Maternal stress effects across generations in a precocial bird

Abstract

Prenatal maternal stress (PMS) is known to shape the phenotype of the first generation offspring (F1) but according to some studies, it could also shape the phenotype of the offspring of the following generations. We previously showed in the Japanese quail that PMS increased the emotional reactivity of F1 offspring in relation to (i) a variation in the levels of some histone post-translational modification (H3K27me3) in their brains and (ii) a modulation of the hormonal composition of the eggs from which they hatched. Here, we wondered whether PMS could also influence the behaviour of the second (F2) and third (F3) generation offspring due to the persistence of the specific marks we identified. Using a principal component analysis, we found that PMS influenced F2 and F3 quail profiles with subtle differences between generations. It increased F2 neophobia, F3 fearfulness and F3 neophobia but only in females. Interestingly, we did not find any variations in the level of histone post-translational modification in F3 brains and we observed inconsistent modulations of androstenedione levels in F1 and F2 eggs. Although they may vary over generations, our results demonstrate that PMS can have phenotypical effects into the third generation.

Keywords: Japanese quail; emotional reactivity; generation; maternal effects; offspring; prenatal stress.

Figure 1.

Results of the F2 quail PCA. (a) Factor loadings of the variables included in the PCA for each component selected (PC1, PC2, PC3 and PC4). Red bars indicate variables with significant contributions (factor loadings ≥ |0.5|). TI_IND: number of inductions during the tonic immobility test; TI_DUR: duration of immobility during the tonic immobility test; EM_LRC_BOX and EM_RC_BOX: latency to emit a rally call and number of rally calls in the starting box during the emergence test, respectively; EM_LAT_BOD: latency to quit the starting box in the emergence test; EM_LRC_DEV and EM_RC_DEV: latency to emit a rally call and number of rally calls in the device during the emergence test, respectively; EM_FEAR: occurrences of fear behaviour during the emergence test; NO_LAPP and NO_LEXP: latencies to approach and explore the cup in the novel object test, respectively; NO_EXPO: occurrences of cup observation and exploration in the novel object test; NO_FEAR: occurrences of fear behaviour in the novel object test. (b) Factorial scores of individuals for each component selected. For PC1, a higher score indicates a lower reaction to social isolation. For PC2 and PC3, higher scores indicate higher neophobia or fearfulness. For PC4, a higher score indicates a lower intrinsic fearfulness. Results are presented independently of the sex of the offspring (non-stressed (NS) and stressed (S)). The box plots represent the median and the first and third quartiles. The tails represent the minimum and maximum values. Dots represent individual factorial score. LM: * p < 0.05.

Figure 2.

Results of the F3 quail PCA. (a) Factor loadings of the variables included in the PCA for each component selected (PC1, PC2, PC3 and PC4). Red bars indicate variables with significant contributions (factor loadings ≥ |0.5|). TI_IND: number of inductions during the tonic immobility test; TI_DUR: duration of immobility during the tonic immobility test; EM_LRC_BOX and EM_RC_BOX: latency to emit a rally call and number of rally calls in the starting box during the emergence test, respectively; EM_LAT_BOD: latency to quit the starting box in the emergence test; EM_LRC_DEV and EM_RC_DEV: latency to emit a rally call and number of rally calls in the device during the emergence test, respectively; EM_FEAR: occurrences of fear behaviour during the emergence test; NO_LAPP and NO_LEXP: latencies to approach and explore the cup in the novel object test, respectively; NO_EXPO: occurrences of cup observation and exploration in the novel object test; NO_FEAR: occurrences of fear behaviour in the novel object test. (b) Factorial scores of individuals for each component selected. For PC1, PC2 and PC3, higher scores indicate higher reaction to social isolation, higher neophobia and higher intrinsic fearfulness, respectively. For PC4, a higher score indicates a lower fearfulness. Results are presented independently of the sex of the offspring (non-stressed (NS) and stressed (S)) except if an interaction between the group and the sex was observed (non-tressed females (NS F), stressed females (S F), non-stressed males (NS M) and stressed males (S M)). The box plots represent the median and the first and third quartiles. The tails represent the minimum and maximum values. Dots represent individual factorial score. LM: * p < 0.05.