Decoding the constraints acting on a coastal fish using landscape transcriptomics

Abstract

Understanding how wild organisms respond to complex mixtures of environmental stressors remains a major challenge in ecology1,2. To move beyond laboratory-based studies of the effect of individual stressors on model species, landscape transcriptomics - the study of how genome-wide expression patterns reveal environmental conditions - has been suggested3. Here, we apply landscape transcriptomics to the damselfish Chrysiptera cyanea, a sentinel species from Okinawas coastal ecosystems, by sampling juveniles and adults across 18 sites from natural to urbanized habitats. We uncover a striking molecular signature of urbanization: fish from human-impacted sites exhibit elevated expression of genes involved in inflammation and immune responses. Remarkably, their transcriptomes resemble those of overfed individuals from laboratory feeding experiments - suggesting that urban reefs act as "fast food" environments, offering energy-rich diets while imposing chronic stress. This pattern is illustrated by the altered expression of key genes in metabolic and stress pathways (e.g., downregulation of ppargc1a and insrb, indicative of dietary intake surplus and insulin resistance; upregulation of interleukins, chemokines, toll-like receptors and caspase linked to the immune response and inflammation). Our results demonstrate that wild transcriptomes capture the invisible biological costs of environmental degradation, positioning fish as living biosensors for coastal ecosystem health.