RESUMEN
In the face of rising global temperatures, the mechanisms behind an organism's ability to acclimate to heat stress remain enigmatic. The rice leaf folder, Cnaphalocrocis medinalis, traditionally viewed as temperature-sensitive, paradoxically exhibits robust larval acclimation to heat stress. This study used the heat-acclimated strain HA39, developed through multigenerational exposure to 39°C during the larval stage, and the unacclimated strain HA27 reared at 27°C to unravel the transgenerational effects of heat acclimation and its regulatory mechanisms. Heat acclimation for larvae incurred a fitness cost in pupae when exposed to high temperature, yet a significant transgenerational effect surfaced, revealing heightened fitness benefit in pupae from HA39, even without additional heat exposure during larval recovery at 27°C. This transgenerational effect exhibited a short-term memory, diminishing after two recovery generations. Moreover, the effect correlated with increased superoxide dismutase (SOD) enzyme activity and expression levels of oxidoreductase genes, representing physiological and molecular foundations of heat acclimation. Heat-acclimated larvae displayed elevated DNA methylation levels, while pupae from HA39, in recovery generations, exhibited decreased methylation indicated by the upregulation of a demethylase gene and downregulation of two methyltransferase genes at high temperatures. In summary, heat acclimation induces DNA methylation, orchestrating heat-stress memory and influencing the expression levels of oxidoreductase genes and SOD activity. Heat-stress memory enhances the acclimation of the migratory insect pest to global warming.