Publication Abstract

Pollution threatens aquatic ecosystems worldwide, but an ability to rapidly develop tolerance to chemical-stressors should enhance resilience of natural populations. We examined whether early-life priming would enhance life-long copper-tolerance in a model fish species (three-spine stickleback; Gasterosteus aculeatus) via developmental plasticity. We pre-exposed stickleback to a low concentration of copper (10 µg/L) during early development (1-217 hpf), reared the fish in clean water for nine months alongside a control group, then exposed adults from both groups to copper (0,10 and 20 µg/L) for 96 h. Priming markedly reduced transcriptomic evidence of copper-toxicity in adult gills (including reduced cellular stress response (CSR) and disruption of ion-homeostasis) and increased inducibility of metallothionein, a metal-binding and detoxifying protein. In parallel, we identified epigenetic and microbiome-mediated mechanisms likely contributing to this copper-tolerance. Pre-exposure induced persistent DNA methylation changes, consistent with a priming effect on CSR and ion-homeostasis pathways. Enhanced copper-tolerance in the gill microbiota of primed fish also likely contributed to reduced toxicity in their host. Our results provide critical evidence for developmental plasticity related to a chemical stressor in animals, highlight the importance of integrated microbiome and epigenetic responses, and contribute to understanding the sensitivity and risk of natural populations exposed to pollution.

Tamsyn M. Uren Webster, Lauren V. Laing, Jemima Onime, Hannah Littler, Rob McFarling, Josie Paris, Jennifer A. Fitzgerald, Anke Lange, Audrey Farbos, Karen Moore, Matthew D. Hitchings, Ronny van Aerle*, Nic R. Bury, Eduarda M. Santos