Skip to main content
Log in

Evolving Concepts of Bacterial Species

  • Synthesis Paper
  • Published:
Evolutionary Biology Aims and scope Submit manuscript

Abstract

The same evolutionary forces that cause diversification in sexual eukaryotes are expected to cause diversification in bacteria. However, in bacteria, the wider variety of mechanisms for gene exchange (or lack thereof) increases the range of expected diversity patterns compared to those of sexual organisms. Two parallel concepts for bacterial speciation have developed, based on ecological divergence or barriers to recombination in turn. Recent evidence from DNA sequence data shows that both processes can generate independently evolving groups that are equivalent to sexual species and that represent separate arenas within which recombination (when it occurs), selection and drift occur. It remains unclear, however, how often different processes act in concert to generate simple units of diversity, or whether a more complex model of diversity is required, specifying hierarchical levels at which different cohesive processes operate. We advocate an integrative approach that evaluates the effects of multiple evolutionary forces on diversity patterns. There is also great potential for laboratory studies of bacterial evolution that test evolutionary mechanisms inferred from population genetic analyses of multi-locus and genome sequence data.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Achtman, M., & Wagner, M. (2008). Microbial diversity and the genetic nature of microbial species. Nature Reviews Microbiology, 6, 431–440.

    PubMed  CAS  Google Scholar 

  • Acinas, S. G., Klepac-Ceraj, V., Hunt, D. E., Pharino, C., Ceraj, I., Distel, D. L., et al. (2004). Fine-scale phylogenetic architecture of a complex bacterial community. Nature, 430, 551–554.

    Article  PubMed  CAS  Google Scholar 

  • Ackerly, D. D. (2003). Community assembly, niche conservatism, and adaptive evolution in changing environments. International Journal of Plant Sciences, 164, S165–S184.

    Article  Google Scholar 

  • Arnold, M. L., & Martin, N. H. (2010). Hybrid fitness across time and habitats. Trends in Ecology & Evolution, 25, 530–536.

    Article  Google Scholar 

  • Balbi, K. J., Barraclough, T. G., & Ellis, R. J. A population genetic approach to defining bacterial species: Coexistence of multiple, independently-recombining bacterial lineages (in preparation).

  • Baltrus, D. A., Guillemin, K., & Phillips, P. C. (2008). Natural transformation increases the rate of adaptation in the human pathogen helicobacter pylori. Evolution, 62, 39–49.

    PubMed  Google Scholar 

  • Barraclough, T. G. (2010). Evolving entities: Towards a unified framework for understanding diversity at the species and higher levels. Philosophical Transactions of the Royal Society of London. Series B, 365, 1801–1813.

    Article  PubMed  Google Scholar 

  • Barraclough, T. G., Birky, C. W., & Burt, A. (2003). Diversification in sexual and asexual organisms. Evolution, 57, 2166–2172.

    PubMed  Google Scholar 

  • Barraclough, T. G., Hughes, M., Ashford-Hodges, N., & Fujisawa, T. (2009). Inferring evolutionarily significant units of bacterial diversity from broad environmental surveys of single-locus data. Biology Letters, 5, 425–428.

    Article  PubMed  Google Scholar 

  • Buckling, A., Maclean, R. C., Brockhurst, M. A., & Colegrave, N. (2009). The Beagle in a bottle. Nature, 457, 824–829.

    Article  PubMed  CAS  Google Scholar 

  • Cadillo-Quiroz, H., Didelot, X., Held, N. L., Herrera, A., Darling, A., et al. (2012). Patterns of gene flow define species of thermophilic Archaea. PLoS Biology, 10(2), e1001265.

    Article  PubMed  CAS  Google Scholar 

  • Carrolo, M., Pinto, F. R., Melo-Cristino, J., & Ramirez, M. (2009). Pherotypes are driving genetic differentiation within Streptococcus pneumoniae. BMC Microbiology, 9, 191. doi:10.1186/1471-2180-9-191.

    Article  PubMed  Google Scholar 

  • Cohan, F. M. (1994). The effects of rare but promiscuous genetic exchange on evolutionary divergence in prokaryotes. American Naturalist, 143, 965–986.

    Article  Google Scholar 

  • Cohan, F. M. (2001). Bacterial species and speciation. System Biology, 50, 513–524.

    Article  CAS  Google Scholar 

  • Cohan, F. M. (2006). Towards a conceptual and operational union of bacterial systematics, ecology, and evolution. Philosophical Transaction of the Royal Society of London. Series B, 361, 1985–1996.

    Article  Google Scholar 

  • Cooper, T. F. (2007). Recombination speeds adaptation by reducing competition between beneficial mutations in populations of Escherichia coli. PLoS Biology, 5, 1899–1905.

    Article  CAS  Google Scholar 

  • Coyne, J. A., & Orr, H. A. (1997). Patterns of speciation in Drosophila revisited. Evolution, 51, 295–303.

    Article  Google Scholar 

  • Coyne, J. A., & Orr, H. A. (2004). Speciation. Sunderland, MA: Sinauer Associates.

    Google Scholar 

  • Curtis, T. P., Head, I. M., Lunn, M., Woodcock, S., Schloss, P. D., & Sloan, W. T. (2006). What is the extent of prokaryotic diversity? Philosophical Transaction of the Royal Society of London. Series B, 361, 2023–2037.

    Article  Google Scholar 

  • de Visser, J. A. G. M., Cooper, T. F., & Elena, S. F. (2011). The causes of epistasis. Philosophical Transactions of the Royal Society of London. Series B, 278, 3617–3624.

    Google Scholar 

  • Didelot, X., Bowden, R., Street, T., Golubchik, T., Spencer, C., McVean, G., et al. (2011). Recombination and Population Structure in Salmonella enterica. PLoS Genetics, 7(7), e1002191. doi:10.1371/journal.pgen.1002191.

    Article  PubMed  CAS  Google Scholar 

  • Doolittle, W. F., & Zhaxybayeva, O. (2009). On the origin of prokaryotic species. 2009. Genome Research, 19, 744–756.

    Article  PubMed  CAS  Google Scholar 

  • Doroghazi, J. R., & Buckley, D. H. (2010). Widespread homologous recombination within and between Streptomyces species. ISME Journal, 4, 1136–1143.

    Article  PubMed  CAS  Google Scholar 

  • Eisen, J. A. (2007). Environmental shotgun sequencing: Its potential and challenges foer studying the hidden world of microbes. PLoS Biology, 5, 384–388.

    Article  CAS  Google Scholar 

  • Ellis, R. J., Lilley, A. K., Lacey, S. J., Murrell, D., & Godfray, H. C. J. (2007). Frequency-dependent advantages of plasmid carriage by Pseudomonas in homogeneous and spatially structured environments. ISME Journal, 1, 92–95.

    Article  PubMed  Google Scholar 

  • Felsenstein, J. (1981). Skepticism towards Santa Rosalia, or why are there so few kinds of animals? Evolution, 35, 124–138.

    Article  Google Scholar 

  • Fisher, R. A. (1930). The genetical theory of natural selection. Oxford: Oxford University Press.

    Google Scholar 

  • Fontaneto, D., Herniou, E. A., Boschetti, C., Caprioli, M., Melone, G., Ricci, C., et al. (2007). Independently evolving species in asexual bdelloid rotifers. PLoS Biology, 5, 914–921.

    Article  CAS  Google Scholar 

  • Fraser, C., Hanage, W. P., & Spratt, B. G. (2005). Neutral microepidemic evolution of bacterial pathogens. Proceedings of the National academy of Sciences of the United States of America, 102, 1968–1973.

    Article  PubMed  CAS  Google Scholar 

  • Fraser, C., Hanage, W. P., & Spratt, B. G. (2007). Recombination and the nature of bacterial speciation. Science, 315, 476–480.

    Article  PubMed  CAS  Google Scholar 

  • Gevers, D., Cohan, F. M., Lawrence, J. G., Spratt, B. G., Coenye, T., Feil, E. J., et al. (2005). Re-evaluating prokaryotic species. Nature Reviews Microbiology, 3, 733–739.

    Article  PubMed  CAS  Google Scholar 

  • Hanage, W. P., Fraser, C., & Spratt, B. G. (2006). Sequences, sequence clusters and bacterial species. Philosophical Transaction of the Royal Society of London. Series B, 361, 1917–1927.

    Article  Google Scholar 

  • Hunt, D. E., David, L. A., Gevers, D., Preheim, S. P., Alm, E. J., & Polz, M. F. (2008). Resource partitioning and sympatric differentiation among closely related bacterioplankton. Science, 320, 1081–1085.

    Article  PubMed  CAS  Google Scholar 

  • Kassen, R., Llewellyn, M., & Rainey, P. B. (2004). Ecological constraints on diversification in a model adaptive radiation. Nature, 431, 984–988.

    Article  PubMed  CAS  Google Scholar 

  • Keymer, D. P., & Boehm, A. B. (2011). Recombination shapes the structure of an environmental vibrio cholerae population. Applied and Environmental Microbiology, 77, 537–544.

    Article  PubMed  CAS  Google Scholar 

  • Koeppel, A., Perry, E. B., Sikorski, J., Krizanc, D., Warner, A., Ward, D. M., et al. (2008). Identifying the fundamental units of bacterial diversity: A paradigm shift to incorporate ecology into bacterial systematics. Proceedings of the National academy of Sciences of the United States of America, 105, 2504–2509.

    Article  PubMed  CAS  Google Scholar 

  • Lawrence, J. G., & Retchless, A. C. (2010). The myth of bacterial species and speciation. Biology and Philosophy, 25, 569–588.

    Article  Google Scholar 

  • Lorenz, M. G., & Wackernagel, W. (1994). Bacterial gene-transfer by natural genetic-transformation in the environment. Nature Reviews Microbiology, 58, 563–602.

    CAS  Google Scholar 

  • Luo, C., Walk, S. T., Gordon, D. M., Feldgarden, M., Tiedje, J. M., & Konstantinidis, K. T. (2011). Genome sequencing of environmental Escherichia coli expands understanding of the ecology and speciation of the model bacterial species. Proceedings of the National academy of Sciences of the United States of America, 108, 7200–7205.

    Article  PubMed  CAS  Google Scholar 

  • Martiny, A. C., Huang, Y., & Li, W. Z. (2009). Occurrence of phosphate acquisition genes in Prochlorococcus cells from different ocean regions. Environmental Microbiology, 11, 1340–1347.

    Article  PubMed  CAS  Google Scholar 

  • McDonald, J. H., & Kreitman, M. (1991). Adaptive protein evolution at the adh locus in Drosophila. Nature, 351, 652–654.

    Article  PubMed  CAS  Google Scholar 

  • Norman, A., Hansen, L. H., & Sorensen, S. J. (2009). Conjugative plasmids: vessels of the communal gene pool. Philosophical Transaction of the Royal Society of London. Series B, 364, 2275–2289.

    Article  CAS  Google Scholar 

  • Nosil, P., Funk, D. J., & Ortiz-Barrientos, D. (2009). Divergent selection and heterogeneous genomic divergence. Molecular Ecology, 18, 375–402.

    Article  PubMed  Google Scholar 

  • O’Sullivan, O., O’Callaghan, J., Sangrador-Vegas, A., McAuliffe, O., Slattery, L., Kaleta, P., et al. (2009). Comparative genomics of lactic acid bacteria reveals a niche-specific gene set. BMC Microbiology, 9, 50. doi:10.1186/1471-2180-9-50.

    Article  PubMed  Google Scholar 

  • Ochman, H., Lawrence, J. G., & Groisman, E. A. (2000). Lateral gene transfer and the nature of bacterial innovation. Nature, 405, 299–304.

    Article  PubMed  CAS  Google Scholar 

  • Ochman, H., Lerat, E., & Daubin, V. (2005). Examining bacterial species under the specter of gene transfer and exchange. Proceedings of the National academy of Sciences of the United States of America, 102, 6595–6599.

    Article  PubMed  CAS  Google Scholar 

  • Papke, R. T., Zhaxybayeva, O., Feil, E. J., Sommerfeld, K., Muise, D., & Doolittle, W. F. (2007). Searching for species in haloarchaea. Proceedings of the National academy of Sciences of the United States of America, 104, 14092–14097.

    Article  PubMed  CAS  Google Scholar 

  • Perron, G. G., Lee, A. E. G., Wang, Y., Huang, W. E., & Barraclough, T. G. (2011). Bacterial recombination promotes the evolution of multi-drug-resistance in functionally diverse populations. Philosophical Transactions of the Royal Society of London. Series B. (Online early).

  • Pons, J., Barraclough, T. G., Gomez-Zurita, J., Cardoso, A., Duran, D. P., Hazell, S., et al. (2006). Sequence-based species delimitation for the DNA taxonomy of undescribed insects. System Biology, 55, 595–609.

    Article  Google Scholar 

  • Qin, J. J., Li, R. Q., Raes, J., Arumugam, M., Burgdorf, K. S., Manichanh, C., et al. (2010). A human gut microbial gene catalogue established by metagenomic sequencing. Nature, 464, 59–65.

    Article  PubMed  CAS  Google Scholar 

  • Rappe, M. S., & Giovannoni, S. J. (2003). The uncultured microbial majority. Annual Review of Microbiology, 57, 369–394.

    Article  PubMed  CAS  Google Scholar 

  • Raymond, B., Wyres, K. L., Sheppard, S. K., Ellis, R. J., & Bonsall, M. B. (2010). Environmental factors determining the epidemiology and population genetic structure of the Bacillus cereus group in the field. PLoS Pathogens, 6(5), e1000905. doi:10.1371/journal.ppat.1000905.

    Article  PubMed  Google Scholar 

  • Roberts, M. S., & Cohan, F. M. (1993). The effect of DNA-Sequence divergence on sexual isolation in Bacillus. Genetics, 134, 402–408.

    Google Scholar 

  • Roberts, M. S., & Cohan, F. M. (1995). Recombination and migration rates in natural populations of Bacillus subtilis and Bacillus mojavensis. Evolution, 49, 1081–1094.

    Article  Google Scholar 

  • Schloss, P. D., & Handelsman, J. (2005). Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Applied and Environmental Microbiology, 71, 1501–1506.

    Article  PubMed  CAS  Google Scholar 

  • Sheppard, S. K., McCarthy, N. D., Falush, D., & Maiden, M. C. J. (2008). Convergence of Campylobacter species: Implications for bacterial evolution. Science, 320, 237–239.

    Article  PubMed  CAS  Google Scholar 

  • Smillie, C. S., Smith, M. B., Friedman, J., Cordero, O. X., David, L. A., & Alm, E. J. (2011). Ecology drives a global network of gene exchange connecting the human microbiome. Nature (Online early).

  • Sobel, J. M., Chen, G. F., Watt, L. R., & Schemske, D. W. (2010). The biology of speciation. Evolution, 64, 295–315.

    Article  PubMed  Google Scholar 

  • Stackebrandt, E., & Ebers, J. (2006). Taxonomic parameters revisited: Tarnished gold standards. Microbiol Today, 33, 152–155.

    Google Scholar 

  • Tautz, D., Arctander, P., Minelli, A., Thomas, R. H., & Vogler, A. P. (2003). A plea for DNA taxonomy. Trends in Ecology & Evolution, 18, 70–74.

    Article  Google Scholar 

  • Templeton, A. (1989). The meaning of species and speciation: a population genetics approach. In D. Otte & J. Endler (Eds.), Speciation and its consequences. Sunderland, MA: Sinauer Associates.

    Google Scholar 

  • Venter, J. C., Remington, K., Heidelberg, J. F., Halpern, A. L., Rusch, D., Eisen, J. A., et al. (2004). Environmental genome shotgun sequencing of the Sargasso Sea. Science, 304, 66–74.

    Article  PubMed  CAS  Google Scholar 

  • Vos, M. (2009). Why do bacteria engage in homologous recombination? Trends in Microbiology, 17, 226–232.

    Article  PubMed  CAS  Google Scholar 

  • Vos, M. (2011). A species concept for bacteria based on adaptive divergence. Trends in Microbiology, 19, 1–7.

    Article  PubMed  CAS  Google Scholar 

  • Vos, M., Birkett, P. J., Birch, E., Griffiths, R. I., & Buckling, A. (2009). Local adaptation of bacteriophages to their bacterial hosts in soil. Science, 325, 833–834.

    Article  PubMed  CAS  Google Scholar 

  • Vulic, M., Lenski, R. E., & Radman, M. (1999). Mutation, recombination, and incipient speciation of bacteria in the laboratory. Proceedings of the National academy of Sciences of the United States of America, 96, 7348–7351.

    Article  PubMed  CAS  Google Scholar 

  • Whitaker, R. J. (2006). Allopatric origins of microbial species. Philosophical Transactions of the Royal Society of London. Series B, 361, 1975–1984.

    Article  PubMed  Google Scholar 

  • Whitaker, R. J., & Banfield, J. F. (2006). Population genomics in natural microbial communities. Trends in Ecology & Evolution, 21, 508–516.

    Article  Google Scholar 

  • Wiedenbeck, J., & Cohan, F. M. (2011). Origins of bacterial diversity through horizontal genetic transfer and adaptation to new ecological niches. FEMS Microbiology Reviews, 35, 957–976.

    Article  PubMed  CAS  Google Scholar 

  • Wu, X., Monchy, S., Taghavi, S., Zhu, W., Ramos, J., & van der Lelie, D. (2011). Comparative genomics and functional analysis of niche-specific adaptation in Pseudomonas putida. FEMS Microbiology Reviews, 35, 299–323.

    Article  PubMed  CAS  Google Scholar 

  • Zawadzki, P., Roberts, M. S., & Cohan, F. M. (1995). The log-linear relationship between sexual isolation and sequence divergence in Bacillus transformation is robust. Genetics, 140, 917–932.

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

These ideas were developed on BBSRC grant BB/G004250/1. We thank Albert Phillimore and two anonymous reviewers for discussions and Frederick Cohan for his many contributions on bacterial speciation, which underpin most of the ideas in this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Timothy G. Barraclough.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Barraclough, T.G., Balbi, K.J. & Ellis, R.J. Evolving Concepts of Bacterial Species. Evol Biol 39, 148–157 (2012). https://doi.org/10.1007/s11692-012-9181-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11692-012-9181-8

Keywords

Navigation