Fuzzy species revisited

Abstract

How species should be defined for bacteria, and the debate over whether such things exist in a form worthy of the name, have been long and mostly sterile controversies. There are several reasons for this, including the difficulty in applying concepts developed for one kingdom of life to another, but in recent years the importance of horizontal gene transfer or recombination has also become a point of contention. Few now disagree that the movement of genetic material between lineages is an essential source of evolutionary innovation, and that bacteria tend towards a 'plug and play' strategy that allows genes specific for quite narrow segments of niche space to be shared among multiple species. (I am using the word 'species' in the sense of 'a group of organisms given that name' and do not intend this to be a comment on whether any 'species concepts' are viable.) However, homologous recombination is also more than capable of transferring core housekeeping loci between species [1]. In our 2005 paper [2] we suggested the term 'fuzzy species' for those that did not form clear and distinct sequence clusters, as assayed by phylogenies of concatenated housekeeping genes. This was illustrated with the example of the Neisseria. Using thousands of sequences gleaned from molecular epidemiology we showed that the sister 'species' Neisseria meningitidis and Neisseria lactamica were not perfectly distinguished by the sequences of seven housekeeping genes, and that there was good evidence for severe taxonomic confusion among other named Neisseria species. In contrast, the gonococcus (Neisseria gonorrhoeae) was clearly distinct. This is likely due to ecology. The imperfect separation we observed between N. lactamica and N. meningitidis was due to mosaic genotypes containing sequence 'typical' of both species. These organisms both colonize the human nasopharynx and so are likely to have frequent opportunities for recombination. In contrast the gonococcus colonizes a different mucosal surface (at least most of the time [3]) and this means the opportunities for recombination with other Neisseria are limited. Such 'fuzziness' has gone on to be found among other recombining bacteria [4,5] and indeed Archaea [6]. However, the significance of this observation can be overstated. It does not mean that bacterial species definitions are all inherently insecure, nor even that this is the case for those species where fuzziness is observed. We must distinguish between species definitions and species concepts. A definition is merely the criteria used to classify an organism, and is important for practical reasons. A coherent species concept that can be applied throughout the kingdoms of life is still elusive. However, if we are agnostic about whether 'species' exist in a way that can be justified by philosophers, we can still ask whether clusters of related strains exist, what the characteristics of those clusters might be, and whether this can be helpful for classification. This is the approach used by multi-locus sequence analysis (MLSA). In some cases, researchers have made use of the internet to allow scientists throughout the academic community to contribute to the study of these 'species' clusters [7]. Moreover, it has been possible to model the emergence of such clusters, and examine the role of recombination in generating them [8,9]. This work has suggested that bacteria may fall into 'clonal' and 'sexual' species, with the latter distinguished from the former by higher recombination rates. In 'clonal' species, clusters are generated in the main by mutational processes and are predicted to appear under neutrality through the random birth and extinction of lineages. In a 'sexual' species, the observed cluster is the result of recombination between different members of the species cluster preventing the budding of distinct daughter lineages. This theory predicts that limiting recombination can lead to a single cluster separating in two, in a way that bears comparison with reproductive isolation. However, removal of the barrier to recombination will result in the two clusters merging once more, unless sufficient divergence has occurred [10]. It has even been suggested that there may be evidence for such 'despeciation' occurring in nature [11].