Extreme genetic signatures of local adaptation in a notorious rice pest, <i>Chilo suppressalis</i>

Climatic variation stands as a significant driving force behind genetic differentiation and the evolution of adaptive traits. Chilo (C.) suppressalis, commonly known as the rice stem borer, is a highly destructive pest that crucially harms rice production. The lack of natural population genomics data has hindered a more thorough understanding of its climate adaptation, particularly the genetic basis underlying adaptive traits. To overcome this obstacle, our study employed completely resequenced genomes of 384 individuals to explore the population structure, demographic history, and gene flow of C. suppressalis in China. This study observed that its gene flow occurred asymmetrically, moving from central populations to peripheral populations. Using genome-wide selection scans and genotype-environment association studies, we identified potential loci that may be associated with climatic adaptation. The most robust signal was found to be associated with cold tolerance, linked to a homeobox gene, goosecoid (GSC), whose expression level was significantly different in low and high latitudes. Moreover, downregulating the expression of this gene by RNAi enhances its cold tolerance phenotypes. Our findings have uncovered and delved into the genetic foundation of the ability of C. suppressalis to adapt to its environment. This is essential in ensuring the continued effectiveness and sustainability of novel control techniques.