Skip to main content

Epigenetics and the Evolution of Human Social Cognition

  • Chapter
  • First Online:
Evolution of Primate Social Cognition

Part of the book series: Interdisciplinary Evolution Research ((IDER,volume 5))

Abstract

Human social cognitive abilities share derived attributes with other primates, but humans excel uniquely with regard to skills such as theory of mind, perspective-taking, sharing intentions and using language. Even these apparently unique abilities, however, must be supported by neurochemistry that is in turn developmentally dependent on genes derived from our primate lineage. In the last decade, epigenetic processes have emerged as an influence on differences both within and between mammalian species, and the brain is a major target for epigenetic processes regulating gene expression. This short review looks at how epigenetic processes may have contributed to human social cognitive evolution, how this relates to differences between human and non-human primate social cognition and to what extent this is consistent with the social brain hypothesis, i.e. increasing human sociality as a driver rather than a consequence of human brain evolution. The evidence ranges from general trends in maternally and paternally expressed genes influencing different parts of the brain, quantitative differences in mechanisms such as DNA methylation and gene expression in the brains of humans and other primates and examples of species-specific epigenetic regulation of genes associated with social cognition and language.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 89.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 119.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adegbola AA et al (2015) Monoallelic expression of the human FOXP2 speech gene. Proc Natl Acad Sci USA 112(22):6848–6854

    Article  CAS  PubMed  Google Scholar 

  • Auger CJ et al (2011) Epigenetic control of vasopressin expression is maintained by steroid hormones in the adult male rat brain. Proc Natl Acad Sci USA 108(10):4242–4247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ayub Q et al (2013) FOXP2 targets show evidence of positive election in European populations. Am J Hum Genet 92(5):696–706

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bateson P et al (2004) Developmental plasticity and human health. Nature 430:419–421

    Article  CAS  PubMed  Google Scholar 

  • Brown WM (2011) The parental antagonism theory of language evolution: preliminary evidence for the proposal. Hum Biol 83(2):213–245

    Article  PubMed  Google Scholar 

  • Cáceres M et al (2003) Elevated gene expression levels distinguish human from non-human primate brains. Proc Natl Acad Sci USA 100(22):13030–13035

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Canli T, Lesh K-P (2007) Long story short: the serotonin transporter in emotion regulation and social cognition. Nat Neurosci 10(9):1103–1109

    Article  CAS  PubMed  Google Scholar 

  • Chadwick BP (2015) Epigenetics: current research and emerging trends. Caister Academic, Norfolk

    Google Scholar 

  • Charrier C, Polleux F (2012) Role of partial duplication of the SRGAP2 gene in the evolution and development of the human brain. Med Sci 28(11):911–914

    Google Scholar 

  • Chimpanzee Sequencing Analysis Consortium (2005) Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 437(7055):69–87

    Article  CAS  Google Scholar 

  • Cochran DM et al (2015) Relationship among glutamine, gamma-aminobutyric acid, and social cognition in autism spectrum disorders. J Child Adolesc Psychopharmacol 25(4):314–322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crespi BJ (2007) Sly FOXP2: genomic conflict in the evolution of language. Trends Ecol Evol 22(4):174–175

    Article  PubMed  Google Scholar 

  • Crişan LG et al (2009) Genetic contributions of the serotonin transporter to social learning of fear and economic decision making. Soc Cogn Affect Neurosci 4(4):399–408

    Article  PubMed  PubMed Central  Google Scholar 

  • Curley JP (2011) Is there a genomically imprinted social brain? Bioessays 33(9):662–668

    Article  PubMed  Google Scholar 

  • Dennis EL et al (2011) Altered structural brain connectivity in healthy carriers of the autism risk gene, CNTNAP2. Brain Connect 1(6):447–459

    Article  PubMed  PubMed Central  Google Scholar 

  • Dennis MY et al (2012) Evolution of human-specific neural SRGAP2 genes by incomplete segmental duplication. Cell 149(4):912–922

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dunbar RIM (1998) The social brain hypothesis. Evol Anthropol 6(5):178–190

    Article  Google Scholar 

  • Dunbar RI (2009) The Social Brain Hypothesis and its implications for social evolution. Ann Hum Biol 36(5):562–572

    Article  CAS  PubMed  Google Scholar 

  • Feuk L et al (2006) Absence of a paternally inherited FOXP2 gene in developmental verbal dyspraxia. Am J Hum Genet 79(5):956–972

    Article  Google Scholar 

  • Foley RA (2016) Mosaic evolution and the pattern of transitions in the hominin lineage. Philos Trans R Soc Lond B Biol Sci 371:20150244

    Article  PubMed  PubMed Central  Google Scholar 

  • Gershon NB, High PC (2015) Epigenetics and child abuse: modern-day Darwinism -the miraculous ability of the human genome to adapt, and then adapt again. Am J Med Genet C Semin Med Genet 169(4):353–360

    Article  PubMed  Google Scholar 

  • Haig D (2002) Genomic imprinting and kinship. Rutgers University, New Brunswick

    Google Scholar 

  • Haig D (2014) Coadaptation and conflict, misconception and muddle, in the evolution of genomic imprinting. Heredity 113(2):96–103

    Article  CAS  PubMed  Google Scholar 

  • Hajj EI et al (2014) Epigenetics and life-long consequences of an adverse nutritional and diabetic intrauterine environment. Reproduction 148(6):R111–R120

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hales CN, Barker DJ (2001) The thrifty phenotype hypothesis. Br Med Bull 60:5–20

    Article  CAS  PubMed  Google Scholar 

  • Hariri AR et al (2002) Serotonin transporter genetic variation and the response of the human amygdala. Science 297:400–403

    Article  CAS  PubMed  Google Scholar 

  • Heijmans BT et al (2008) Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci USA 105:17046–17049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holloway T, Gonzalez-Maeso J (2015) Epigenetic mechanisms of serotonin signalling. ACS Chem Neurosci 6(7):1099–1199

    Article  CAS  PubMed  Google Scholar 

  • Hsieh J, Zhao X (2016) Genetics and epigenetics in adult neurogenesis. Cold Spring Harb Perspect Biol 8(6):a018911

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Isles AR et al (2002) A possible role for imprinted genes in inbreeding avoidance and dispersal from the natal area in mice. Proc Biol Sci 269(1492):665–670

    Article  PubMed  PubMed Central  Google Scholar 

  • Jablonka E (2013) Epigenetic inheritance and plasticity: the responsive germline. Prog Biophys Mol Biol 111:99–107

    Article  PubMed  Google Scholar 

  • Jablonka E, Lamb MJ (2005) Evolution in four dimensions: genetic, epigenetic, behavioural and symbolic variation in the history of life. MIT, Cambridge

    Google Scholar 

  • Jablonka E, Raz G (2009) Transgenerational epigenetic inheritance: prevalence, mecahnisms and implications for the study of heredity and evolution. Q Rev Biol 84(2):131–176

    Article  PubMed  Google Scholar 

  • Jack KM, Isbell LA (2009) Dispersal in primates: advancing an individualized approach. Behaviour 146:429–436

    Article  Google Scholar 

  • Jack A et al (2012) DNA methylation of the oxytocin receptor gene predicts neural response to ambiguous social stimuli. Front Hum Neurosci 6:a280

    Article  CAS  Google Scholar 

  • Jiang YH et al (1998) Mutation of the angelman ubiquitin ligase in mice causes increased cytoplasmic p53 and deficits of contextual learning and long-term potentiation. Neuron 21(4):799–911

    Article  CAS  PubMed  Google Scholar 

  • Jirtle RL, Skinner MK (2016) Environmental epigenomics and disease susceptibility. Nat Rev Genet 8:253–262

    Article  CAS  Google Scholar 

  • Kappil M et al (2015) Environmental influences on genomic imprinting. Curr Environ Health Rep 2:155. https://doi.org/10.1007/s40572-015-0046-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karg K et al (2011) The serotonin transporter promoter variant (5-HTTLPR), stress, and depression meta-analysis revisited: evidence of genetic moderation. Arch Gen Psychiatry 68(5):444–454

    Article  PubMed  PubMed Central  Google Scholar 

  • Keebaugh AC, Young LJ (2011) Increasing oxytocin receptor expression in the nucleus accumbens of pre-pubertal female prairie voles enhances alloparental responsiveness and partner preference formation as adults. Horm Behav 60(5):498–504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keller TE, Yi SV (2014) DNA methylation and evolution of duplicate genes. Proc Natl Acad Sci USA 111(16):5932–5937

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keverne EB (2014) Significance of epigenetics for understanding brain development, brain evolution and behaviour. Neuroscience 264:207–217

    Article  CAS  PubMed  Google Scholar 

  • Keverne EB et al (1996) Genomic imprinting and the differential roles of parental genomes in brain development. Dev Brain Res 92(1):91–200

    Article  CAS  Google Scholar 

  • Klironomos FD, Berg J, Collins S (2013) How epigenetic mutations can affect genetic evolution: model and mechanism. Bioessays 35(6):571–578

    Article  PubMed  Google Scholar 

  • Koenig A, Borries C (2012) Hominoid dispersal and human evolution. Evol Anthropol 21(3):108–112

    Article  PubMed  Google Scholar 

  • Lillycrop KA, Burdge GC (2015) Maternal diet as a modifier of offspring epigenetics. J Dev Orig Health Dis 6(2):88–95

    Article  CAS  PubMed  Google Scholar 

  • Maricic T et al (2013) A recent evolutionary change affects a regulatory element in human FOXP2 gene. Mol Biol Evol 30(4):844–852

    Article  CAS  PubMed  Google Scholar 

  • Monk C et al (2012) Linking prenatal maternal adversity to developmental outcomes in infants: the role of epigenetic pathways. Dev Psychopathol 24(4):1361–1376

    Article  PubMed  PubMed Central  Google Scholar 

  • Moriam S, Sobhani M (2013) Epigenetic effect of chronic stress on dopamine signaling and depression. Genet Epigenet 5:11–16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mozzi A et al (2016) The evolutionary history of genes involved in spoken and written language: beyond FOXP2. Sci Rep 6:a22157

    Article  CAS  Google Scholar 

  • Munoa I et al (2015) The epigenetic regulation of the opioid system: new individualized prompt prevention and treatment strategies. J Cell Biochem 116(11):2419–2426

    Article  CAS  PubMed  Google Scholar 

  • Nagy C, Turecki G (2015) Transgenerational epigenetic inheritance: an open discussion. Epigenomics 7(5):781–790

    Article  CAS  PubMed  Google Scholar 

  • Nikolova YS et al (2014) Beyond genotype: serotonin transporter epigenetic modification predicts human brain function. Nat Neurosci 17(9):1153–1155

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nowick K et al (2009) Differences in human and chimpanzee gene expression patterns define an evolving network of transcription factors in brain. Proc Natl Acad Sci USA 106(52):22358–22363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pai AA et al (2011) A genome-wide study of DNA methylation patterns and gene expression in multiple human and chimpanzee tissues. PLoS Genet 7(2). https://doi.org/10.1371/journal.pgen.1001316

  • Perroud N et al (2014) The Tutsi genocide and transgenerational transmission of maternal stress: the epigenetics and biology of the HPA axis. World J Biol Psychiatry 15(4):334–345

    Article  PubMed  Google Scholar 

  • Petito A et al (2016) The relationship between personality traits, the 5HTT polymorphisms, and the occurrence of anxiety and depressive symptoms in elite athletes. PLoS One 11(6):e0156601. https://doi.org/10.1371/journal.pone.0156601

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Prokopuk L et al (2015) Transgenerational epigenetic inheritance: adaptation through the germline epigenome? Epigenomics 7(5):829–846

    Article  CAS  PubMed  Google Scholar 

  • Puglia MH et al (2015) Epigenetic modification of the oxytocin receptor gene influences the perception of anger and fear in the human brain. Proc Natl Acad Sci USA 112(11):3308–3313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ragsdale G, Foley RA (2011) A maternal influence on theory of mind mediated by executive function: differential parental influences on full and half-siblings. PLoS One 6(8). https://doi.org/10.1371/journal.pone.0023236)

  • Ragsdale G, Foley RA (2012) Testing the imprinted brain: parent-of-origin effects on empathy and systemising. Evol Hum Behav 33(4):402–410

    Article  Google Scholar 

  • Sadakierska-Chudy A et al (2015a) A comprehensive view of the epigenetic landscape part I: DNA methylation, passive and active DNA demethylation pathways and histone variants. Neurotox Res 27(1):84–97

    Article  CAS  PubMed  Google Scholar 

  • Sadakierska-Chudy A et al (2015b) A comprehensive view of the epigenetic landscape part II: histone post-translational modification, nucleosome level, and chromatin regulation by ncRNAs. Neurotox Res 27(2):172–197

    Article  CAS  PubMed  Google Scholar 

  • Schneider E et al (2014) Widespread differences in cortex DNA methylation of the “language gene” CNTNAP2 between humans and chimpanzees. Epigenetics 9(4):533–545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schulz LC (2010) The Dutch Hunger Winter and the developmental origins of health and disease. Proc Natl Acad Sci USA 107(39):16757–16758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shultz S, Opie C, Atkinson QD (2011) Stepwise evolution of stable sociality in primates. Nature 479(7372):219–U96

    Article  CAS  PubMed  Google Scholar 

  • Silverman JL et al (2015) GABA(B) receptor agonist R-Baclofen reverses social deficits and reduces repetitive behaviour in two mouse models of autism. Neuropsychopharmacology 40(9):2228–2239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Skuse D (2006) Genetic influences on the neural basis of social cognition. Philos Trans R Soc Lond Ser B Biol Sci 361(1476):2129–2141

    Article  CAS  Google Scholar 

  • Stimpson CD et al (2016) Differential serotonergic innervation of the amygdala in bonobos and chimpanzees. Soc Cogn Affect Neurosci 11(3):413422. https://doi.org/10.1093/scan/nsv128

    Article  Google Scholar 

  • Strathearn L (2011) Maternal neglect: oxytocin, dopamine and the neurobiology of attachment. J Neuroendocrinol 23(11):1054–1065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stuppia L et al (2015) Epigenetics and male reproduction: the consequences of paternal lifestyle on fertility, embryo development, and children lifetime health. Clin Epigenetics 7:a120

    Article  CAS  Google Scholar 

  • Thomas AC et al (2012) The speech gene FOXP2 is not imprinted. J Med Genet 49(11):669–670

    Article  CAS  PubMed  Google Scholar 

  • Tobi EW et al (2009) DNA methylation differences after exposure to prenatal famine are common and timing and sex-specific. Hum Mol Genet 18:4046–4053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uher R et al (2011) Serotonin transporter gene moderates childhood maltreatment’s effects on persistent but not single-episode depression: replications and implications for resolving inconsistent results. J Affect Disord 135(1–3):56–65

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vangeel EB et al (2015) DNA methylation in imprinted genes IGF2 and GNASXL is associated with prenatal maternal stress. Genes Brain Behav 14(8):573–582. https://doi.org/10.1111/gbb.12249

    Article  CAS  PubMed  Google Scholar 

  • Vernes SC et al (2008) A functional genetic link between distinct developmental language disorders. N Engl J Med 359(22):2337–2345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang H et al (2013) Histone deacetylase inhibitors facilitate partner preference formation in female prairie voles. Nat Neurosci 16(7):919–924

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Webster MT (2013) Human-specific accelerated evolution of noncoding sequences. eLS. https://doi.org/10.1002/9780470015902.a0020849.pub2

  • Wendland JR et al (2006) Differential functional variability of serotonin transporter and monoamine oxidase a genes in macaque species displaying contrasting levels of aggression-related behaviour. Behav Genet 36(2):163–172

    Article  PubMed  Google Scholar 

  • Yehuda NP et al (2014) Influences of maternal and paternal PTSD on epigenetic regulation of the glucocorticoid receptor gene in holocaust survivor offspring. Am J Psychiatry 171(8):872–880. https://doi.org/10.1176/appi.ajp.2014.13121571

    Article  PubMed  PubMed Central  Google Scholar 

  • Zeng J, Konopka G, Hunt BG, Preuss TM, Geschwind D, Soojin VY (2012) Divergent whole-genome methylation maps of human and chimpanzee brains reveal epigenetic basis of human regulatory evolution. Am J Hum Genet 91(3):455–465

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gillian Ragsdale .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer International Publishing AG, part of Springer Nature

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Ragsdale, G., Foley, R.A. (2018). Epigenetics and the Evolution of Human Social Cognition. In: Di Paolo, L.D., Di Vincenzo, F., De Petrillo, F. (eds) Evolution of Primate Social Cognition. Interdisciplinary Evolution Research, vol 5. Springer, Cham. https://doi.org/10.1007/978-3-319-93776-2_11

Download citation

Publish with us

Policies and ethics