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.
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Achtman, M., & Wagner, M. (2008). Microbial diversity and the genetic nature of microbial species. Nature Reviews Microbiology, 6, 431–440.
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.
Ackerly, D. D. (2003). Community assembly, niche conservatism, and adaptive evolution in changing environments. International Journal of Plant Sciences, 164, S165–S184.
Arnold, M. L., & Martin, N. H. (2010). Hybrid fitness across time and habitats. Trends in Ecology & Evolution, 25, 530–536.
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.
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.
Barraclough, T. G., Birky, C. W., & Burt, A. (2003). Diversification in sexual and asexual organisms. Evolution, 57, 2166–2172.
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.
Buckling, A., Maclean, R. C., Brockhurst, M. A., & Colegrave, N. (2009). The Beagle in a bottle. Nature, 457, 824–829.
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.
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.
Cohan, F. M. (1994). The effects of rare but promiscuous genetic exchange on evolutionary divergence in prokaryotes. American Naturalist, 143, 965–986.
Cohan, F. M. (2001). Bacterial species and speciation. System Biology, 50, 513–524.
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.
Cooper, T. F. (2007). Recombination speeds adaptation by reducing competition between beneficial mutations in populations of Escherichia coli. PLoS Biology, 5, 1899–1905.
Coyne, J. A., & Orr, H. A. (1997). Patterns of speciation in Drosophila revisited. Evolution, 51, 295–303.
Coyne, J. A., & Orr, H. A. (2004). Speciation. Sunderland, MA: Sinauer Associates.
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.
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.
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.
Doolittle, W. F., & Zhaxybayeva, O. (2009). On the origin of prokaryotic species. 2009. Genome Research, 19, 744–756.
Doroghazi, J. R., & Buckley, D. H. (2010). Widespread homologous recombination within and between Streptomyces species. ISME Journal, 4, 1136–1143.
Eisen, J. A. (2007). Environmental shotgun sequencing: Its potential and challenges foer studying the hidden world of microbes. PLoS Biology, 5, 384–388.
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.
Felsenstein, J. (1981). Skepticism towards Santa Rosalia, or why are there so few kinds of animals? Evolution, 35, 124–138.
Fisher, R. A. (1930). The genetical theory of natural selection. Oxford: Oxford University Press.
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.
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.
Fraser, C., Hanage, W. P., & Spratt, B. G. (2007). Recombination and the nature of bacterial speciation. Science, 315, 476–480.
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.
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.
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.
Kassen, R., Llewellyn, M., & Rainey, P. B. (2004). Ecological constraints on diversification in a model adaptive radiation. Nature, 431, 984–988.
Keymer, D. P., & Boehm, A. B. (2011). Recombination shapes the structure of an environmental vibrio cholerae population. Applied and Environmental Microbiology, 77, 537–544.
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.
Lawrence, J. G., & Retchless, A. C. (2010). The myth of bacterial species and speciation. Biology and Philosophy, 25, 569–588.
Lorenz, M. G., & Wackernagel, W. (1994). Bacterial gene-transfer by natural genetic-transformation in the environment. Nature Reviews Microbiology, 58, 563–602.
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.
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.
McDonald, J. H., & Kreitman, M. (1991). Adaptive protein evolution at the adh locus in Drosophila. Nature, 351, 652–654.
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.
Nosil, P., Funk, D. J., & Ortiz-Barrientos, D. (2009). Divergent selection and heterogeneous genomic divergence. Molecular Ecology, 18, 375–402.
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.
Ochman, H., Lawrence, J. G., & Groisman, E. A. (2000). Lateral gene transfer and the nature of bacterial innovation. Nature, 405, 299–304.
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.
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.
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.
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.
Rappe, M. S., & Giovannoni, S. J. (2003). The uncultured microbial majority. Annual Review of Microbiology, 57, 369–394.
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.
Roberts, M. S., & Cohan, F. M. (1993). The effect of DNA-Sequence divergence on sexual isolation in Bacillus. Genetics, 134, 402–408.
Roberts, M. S., & Cohan, F. M. (1995). Recombination and migration rates in natural populations of Bacillus subtilis and Bacillus mojavensis. Evolution, 49, 1081–1094.
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.
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.
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.
Stackebrandt, E., & Ebers, J. (2006). Taxonomic parameters revisited: Tarnished gold standards. Microbiol Today, 33, 152–155.
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.
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.
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.
Vos, M. (2009). Why do bacteria engage in homologous recombination? Trends in Microbiology, 17, 226–232.
Vos, M. (2011). A species concept for bacteria based on adaptive divergence. Trends in Microbiology, 19, 1–7.
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.
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.
Whitaker, R. J. (2006). Allopatric origins of microbial species. Philosophical Transactions of the Royal Society of London. Series B, 361, 1975–1984.
Whitaker, R. J., & Banfield, J. F. (2006). Population genomics in natural microbial communities. Trends in Ecology & Evolution, 21, 508–516.
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.
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.
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.
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.
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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
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DOI: https://doi.org/10.1007/s11692-012-9181-8