DOI: 10.1098/rstb.2006.1925. Mismatch induced speciation in<i>Salmonella</i>: model and data

Mismatch induced speciation inSalmonella: model and data

10.1098/rstb.2006.1925

Crossref journal-article

The Royal Society

Philosophical Transactions of the Royal Society B: Biological Sciences (175)

Abstract

In bacteria, DNA sequence mismatches act as a barrier to recombination between distantly related organisms and can potentially promote the cohesion of species. We have performed computer simulations which show that the homology dependence of recombination can causede novospeciation in a neutrally evolving population once a critical population size has been exceeded. Our model can explain the patterns of divergence and genetic exchange observed in the genusSalmonella, without invoking either natural selection or geographical population subdivision. If this model was validated, based on extensive sequence data, it would imply that the named subspecies ofSalmonella entericacorrespond to good biological species, making species boundaries objective. However, multilocus sequence typing data, analysed using several conventional tools, provide a misleading impression of relationships withinS. entericasubspeciesentericaand do not provide the resolution to establish whether new species are presently being formed.

Authors 6

Daniel Falush (first)
Mia Torpdahl (additional)
Xavier Didelot (additional)
Donald F Conrad (additional)
Daniel J Wilson (additional)
Mark Achtman (additional)

References 36 Referenced 99

10.1073/pnas.85.20.7753
10.1073/pnas.2634406100
10.1111/j.1558-5646.1995.tb05968.x
Didelot X. Achtman M. Parkhill J. Thomson N.R. & Falush D. In press. A bimodal pattern of relatedness between the Salmonella paratyphi A and typhi genomes: convergence or divergence by homologous recombination? Genome Res .
10.1128/jb.173.22.7257-7268.1991
10.1093/genetics/164.4.1567 / Genetics / Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies by Falush D (2003)
10.1086/284325
Fisher R.A The genetical theory of natural selection. 1930 Oxford UK:Clarendon Press. (10.5962/bhl.title.27468)
10.1186/1741-7007-3-6
10.1093/genetics/138.1.227 / Genetics / Selection intensity for codon bias by Hartl D.L (1994)
Hey J Genes categories and species: the evolutionary and cognitive cause of the species problem. 2001 Oxford UK:Oxford University Press. (10.1093/oso/9780195144772.001.0001)
10.1016/S1567-1348(02)00089-8
10.1128/JCM.40.5.1626-1635.2002
10.1002/bies.950180812
10.1093/bioinformatics/17.12.1244
10.1006/tpbi.2002.1587
{'key': 'e_1_3_2_18_1', 'first-page': '245', 'article-title': 'A proposal for Salmonella nomenclature', 'volume': '133', 'author': 'Le Minor L', 'year': '1982', 'journal-title': 'Ann. Microbiol. (Paris)'} / Ann. Microbiol. (Paris) / A proposal for Salmonella nomenclature by Le Minor L (1982)
{'key': 'e_1_3_2_19_1', 'first-page': '223', 'article-title': 'The taxonomy of Salmonella', 'volume': '133', 'author': 'Le Minor L', 'year': '1982', 'journal-title': 'Ann. Microbiol. (Paris)'} / Ann. Microbiol. (Paris) / The taxonomy of Salmonella by Le Minor L (1982)
10.1128/JB.182.4.1016-1023.2000
10.1128/JB.182.20.5922-5924.2000
10.1038/ng1470
10.1099/00207713-47-4-1145
Popoff M Antigenic formulas of the Salmonella serovar . Salmonella Institut Pasteur 2001 Paris France:WHO collaborating centre for reference and research on Salmonella Institut Pasteur.
10.1093/genetics/155.2.945 / Genetics / Inference of population structure using multilocus genotype data by Pritchard J.K (2000)
10.1128/JCM.27.2.313-320.1989 / J. Clin. Microbiol / Clonal nature of Salmonella typhi and its genetic relatedness to other salmonellae as shown by multilocus enzyme electrophoresis, and proposal of Salmonella bongori comb. nov by Reeves M.W (1989)
10.1093/genetics/134.2.401 / Genetics / The effect of DNA sequence divergence on sexual isolation in Bacillus by Roberts M.S (1993)
Selander R.K Li J& Nelson K Curtiss R Ingraham J.L Lin E.C.C Low K.B Magasanik B Reznikoff W.S Riley M Schaechter M& Umbarger H.E. 1996pp. 2691–2707. Eds. Washington DC:ASM Press.
10.1093/genetics/112.3.441 / Genetics / Homologous recombination in Escherichia coli: dependence on substrate length and homology by Shen P (1986)
10.1073/pnas.90.10.4384
10.1099/ijs.0.63580-0
10.1016/j.mimet.2005.03.006
10.1016/0960-9822(93)90001-5
10.1093/genetics/155.1.451 / Genetics / The coalescent with gene conversion by Wiuf C (2000)
10.1093/genetics/16.2.97 / Genetics / Evolution in mendelian populations by Wright S (1931)
10.1073/pnas.94.18.9786
10.1093/genetics/140.3.917 / Genetics / The log-linear relationship between sexual isolation and sequence divergence in Bacillus transformation is robust by Zawadzki P (1995)

Dates

Type	When
Created	18 years, 10 months ago (Oct. 15, 2006, 7:38 a.m.)
Deposited	1 year, 6 months ago (Feb. 7, 2024, 9:38 a.m.)
Indexed	2 weeks, 3 days ago (Aug. 12, 2025, 5:31 p.m.)
Issued	18 years, 10 months ago (Oct. 11, 2006)
Published	18 years, 10 months ago (Oct. 11, 2006)
Published Online	18 years, 10 months ago (Oct. 11, 2006)
Published Print	18 years, 9 months ago (Nov. 29, 2006)

Funders 0

None

BibTeX

@article{Falush_2006, title={Mismatch induced speciation inSalmonella: model and data}, volume={361}, ISSN={1471-2970}, url={http://dx.doi.org/10.1098/rstb.2006.1925}, DOI={10.1098/rstb.2006.1925}, number={1475}, journal={Philosophical Transactions of the Royal Society B: Biological Sciences}, publisher={The Royal Society}, author={Falush, Daniel and Torpdahl, Mia and Didelot, Xavier and Conrad, Donald F and Wilson, Daniel J and Achtman, Mark}, year={2006}, month=oct, pages={2045–2053} }

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