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Prepubertal start of father's smoking and increased body fat in his sons: further characterisation of paternal transgenerational responses.

ABSTRACT: Despite interest in the idea that transgenerational effects of adverse exposures might contribute to population health trends, there are few human data. This non-genetic inheritance is all the more remarkable when transmission is down the male-line as reported in a historical Swedish study, where the paternal grandfather's food supply in mid childhood was associated with the mortality rate in his grandsons. Using the Avon Longitudinal Study of Parents and Children's questionnaire data on smoking and smoking onset from 9886 fathers, we examined the growth of their children from 7-17 years. Adjusting for potential confounders, we assessed associations between body mass index (BMI), waist circumference, total fat mass and lean mass with the age at which the father had started smoking regularly. Of 5376 fathers who reported having ever smoked, 166 reported regular smoking <11 years of age. Before adjustment, those offspring whose fathers started smoking <11 years had the highest mean BMIs at each age tested. The adjusted mean differences in BMI, waist circumference and total fat mass in those sons whose fathers started smoking <11 years, compared with all other sons, increased with age, being significantly greater from 13 years onwards. There were no significant BMI associations in daughters, but they showed a reduction in total lean mass. Our results highlight the importance of the developmental timing of the paternal exposure as well as gender differences in offspring outcomes. Smoking by boys in mid childhood may contribute to obesity in adolescent boys of the next generation.

SUBMITTER: Northstone K

PROVIDER: S-EPMC4085023 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Intergenerational plasticity or parental effects-when parental environments alter the phenotype of future generations-can influence how organisms cope with environmental change. An intriguing, underexplored possibility is that sex-of both the parent and the offspring-plays an important role in driving the evolution of intergenerational plasticity in both adaptive and non-adaptive ways. Here, we evaluate the potential for sex-specific parental effects in a freshwater population of three-spined sticklebacks Gasterosteus aculeatus by independently and jointly manipulating maternal and paternal experiences and separately evaluating their phenotypic effects in sons versus daughters. We tested the adaptive hypothesis that daughters are more responsive to cues from their mother, whereas sons are more responsive to cues from their father. We exposed mothers, fathers or both parents to visual cues of predation risk and measured offspring antipredator traits and brain gene expression. Predator-exposed fathers produced sons that were more risk-prone, whereas predator-exposed mothers produced more anxious sons and daughters. Furthermore, maternal and paternal effects on offspring survival were non-additive: offspring with a predator-exposed father, but not two predator-exposed parents, had lower survival against live predators. There were also strong sex-specific effects on brain gene expression: exposing mothers versus fathers to predation risk activated different transcriptional profiles in their offspring, and sons and daughters strongly differed in the ways in which their brain gene expression profiles were influenced by parental experience. We found little evidence to support the hypothesis that offspring prioritize their same-sex parent's experience. Parental effects varied with both the sex of the parent and the offspring in complicated and non-additive ways. Failing to account for these sex-specific patterns (e.g. by pooling sons and daughters) would have underestimated the magnitude of parental effects. Altogether, these results draw attention to the potential for sex to influence patterns of intergenerational plasticity and raise new questions about the interface between intergenerational plasticity and sex-specific selective pressures, sexual conflict and sexual selection.

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Prepubertal start of father's smoking and increased body fat in his sons: further characterisation of paternal transgenerational responses.

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