Artificial light at night leads to circadian disruption in a songbird: integrated evidence from behavioural, genomic and metabolomic data

Abstract

Globally increasing levels of artificial light at night (ALAN) are associated with shifts in circadian rhythms of behaviour in many wild species. However, it is still unclear whether changes in behavioural timing are underlined by parallel shifts in the molecular clock, and whether such internal shifts may differ between different tissues and physiological pathways, which could highlight circadian disruption. We tackled these questions in a comprehensive study that integrated behavioural, gene expression and metabolomic analyses. We exposed captive male great tits (Parus major) to three ALAN intensities or to dark nights, recorded their activity rhythms and obtained mid-day and midnight samples of brain, liver, spleen and blood. ALAN advanced wake-up time, and this shift was paralleled by an advance in the expression of the clock gene BMAL1 in all tissues, suggesting close links of brain and peripheral clock gene expression with activity rhythms. However, several metabolic and immune genes were desynchronised the shifted BMAL1 expression, suggesting circadian disruption of behaviour and physiology. This result was reinforced by untargeted metabolomic profiling, which showed that only 9.7% of the 755 analysed metabolites followed the behavioural shift. We suggest circadian as a key mediator of the health impacts of ALAN on wild animals.

Artificial Light at Night, Higher Brain Functions and Associated Neuronal Changes: An Avian Perspective

“…Similarly, female Zebra Finches born under LL showed loss of rhythmic expression of clock genes in the hypothalamus and peripheral tissues [28]. Further, dLAN affects the expression of bmal1 in brain, liver, spleen, and blood tissues in Great Tits, along with alteration in metabolic and immune genes [25]. dLAN reduced the peak amplitude of the per2 gene rhythm, but not bmal1, in the hypothalamus of zebra finches.…”

“…Clock (Circadian locomotor output cycles kaput) and bmal1 (Brain and muscle Arnt-like protein-1) form the positive limb, and per (Period) and cry (Cryptochrome) genes form the negative limb of the molecular clock. Recent evidence suggests that ALAN-induced behavioural and physiological changes are associated with disruption of circadian clock gene expression in birds [25,26]. Zebra Finches born under an LL environment in the laboratory showed differential effects with loss of rhythmicity in the activity and singing behaviour in 30% in males.…”

Dim artificial light at night alters immediate early gene expression throughout the avian brain

“…ALAN, even at dim levels, disrupts physiological and behavioral processes ( Ouyang et al, 2018 ). However, these changes appear uncoupled from canonical circadian genes, which synchronize behavior and physiology to the natural photoperiod ( Spoelstra et al, 2018 ; Alaasam et al, 2021 ), but see ( Dominoni et al, 2020 ). Therefore, how dim ALAN affects neuronal activity to disrupt downstream physiological and behavioral processes remains unknown.…”

Exploratory behaviour of territorial passerines toward a novel object in different anthropogenic habitats

“…Urban habitats confront species with new challenges and threats that can alter their abundance and diversity, or provide an opportunity to compete with other species and expand their distribution (Case, 1996;Sol et al, 2014). Succeeding in urban habitats requires gene polyphormisms, behavioural, morphological and physiological traits that enhance a species ability to disperse and reproduce in novel habitats (Crispo, 2008;Dominoni et al, 2018;Evans et al, 2009;Fidler et al, 2007;Partecke et al, 2006;…”