Maternal temperature exposure triggers emotional and cognitive disorders and dysregulation of neurodevelopment genes in fish

Fish are sensitive to temperature, but the intergenerational consequences of maternal exposure to high temperature on offspring adaptive behaviour and underlying mechanisms are unknown. Here we show that a thermal maternal stress induces emotional and cognitive disorders in offspring. Thermal stress in mothers triggered the inhibition of fear responses and decreased spatial learning abilities in progeny. Impaired behavioural phenotypes were associated with the dysregulation of several genes known to play major roles in neurodevelopment, including auts2, a key gene for neurodevelopment, more specifically neuronal migration and neurite extension, and critical for the acquisition of neurocognitive function. In addition, our analysis revealed the dysregulation of another neurodevelopment gene (dpysl5) as well as genes associated with human cognitive disorders (arv1,plp2). We observed major differences in maternal mRNA abundance in the eggs following maternal exposure to high temperature indicating that some of the observed intergenerational effects are mediated by maternally-inherited mRNAs accumulated in the egg. Together, our observations shed new light on the intergenerational determinism of fish behaviour and associated underlying mechanisms. They also stress the importance of maternal history on fish adaptive capacities in a context of global climate changes.