Natural selection and repeated patterns of molecular evolution following allopatric divergence

Background: Geographic speciation is a major force in generating biodiversity. However, how genomes diverge over time after geographic isolation has halted gene flow has remained unclear. We examine genome-wide divergence of putatively single-copy orthologous genes (POGs) from transcriptomes in 20 allopatric species/variety pairs from diverse angiosperm clades. Sixteen of these pairs reflect the well-known eastern Asia – eastern North America floristic disjunction; these species have been isolated for different lengths of time, from the Miocene to Pleistocene. Results: Molecular evolutionary analyses revealed that >90% of the genes examined are under purifying selection and <10% are under positive selection, and this pattern was observed for all taxon pairs, despite differences in divergence time. The divergence level at synonymous sites shared by most POGs in each taxon pair predicts the divergence time between the species/varieties. Divergence time estimates were positively correlated with abundance of genes under moderate purifying selection, but negatively correlated with abundance of genes under strong purifying selection. We identified 200 genes under strong positive selection across the species pairs, with 14 shared by 10-15 pairs and one shared by all taxon pairs. An additional 15 loci annotated to biological processes responding to various stimuli were present in 1-3 pairs.Conclusions: Our results suggest a common “most genes conserved–few genes adaptive” genomic architecture for the taxon pairs, which may be a key for maintaining a balance between the ability to conserve ancestral functions and the ability to evolve new features beneficial for new adaptations. As geographic isolation proceeds through time, the evolutionary trajectory of some genes changed from strong purifying selection to more relaxed selection. The allopatric divergence of these taxon pairs involved both neutral and adaptive evolution of functional genes.