Fish are sensitive to temperature, but the intergenerational consequences of maternal exposure to high temperature on offspring behavioural plasticity and underlying mechanisms are unknown. Here we show that a thermal maternal stress induces impaired emotional and cognitive responses in offspring rainbow trout (Oncorhynchus mykiss). Thermal stress in mothers triggered the inhibition of locomotor fear-related responses upon exposure to a novel environment 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 (autism susceptibility candidate 2), 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 behavioural plasticity.

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.

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. 84 marked (external tag placed on the dorsal fin) females were kept in 2.5 m 3 tanks (2 x 2 x 85 0.62 m, length × width × water height). In the 17°C group, females initially reared at 12°C 86 were acclimated for five days to an increase of 1°C/day until 17°C. For three weeks 87 preceding ovulation, females were checked every two-three days to detect ovulation. In 88 both experimental group, eggs originating from four simultaneously ovulating females of 89 each group were collected and fertilized using a pool of sperm collected from four males 90 held at 12°C. Fertilization was performed immediately in both groups in order to avoid any 91 bias on subsequent behavioural phenotypes that would have been induced by differences 92 during embryo development. For each of the eight females, fertilizations of 800 eggs were 93 performed at 10°C using the medium ActiFish (IMV, L'Aigle, France; 100 ml ActiFish + 400 94 ml water) and fertilized eggs were distributed within a tray (20 x 50 cm) in two incubators 132 Fish propensity to express adapted fear-related behaviour (e.g. emotional reactivity) was 133 evaluated individually in a novel-tank test at 75-76 dpf (social isolation in a novel tank).134 The novel tank (30 x 19 x 16 cm) was supplied with 12°C flow-though recycled water.135 Fifteen fish per female were observed. The treatment order was randomly chosen.