Coordinated molecular and physiological adaptations enable activity at sub-freezing temperatures in the snow fly...

Snow flies (Chionea) are wingless crane flies uniquely adapted to extreme cold environments. Adults remain active throughout winter and move rapidly across the snow, even at temperatures below freezing. To investigate the molecular adaptations that make this possible, we sequenced and annotated the genome of Chionea alexandriana and compared it with related species and with the cold-adapted midge, Belgica antarctica. We identify ∼20 lineage-specific and 8 shared gene-family expansions in Chionea and Belgica, corresponding to functions ranging from sensory signaling to DNA packaging. The Chionea genome encodes antifreeze proteins (AFPs), and we show that transgenic expression of an AFP in Drosophila is sufficient to protect larvae from freezing-induced death. Our results also reveal a coordinated expansion of mitochondrial and peroxisomal enzymes, as well as regulators of peroxisome-mitochondria interactions involved in mammalian thermogenesis. Consistent with this, direct measurements reveal that snow flies produce brief bursts of endogenous heat in response to cooling at sub-freezing temperatures, indicating active thermogenic capacity. Finally, our results demonstrate that Chionea has evolved mechanisms to cope with high levels of reactive oxygen species (ROS), a byproduct of mitochondrial activity and a hallmark of cold exposure. These include a 35-fold increase in the threshold for ROS activation of the insect nociceptor TRPA1, as measured in vitro by patch-clamp electrophysiology. Together, our results reveal specific molecular adaptations that enable the snow fly to thrive in extreme cold conditions and suggest that selective gene-family expansion may represent a key mechanism for the adaptation of insects to cold environments.