Adaptation to Nighttime Light via Gene Expression Regulation in Drosophila suzukii

Abstract

Urbanization causes environmental changes like habitat loss, fragmentation, and pollution, which reduce biodiversity. Urban organisms face stressors, such as heat islands, air and water pollution, and anthropogenic noise, all of which can disrupt their development, behavior, and physiology. While some species adapt to urban environments, their responses and the role of evolution in urbanization are limited, as most studies focus on phenotypic traits. Artificial light at night (ALAN), a common urban stressor, disrupts behaviors and physiological processes, including circadian rhythms, sleep, and reproduction. The present study examined the effect of ALAN on body size, survival, activity rhythms, and gene expression in urban and rural strains of Drosophila suzukii in common garden experiments. ALAN reduced wing and thorax sizes regardless of sex and origin, decreased survival in rural populations, and increased it in urban populations. ALAN elevated overall activity, especially in the early night, while urban females displayed reduced sensitivity regarding activity and sleep. The circadian rhythm length was disrupted in rural populations but not in urban populations. Transcriptomic analysis revealed ALAN-induced gene expression changes, particularly in urban females, with photoreceptor- and circadian rhythm-related genes responding differently between urban and rural populations. These results indicate that urban populations have evolved adaptive mechanisms to counter ALAN's effects, likely mediated through gene regulation. This study highlights ALAN's impact on diverse traits and its potential for adaptive evolution in urban environments. Evolutionary adaptations in traits related to urban stress responses may enhance the ecological success of D. suzukii in urban habitats.

Keywords: circadian rhythm; gene regulation; light pollution; plasticity; transcriptomics; urban adaptation.

FIGURE 1

Effect of artificial light at night on the body size of individuals from urban and rural populations. (A) Thorax length and (B) wing length.

FIGURE 2

Survival curves of flies under control and ALAN conditions. The dotted lines represent the estimated median, which is the age at which the curves intersect at 50%. Since there was no difference in survival rate between males and females, they are plotted together without separating by sex. The arrows indicate the change in the number of days until 50% survival when the condition shifts from no light to light.

FIGURE 3

Effects of ALAN on activity patterns of urban and rural populations. (A) Each population's locomotor activity counts per hour under control and ALAN treatments. Gray shading indicates the potential nighttime. (B) Individuals' daily physical activity patterns divided according to the level of PC values (small panels). Relationship between light condition and PC1 value (upper large panels) or PC2 value (lower large panels). (C) Fraction of time spent sleeping averaged within a 30‐min time window. (D) Relationship between the light condition and the fraction of time spent sleeping.

FIGURE 4

Effects of ALAN on the circadian rhythm period of individuals from urban and rural populations.

FIGURE 5

Effects of ALAN on the gene expression of individuals from urban and rural populations. (A) PCA plots representing changes in the gene expression profile with ALAN exposure. Each point represents an independent biological replicate. (B) Changes in PC1 and PC2 scores with ALAN exposure. (C) Number of DEGs. (D) Heatmap of DEGs for light treatments, urbanization types, and their interaction. (E) GO terms for BP enriched in DEGs of the interaction between light treatment and urbanization type. (F) Effects of ALAN on the gene expression level of LARK in individuals of urban and rural populations. Small plots and thin lines represent the expression level for each population.