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Background  Tracing the association between insect cold tolerance and latitudinally and locally varying environmental conditions, as well as key morphological traits and molecular mechanisms, is essential for understanding the processes involved in adaptation. We explored these issues in two closely-related species,  Drosophila montana  and  Drosophila flavomontana , originating from diverse climatic locations across several latitudes on the coastal and mountainous regions of North America. We also investigated the association between sequence variation in one of the key circadian clock genes,  vrille , and cold tolerance in both species. Finally, we studied the impact of  vrille  on fly cold tolerance and cold acclimation ability by silencing it with RNA interference in  D. montana .    Results  We performed a principal component analysis (PCA) on variables representing bioclimatic conditions on the study sites and used latitude as a proxy of photoperiod. PC1 separated the mountainous continental sites from the coastal ones based on temperature variability and precipitation, while PC2 arranged the sites based on summer and annual mean temperatures. Cold tolerance tests showed  D. montana  to be more cold-tolerant than  D. flavomontana  and chill coma resistance (CT min ) of this species showed an association with PC2. Chill coma recovery time (CCRT) of both species improved towards northern latitudes, and in  D. flavomontana  this trait was also associated with PC1.  D. flavomontana  flies were darkest in the coast and in the northern mountainous populations, but coloration showed no linkage with cold tolerance. Body size decreased towards cold environments in both species, but only within  D. montana  populations largest flies showed fastest recovery from cold. Finally, both the sequence analysis and RNAi study on  vrille  suggested this gene to play an essential role in  D. montana  cold resistance and acclimation, but not in recovery time.    Conclusions  Our study demonstrates the complexity of insect cold tolerance and emphasizes the need to trace its association with multiple environmental variables and morphological traits to identify potential agents of natural selection. It also shows that a circadian clock gene  vrille  is essential both for short- and long-term cold acclimation, potentially elucidating the connection between circadian clock system and cold tolerance.    Supplementary Information  The online version contains supplementary material available at 10.1186/s12862-021-01849-y.

Multiple paths to cold tolerance: the role of environmental cues, morphological traits and the circadian clock gene vrille