Ocean warming shapes embryonic developmental prospects of the next generation in Atlantic cod

Abstract

Although early embryonic protein production relies exclusively on maternal molecules such as messenger RNAs (mRNAs) incorporated into ovarian follicles, knowledge about any thermally induced, intergenerational effects is scarce in ectotherms. Here, we investigated how elevated temperatures (9°–12°C vs. 6°C) during oogenesis influenced the next generation by targeting maternal mRNAs in Atlantic cod (Gadus morhua) embryos, in view of up- and down-regulated genes in ovarian follicles of pre-spawning adults. Overall, the spawning female liver showed significantly higher levels of free amino acids and N-metabolites at 9°C than at 6°C. Higher-than-optimal temperatures induced adjustments in embryo transcriptome proportional to the temperature increase relative to the control group. The adjustments included alterations in maternal-effect genes, which are developmentally conserved among vertebrates. The transcriptomic differences for a selection of genes in embryos were reflected in ovarian follicles (containing multiple cell types) several months ahead of the spawning season, implying that environmental conditions of the adults are key for adjusting the genetic instructions for offspring development. This programming of fundamental traits from mother to offspring appears part of a sophisticated process to adapt the offspring to a changing ocean, though within life stage-specific, physiological thermal tolerance windows.