Advanced search
Publication Cover
Epigenomics Volume 3, 2011 - Issue 2
Submit an article Journal homepage
6,234
Views
0
CrossRef citations to date
0
Altmetric
Perspective

Timescales of Human Adaptation: The Role of Epigenetic Processes

Christopher W Kuzawa1 Department of Anthropology, Northwestern University, Evanston, IL60208, USA;2 Cells 2 Society, The Center on Social Disparities & Health at the Institute for Policy Research, Northwestern University, Evanston, IL60208, USA.Correspondence[email protected]
&
Zaneta M Thayer1 Department of Anthropology, Northwestern University, Evanston, IL60208, USA
Pages 221-234 | Published online: 20 Apr 2011

Bibliography

  • Barker D : The fetal origins of adult disease.Fetal Maternal Med. Rev.6(2) , 71–80 (1994).
  • Gluckman PD , HansonMA, CooperC, ThornburgKL: Effect of in utero and early-life conditions on adult health and disease.N. Engl. J. Med.359(1) , 61–73 (2008).
  • Cameron NM , ShahrokhD, Del Corpo A et al.: Epigenetic programming of phenotypic variations in reproductive strategies in the rat through maternal care. J. Neuroendocrinol.20(6) , 795–801 (2008).
  • Kuzawa CW : Developmental origins of life history: growth, productivity, and reproduction.Am. J. Hum. Biol.19(5) , 654–661 (2007).
  • Kuzawa CW , PikeIL: Introduction. Fetal origins of developmental plasticity.Am. J. Hum. Biol.17(1) , 1–4 (2005).
  • West-Eberhard M : Developmental Plasticity and Evolution. Oxford University Press, NY, USA (2003).
  • Mcmillen IC , RobinsonJS: Developmental origins of the metabolic syndrome: prediction, plasticity, and programming.Physiol. Rev.85(2) , 571–633 (2005).
  • Symonds ME , SebertSP, BudgeH: The impact of diet during early-life and its contribution to later disease: critical checkpoints in development and their long-term consequences for metabolic health.Proc. Nutr. Soc.68(4) , 416–421 (2009).
  • Jasienska G , ZiomkiewiczA, LipsonSF, ThuneI, EllisonPT: High ponderal index at birth predicts high estradiol levels in adult women.Am. J. Human Biol.18(1) , 133–140 (2006).
  • Kuzawa CW , McDadeTW, AdairLS, LeeN: Rapid weight gain after birth predicts life history and reproductive strategy in Filipino males.Proc. Natl Acad. Sci. USA107(39) , 16800–16805 (2010).
  • Sanchez J , PriegoT, PalouM, TobaruelaA, PalouA, PicoC: Oral supplementation with physiological doses of leptin during lactation in rats improves insulin sensitivity and affects food preferences later in life.Endocrinology149(2) , 733–740 (2008).
  • Entringer S , KumstaR, HellhammerDH, WadhwaPD, WustS: Prenatal exposure to maternal psychosocial stress and HPA axis regulation in young adults.Horm. Behav.55(2) , 292–298 (2009).
  • Pembrey ME , BygrenLO, KaatiGet al.: Sex-specific, male-line transgenerational responses in humans.Eur. J. Hum. Genet.14(2) , 159–166 (2005).
  • Pembrey ME : Male-line transgenerational responses in humans.Hum. Fertil.13(4) , 268–271 (2010).
  • Franklin TB , RussigH, WeissICet al.: Epigenetic transmission of the impact of early stress across generations.Biol. Psych.68(5) , 408–415 (2010).
  • Anway MD , CuppAS, UzumcuM, SkinnerMK: Epigenetic transgenerational actions of endocrine disruptors and male fertility.Science308(5727) , 1466–1469 (2005).
  • Ellison PT , JasienskaG: Constraint, pathology, and adaptation: how can we tell them apart?Am. J. Hum. Biol.19(5) , 622–630 (2007).
  • Gluckman PD , HansonMA, SpencerHG, BatesonP: Environmental influences during development and their later consequences for health and disease: implications for the interpretation of empirical studies.Proc. Biol. Sci.272(1564) , 671–677 (2005).
  • Schell LM , MagnusP: Is there an elephant in the room? Addressing rival approaches to the interpretation of growth perturbations and small size.Am. J. Human Biol.19(5) , 606–614 (2007).
  • Prins GS : Estrogen imprinting: when your epigenetic memories come back to haunt you.Endocrinology149(12) , 5919–5921 (2008).
  • Newbold RR , Padilla-BanksE, JeffersonWN: Adverse effects of the model environmental estrogen diethylstilbestrol are transmitted to subsequent generations.Endocrinology147(6) , S11–S17 (2006).
  • Titus-Ernstoff L , TroisiR, HatchEEet al.: Menstrual and reproductive characteristics of women whose mothers were exposed in utero to diethylstilbestrol (DES).Int. J. Epidemiol.35(4) , 862–868 (2006).
  • Bateson P : Fetal experience and good adult design.Int. J. Epidemiol.30(5) , 928–934 (2001).
  • Gluckman PD , HansonM: The fetal matrix: Evolution, Development, and Disease. Peter Gluckman PD, Hanson M (Eds). Cambridge University Press, NY, USA (2005).
  • Kuzawa CW : Fetal origins of developmental plasticity: are fetal cues reliable predictors of future nutritional environments?Am. J. Human Biol.17(1) , 5–21 (2005).
  • Kuzawa C , GluckmanP, HansonM, BeedleA: Evolution, developmental plasticity, and metabolic disease. In: Evolution in Health and Disease. Stearns S, Koella J (Eds). Oxford University Press, Oxford, UK, 253–264 (2008).
  • Martorell R : Body size, adaptation and function.Human Organization48(1) , 15–20 (1989).
  • Seckl JR , HolmesMC: Mechanisms of disease: glucocorticoids, their placental metabolism and fetal ‘programming‘ of adult pathophysiology.Nat. Clin. Pract. Endocrinol. Metab.3(6) , 479–488 (2007).
  • Schoof E , GirstlM, FrobeniusWet al.: Course of placental 11β-hydroxysteroid dehydrogenase type 2 and 15-hydroxyprostaglandin dehydrogenase mRNA expression during human gestation.Eur. J. Endocrinol.145(2) , 187–192 (2001).
  • Welberg LA , ThrivikramanKV, PlotskyPM: Chronic maternal stress inhibits the capacity to up-regulate placental 11β-hydroxysteroid dehydrogenase type 2 activity.J . Endocrinol.186(3) , R7–R12 (2005).
  • Alfaidy N , GuptaS, DemarcoC, CaniggiaI, ChallisJR: Oxygen regulation of placental 11 β-hydroxysteroid dehydrogenase 2: physiological and pathological implications.J. Clin. Endocrinol. Metab.87(10) , 4797–4805 (2002).
  • Sarkar S , TsaiSW, NguyenTT, PlevyakM, PadburyJF, RubinLP: Inhibition of placental 11β-hydroxysteroid dehydrogenase type 2 by catecholamines via α-adrenergic signaling.Am. J. Physiol. Regul. Integr. Comp. Physiol.281(6) , R1966–1974 (2001).
  • Langley-Evans S : Fetal programming of cardiovascular function through exposure to maternal undernutrition.Proc. Nutr. Soc.60 , 505–513 (2001).
  • Stocker C , O‘DowdJ, MortonNMet al.: Modulation of susceptibility to weight gain and insulin resistance in low birthweight rats by treatment of their mothers with leptin during pregnancy and lactation.Int. J. Obes. Relat. Metab. Disord.28(1) , 129–136 (2004).
  • Pike IL : Maternal stress and fetal responses: evolutionary perspectives on preterm delivery.Am. J. Hum. Biol.17(1) , 55–65 (2005).
  • Wada H : Glucocorticoids: mediators of vertebrate ontogenetic transitions.Gen. Comp. Endocrinol.156(3) , 441–453 (2008).
  • Entringer S , WüstS, KumstaRet al.: Prenatal psychosocial stress exposure is associated with insulin resistance in young adults.Am. J. Obstetr. Gynecol.199(5) , 498.e1–e7 (2008).
  • Entringer S , KumstaR, NelsonEL, HellhammerDH, WadhwaPD, WüstS: Influence of prenatal psychosocial stress on cytokine production in adult women.Dev. Psychobiol.50(6) , 579–587 (2008).
  • Mychasiuk R , IlnytskyyS, KovalchukO, KolbB, GibbR: Intensity matters: brain, behaviour and the epigenome of prenatally stressed rats.Neuroscience (2010) (Epub ahead of print).
  • Oberlander TF , WeinbergJ, PapsdorfM, GrunauR, MisriS, DevlinAM: Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses.Epigenetics3(2) , 97–106 (2008).
  • Champagne FA : Epigenetic mechanisms and the transgenerational effects of maternal care.Front. Neuroendocrinol.29(3) , 386–397 (2008).
  • Weaver ICG , CervoniN, ChampagneFAet al.: Epigenetic programming by maternal behavior.Nat. Neurosci.7(8) , 847–854 (2004).
  • Zhang T -Y, Meaney MJ: Epigenetics and the environmental regulation of the genome and its function. Ann. Rev. Psychol.61(1) , 439–466 (2010).
  • Stocking GW : Race, Culture and Evolution: Essays in the History of Anthropology. Free Press, NY, USA (1968).
  • Boas F : Changes in the bodily form of descendents of immigrants.Am. Anthropol.14(3) , 530–562 (1912).
  • Kuzawa CW , SweetE: Epigenetics and the embodiment of race: developmental origins of US racial disparities in cardiovascular health.Am. J. Hum. Biol.21(1) , 2–15 (2009).
  • Gould SJ : The Mismeasure of Man. WW Norton and Company, NY, USA (1981).
  • Washburn S : The new physical anthropology.Trans. NY Acad. Sci.13(7) , 298–304 (1951).
  • Lasker G : Human biological adaptability.Science166(3912) , 1480–1486 (1969).
  • Ellison PT : Evolutionary perspectives on the fetal origins hypothesis.Am. J. Human Biol.17(1) , 113–118 (2005).
  • Bateson G : The role of somatic change in biological evolution.Evolution17 , 529–539 (1963).
  • Frisancho A : Developmental adaptation to high altitude hypoxia.Int. J. Biometerol.21(2) , 135–146 (1977).
  • Edelman GM : Neural Darwinism: Selection and reentrant signaling in higher brain function.Neuron10(2) , 115–125 (1993).
  • Changeux J -P: Neuronal Man: The Biology of Mind. Oxford University Press, NY, USA (1986).
  • McDade TW , WorthmanCM: Evolutionary process and the ecology of human immune function.Am. J. Human Biol.11(6) , 705–717 (1999).
  • Bogin B : Patterns of Human Growth, (2nd Edition). Cambridge University Press, Cambridge, UK (1999).
  • Wells JC : The thrifty phenotype as an adaptive maternal effect.Biol. Rev. Camb. Philos. Soc.82(1) , 143–172 (2007).
  • Kuzawa C : The developmental origins of adult health: intergenerational inertia in adaptation and disease. In: Evolutionary Medicine: New Perspectives. Trevathan ES, Mckenna J (Eds). Oxford University Press, Oxford, UK, 325–349 (2008).
  • Potts R : Environmental hypotheses of hominin evolution.Am. J. Phys. Anthropol. (Suppl. 27), 93–136 (1998).
  • Wells JC , StockJT: The biology of the colonizing ape.Am. J. Phys. Anthropol. (Suppl. 45), 191–222 (2007).
  • Wells JC : The thrifty phenotype hypothesis: thrifty offspring or thrifty mother?J. Theor. Biol.221(1) , 143–161 (2003).
  • Belsky J , SteinbergL, DraperP: Childhood experience, interpersonal development, and reproductive strategy: and evolutionary theory of socialization.Child Dev.62(4) , 647–670 (1991).
  • Chisholm JS : Death, hope, and sex: life-history theory and the development of reproductive strategies.Curr. Anthropol.34(1) , 1–24 (1993).
  • Ellis B , FigueredoA, BrumbachB, SchlomerG: Fundamental dimensions of environmental risk.Hum. Nat.20 , 204–268 (2009).
  • Barker DJ , OsmondC, GoldingJ, KuhD, WadsworthME: Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease.BMJ298(6673) , 564–567 (1989).
  • Newsome CA , ShiellAW, FallCHD, PhillipsDIW, ShierR, LawCM: Is birthweight related to later glucose and insulin metabolism? A systematic review.Diabetic Med.20(5) , 339–348 (2003).
  • Kind KL , CliftonPM, GrantPAet al.: Effect of maternal feed restriction during pregnancy on glucose tolerance in the adult guinea pig.Am. J. Physiol. Regul. Integr. Comp. Physiol.284(1) , R140–R152 (2003).
  • Kind KL , SimonettaG, CliftonPM, RobinsonJS, OwensJA: Effect of maternal feed restriction on blood pressure in the adult guinea pig.Exp. Physiol.87(4) , 469–477 (2002).
  • Harding JE : The nutritional basis of the fetal origins of adult disease.Int. J. Epidemiol.30(1) , 15–23 (2001).
  • Rasmussen KM , Habicht J-P: Maternal supplementation differentially affects the mother and newborn. J. Nutr.140(2) , 402–406 (2010).
  • Adair L , PollittE: Outcome of maternal nutritional supplementation: a comprehensive review of the Bacon Chow study.Am. J. Clin. Nutr.41(5) , 948–978 (1985).
  • Abu-Saad K , FraserD: Maternal nutrition and birth outcomes.Epidemiol. Rev.32(1) , 5–25 (2010).
  • Osrin D , ProstA: Perinatal interventions and survival in resource-poor settings: which work, which don‘t, which have the jury out?Arch. Dis. Childhood95(12) , 1039–1046 (2010).
  • Merialdi M , CarroliG, VillarJet al.: nutritional interventions during pregnancy for the prevention or treatment of impaired fetal growth: an overview of randomized controlled trials.J. Nutr.133(5) , 1626S–1631S (2003).
  • Villar J , MerialdiM, GülmezogluAMet al.: Nutritional interventions during pregnancy for the prevention or treatment of maternal morbidity and preterm delivery: an overview of randomized controlled trials.J. Nutr.133(5) , 1606S–1625S (2003).
  • Kramer MS , KakumaR: Energy and protein intake in pregnancy.Cochrane Database Syst. Rev.3 , 1–74 (2010).
  • Medicine IO: Nutrition During Pregnancy. Part I, Weight Gain. National Academy Press, Washington, DC, USA (1990).
  • Ounsted M , ScottA, OunstedC: Transmission through the female line of a mechanism constraining human fetal growth.Ann. Hum. Biol.13(2) , 143–151 (1986).
  • Morton S : Maternal nutrition and fetal growth and development. In: Developmental Origins of Health and Disease, Gluckman PD, Hanson MA (Eds). Cambridge University Press, NY, USA, 98–129 (2006).
  • Lawlor DA , Davey Smith G, Ebrahim S: Association between leg length and offspring birthweight: partial explanation for the trans-generational association between birthweight and cardiovascular disease: findings from the British Women‘s Heart and Health Study. Paediatr. Perinat. Epidemiol.17(2) , 148–155 (2003).
  • Rutherford JN : Fetal signaling through placental structure and endocrine function: illustrations and implications from a nonhuman primate model.Am. J. Hum. Biol.21(6) , 745–753 (2009).
  • Lechtig A , Habicht J-P, Delgado H, Klein RE, Yarbrough C, Martorell R: Effect of food supplementation during pregnancy on birthweight. Pediatrics56(4) , 508–520 (1975).
  • Stein AD , BarnhartHX, HickeyM, RamakrishnanU, SchroederDG, MartorellR: Prospective study of protein-energy supplementation early in life and of growth in the subsequent generation in Guatemala.Am. J. Clin. Nutr.78(1) , 162–167 (2003).
  • Behrman JR , CalderonMC, PrestonSH, HoddinottJ, MartorellR, SteinAD: Nutritional supplementation in girls influences the growth of their children: prospective study in Guatemala.Am. J. Clin. Nutr.90(5) , 1372–1379 (2009).
  • Villar J , RiveraJ: Nutritional supplementation during two consecutive pregnancies and the interim lactation period: effect on birth weight.Pediatrics81(1) , 51–57 (1988).
  • Arenz S , RuckerlR, KoletzkoB, Von Kries R: Breast-feeding and childhood obesity – a systematic review. Int. J. Obes. Relat. Metab. Disord.28(10) , 1247–1256 (2004).
  • Kuzawa C , QuinnE: Developmental origins of adult function and health: evolutionary hypotheses.Ann. Rev. Anthropol.38 , 131–147 (2009).
  • Savino F , LiguoriSA, FissoreMF, OggeroR: Breast milk hormones and their protective effect on obesity.Int. J. Pediatr. Endocrinol.2009 , 327505 (2009).
  • Doneray H , OrbakZ, YildizL: The relationship between breast milk leptin and neonatal weight gain.Acta Paediatr.98(4) , 643–647 (2009).
  • Miralles O , SanchezJ, PalouA, PicoC: A physiological role of breast milk leptin in body weight control in developing infants.Obesity (Silver Spring)14(8) , 1371–1377 (2006).
  • Ilcol YO , HizliZB, OzkanT: Leptin concentration in breast milk and its relationship to duration of lactation and hormonal status.Int. Breastfeed J.1 , 21 (2006).
  • Savino F , LiguoriSA, OggeroR, SilvestroL, MinieroR: Maternal BMI and serum leptin concentration of infants in the first year of life.Acta Paediatr.95(4) , 414–418 (2006).
  • Kuzawa CW : Adipose tissue in human infancy and childhood: an evolutionary perspective.Am. J. Phys. Anthropol. (Suppl. 27), 177–209 (1998).
  • Kuzawa CW : Beyond feast-famine: brain evolution, human life history, and the metabolic syndrome. In: Human Evolutionary Biology. Muehlenbein M (Ed.). Cambridge University Press, Cambridge, UK (2010).
  • Mcgowan PO , SasakiA, D‘AlessioACet al.: Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse.Nat. Neurosci.12(3) , 342–348 (2009).
  • Gluckman PD , LillycropKA, VickersMHet al.: Metabolic plasticity during mammalian development is directionally dependent on early nutritional status.Proc. Natl Acad. Sci. USA104(31) , 12796–12800 (2007).
  • Trivers RL : Parent-offspring conflict.Am. Zoologist14(1) , 249–264 (1974).
  • Haig D : Genetic conflicts in human pregnancy.Q. Rev. Biol.68(4) , 495–532 (1993).
  • Hawkes K : Colloquium paper: how grandmother effects plus individual variation in frailty shape fertility and mortality: guidance from human–chimpanzee comparisons.Proc. Natl Acad. Sci. USA107(Suppl. 2) , 8977–8984 (2010).
  • De Rooij SR , PainterRC, PhillipsDIWet al.: Hypothalamic-pituitary-adrenal axis activity in adults who were prenatally exposed to the Dutch famine.Eur. J. Endocrinol.155(1) , 153–160 (2006).
  • De Rooij SR , PainterRC, HollemanF, BossuytPM, RoseboomTJ: The metabolic syndrome in adults prenatally exposed to the Dutch famine.Am. J. Clin. Nutr.86(4) , 1219–1224 (2007).
  • Calder WA : Size, Function, and Life History. Harvard University Press, Cambridge, MA, USA (1984).
  • Mccance R , WiddowsonE: Glimpses of comparative growth and development. In: Human Growth. A Comprehensive Treatise, Volume 1. Developmental Biology, Prenatal Growth. Tanner J, Falkner F (Eds). Plenum, NY, USA, 133–151 (1986).
  • Rollo CD : Growth negatively impacts the life span of mammals.Evol. Devel.4(1) , 55–61 (2002).
  • Flohn H : Short-term climate fluctuations and their economic role. In: Climate and History. Studies in Past Climate and their Impact on Man. Wigley T, Ingram M, Farmer G (Eds). Cambridge University Press, Cambridge, UK, 310–336 (1981).
  • Ozaki T , NishinaH, HansonMA, PostonL: Dietary restriction in pregnant rats causes gender-related hypertension and vascular dysfunction in offspring.J. Physiol.530(1) , 141–152 (2001).
  • Gopalakrishnan GS , GardnerDS, RhindSMet al.: Programming of adult cardiovascular function after early maternal undernutrition in sheep.Am. J. Physiol.287(1) , R12–R20 (2004).
  • Roseboom TJ , Van Der Meulen JHP, Ravelli ACJ, Osmond C, Barker DJP, Bleker OP: Effects of prenatal exposure to the Dutch famine on adult disease in later life: an overview. Mol. Cell. Endocrinol.185(1–2) , 93–98 (2001).
  • Franco Mdo C , ArrudaRM, DantasAPet al.: Intrauterine undernutrition: expression and activity of the endothelial nitric oxide synthase in male and female adult offspring.Cardiovasc. Res.56(1) , 145–153 (2002).
  • Gardner DS , TingeyK, Van Bon BWM et al.: Programming of glucose-insulin metabolism in adult sheep after maternal undernutrition. Am. J. Physiol.289(4) , R947–R954 (2005).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Order Reprints Request Corporate Permissions

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

Request Academic Permissions

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.