Light pollution increases West Nile virus competence of a ubiquitous passerine reservoir species

Abstract

Among the many anthropogenic changes that impact humans and wildlife, one of the most pervasive but least understood is light pollution. Although detrimental physiological and behavioural effects resulting from exposure to light at night are widely appreciated, the impacts of light pollution on infectious disease risk have not been studied. Here, we demonstrate that artificial light at night (ALAN) extends the infectious-to-vector period of the house sparrow (Passer domesticus), an urban-dwelling avian reservoir host of West Nile virus (WNV). Sparrows exposed to ALAN maintained transmissible viral titres for 2 days longer than controls but did not experience greater WNV-induced mortality during this window. Transcriptionally, ALAN altered the expression of gene regulatory networks including key hubs (OASL, PLBD1 and TRAP1) and effector genes known to affect WNV dissemination (SOCS). Despite mounting anti-viral immune responses earlier, transcriptomic signatures indicated that ALAN-exposed individuals probably experienced pathogen-induced damage and immunopathology, potentially due to evasion of immune effectors. A simple mathematical modelling exercise indicated that ALAN-induced increases of host infectious-to-vector period could increase WNV outbreak potential by approximately 41%. ALAN probably affects other host and vector traits relevant to transmission, and additional research is needed to advise the management of zoonotic diseases in light-polluted areas.

Keywords: anthropogenic; ecoimmunology; host competence; light pollution; reservoir host.

Figure 1.

West Nile virus infection viraemia, body mass and WNV-induced mortality results. Effects of experimental West Nile virus exposure on house sparrows (Passer domesticus) exposed to artificial light at night (ALAN; 8 lx during night hours for two to three weeks prior to WNV exposure) versus controls (animals kept on 12 L : 12 D for duration of experiment). Blue points and dashed lines signify ALAN-exposed individuals, and black points and solid lines signify controls. (a) Individuals exposed to ALAN had significantly higher viral titers on d6 post-exposure, indicated by the asterisk. The horizontal dashed light represents the conservative transmission threshold or the minimum amount of virus in circulation required to transmit WNV to a vector (i.e. 10⁵ PFU). (b) Effects of WNV and ALAN on change in group mean body mass throughout the course of WNV infection. On d6, ALAN-exposed individuals lost appreciable mass whereas controls continued to gain body mass. (c) Relationship between WNV titre and body mass change on d6 post-WNV exposure. The vertical dashed line represents the WNV transmission threshold; individuals to the right of this dashed line are infectious to mosquitoes, and individuals to the left of this dashed line are not. Only ALAN-exposed individuals were infectious on d6. (d) No effect of ALAN on WNV-induced mortality. (Online version in colour.)

Figure 2.

WGCNA results for significantly enriched WNV immune defense modules. (a) Heatmap of eigengene expression for purple module (235 genes), showing downregulation in d2 control birds. Columns are organized by day and treatment; each row represents a module gene and row colours correspond to relative expression levels, where orange represents upregulation and blue represents downregulation. (b) Visant network of the most interconnected genes in the purple module (greater than 28 connections). Each dot represents a gene and diamonds highlight hub genes. (c) Heatmap of eigengene expression for turquoise module (3274 genes), showing upregulation in d6 ALAN birds. Columns are organized by day and treatment, each row represents a module gene and row colours correspond to relative expression levels, where orange represents upregulation and blue represents downregulation. (d) Visant network of the most interconnected genes in the turquoise module (greater than 44 connections). Each dot represents a gene and diamonds highlight hub genes. (e) Heatmap of eigengene expression for tan module (206 genes), showing upregulation in d6 ALAN birds. Columns are organized by day and treatment, each row represents a module gene and row colours correspond to relative expression levels, where orange represents upregulation and blue represents downregulation. (f) Visant network of the most interconnected genes in the tan module (greater than 60 connections). Each dot represents a gene and diamonds highlight hub genes. (Online version in colour.)

Figure 3.

Normalized counts for (a) SOCS1 and (b) SOCS3 across treatment groups. Each dot represents a sample. Black dots and boxplots correspond to control and blue dot and boxplots correspond to ALAN. Significance bars indicate ***p < 0.001 and *p < 0.05. (Online version in colour.)