Coldness Triggers Northward Flight in Remigrant Monarch Butterflies

Each fall, eastern North American monarch butterflies (Danaus plexippus) migrate from their northern range to their overwintering grounds in central Mexico [1–3]. Fall migrants are in reproductive diapause, and they use a time-compensated sun compass to navigate during the long journey south [4–6]. Eye-sensed directional cues from the daylight sky (e.g., the horizontal or azimuthal position of the sun) are integrated in the sun compass in the midbrain central complex region [7, 8]. Sun compass output is time compensated by circadian clocks in the antennae so that fall migrants can maintain a fixed flight direction south [9, 10]. In the spring, the same migrants remigrate northward to the southern United States to initiate the northern leg of the migration cycle. Here we show that spring remigrants also use an antenna-dependent time-compensated sun compass to direct their northward flight. Remarkably, fall migrants prematurely exposed to overwintering-like coldness reverse their flight orientation to the north. The temperature microenvironment at the overwintering site is essential for successful completion of the migration cycle, because without cold exposure, aged migrants continue to orient south. Our discovery that coldness triggers the northward flight direction in spring remigrants solves one of the long-standing mysteries of the monarch migration. ► Remigrant monarchs use a time-compensated sun compass to fly north in the spring ► Fall migrants prematurely exposed to overwintering-like coldness orient north ► Fall migrants without cold exposure during overwintering continue to orient south ► The overwintering thermal environment is necessary for successful migration