Warming during embryogenesis induces a lasting transcriptomic signature in fishes

• Published in: The Science of the total environment Vol. 902; p. 165954
• Main Authors: Ripley, Daniel M., Garner, Terence, Hook, Samantha A., Veríssimo, Ana, Grunow, Bianka, Moritz, Timo, Clayton, Peter, Shiels, Holly A., Stevens, Adam
• Format: Journal Article
• Language: English
• Published: Netherlands Elsevier B.V 01.12.2023
• Subjects: acclimation; Climate change; Danio rerio; Developmental plasticity; Dicentrarchus labrax; embryogenesis; entropy; environment; Gasterosteus aculeatus; gene expression regulation; gene interaction; genes; Hypergraph; Long-term effect; Network models; probability; RNA-seq; Scyliorhinus canicula; Sharks; species; temperature; transcriptome; transcriptomics; Hypergraph; Climate change; RNA-seq; Long-term effect; Developmental plasticity; Sharks; Network models
• ISSN: 0048-9697; 1879-1026; 1879-1026
• DOI: 10.1016/j.scitotenv.2023.165954

Exposure to elevated temperatures during embryogenesis can influence the plasticity of tissues in later life. Despite these long-term changes in plasticity, few differentially expressed genes are ever identified, suggesting that the developmental programming of later life plasticity may occur through the modulation of other aspects of transcriptomic architecture, such as gene network organisation. Here, we use network modelling approaches to demonstrate that warm temperatures during embryonic development (developmental warming) have consistent effects in later life on the organisation of transcriptomic networks across four diverse species of fishes: Scyliorhinus canicula, Danio rerio, Dicentrarchus labrax, and Gasterosteus aculeatus. The transcriptomes of developmentally warmed fishes are characterised by an increased entropy of their pairwise gene interaction networks, implying a less structured, more ‘random’ set of gene interactions. We also show that, in zebrafish subject to developmental warming, the entropy of an individual gene within a network is associated with that gene's probability of expression change during temperature acclimation in later life. However, this association is absent in animals reared under ‘control’ conditions. Thus, the thermal environment experienced during embryogenesis can alter transcriptomic organisation in later life, and these changes may influence an individual's responsiveness to future temperature challenges. [Display omitted] •Warming during embryogenesis causes a less ordered transcriptome in adult fishes.•Transcriptional organisation correlates with future gene expression changes.•This correlation was not observed in fishes from ‘control’ embryonic backgrounds.