There is growing evidence for a discontinuity between genomic and ecological divergence in several groups of bacteria. This evidence is difficult to reconcile with the traditional concept that ecologically divergent species maintain a cohesive gene pool isolated from other gene pools by barriers to homologous recombination (HR). There have been several innovative models of bacterial divergence that permit such discontinuity; we refer to these, collectively, as "mosaic genome concepts" (MGCs). These concepts remain a point of contention. Here, we undertake an investigation among ecologically divergent lineages of genus Listeria, and report our assessment of both niche-specific selection pressure and HR in their core genome. We find evidence of a mosaic Listeria core genome. Some core genes appear to have been free to recombine across ecologically divergent lineages or across named species. In contrast, other core genes have histories consistent with the expected organism relationships and have evolved under niche-specific selective pressures. The products of some of those genes can even be linked to metabolic phenotypes with ecological significance. This finding indicates a potentially strong connection between ecological divergence and core-genome evolution, even among lineages that also experience frequent recombination. Based on these findings, we propose an expanded role for natural selection in core-genome evolution under the MGC.

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