Positive selection alone is sufficient for whole genome differentiation at the early stage of speciation process in the fall armyworm.

Background: The process of speciation involves differentiation of whole genome sequences between a pair of diverging taxa. In the absence of a geographic barrier and in the presence of gene flow, genomic differentiation may occur when the homogenizing effect of recombination is overcome across the whole genome. The fall armyworm is observed as two sympatric strains with different host-plant preferences across the entire habitat. These two strains exhibit a very low level of genetic differentiation across the whole genome, suggesting that genomic differentiation occurred at an early stage of speciation. In this study, we aim at identifying critical evolutionary forces responsible for genomic differentiation in the fall armyworm.

Results: These two strains exhibit a low level of genomic differentiation (F_ST = 0.0174), while 99.2% of 200 kb windows have genetically differentiated sequences (F_ST > 0). We found that the combined effect of mild positive selection and genetic linkage to selectively targeted loci are responsible for the genomic differentiation. However, a single event of very strong positive selection appears not to be responsible for genomic differentiation. The contribution of chromosomal inversions or tight genetic linkage among positively selected loci causing reproductive barriers is not supported by our data. Phylogenetic analysis shows that the genomic differentiation occurred by sub-setting of genetic variants in one strain from the other.

Conclusions: From these results, we concluded that genomic differentiation may occur at the early stage of a speciation process in the fall armyworm and that mild positive selection targeting many loci alone is sufficient evolutionary force for generating the pattern of genomic differentiation. This genomic differentiation may provide a condition for accelerated genomic differentiation by synergistic effects among linkage disequilibrium generated by following events of positive selection. Our study highlights genomic differentiation as a key evolutionary factor connecting positive selection to divergent selection.