The heterogeneous selection landscape of genome evolution in prokaryotes

Evolution of prokaryote genomes appears to be defined by the interplay of selection for genome streamlining, deletion bias, and selection for functional diversification. The previously observed overall positive correlation between the strength of selection, measured as the ratio of nonsynonymous to synonymous nucleotide substitutions (dN/dS), points to diversification as the primary factor of prokaryote genome evolution. Here, we investigated the interplay between genome size and selection pressure by analyzing an expanded collection of closely related prokaryotic genomes, evaluating genome-wide selection by measuring dN/dS by using an accurate, phylogeny-based method and decomposing the resulting values into lineage-specific and gene-specific components. These analyses reveal a pronounced heterogeneity in the relationship between genome size and the strength of selection across the diversity of prokaryotes. Most bacteria display a positive correlation consistent with selection for diversification, whereas all analyzed archaeal lineages show strong negative correlation which is the signature of streamlining. These findings indicate that the selection regimes broadly vary across the diversity of prokaryotes rather than following a single, universal pattern. Genome streamlining, selection for functional diversity and drift in small populations are all important factors of evolution, with their relative contributions depending on the population genetics and ecology of a given lineage.