Rapid evolution of Ophraella communa cold tolerance in new low-temperature environments

Low winter temperatures severely stress newly arriving insect species. Adaptive evolutionary changes in cold tolerance can facilitate their establishment in new environments. Ambrosia artemisiifolia, a noxious invasive plant, occurs throughout China. Ophraella communa, a biological control agent of A. artemisiifolia, mainly occurs in southern China. However, in 2012, it established populations in Beijing (39.98°N, 115.97°E) following introduction from Laibin (23.62°N, 109.37°E), implying cold adaptation. The mechanisms underlying its rapid evolution of cold tolerance remain unknown. We investigated the levels of cryoprotectants and energy reserves in adult O. communa from two latitudes. In high-latitude insects, we found high trehalose, proline, glycerol, total sugar, and lipid levels; five potential genes (Tret1a, Tret1b, Tret1-2, P5CS, and GST), responsible for regulating cold tolerance and involved in trehalose transport, proline biosynthesis, and glutathione S-transferase activation, were highly expressed. These hybridisation changes could facilitate cold temperature adaptation. We demonstrate the genetic basis underlying rapid adaptation of cold tolerance in O. communa, explaining its extension to higher latitudes. Thus, specialist herbivores can follow host plants by adapting to new temperature environments via rapid genetic evolution.