Artificial light at night shifts the circadian system but still leads to physiological disruption in a wild bird

Globally increasing levels of artificial light at night (ALAN) have been associated with shifts in behavioral rhythms of many wild organisms. It is however unknown to what extent this change in behavior is due to shifts in the circadian clock, and, importantly, whether the physiological pathways orchestrated by the circadian clock are desynchronized by ALAN. Such circadian disruption could have severe consequences for wildlife health, as shown for humans. Here, we analyze the effects of experimental ALAN on rhythmic behavior, gene expression and metabolomic profiles in a wild songbird, the great tit (Parus major). We exposed 34 captive males to three ALAN intensities or to dark nights and recorded their activity rhythms. After three weeks, we collected mid-day and midnight samples of hypothalamus, hippocampus, liver, spleen and plasma. ALAN advanced wake-up time, and this shift was paralleled by an advance in hypothalamic expression of the clock gene BMAL1, which is key to integrating physiological pathways. BMAL1 advances were remarkably consistent across tissues, suggesting close links of brain and peripheral clock gene expression with activity rhythms. However, only a minority of other candidate genes (4 out of 12) paralleled the shifted BMAL1 expression. Moreover, metabolomic profiling showed that only 9.7% of the 755 analyzed metabolites followed the circadian shift. Thus, despite the shifted timing of key clock functions under ALAN, birds suffered internal desynchronization. We thus suggest circadian disruption to be a key link between ALAN and health impacts, in birds and humans alike. Significance StatementShifts in daily activity are a common consequence of artificial light at night (ALAN). In humans, shifted activity cycles often become desynchronized from internal physiological rhythms, with serious health implications. To what extent a similar desynchronization occurs in wild animals experiencing ALAN is currently unknown. We exposed captive great tits to increasing levels of LAN, and found that activity patterns and a core clock gene, BMAL1, shifted in concert. However, only a minority of additional candidate genes and less than 10% of the metabolites followed this circadian shift, suggesting internal desynchronization of physiological rhythms. Our study emphasizes the massive potential for ALAN to impact the health of wild animals through circadian disruption.