From clock genes to fitness: Molecular and behavioral rhythms, parental behavior, and reproductive success across a light pollution gradient

Abstract

Rapid urbanization around the globe has introduced novel stressors, such as artificial light at night (ALAN) to wildlife, perturbing critical time-keeping mechanisms. To gain a holistic understanding of the mechanisms and consequences of light pollution, we continuously monitored free-living breeding house sparrows (Passer domesticus) to assess their locomotor activity, circadian gene expression, parental behavior, and fitness. We integrate genome to phenome analyses of birds exposed to three levels of ALAN (5, 10, 25 lux). We found that urban individuals elongated their window of daily activity and were more restless at night: activity onset advanced with increasing ALAN intensity, activity offset was delayed under >5 lux ALAN, and nocturnal activity increased with increasing ALAN. Urban parents provisioned their offspring at lower rates and raised lighter fledglings. Although there were no significant differences in hypothalamic Cryptochrome 1 (Cry1), Period 2 (Per2), or Period 3 (Per3) expression among individuals exposed to different light pollution levels, Brain and muscle Arnt-like protein-1 (Bmal1) showed a significant earlier phase shift in individuals exposed to 10 and 25 lux compared to 5 lux of ALAN. Furthermore, Bmal1 expression strongly predicts average activity onset, demonstrating a link between circadian gene expression and behavioral rhythms. We report clear associations between circadian gene expression, daily behavioral patterns, and fitness in free-living, urban-adapted individuals. The dose-dependent nature of the observed behavioral and genetic changes supports urban planning measures, such as the reduction of ALAN intensities to a level that preserves wildlife health.

Keywords: Artificial light at night; Circadian; Global change; House sparrow; Songbird; Urbanization.