Footprints of global change in marine life: inferring past environment based on DNA methylation and gene expression marks
Ocean global warming affects the distribution, life history and physiology of marine life. Extreme events, like marine heatwaves, are increasing in frequency and intensity. During sensitive developmental windows of fish, the consequences may be long-lasting and mediated by epigenetic mechanisms. Here, we used adult European sea bass as a model to study the effects of a marine heatwave during development. We measured DNA methylation and gene expression in four tissues (brain, muscle, liver and testis) and detected differentially methylated regions (DMRs). Six genes were differentially expressed and contained DMRs three years after exposure to increased temperature, indicating direct phenotypic consequences and representing persistent changes. Interestingly, nine genes contained DMRs around the same genomic regions across tissues, therefore consisting of common footprints of developmental temperature in environmentally responsive loci. These loci are, to our knowledge, the first metastable epialleles (MEs) described in fish. MEs may serve as biomarkers to infer past life history events linked with persistent consequences. These results highlight the importance of subtle phenotypic changes mediated by epigenetics to extreme weather events during sensitive life stages. Also, to our knowledge, it is the first time the molecular effects of a marine heatwave during the lifetime of individuals are assessed. MEs could be used in surveillance programs aimed at determining the footprints of climate change on marine life. Our study paves the way for the identification of conserved MEs that respond equally to environmental perturbations across species. Conserved MEs would constitute a tool of assessment of global change effects in marine life at a large scale. Overall design: We analyzed genome-wide methylation and gene expression patterns in adult fish that had experienced 4°C of developmental temperature differences. At seven days post fertilization (dpf), temperature increased from 13.5±1°C to 16.5±1°C in the low temperature group and from 13.5±1°C to 20.5±1°C in the high temperature group. The temperature differences were maintained until 68 dpf when temperature started following natural conditions until fish were 3 years old adults and sampled. Genome-wide methylation patterns were analyzed by performing Reduced Representation Sequencing (RRBS) of four tissues representative of the embryonic layers: brain (ectoderm), muscle (paraxial mesoderm), testis (intermediate mesoderm) and liver (endoderm) from three fish reared at low and three fish reared at high temperature. Gene expression patterns were analyzed by RNA-seq in the brain, muscle, testis and liver of five low and five high temperature fish. The RRBS and RNA-seq data of fish reared at low temperature are already published under the GEO Series accession number GSE125124 and are the samples of farmed fish from this series. Please note that each *Feature_Counts.txt was generated from all replicates and is linked to the corresponding repl1 sample records (e.g. *1-RNAseq-HighTemperature).