Altered spawning seasons of Atlantic salmon broodstock transcriptionally and epigenetically influence cell cycle and lipid-mediated regulations in their offspring

Abstract Manipulating spawning seasons of Atlantic salmon ( Salmo salar ) is a common practice to facilitate year-round harvesting in salmon aquaculture. This process involves adjusting water temperature and light regime to control female broodstock maturation. However, recent studies have indicated that altered spawning seasons can significantly affect the nutritional status and growth performance of the offspring. Therefore, gaining a deeper understanding of the biological regulations influenced by these alterations is crucial to enhance the growth performance of fish over multiple generations. In this study, we investigated omics data from four different spawning seasons achieved through recirculating aquaculture systems (RAS) and sea-pen-based approaches. In addition to the normal spawning season in November (sea-pen), three altered seasons were designated: off-season (five-month advance, RAS), early season (two-month advance, sea-pen), and late season (two-month delay, sea-pen). We conducted comprehensive gene expression and DNA methylation analysis on liver samples collected from the start-feeding larvae of the next generation. Our results revealed distinct gene expression and DNA methylation patterns associated with the altered spawning seasons. Specifically, offspring from RAS-based off-season exhibited altered lipid-mediated regulation, while those from sea-pen-based early and late seasons showed changes in cellular processes, particularly in cell cycle regulation when compared to the normal season. The consequences of our findings are significant for growth and health, potentially providing information for developing valuable tools for assessing growth potential and optimizing production strategies in aquaculture. Author Summary This study examines the impact of manipulating Atlantic salmon spawning seasons in aquaculture on genetic and epigenetic regulations in their offspring. Manipulating water temperature and light cycles during broodstock rearing allows for year-round harvesting. In aquaculture, altering spawning seasons is a common practice; however, recent research suggests that these changes affect the nutritional status and growth of offspring. To understand these effects at the molecular level, we analysed transcriptomic and epigenetic data from salmon offspring born to broodstock with four different spawning seasons. Our results reveal distinct transcriptomic and epigenetic patterns associated with altered seasons, influencing lipid metabolism and cell cycle regulation. These findings hold significant implications for improving aquaculture practices, potentially enhancing growth performance and nutritional quality of farmed salmon across generations as temperature and light are crucial abiotic factors influencing the next generation. Furthermore, our study potentially contributes to understanding the impact of climate change on the spawning behaviour of aquatic vertebrates, particularly in relation to increasing global ocean temperatures and the resulting changes in photoperiod as species migrate northward in the Northern Hemisphere, experiencing longer daylight in summer and shorter daylight in winter.