup is concentrated at nonsynonymous sites.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Relaxed selection has been implicated as both a driver of speciation and a precursor to extinction.
“Relaxed selection has also been implicated as both a driver of speciation (Templeton 2008) and a precursor to extinction (Moran 1996).”
From RELAX: Detecting Relaxed Selection in a Phylogenetic Framework (2015) · cites this paper as Moran 1996
The effective population size of bacterial endosymbionts is smaller than that of their free-living relatives, partially due to the transmission bottleneck across insect generations.
“The effective population size of bacterial endosymbionts is smaller than that of their free-living relatives, partially due to the transmission bottleneck across insect generations (Moran 1996;Funk et al. 2001;Herbeck et al. 2003).”
From RELAX: Detecting Relaxed Selection in a Phylogenetic Framework (2015) · cites this paper as Moran 1996
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Woese, C. R. (1987) · Microbiological Reviews · doi:10.1128/mr.51.2.221-271.1987 · Cited by 5,042 · see citing works
Flagged first, then by citations
Research works printed but not linked: 16
- [1]Kimura, M. (1983) The Neutral Theory of Molecular Evolution (Cambridge Univ. Press, New York).
- [9]Ochman, H. & Wilson, A. C. (1987) in Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology, ed. Neidhardt, F. (Am. Soc. for Microbiol., Washington, DC), pp. 1649-1654.
- [11]Selander, R. K., Caugant, D. A. & Whittam, T. S. (1987) in Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology, ed. Neidhardt, F. (Am. Soc. for Microbiol., Washington, DC), pp. 1625–1648.
- [25]Moran, N. A., Munson, M. A., Baumann, P. & Ishikawa, H. (1993) Proc. R. Soc. London B. 253, 167–171.
- [32]Wu, C.-I. & Li, W.-H. (1985) Proc. Natl. Acad. Sci. USA 82, 1741-1745.
- [36]Lai, C.-Y., Baumann, P. & Baumann, L. (1994) Proc. Natl. Acad. Sci. USA 91, 3819–3823.
- [38]Heie, O. E. (1987) in World Crop Pests, Aphids, eds. Minks, A. K. & Harrewijn, P. (Elsevier, Amsterdam), Vol. 2A, pp. 367–391.
- [41]O'Neill, S. L., Giordano, R., Colbert, A., Karr, T. L. & Robertson, H. M. (1992) Proc. Natl. Acad. Sci. USA 89, 2699–2702.
- [50]Muto, A. & Osawa, S. (1987) Proc. Natl. Acad. Sci. USA 84, 166-169.
- [52]Sueoka, N. (1988) Proc. Natl. Acad. Sci. USA 85, 2653–2657.
- [51]Sueoka, N. (1961) Proc. Natl. Acad. Sci. USA 47, 1141–1149.
- [53]Sharp, P. M. (1989) in Evolution and Animal Breeding, eds. Hill, W. G. & MacKay, T. F. C. (CAB, London), pp. 23–32.
- [58]Swanson, W. J. & Vacquier, V. D. (1995) Proc. Natl. Acad. Sci. USA 92, 4957–4961.
- [61]Riley, M. & Krawiec, S. (1987) in Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology, ed. Neidhardt, F. (Am. Soc. for Microbiol., Washington, DC), pp. 967–981.
- [63]Kimura, M. (1989) in Evolution and Animal Breeding, eds. Hill, W. G. & MacKay, T. F. C. (CAB, London), pp. 13–16.
- [66]Gillham, N. W. (1994) Organelle Genes and Genomes (Oxford Univ. Press, New York), pp. 92–108.
Cited by
Sorted by citations
Evolution Experiments with Microorganisms: The Dynamics and Genetic Bases of Adaptation
Elena, S. F., & Lenski, R. E. (2003) · Nature Reviews Genetics · doi:10.1038/nrg1088 · Cited by 1,386 · see citing works
Domingo, E., Sheldon, J., & Perales, C. (2012) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.05023-11 · Cited by 1,009 · see citing works
A complex journey: transmission of microbial symbionts.
Bright, M., & Bulgheresi, S. (2010) · Nature Reviews Microbiology · doi:10.1038/nrmicro2262 · Cited by 894 · see citing works
Wu, M., Sun, L. V., Vamathevan, J., Riegler, M., Deboy, R., Brownlie, J. C., McGraw, E. A., Martin, W., Esser, C., Ahmadinejad, N., et al. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020069 · Cited by 851 · see citing works
“A general inefficiency of natural selection (especially purifying selection) has been suggested previously for intracellular bacteria, based in part on observations that these bacteria have higher evolutionary rates than free-living bacteria (e.g., Moran 1996).”
RELAX: Detecting Relaxed Selection in a Phylogenetic Framework
Wertheim, J. O., Murrell, B., Smith, M. D., Kosakovsky Pond, S. L., & Scheffler, K. (2015) · Molecular Biology and Evolution · doi:10.1093/molbev/msu400 · Cited by 778 · see citing works
Gene Transfer from Organelles to the Nucleus: How Much, What Happens, and Why?1
Martin, W., & Herrmann, R. G. (1998) · Plant Physiology · doi:10.1104/pp.118.1.9 · Cited by 704 · see citing works
Bromham, L., & Penny, D. (2003) · Nature Reviews Genetics · doi:10.1038/nrg1020 · Cited by 615 · see citing works
McVean, G. A. T., & Charlesworth, B. (2000) · Genetics · doi:10.1093/genetics/155.2.929 · Cited by 336 · see citing works
Cyanobacteria and biogeochemical cycles through Earth history
Sánchez-Baracaldo, P., Bianchini, G., Wilson, J. D., & Knoll, A. H. (2022) · Trends in Microbiology · doi:10.1016/j.tim.2021.05.008 · Cited by 279 · see citing works
Genomic diversity, lifestyles and evolutionary origins of DPANN archaea
Dombrowski, N., Lee, J.-H., Williams, T. A., Offre, P., & Spang, A. (2019) · FEMS Microbiology Letters · doi:10.1093/femsle/fnz008 · Cited by 230 · see citing works
Protein Homeostasis and the Phenotypic Manifestation of Genetic Diversity: Principles and Mechanisms
Jarosz, D. F., Taipale, M., & Lindquist, S. (2010) · Annual Review of Genetics · doi:10.1146/annurev.genet.40.110405.090412 · Cited by 179 · see citing works
Evolution in<i>Candida albicans</i>Populations During a Single Passage Through a Mouse Host
Forche, A., Magee, P. T., Selmecki, A., Berman, J., & May, G. (2009) · Genetics · doi:10.1534/genetics.109.103325 · Cited by 147 · see citing works
Takeuchi, N., Kaneko, K., & Koonin, E. V. (2014) · G3 Genes|Genomes|Genetics · doi:10.1534/g3.113.009845 · Cited by 125 · see citing works
Inevitability of Genetic Parasites
Iranzo, J., Puigbò, P., Lobkovsky, A. E., Wolf, Y. I., & Koonin, E. V. (2016) · Genome Biology and Evolution · doi:10.1093/gbe/evw193 · Cited by 90 · see citing works
“This trend is indeed strikingly apparent in microbes whose life style leads to curtailment of HGT, such as obligate endosymbiotic bacteria (Moran 1996; Mamirova et al. 2007; Moran et al. 2008).”
BackgroundBryant, J., Chewapreecha, C., & Bentley, S. D. (2012) · Future Microbiology · doi:10.2217/fmb.12.108 · Cited by 98 · see citing works
Kneip, C., Voβ, C., Lockhart, P. J., & Maier, U. G. (2008) · BMC Evolutionary Biology · doi:10.1186/1471-2148-8-30 · Cited by 94 · see citing works
“Typically, endosymbiont genes diverge rapidly in comparison to their homologues in free-living relatives, a phenomenon that perhaps reflects genetic drift operating on small population size [3,4] and/or relaxation of structural/functional constraints on endosymbiont protein evolution [5].”
BackgroundEvolutionary dynamics of the chromatophore genome in three photosynthetic Paulinella species
Lhee, D., Ha, J.-S., Kim, S., Park, M. G., Bhattacharya, D., & Yoon, H. S. (2019) · Scientific Reports · doi:10.1038/s41598-019-38621-8 · Cited by 54 · see citing works
- Authors
- Moran, N. A.
- Affiliations
- University of Arizona (US)
- Corresponding author
- Moran, N A
- ORCID
- Moran, N A
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 1996-04-02
- Volume
- 93
- Issue
- 7
- Pages
- 2873-2878
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC39726
- OpenAlex
- W1968179480
- Cited by
- 1,017
- References
- 1
- Citations by year
- 2026: 17 · 2025: 26 · 2024: 24 · 2023: 24 · 2022: 44 · 2021: 61 · 2020: 44 · 2019: 25 · 2018: 49 · 2017: 43 · 2016: 51 · 2015: 27 · 2014: 59 · 2013: 40 · 2012: 33
- FWCI
- 39.88
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect symbiosis and bacterial influences
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- Muller's ratchet, endosymbiotic bacteria, Buchnera, aphid endosymbionts, deleterious mutation accumulation, mutational bias, nonsynonymous substitution rate, synonymous substitution rate, cytoplasmic inheritance, asexual populations, compensatory evolution, 16S rRNA gene, nucleotide composition
- MeSH terms
- Animals, Aphids, Codon, DNA, Bacterial, DNA, Ribosomal, Escherichia coli, Biological Evolution, Insecta, Lactobacillus, RNA, Ribosomal, 16S, Salmonella typhimurium, Symbiosis
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review