Insights into the Role of Differential Gene Expression on Species Origin: A Case Study on Wild Rice

The genetic basis of speciation and adaptation to different environments is a fundamental question in evolutionary biology. Of various models of speciation, ecological speciation has been assumed to play a prominent role in origin of species. Despite great efforts, the role of gene expression in ecological speciation is poorly understood. Oryza nivara and O. rufipogon, the direct progenitors of cultivated rice, are sympatric but distinct morphologically and ecologically, thus providing a unique system to study ecological speciation. Here, we conducted a genome-wide gene expression investigation of the two Oryza species using digital gene expression (DGE) technology and RNA-Seq method. Of the 21,415 expressed genes identified, ~8% (1717) differed significantly in expression levels between the two species and these differentially expressed genes are randomly distributed across the genome. Moreover, 62% (1064) of the differentially expressed genes exhibited a signature of directional selection in at least one species. Importantly, the genes with differential expression between species evolved more rapidly at the 5’flanking sequences than the genes without differential expression relative to coding sequences, suggesting that cis-regulatory changes are adaptive and play an important role in the ecological divergence of the two species. Finally, we observed that genes with differential expression were overrepresented with functional terms involving phenotypic and ecological differentiation between the two species, including reproduction- and stress-related characteristics. Our findings demonstrate that ecological speciation is associated with widespread and adaptive alterations in genome-wide gene expression and highlight the dominant role of regulatory evolution in ecological divergence and adaptation.