Integrated molecular and behavioural data reveal deep circadian disruption in response to artificial light at night in male Great tits (Parus major)

TY - JOUR

T1 - Integrated molecular and behavioural data reveal deep circadian disruption in response to artificial light at night in male Great tits (Parus major)

AU - Dominoni, Davide M.

AU - de Jong, Maaike

AU - van Oers, Kees

AU - O’Shaughnessy, Peter

AU - Blackburn, Gavin J.

AU - Atema, Els

AU - Mateman, A. Christa

AU - D’Amelio, Pietro B.

AU - Trost, Lisa

AU - Bellingham, Michelle

AU - Clark, Jessica

AU - Visser, Marcel E.

AU - Helm, Barbara

N1 - 7391, AnE

PY - 2022

Y1 - 2022

N2 - Globally increasing levels of artificial light at night (ALAN) are associated with shifting rhythms of behaviour in many wild species. However, it is unclear whether changes in behavioural timing are paralleled by consistent shifts in the molecular clock and its associated physiological pathways. Inconsistent shifts between behavioural and molecular rhythms, and between different tissues and physiological systems, disrupt the circadian system, which coordinates all major body functions. We therefore compared behavioural, transcriptional and metabolomic responses of captive great tits (Parus major) to three ALAN intensities or to dark nights, recording activity and sampling brain, liver, spleen and blood at mid-day and midnight. ALAN advanced wake-up time, and this shift was paralleled by advanced expression of the clock gene BMAL1 in all tissues, suggesting close links between behaviour and clock gene expression across tissues. However, further analysis of gene expression and metabolites revealed that clock shifts were inconsistent across physiological systems. Untargeted metabolomic profiling showed that only 9.7% of the 755 analysed metabolites followed the behavioural shift. This high level of desynchronization indicates that ALAN disrupted the circadian system on a deep, easily overlooked level. Thus, circadian disruption could be a key mediator of health impacts of ALAN on wild animals.

AB - Globally increasing levels of artificial light at night (ALAN) are associated with shifting rhythms of behaviour in many wild species. However, it is unclear whether changes in behavioural timing are paralleled by consistent shifts in the molecular clock and its associated physiological pathways. Inconsistent shifts between behavioural and molecular rhythms, and between different tissues and physiological systems, disrupt the circadian system, which coordinates all major body functions. We therefore compared behavioural, transcriptional and metabolomic responses of captive great tits (Parus major) to three ALAN intensities or to dark nights, recording activity and sampling brain, liver, spleen and blood at mid-day and midnight. ALAN advanced wake-up time, and this shift was paralleled by advanced expression of the clock gene BMAL1 in all tissues, suggesting close links between behaviour and clock gene expression across tissues. However, further analysis of gene expression and metabolites revealed that clock shifts were inconsistent across physiological systems. Untargeted metabolomic profiling showed that only 9.7% of the 755 analysed metabolites followed the behavioural shift. This high level of desynchronization indicates that ALAN disrupted the circadian system on a deep, easily overlooked level. Thus, circadian disruption could be a key mediator of health impacts of ALAN on wild animals.

KW - international

KW - Plan_S-Compliant-OA

KW - Light Pollution

U2 - 10.1038/s41598-022-05059-4

DO - 10.1038/s41598-022-05059-4

M3 - Article

C2 - 35091579

AN - SCOPUS:85123873312

SN - 2045-2322

VL - 12

SP - 1553

JO - Scientific Reports

JF - Scientific Reports

IS - 1

M1 - 1553

ER -