Paternal Age in Relation to Offspring Intelligence in the West of Scotland Twenty-07 Prospective Cohort Study

Background

The adverse effects of advancing maternal age on offspring''s health and development are well understood. Much less is known about the impact of paternal age.

Methods

We explored paternal age-offspring cognition associations in 772 participants from the West of Scotland Twenty-07 study. Offspring cognitive ability was assessed using Part 1 of the Alice Heim 4 (AH4) test of General Intelligence and by reaction time (RT).

Results

There was no evidence of a parental age association with offspring RT. However, we observed an inverse U-shaped association between paternal age and offspring AH4 score with the lowest scores observed for the youngest and oldest fathers. Adjustment for parental education and socioeconomic status somewhat attenuated this association. Adjustment for number of, particularly older, siblings further reduced the scores of children of younger fathers and appeared to account for the lower offspring scores in the oldest paternal age group.

Conclusion

We observed a paternal age association with AH4 but not RT, a measure of cognition largely independent of social and educational experiences. Factors such as parental education, socioeconomic status and number of, particularly older, siblings may play an important role in accounting for paternal age-AH4 associations. Future studies should include parental intelligence.     

Further investigations of educational and occupational attainment in the Hawaii family study of cognition

Abstract

Associations of measures of grandparental status, parental status, cognitive abilities, and personality, and own cognitive abilities and personality with educational and occupational attainment are reported for 249 offspring, now 25 years or older, from the Hawaii Family Study of Cognition (HFSC). In general, across two ethnic groups (Americans of European ancestry (AEA) and Americans of Japanese ancestry (AJA)), the data suggest that family background had a relatively trivial influence, own cognitive abilities (particularly verbal ability and general intelligence) substantial influence, and own personality some influence on the educational and occupational attainment of males, while family background had a far more substantial influence than own ability on the attainment of females. Educational attainment was generally found to be substantially predictive of occupational attainment. Hierarchal multiple regression analyses were conducted to assess the influence of parents’ abilities over and above grandparental status and the influence of offsprings’ abilities over and above parental status and abilities on their respective educational and occupational attainments. These analyses also indicated that family background was a much greater influence than own ability on the attainment of AEA female parents and both AEA and AJA female offspring. These findings for female offspring were further confirmed by analyses of parent‐offspring and within‐sibship differences in attainment.     

Trade-offs in modern parenting: a longitudinal study of sibling competition for parental care

Evolutionary and economic models of the family propose that parents face a fundamental trade-off between fertility and investment per offspring. However, tests of this hypothesis have focused primarily on offspring outcomes rather than direct measures of parental investment. Existing studies of parenting also suffer a number of methodological problems now recognized as common sources of error in sociodemographic studies. Here, we present a more definitive picture of the effects of family structure on parental care by analyzing an extensive longitudinal dataset of contemporary British families (the Avon Longitudinal Study of Parents and Children). Unlike other studies, we simultaneously track maternal and paternal behaviors within the same family and consider variation both across time and between distinct population subgroups. Parental investment was measured as frequency of engagement in key care activities over the first decade of life. For both parents, larger family size was traded off against investment per offspring, representing the strongest explanatory variable considered in our analysis. However, contrary to the predictions of traditional quantity–quality trade-off models, increasing family socioeconomic status did not alleviate this effect. In fact, for paternal care in particular, increases in wealth and education created stronger trade-offs. We also demonstrate that large sibships were particularly costly for later-born offspring. Sex of siblings did not influence parental care, however maternal investment was biased towards daughters and paternal investment biased towards sons. Unrelated father figures were also associated with lower investment from both parents. Results are discussed in relation to parental investment theory and evolutionary models of modern low fertility.     

Effect of neonatal handling and paternal care on offspring cognitive development in the monogamous California mouse (Peromyscus californicus)

In the laboratory rat and mouse, neonatal handling enhances hippocampal-dependent learning in adulthood, an effect mediated by changes in maternal behavior toward the handled young. In the present study, we examined the interaction between neonatal handling and biparental care during the early postnatal period and its effect on cognitive function in adult California mice (Peromyscus californicus). We characterized the parental behavior of handled and nonhandled father-present and father-absent families over the first 15 days of life. We then assessed cognitive performance of male and female offspring in the Barnes maze and object recognition test after they were 60 days of age. We found that the amount of licking and grooming received by pups was decreased in father-absent families. By postnatal days 12-15, licking and grooming in handled, father-absent families were equivalent to that of nonhandled, father-present families. Handling enhanced novel object recognition in father-present male mice with no effect in females. In the nonhandled group, the presence of the father had no effect on object recognition learning in male or female mice. Handling also enhanced spatial learning in the Barnes maze. In nonhandled families, the presence of the father appeared to have no effect on spatial learning in the male offspring. Interestingly, spatial learning in nonhandled, father-absent, female offspring was similar to that of handled animals. The average amount of licking and grooming received by pups was negatively correlated with the average number of errors made on the first day of reversal training in the Barnes maze. These data support previous findings that neonatal handling facilitates learning and memory in adulthood, suggest that under certain environmental conditions, there is a sex difference in the response of pups to paternal care, and further demonstrate the importance of active parental investment for offspring cognitive development.     

Advanced Parental Age Impaired Fear Conditioning and Hippocampal LTD in Adult Female Rat Offspring

Advanced maternal or paternal age is associated with increased risks of cognitive and emotional disorders. Chronic stress is also a common experience in human life that causes psychiatric diseases. However, the synergistic effects of these two factors on offspring are rarely studied. In the present study, the offspring of both young (3–4 months) and old (12–14 months) rat parents were given CUMS for 21 days at the age of 4 weeks. The effects of advanced parental age and chronic unpredictable mild stress (CUMS) on emotional and cognitive behaviors and the related cellular mechanisms were investigated by using behavioral and electrophysiological techniques. We found that CUMS decreased sucrose consumption, increased anxiety, and impaired learning and memory in offspring from both old and young breeders. However, advanced parental age impaired fear memory and spatial memory mainly in female offspring. The serum corticosterone of female offspring was lower than males, but advanced parental age significantly elevated serum corticosterone in female offspring in response to electrical foot shocks. In addition, hippocampal LTD was severely impaired in female offspring from older parents. Our results indicated that female offspring from older breeders might be more sensitive to stress, and the hippocampal function was more vulnerable. These results might provide experimental basis for the prevention and treatment of advanced parental age related psychiatric disorders in future.     

Childhood IQ of parents related to characteristics of their offspring: linking the Scottish Mental Survey 1932 to the Midspan Family Study

The objective of the study was to investigate the relationship between childhood IQ of parents and characteristics of their adult offspring. It was a prospective family cohort study linked to a mental ability survey of the parents and set in Renfrew and Paisley in Scotland. Participants were 1921-born men and women who took part in the Scottish Mental Survey in 1932 and the Renfrew/Paisley study in the 1970s, and whose offspring took part in the Midspan Family study in 1996. There were 286 offspring from 179 families. Parental IQ was related to some, but not all characteristics of offspring. Greater parental IQ was associated with taller offspring. Parental IQ was inversely related to number of cigarettes smoked by offspring. Higher parental IQ was associated with better education, offspring social class and offspring deprivation category. There were no significant relationships between parental IQ and offspring systolic blood pressure, diastolic blood pressure, cholesterol, glucose, lung function, weight, body mass index, waist hip ratio, housing, alcohol consumption, marital status, car use and exercise. Structural equation modelling showed parental IQ associated with offspring education directly and mediated via parental social class. Offspring education was associated with offspring smoking and social class. The smoking finding may have implications for targeting of health education.     

Paternal effort and its relation to mating success in the European ground squirrel

The necessity for parental care is a driving force for determining mating systems and social organization. The European ground squirrel, Spermophilus citellus, is a polygynous, gregarious species in which male parental behaviour would not be expected. We had observed males digging in litter burrows that were later occupied by females and their offspring. Males never stayed overnight within these burrows. To determine whether this was some kind of paternal effort we tested the following hypotheses: (1) that male burrowing behaviour was directed towards the male's own offspring or towards the pregnant or lactating mother of the male's offspring; (2) that this behaviour had costs in terms of condition, decreased survival or fecundity; and (3) that it benefited offspring condition or survival. All three assumptions were met. Males worked on the litter burrow of their copulatory partners. Thus, this behaviour was directed towards the male's potential offspring. Male burrowing costs were seen in decreased foraging time and increased body mass loss. Offspring benefits were evident in increased mass at natal emergence. We conclude that male digging at litter burrows can be considered as paternal effort. Lastly, we considered the effects of polygyny on this male parental effort by comparing mating effort, mating success and paternal effort. High mating success was associated with high mating effort and low paternal effort. Moderate to low mating success was associated with lower mating effort and higher paternal effort, indicating a trade-off between the two.     

The Influence of Socioeconomic Status on Children's Brain Structure

Children's cognitive abilities and school achievements are deeply affected by parental socioeconomic status (SES). Numerous studies have reported lower cognitive performance in relation to unfavorable environments, but little is known about the effects of SES on the child's neural structures. Here, we systematically explore the association between SES and brain anatomy through MRI in a group of 23 healthy 10-year-old children with a wide range of parental SES. We confirm behaviorally that language is one of the cognitive domains most affected by SES. Furthermore, we observe widespread modifications in children's brain structure. A lower SES is associated with smaller volumes of gray matter in bilateral hippocampi, middle temporal gyri, left fusiform and right inferior occipito-temporal gyri, according to both volume- and surface-based morphometry. Moreover, we identify local gyrification effects in anterior frontal regions, supportive of a potential developmental lag in lower SES children. In contrast, we found no significant association between SES and white matter architecture. These findings point to the potential neural mediators of the link between unfavourable environmental conditions and cognitive skills.     

Association of assisted reproductive technology,germline de novo mutations and congenital heart defects in a prospective birth cohort study

Emerging evidence suggests that children conceived through assisted reproductive technology (ART) have a higher risk of congenital heart defects (CHDs) even when there is no family history. De novo mutation (DNM) is a well-known cause of sporadic congenital diseases; however, whether ART procedures increase the number of germline DNM (gDNM) has not yet been well studied. Here, we performed whole-genome sequencing of 1137 individuals from 160 families conceived through ART and 205 families conceived spontaneously. Children conceived via ART carried 4.59 more gDNMs than children conceived spontaneously, including 3.32 paternal and 1.26 maternal DNMs, after correcting for parental age at conception, cigarette smoking, alcohol drinking, and exercise behaviors. Paternal DNMs in offspring conceived via ART are characterized by C>T substitutions at CpG sites, which potentially affect protein-coding genes and are significantly associated with the increased risk of CHD. In addition, the accumulation of non-coding functional mutations was independently associated with CHD and 87.9% of the mutations were originated from the father. Among ART offspring, infertility of the father was associated with elevated paternal DNMs; usage of both recombinant and urinary follicle-stimulating hormone and high-dosage human chorionic gonadotropin trigger was associated with an increase of maternal DNMs. In sum, the increased gDNMs in offspring conceived by ART were primarily originated from fathers, indicating that ART itself may not be a major reason for the accumulation of gDNMs. Our findings emphasize the importance of evaluating the germline status of the fathers in families with the use of ART.Subject terms: Genomic analysis, Developmental biology     

Correlation of parental socioeconomic status indicators with morphological and motor dimensions of preschool children

Measuring instruments for assessment of parental socioeconomic status, anthropometric characteristics and motor abilities were used in a sample of 643 preschool children aged 4-6 years and their parents, recruited from preschool institutions in several towns in Voivodina, Serbia. The aim was to analyze the correlation of parental socioeconomic status indicators with morphological and motor dimensions of preschool children. Study results showed the socioeconomic status of the children's families to be relatively homogeneous, with no statistically significant differences in any of the socioeconomic status indicators between families with male and female children. Male and female children differed significantly in the overall space of anthropometric and motor variables, and to a lesser extent in individual variables. The general morphological factor treated as the children's growth and development, and general motor factor were qualitatively comparable. The correlations of socioeconomic factor with general morphological and motor factors of the children were not statistically significant, with the exception of motor factor in 6-year-old male children, at elementary school enrolment. Study results suggested the differences in biological growth and development and motor development recorded in preschool children from Voivodina, Serbia, to be attributable to hereditary factor rather than socioeconomic and environmental factors. Inclusion of older children and use of more socioeconomic status indicators along with some additional indicators should probably yield more reliable results on the issue.     

Implications of Advancing Paternal Age: Does It Affect Offspring School Performance?

Average paternal age is increasing in many high income countries, but the implications of this demographic shift for child health and welfare are poorly understood. There is equivocal evidence that children of older fathers are at increased risk of neurodevelopmental disorders and reduced IQ. We therefore report here on the relationship between paternal age and a composite indicator of scholastic achievement during adolescence, i.e. compulsory school leaving grades, among recent birth cohorts in Stockholm County where delayed paternity is notably common. We performed a record-linkage study comprising all individuals in Stockholm County who finished 9 years of compulsory school from 2000 through 2007 (n = 155,875). Data on school leaving grades and parental characteristics were retrieved from administrative and health service registers and analyzed using multiple linear regression. Advancing paternal age at birth was not associated with a decrease in school leaving grades in adolescent offspring. After adjustment for year of graduation, maternal age and parental education, country of birth and parental mental health service use, offspring of fathers aged 50 years or older had on average 0.3 (95% CI −3.8, 4.4) points higher grades than those of fathers aged 30–34 years. In conclusion, advancing paternal age is not associated with poorer school performance in adolescence. Adverse effects of delayed paternity on offspring cognitive function, if any, may be counterbalanced by other potential advantages for children born to older fathers.     

Links between parental life histories of wild salmon and the telomere lengths of their offspring

The importance of parental contributions to offspring development and subsequent performance is self‐evident at a genomic level; however, parents can also affect offspring fitness by indirect genetic and environmental routes. The life history strategy that an individual adopts will be influenced by both genes and environment; and this may have important consequences for offspring. Recent research has linked telomere dynamics (i.e., telomere length and loss) in early life to future viability and longevity. Moreover, a number of studies have reported a heritable component to telomere length across a range of vertebrates, although the effects of other parental contribution pathways have been far less studied. Using wild Atlantic salmon with different parental life histories in an experimental split‐brood in vitro fertilization mating design and rearing the resulting families under standardized conditions, we show that there can be significant links between parental life history and offspring telomere length (studied at the embryo and fry stage). Maternal life history traits, in particular egg size, were most strongly related to offspring telomere length at the embryonic stage, but then became weaker through development. In contrast, paternal life history traits, such as the father's growth rate in early life, had a greater association in the later stages of offspring development. However, offspring telomere length was not significantly related to either maternal or paternal age at reproduction, nor to paternal sperm telomere length. This study demonstrates both the complexity and the importance of parental factors that can influence telomere length in early life.     

The effect of maternal and paternal environments on seed characters in the herbaceous plant Campanula Americana (Campanulaceae)

Maternal environments typically influence the phenotype of their offspring. However, the effect of the paternal environment or the potential for joint effects of both parental environments on offspring characters is poorly understood. Two populations of Campanula americana, a woodland herb with a variable life history, were used to determine the influence of maternal and paternal light and nutrient environments on offspring seed characters. Families were grown in the greenhouse in three levels of light or three levels of nutrients. Crosses were conducted within each environmental gradient to produce seeds with all combinations of maternal and paternal environments. On average, increasing maternal nutrient and light levels increased seed mass and decreased percentage germination. The paternal environment affected seed mass, germination time, and percentage germination. However, the influence of the paternal environment varied across maternal environments, suggesting that paternal environmental effects should be evaluated in the context of maternal environments. Significant interactions between family and the parental environments for offspring characters suggest that parental environmental effects are genetically variable. In C. americana, the timing of germination determines life history. Therefore parental environmental effects on germination timing, and genetic variation in those parental effects, suggest that parental environments may influence life history evolution in this system.     

Effects of neonatal paternal deprivation or early deprivation on anxiety and social behaviors of the adults in mandarin voles

This study examined whether neonatal paternal deprivation (PD: father was removed and pups were raised just by mother) or early deprivation (ED: pups were raised by both parents except separated from not only the dam but also the peers for three hours a day from PND 0 to 13) has long-term effects on anxiety and social behaviors of adult mandarin voles. Newborn mandarin voles of F2 generation were randomly assigned to one of three groups: bi-parental care (PC: pups were raised by both parents), PD and ED. The parental care behaviors of F1 generation were observed at the age of 0, 13 and 21 days (PND 0, 13, 21) of F2 generation of PC and PD groups. Moreover, each mandarin vole of F2 generation received an open field test and a social interaction test on PND 70 and PND 75, respectively. No significant differences of parental behavior were observed between mothers and fathers from PC families, showing typical parental behavior of socially monogamous rodents. In addition, no significant differences of maternal behaviors were found between mothers from PC and PD families, indicating no maternal compensation towards pups for the absence of the paternal care. In the open field test, mandarin voles from both PD and ED families displayed higher levels of anxiety and lower locomotor activity, relative to offspring of PC family. In the social interaction test, both PD and ED mandarin voles also showed lower levels of social behavior and higher levels of anxiety. Thus, both PD and ED significantly increase anxiety and reduce social behavior of adult mandarin voles, suggesting that variation in parental investment may lead to variation in anxiety and social behaviors in rodents with different mating systems.     

Periconceptional parental conditions and perimembranous ventricular septal defects in the offspring

Background: The perimembranous ventricular septal (pVSD) defect is the most common congenital heart disease phenotype. Several parental factors are associated with pVSD risk in the offspring. To contribute to the future prevention of pVSDs, we investigated associations with nongenetic parental conditions. Methods: In a case–control study with standardized data collection at 17 months after birth, 115 parents of a child with pVSD and 484 parents of a healthy child completed questionnaires about periconceptional nongenetic conditions. Univariable and multivariable logistic regression analyses were used to estimate odds ratios (OR) with 95% confidence intervals (95% CI). Results: Complete data were available for 588 families (98%). Maternal risk conditions associated with pVSD offspring were a positive family history of congenital heart disease (OR, 2.61; 95%CI, 0.98–6.91), medication use (OR, 1.80; 95%CI, 1.13–2.85) and advanced age (OR, 1.07; 95%CI, 1.02–1.12). Exposure to phthalates (OR, 1.93; 95%CI, 1.05–3.54) was the only paternal risk condition associated with pVSD offspring. Conclusion: Four periconceptional parental conditions contributed to pVSD risk in the offspring. Couples planning pregnancy should be counseled on these risk conditions which are partially modifiable to contribute to the future prevention of pVSDs. Birth Defects Research (Part A) 100:944–950, 2014. © 2014 Wiley Periodicals, Inc.     

The effect of maternal and paternal immune challenge on offspring immunity and reproduction in a cricket

Trans‐generational immune priming is the transmission of enhanced immunity to offspring following a parental immune challenge. Although within‐generation increased investment into immunity demonstrates clear costs on reproductive investment in a number of taxa, the potential for immune priming to impact on offspring reproductive investment has not been thoroughly investigated. We explored the reproductive costs of immune priming in a field cricket, Teleogryllus oceanicus. To assess the relative importance of maternal and paternal immune status, mothers and fathers were immune‐challenged with live bacteria or a control solution and assigned to one of four treatments in which one parent, neither or both parents were immune‐challenged. Families of offspring were reared to adulthood under a food‐restricted diet, and approximately 10 offspring in each family were assayed for two measures of immunocompetence. We additionally quantified offspring reproductive investment using sperm viability for males and ovary mass for females. We demonstrate that parental immune challenge has significant consequences for the immunocompetence and, in turn, reproductive investment of their male offspring. A complex interaction between maternal and paternal immune status increased the antibacterial immune response of male offspring. This increased immune response was associated with a reduction in son's sperm viability, implicating a trans‐generational resource trade‐off between investment into immunocompetence and reproduction. Our data also show that these costs are sexually dimorphic, as daughters did not demonstrate a similar increase in immunity, despite showing a reduction in ovary mass.     

Effect of Prenatal Alcohol Exposure on Childhood Academic Outcomes: Contrasting Maternal and Paternal Associations in the ALSPAC Study

Background

The impact of low-to-moderate levels of alcohol consumption during pregnancy on child cognitive outcomes has been of recent concern. This study has tested the hypothesis that low-to-moderate maternal alcohol use in pregnancy is associated with lower school test scores at age 11 in the offspring via intrauterine mechanisms.

Methods

We used data from the Avon Longitudinal Study of Parents and Children (ALSPAC), a birth cohort study based in the South West of England. Analyses were conducted on 7062 participants who had complete data on: maternal and paternal patterns of alcohol use in the first trimester and at 18 weeks'' gestation, child''s academic outcomes measured at age 11, gender, maternal age, parity, marital status, ethnicity, household crowding, home ownership status and parental education. We contrasted the association of mother''s alcohol consumption during pregnancy with child''s National Curriculum Key Stage 2 (KS2) test scores with the association for father''s alcohol consumption (during the time the mother was pregnant) with child''s National Curriculum Key Stage 2 (KS2) test scores. We used multivariate linear regression to estimate mean differences and 95% confidence intervals [CI] in KS2 scores across the exposure categories and computed f statistics to compare maternal and paternal associations.

Findings and conclusions

Drinking up to 1 unit of alcohol a day during pregnancy was not associated with lower test scores. However, frequent prenatal consumption of 4 units (equivalent to 32 grams of alcohol) on each single drinking occasion was associated with reduced educational attainment [Mean change in offspring KS2 score was −0.68 (−1.03, −0.33) for maternal alcohol categories compared to 0.27 (0.07, 0.46) for paternal alcohol categories]. Frequent consumption of 4 units of alcohol during pregnancy may adversely affect childhood academic outcomes via intrauterine mechanisms.     

Elevation‐Related Differences in Parental Risk‐Taking Behavior are Associated with Cognitive Variation in Mountain Chickadees

Breeding animals must balance their current reproductive effort with potential costs to their own survival and consequently to future reproduction. Life‐history theory predicts that variation in reproductive investment should be based on fecundity and life expectancy with longer‐lived species favoring their own survival over parental investment. Recently, variation in parental risk taking was also linked with differences in cognition suggesting a potential trade‐off between cognitive ability and risk taking. Here, we tested whether mountain chickadees from two different elevations with known differences in cognitive ability differ in their parental risk taking by comparing the responses of nesting birds to a potential predator. Higher elevations are associated with shorter breeding season limiting renesting opportunities, but chickadees at high elevations also have better cognitive abilities, which might be potentially associated with better survival. Compared to lower elevations, high‐elevation chickadees laid larger clutches, showed longer latencies to return to the nest in the presence of a hawk, had lower fledging success, and exhibited higher rate of complete nest failures. Nestling development among successful nests, however, was similar between elevations. These data are not consistent with life‐history hypothesis because birds at high elevation invest more in the clutch, while at the same time take less risk when facing potential danger to themselves, which could jeopardize their current reproductive success. These data, however, are consistent with the hypothesis that better cognitive abilities might be associated with less parental risk taking.