Scattered differentiation of unlinked loci across the genome underlines ecological divergence of the selfing grass Brachypodium stacei

Ecological divergence without geographic isolation, as an early speciation process that may lead finally to reproductive isolation through natural selection, remains one of the most interesting issues in evolutionary biology. However, the patterns of the underlying genetic divergences across the genome vary between different groups. Here we report that Brachypodium stacei, an inbreeding grass species, has been involved in sympatric ecological divergence without geographic isolation. Genomic, transcriptomic, and metabolomic analyses suggest that diploid B. stacei diverged sympatrically in two slopes with contrasting biomes at Evolution Canyon I (ECI), Mount Carmel, Israel, where gene flow has continued freely but reduced with the time. This ecological divergence involved the scattered divergence of many unlinked loci across the total genome that include both coding and non-coding regions. We also identified significantly differential expressions of ABA signaling pathway genes, and contrasting metabolome composition between the arid-vs forest-adapted B. stacei ECI populations. These results suggest that many small loci involved in environmental responses act additively to account for the ecological usages of this species in contrasted environments with gene flow. SignificanceEcological divergence provides evidence for the origin of species through natural selection that has governed evolutionists attention since Darwin. In this study, we present multiple-omics analyses of two plant populations growing sympatrically in contrasted environments and revealed their distinct differentiation across all examined data. These two populations share the most recent ancestor compared with other populations and their divergence started in the early Holocene. We revealed that gene flow had continued but with a progressive reduction over time. The genetic divergences are scattered across the total genome involving many unlinked coding and non-coding regions. These findings highlight the significance of natural selection in the ecological divergence that may finally lead to species formation without geographic isolation.