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1. Early life social and ecological determinants of global DNA methylation in wild spotted hyenas

   https://doi.org/10.1111/mec.15174  

   Laubach, Zachary M. ; Faulk, Christopher D. ; Dolinoy, Dana C. ; Montrose, Luke ; Jones, Tamara R. ; Ray, Donna ; Pioon, Malit O. ; Holekamp, Kay E. ( August 2019 , Molecular Ecology)

   Environmental factors early in life can have lasting influence on the development and phenotypes of animals, but the underlying molecular modifications remain poorly understood. We examined cross‐sectional associations among early life socioecological factors and global DNA methylation in 293 wild spotted hyenas (Crocuta crocuta) in the Masai Mara National Reserve, Kenya, grouped according to three age classes (cub, subadult and adult). Explanatory variables of interest included annual maternal rank based on outcomes of dyadic agonistic interactions, litter size, wild ungulate prey density and anthropogenic disturbance in the year each hyena was born based on counts of illegal livestock in the Reserve. The dependent variable of interest was global DNA methylation, assessed via the LUminometric Methylation Assay, which provides a percentage methylation value calculated at CCGG sites across the genome. Among cubs, we observed approximately 2.75% higher CCGG methylation in offspring born to high‐ than low‐ranking mothers. Among cubs and subadults, higher anthropogenic disturbance corresponded with greater %CCGG methylation. In both cubs and adults, we found an inverse association between prey density measured before a hyena was 3 months old and %CCGG methylation. Our results suggest that maternal rank, anthropogenic disturbance and prey availability early in life are associated with later life global DNA methylation. Future studies are required to understand the extent to which these DNA methylation patterns relate to adult phenotypes and fitness outcomes.

    

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2. Relationship between maternal environment and DNA methylation patterns of estrogen receptor alpha in wild Eastern Bluebird ( Sialia sialis ) nestlings: a pilot study

   https://doi.org/10.1002/ece3.2162  

   Bentz, Alexandra B. ; Sirman, Aubrey E. ; Wada, Haruka ; Navara, Kristen J. ; Hood, Wendy R. ( June 2016 , Ecology and Evolution)

   There is mounting evidence that, across taxa, females breeding in competitive environments tend to allocate more testosterone to their offspring prenatally and these offspring typically have more aggressive and faster‐growing phenotypes. To date, no study has determined the mechanisms mediating this maternal effect's influence on offspring phenotype. However, levels of estrogen receptor alpha (ERα) gene expression are linked to differences in early growth and aggression; thus, maternal hormones may alter gene regulation, perhaps viaDNAmethylation, ofERαin offspring during prenatal development. We performed a pilot study to examine natural variation in testosterone allocation to offspring through egg yolks in wild Eastern Bluebirds (Sialia sialis) in varying breeding densities and percentDNAmethylation ofCGdinucleotides in theERαpromoter in offspring brain regions associated with growth and behavior. We hypothesized that breeding density would be positively correlated with yolk testosterone, and prenatal exposure to maternal‐derived yolk testosterone would be associated with greater offspring growth and decreasedERαpromoter methylation. Yolk testosterone concentration was positively correlated with breeding density, nestling growth rate, and percentDNAmethylation of one out of five investigated CpG sites (site 3) in the diencephalonERαpromoter, but none in the telencephalon (n = 10). PercentDNAmethylation of diencephalon CpG site 3 was positively correlated with growth rate. These data suggest a possible role for epigenetics in mediating the effects of the maternal environment on offspring phenotype. Experimentally examining this mechanism with a larger sample size in future studies may help elucidate a prominent way in which animals respond to their environment. Further, by determining the mechanisms that mediate maternal effects, we can begin to understand the potential for the heritability of these mechanisms and the impact that maternal effects are capable of producing at an evolutionary scale.

    

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3. Maternal educational attainment in pregnancy and epigenome-wide DNA methylation changes in the offspring from birth until adolescence

   https://doi.org/10.1038/s41380-023-02331-5  

   Choudhary, Priyanka ; Monasso, Giulietta S. ; Karhunen, Ville ; Ronkainen, Justiina ; Mancano, Giulia ; Howe, Caitlin G. ; Niu, Zhongzheng ; Zeng, Xuehuo ; Guan, Weihua ; Dou, John ; et al ( December 2023 , Molecular Psychiatry)

   Maternal educational attainment (MEA) shapes offspring health through multiple potential pathways. Differential DNA methylation may provide a mechanistic understanding of these long-term associations. We aimed to quantify the associations of MEA with offspring DNA methylation levels at birth, in childhood and in adolescence. Using 37 studies from high-income countries, we performed meta-analysis of epigenome-wide association studies (EWAS) to quantify the associations of completed years of MEA at the time of pregnancy with offspring DNA methylation levels at birth (n = 9 881), in childhood (n = 2 017), and adolescence (n = 2 740), adjusting for relevant covariates. MEA was found to be associated with DNA methylation at 473 cytosine-phosphate-guanine sites at birth, one in childhood, and four in adolescence. We observed enrichment for findings from previous EWAS on maternal folate, vitamin-B₁₂concentrations, maternal smoking, and pre-pregnancy BMI. The associations were directionally consistent with MEA being inversely associated with behaviours including smoking and BMI. Our findings form a bridge between socio-economic factors and biology and highlight potential pathways underlying effects of maternal education. The results broaden our understanding of bio-social associations linked to differential DNA methylation in multiple early stages of life. The data generated also offers an important resource to help a more precise understanding of the social determinants of health.

    

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4. Early life adversity has long-term effects on sociality and interaction style in female baboons

   https://doi.org/10.1098/rspb.2021.2244  

   Patterson, Sam K. ; Strum, Shirley C. ; Silk, Joan B. ( February 2022 , Proceedings of the Royal Society B: Biological Sciences)

   Social bonds enhance fitness in many group-living animals, generating interest in the processes that create individual variation in sociality. Previous work on female baboons shows that early life adversity and temperament both influence social connectedness in adulthood. Early life adversity might shape sociality by reducing ability to invest in social relationships or through effects on attractiveness as a social partner. We examine how females’ early life adversity predicts sociality and temperament in wild olive baboons, and evaluate whether temperament mediates the relationship between early life adversity and sociality. We use behavioural data on 31 females to quantify sociality. We measure interaction style as the tendency to produce grunts (signals of benign intent) in contexts in which the vocalization does not produce immediate benefits to the actor. Early life adversity was negatively correlated with overall sociality, but was a stronger predictor of social behaviours received than behaviours initiated. Females who experienced less early life adversity had more benign interaction styles and benign interaction styles were associated with receiving more social behaviours. Interaction style may partially mediate the association between early life adversity and sociality. These analyses add to our growing understanding of the processes connecting early life experiences to adult sociality.

    

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5. Mother of all bonds: Influences on spatial association across the lifespan in capuchins

   https://doi.org/10.1111/desc.13486  

   Godoy, Irene ; Korsten, Peter ; Perry, Susan E. ( February 2024 , Developmental Science)

   In humans, being more socially integrated is associated with better physical and mental health and/or with lower mortality. This link between sociality and health may have ancient roots: sociality also predicts survival or reproduction in other mammals, such as rats, dolphins, and non‐human primates. A key question, therefore, is which factors influence the degree of sociality over the life course. Longitudinal data can provide valuable insight into how environmental variability drives individual differences in sociality and associated outcomes. The first year of life—when long‐lived mammals are the most reliant on others for nourishment and protection—is likely to play an important role in how individuals learn to integrate into groups. Using behavioral, demographic, and pedigree information on 376 wild capuchin monkeys (Cebus imitator) across 20 years, we address how changes in group composition influence spatial association. We further try to determine the extent to which early maternal social environments have downstream effects on sociality across the juvenile and (sub)adult stages. We find a positive effect of early maternal spatial association, where female infants whose mothers spent more time around others also later spent more time around others as juveniles and subadults. Our results also highlight the importance of kin availability and other aspects of group composition (e.g., group size) in dynamically influencing spatial association across developmental stages. We bring attention to the importance of—and difficulty in—determining the social versus genetic influences that parents have on offspring phenotypes.

   Having more maternal kin (mother and siblings) is associated with spending more time near others across developmental stages in both male and female capuchins.

   Having more offspring as a subadult or adult female is additionally associated with spending more time near others.

   A mother's average sociality (time near others) is predictive of how social her daughters (but not sons) become as juveniles and subadults (a between‐mother effect).

   Additional variation within sibling sets in this same maternal phenotype is not predictive of how social they become later relative to each other (no within‐mother effect).

    

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