The epigenetic side of human adaptation: hypotheses, evidences and theories

Abstract Context: Epigenetics represents a still unexplored research field in the understanding of micro- and macro-evolutionary mechanisms, as epigenetic changes create phenotypic diversity within both individuals and populations. Objective: The purpose of this review is to dissect the landscape of studies focused on DNA methylation, one of the most described epigenetic mechanisms, emphasizing the aspects that could be relevant in human adaptations. Methods: Theories and results here considered were collected from the most recent papers published. Results: The matter of DNA methylation inheritance is here described as well as the recent evolutionary theories regarding the role of DNA methylation—and epigenetics in a broader sense—in human evolution. The complex relation between (1) DNA methylation and genetic variability and (2) DNA methylation and the environmental stimuli crucial in shaping genetic and phenotypic variability through the human lineage—such as diet, climate and pathogens exposure—are described. Papers about population epigenetics are also illustrated due to their high relevance in this context. Conclusion: Genetic, epigenetic and phenotypic variations of the species, together with cultural ones, are considerably shaped by a vast range of environmental stimuli, thus representing the foundation of all human bio-cultural adaptations.

[1]  Hiroki Nagase,et al.  Association of tissue-specific differentially methylated regions (TDMs) with differential gene expression. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[2]  M. Hallett,et al.  Low paternal dietary folate alters the mouse sperm epigenome and is associated with negative pregnancy outcomes , 2013, Nature Communications.

[3]  Jonathan K. Pritchard,et al.  Adaptations to Climate-Mediated Selective Pressures in Humans , 2011, PLoS genetics.

[4]  R. Singal,et al.  Methylation mediated silencing of TMS1/ASC gene in prostate cancer , 2006, Molecular Cancer.

[5]  J. Ott,et al.  Ethnic diversity of DNA methylation in the OPRM1 promoter region in lymphocytes of heroin addicts , 2010, Human Genetics.

[6]  Paolo Garagnani,et al.  Present and future of anti-ageing epigenetic diets , 2014, Mechanisms of Ageing and Development.

[7]  Michael K. Skinner,et al.  Epigenetic transgenerational actions of environmental factors in disease etiology , 2010, Trends in Endocrinology & Metabolism.

[8]  A. McCann,et al.  Epigenetics: The epicenter of the hypoxic response , 2010, Epigenetics.

[9]  J. Connelly,et al.  Epigenetic origins of metabolic disease: The impact of the maternal condition to the offspring epigenome and later health consequences , 2013 .

[10]  M. Pellegrini,et al.  Genome-wide erasure of DNA methylation in mouse primordial germ cells is affected by AID deficiency , 2010, Nature.

[11]  C. Franceschi,et al.  Space/Population and Time/Age in DNA methylation variability in humans: a study on IGF2/H19 locus in different Italian populations and in mono- and di-zygotic twins of different age , 2012, Aging.

[12]  M. Torbenson,et al.  Hepatitis B Virus Replication Induces Methylation of both Host and Viral DNA , 2010, Journal of Virology.

[13]  J. O’Sullivan,et al.  Generation of an epigenetic signature by chronic hypoxia in prostate cells. , 2009, Human molecular genetics.

[14]  P. Vineis,et al.  Methylation patterns in sentinel genes in peripheral blood cells of heavy smokers: Influence of cruciferous vegetables in an intervention study , 2011, Epigenetics.

[15]  T. Uller,et al.  Three epigenetic information channels and their different roles in evolution , 2011, Journal of evolutionary biology.

[16]  R. Jirtle,et al.  Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development , 2007, Proceedings of the National Academy of Sciences.

[17]  L. Huicho,et al.  Adaptation and Mal-Adaptation to Ambient Hypoxia; Andean, Ethiopian and Himalayan Patterns , 2008, PloS one.

[18]  F. Klironomos,et al.  How epigenetic mutations can affect genetic evolution: model and mechanism. , 2013, BioEssays : news and reviews in molecular, cellular and developmental biology.

[19]  V. Rakyan,et al.  Transgenerational inheritance of epigenetic states at the murine AxinFu allele occurs after maternal and paternal transmission , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[20]  V. Rakyan,et al.  Metastable epialleles in mammals. , 2002, Trends in genetics : TIG.

[21]  Marcus W. Feldman,et al.  The great human expansion , 2012, Resonance.

[22]  G. Semenza,et al.  Epigenetic regulation of hypoxic sensing disrupts cardiorespiratory homeostasis , 2012, Proceedings of the National Academy of Sciences.

[23]  K. Verstrepen,et al.  Timescales of Genetic and Epigenetic Inheritance , 2007, Cell.

[24]  T. Spector,et al.  Epigenetic differences arise during the lifetime of monozygotic twins. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[25]  R. Jaenisch,et al.  Retrovirus-induced de novo methylation of flanking host sequences correlates with gene inactivity , 1985, Nature.

[26]  G. Castellani,et al.  Methylation of ELOVL2 gene as a new epigenetic marker of age , 2012, Aging cell.

[27]  M. Fraga,et al.  Effects of short-term high-fat overfeeding on genome-wide DNA methylation in the skeletal muscle of healthy young men , 2012, Diabetologia.

[28]  Lynn M Almli,et al.  Methylation quantitative trait loci (meQTLs) are consistently detected across ancestry, developmental stage, and tissue type , 2014, BMC Genomics.

[29]  E. Li,et al.  Establishment and Maintenance of Genomic Methylation Patterns in Mouse Embryonic Stem Cells by Dnmt3a and Dnmt3b , 2003, Molecular and Cellular Biology.

[30]  W. Reik,et al.  Epigenetic Reprogramming in Plant and Animal Development , 2010, Science.

[31]  Robert A. Waterland,et al.  Transposable Elements: Targets for Early Nutritional Effects on Epigenetic Gene Regulation , 2003, Molecular and Cellular Biology.

[32]  D. Haber,et al.  DNA Methyltransferases Dnmt3a and Dnmt3b Are Essential for De Novo Methylation and Mammalian Development , 1999, Cell.

[33]  N. Jablonski,et al.  The evolution of human skin coloration. , 2000, Journal of human evolution.

[34]  Peter A. Jones Functions of DNA methylation: islands, start sites, gene bodies and beyond , 2012, Nature Reviews Genetics.

[35]  R. Yuen,et al.  Hypoxia alters the epigenetic profile in cultured human placental trophoblasts , 2013, Epigenetics.

[36]  V. Rakyan,et al.  Transgenerational epigenetic inheritance , 2003, Current Biology.

[37]  B. Korn,et al.  Aging and Chronic Sun Exposure Cause Distinct Epigenetic Changes in Human Skin , 2010, PLoS genetics.

[38]  A. Feinberg,et al.  Genome-wide methylation analysis of human colon cancer reveals similar hypo- and hypermethylation at conserved tissue-specific CpG island shores , 2008, Nature Genetics.

[39]  Matthew D. Schultz,et al.  Transgenerational Epigenetic Instability Is a Source of Novel Methylation Variants , 2011, Science.

[40]  A. Riggs,et al.  DNA methylation and gene function. , 1980, Science.

[41]  R. Martienssen,et al.  Transgenerational Epigenetic Inheritance: Myths and Mechanisms , 2014, Cell.

[42]  Isabelle M. Mansuy,et al.  Epigenetic inheritance in mammals: Evidence for the impact of adverse environmental effects , 2010, Neurobiology of Disease.

[43]  N. J. Eastman Mount Everest in utero. , 1954, American journal of obstetrics and gynecology.

[44]  David I. K. Martin,et al.  Epigenetic inheritance at the agouti locus in the mouse , 1999, Nature Genetics.

[45]  International Human Genome Sequencing Consortium Initial sequencing and analysis of the human genome , 2001, Nature.

[46]  J. Issa,et al.  A simple method for estimating global DNA methylation using bisulfite PCR of repetitive DNA elements. , 2004, Nucleic acids research.

[47]  E. Susser,et al.  Genomic DNA Methylation among Women in a Multiethnic New York City Birth Cohort , 2008, Cancer Epidemiology Biomarkers & Prevention.

[48]  Jonathan K. Pritchard,et al.  The Genetic Architecture of Adaptations to High Altitude in Ethiopia , 2012, PLoS genetics.

[49]  P. Gluckman,et al.  Predictive adaptive responses and human evolution. , 2005, Trends in ecology & evolution.

[50]  E. Jablonka,et al.  Evolution in Four Dimensions: Genetic, Epigenetic, Behavioral, and Symbolic Variation in the History of Life , 2005 .

[51]  G. Pfeifer,et al.  Deamination of 5-Methylcytosines within Cyclobutane Pyrimidine Dimers Is an Important Component of UVB Mutagenesis* , 2003, The Journal of Biological Chemistry.

[52]  H. Putter,et al.  DNA methylation differences after exposure to prenatal famine are common and timing- and sex-specific. , 2009, Human molecular genetics.

[53]  C. Shin,et al.  Hepatitis B virus inhibits liver regeneration via epigenetic regulation of urokinase‐type plasminogen activator , 2013, Hepatology.

[54]  E. Whitelaw,et al.  Understanding transgenerational epigenetic inheritance via the gametes in mammals , 2012, Nature Reviews Genetics.

[55]  S. Langley-Evans,et al.  Nutrition in early life and the programming of adult disease: a review. , 2015, Journal of human nutrition and dietetics : the official journal of the British Dietetic Association.

[56]  S E Ozanne,et al.  Pathways linking the early environment to long-term health and lifespan. , 2011, Progress in biophysics and molecular biology.

[57]  T. Marquès-Bonet,et al.  DNA methylation contributes to natural human variation , 2013, Genome research.

[58]  T. Ideker,et al.  Genome-wide methylation profiles reveal quantitative views of human aging rates. , 2013, Molecular cell.

[59]  Jingde Zhu,et al.  Hepatitis virus infection affects DNA methylation in mice with humanized livers. , 2014, Gastroenterology.

[60]  M. Grocott,et al.  Concepts in hypoxia reborn , 2010, Critical care.

[61]  A. Feinberg,et al.  Stochastic epigenetic variation as a driving force of development, evolutionary adaptation, and disease , 2010, Proceedings of the National Academy of Sciences.

[62]  Leif Groop,et al.  A Six Months Exercise Intervention Influences the Genome-wide DNA Methylation Pattern in Human Adipose Tissue , 2013, PLoS genetics.

[63]  D. Weigel,et al.  Epigenetic variation: origin and transgenerational inheritance. , 2012, Current opinion in plant biology.

[64]  R. Cardarelli,et al.  Significant differences in global genomic DNA methylation by gender and race/ethnicity in peripheral blood , 2011, Epigenetics.

[65]  B. Turner Environmental sensing by chromatin: An epigenetic contribution to evolutionary change , 2011, FEBS letters.

[66]  Navin Elango,et al.  DNA methylation and structural and functional bimodality of vertebrate promoters. , 2008, Molecular biology and evolution.

[67]  Hunter B. Fraser,et al.  Population-specificity of human DNA methylation , 2012, Genome Biology.

[68]  Paul Haggarty,et al.  Population Epigenetics , 2017, Methods in Molecular Biology.

[69]  R. Nielsen,et al.  Signatures of Environmental Genetic Adaptation Pinpoint Pathogens as the Main Selective Pressure through Human Evolution , 2011, PLoS genetics.

[70]  M. Surani,et al.  Genetic and Epigenetic Regulators of Pluripotency , 2007, Cell.

[71]  Thomas Lengauer,et al.  CpG Island Methylation in Human Lymphocytes Is Highly Correlated with DNA Sequence, Repeats, and Predicted DNA Structure , 2006, PLoS genetics.

[72]  R. Casadio,et al.  Searching for signatures of cold adaptations in modern and archaic humans: hints from the brown adipose tissue genes , 2014, Heredity.

[73]  Hein Putter,et al.  Persistent epigenetic differences associated with prenatal exposure to famine in humans , 2008, Proceedings of the National Academy of Sciences.

[74]  F. Antequera,et al.  Structure, function and evolution of CpG island promoters , 2003, Cellular and Molecular Life Sciences CMLS.

[75]  Kent Hutchison,et al.  Identification of Genetic and Epigenetic Marks Involved in Population Structure , 2010, PloS one.