Abstract
Recent studies of bacterial speciation have claimed to support the biological species concept—that reduced recombination is required for bacterial populations to diverge into species. This conclusion has been reached from the discovery that ecologically distinct clades show lower rates of recombination than that which occurs among closest relatives. However, these previous studies did not attempt to determine whether the more-rapidly recombining close relatives within the clades studied may also have diversified ecologically, without benefit of sexual isolation. Here we have measured the impact of recombination on ecological diversification within and between two ecologically distinct clades (A and B') of Synechococcus in a hot spring microbial mat in Yellowstone National Park, using a cultivation-free, multi-locus approach. Bacterial artificial chromosome (BAC) libraries were constructed from mat samples collected at 60°C and 65°C. Analysis of multiple linked loci near Synechococcus 16S rRNA genes showed little evidence of recombination between the A and B' lineages, but a record of recombination was apparent within each lineage. Recombination and mutation rates within each lineage were of similar magnitude, but recombination had a somewhat greater impact on sequence diversity than mutation, as also seen in many other bacteria and archaea. Despite recombination within the A and B' lineages, there was evidence of ecological diversification within each lineage. The algorithm Ecotype Simulation identified sequence clusters consistent with ecologically distinct populations (ecotypes), and several hypothesized ecotypes were distinct in their habitat associations and in their adaptations to different microenvironments. We conclude that sexual isolation is more likely to follow ecological divergence than to precede it. Thus, an ecology-based model of speciation appears more appropriate than the biological species concept for bacterial and archaeal diversification.
Highlights
For much of the last century, theories of the origin of species have revolved around genetic exchange (Mayr, 1942, 1963; Dobzhansky, 1951; Coyne and Orr, 2004)
We suggest that an ecology-based model of speciation is more appropriate than the biological species concept for bacterial speciation in hot spring Synechococcus, and possibly many other bacteria and archaea in diverse environments
Because a reduction in recombination does not appear necessary for ecological divergence, and because ecological patterning of bacterial and archaeal diversity is common, the Biological Species Concept does not appear appropriate for bacterial and archaeal speciation
Summary
For much of the last century, theories of the origin of species have revolved around genetic exchange (Mayr, 1942, 1963; Dobzhansky, 1951; Coyne and Orr, 2004). Speciation theories based on Mayr’s Biological Species Concept see the breaking of recombination between populations as a critical step in population divergence; in this view, populations can diverge ecologically and irreversibly only after their genetic exchange is blocked (Coyne and Orr, 2004). According to a theory developed long ago by Haldane, rare introduction of genes from one population to another cannot reverse the adaptive divergence between populations (Haldane, 1932) This is because natural selection against niche-specifying genes from other populations can limit these foreign genes to negligible frequencies, especially if the rate of recombination between populations is very low. It can be inferred that recombination rates are much too low to reverse adaptive divergence of microbial populations, and that recombination is unlikely to prevent ecological divergence among the most closely related bacteria and archaea (Wiedenbeck and Cohan, 2011)
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