Social determinants of health and survival in humans and other animals

Snyder‐Mackler, Noah; Burger, Joseph R.; Gaydosh, Lauren; Belsky, Daniel W.; Noppert, Grace A.; Campos, Fernando A.; Bartolomucci, Alessandro; Yang, Yang Claire; Aiello, Allison E.; O’Rand, Angela M.; Harris, Kathleen Mullan; Shively, Carol A.; Alberts, Susan C.; Tung, Jenny

doi:10.1126/science.aax9553

Cited by 416 publications

(455 citation statements)

References 189 publications

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“…Robine et al, 2012 in the context of climatic variables), there is increasing evidence that environmental factors modulate ageing patterns in the wild (Nussey et al 2007;Holand et al 2016). For instance, it is increasingly recognized that the social environment can have a major influence on health and mortality risk at late ages (Berger et al 2018;Snyder-Mackler et al 2020), by notably interacting with some hallmarks of ageing (e.g. telomere dynamics in Seychelle warblers, Acrocephalus sechellensis, Hammers et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

Epigenetic clock and DNA methylation studies of roe deer in the wild

Lemaître¹,

Rey²,

Gaillard³

et al. 2020

Preprint

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DNA methylation-based biomarkers of aging (epigenetic clocks) promise to lead to new insights in the evolutionary biology of ageing. Relatively little is known about how the natural environment affects epigenetic aging effects in wild species. In this study, we took advantage of a unique long-term (>40 years) longitudinal monitoring of individual roe deer (Capreolus capreolus) living in two wild populations (Chize and Trois Fontaines, France) facing different ecological contexts to investigate the relationship between chronological age and levels of DNA methylation (DNAm). We generated novel DNA methylation data from n=90 blood samples using a custom methylation array (HorvathMammalMethylChip40). We present several three DNA methylation-based estimators of age (DNAm or epigenetic age), which were trained in males, females, and both sexes combined. We investigated how sex differences influenced the relationship between DNAm age and chronological age through the use of sex-specific epigenetic clocks. Our results highlight that both populations and sex influence the epigenetic age, with the bias toward a stronger male average age acceleration (i.e. differences between epigenetic age and chronological ages) particularly pronounced in the population facing harsh environmental conditions. Further, we identify the main sites of epigenetic alteration that have distinct aging patterns across the two sexes. These findings open the door to promising avenues of research at the crossroad of evolutionary biology and biogerontology.

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Section: Introductionmentioning

confidence: 99%

Epigenetic clock and DNA methylation studies of roe deer in the wild

Lemaître¹,

Rey²,

Gaillard³

et al. 2020

Preprint

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“…Our finding implies that the presence of the DLX5/6-N-Haplotype, although positive for certain aspects, could be associated to traits reducing human healthy aging and life expectancy. This observation could well be integrated within current ideas on the biology of ageing which suggest that ageing rates, and consequently lifespans, evolve as a function of trade-offs with other characters including social, cognitive and reproductive capacities (Yang, et al 2016;Snyder-Mackler, et al 2020). A) 93% of control mice emitted less than 700 vocalizations during the 10 minute tests, only one outlier emitted 849 calls.…”

Section: Discussionmentioning

confidence: 68%

DLX5/6GABAergic expression affects social vocalization: implications for human evolution

Levi

Lombares

Giuliani

et al. 2020

Preprint

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DLX5 and DLX6 are two closely related transcription factors involved in brain development and in GABAergic differentiation. The DLX5/6 locus is regulated by FoxP2, a gene involved in language evolution and has been associated to neurodevelopmental disorders and mental retardation. Targeted inactivation of Dlx5/6 in mouse GABAergic neurons (Dlx5/6VgatCre mice) results in behavioural and metabolic phenotypes notably increasing lifespan by 33%.Here, we show that Dlx5/6VgatCre mice present an hyper-vocalization and hyper-socialization phenotype. While only 7% of control mice emitted more than 700 vocalizations/10min, 30% and 56% of heterozygous or homozygous Dlx5/6VgatCre mice emitted more than 700 and up to 1400 calls/10min with longer, uninterrupted, call sequences and a higher proportion of complex and modulated calls. Hyper-vocalizing animals were more sociable: the time they spent in dynamic interactions with an unknown visitor was more than doubled compared to low-vocalizing individuals.We then compared the DLX5/6 genomic regions from Neanderthal and modern humans to examine if DLX5/6 GABAergic expression could have been involved in human social evolution. We identify an introgressed Neanderthal haplotype (DLX5/6-N-Haplotype) present in 12.6% of European individuals that covers DLX5/6 coding and regulatory sequences. The DLX5/6-N-Haplotype is not significantly associated to Autism Spectrum Disorders (ASDs) but includes the binding site for GTF2I, a gene associated to Williams-Beuren syndrome, a neurodevelopmental disorder characterized by hyper-sociability and hyper-vocalization. Interestingly, the DLX5/6-N-Haplotype is significantly underrepresented in semi-supercentenarians (>105y of age), a well-established human model of healthy ageing and longevity, suggesting its potential involvement in the co-evolution of longevity, sociability and speech.

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“…In each case, the reported influence is during adolescence or adulthood, whereby mothers who maintain bonds with their sons gain indirect fitness benefits in the form of grandoffspring. In species where females are the philopatric rather than the dispersing sex, coresidence and social bond maintenance of adult daughters with mothers is well known to provide direct and indirect benefits to both mothers and daughters, by increasing the survival of each other and of their offspring ( 50 – 52 ). In addition, in female baboons, maternal loss in the juvenile period is known to affect later survival ( 7 ).…”

Section: Discussionmentioning

confidence: 99%

“…What remains unclear and needs to be addressed in future studies is by what mechanisms mothers’ presence enhances reproductive success of her offspring and how much active investment and care is involved. Of particular interest in socially complex species that gain fitness through building long-term relationships ( 50 – 52 ) is how much mothers contribute to learning of social skills required to maintain these relationships.…”

Section: Discussionmentioning

confidence: 99%

Postweaning maternal care increases male chimpanzee reproductive success

et al. 2020

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Humans are unusual among animals for continuing to provision and care for their offspring until adulthood. This “prolonged dependency” is considered key for the evolution of other notable human traits, such as large brains, complex societies, and extended postreproductive lifespans. Prolonged dependency must therefore have evolved under conditions in which reproductive success is gained with parental investment and diminished with early parental loss. We tested this idea using data from wild chimpanzees, which have similarly extended immature years as humans and prolonged mother-offspring associations. Males who lost their mothers after weaning but before maturity began reproducing later and had lower average reproductive success. Thus, persistent mother-immature son associations seem vital for enhancing male reproductive success, although mothers barely provision sons after weaning. We posit that these associations lead to social gains, crucial for successful reproduction in complex social societies, and offer insights into the evolution of prolonged dependency.

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Social determinants of health and survival in humans and other animals

Cited by 416 publications

References 189 publications

Epigenetic clock and DNA methylation studies of roe deer in the wild

Epigenetic clock and DNA methylation studies of roe deer in the wild

DLX5/6GABAergic expression affects social vocalization: implications for human evolution

Postweaning maternal care increases male chimpanzee reproductive success

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