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Epigenetic legacy of parental experiences: Dynamic and interactive pathways to inheritance

Published online by Cambridge University Press:  30 September 2016

Frances A. Champagne
Frances A. Champagne*
Affiliation:
Columbia University
*
Address correspondence and reprint requests to: Frances A. Champagne, Department of Psychology, Columbia University, 406 Schermerhorn Hall, 1190 Amsterdam Avenue, New York, NY 10027; E-mail: [email protected].
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Abstract

The quality of the environment experienced by an individual across his or her lifespan can result in a unique developmental trajectory with consequences for adult phenotype and reproductive success. However, it is also evident that these experiences can impact the development of offspring with continued effect on subsequent generations. Epigenetic mechanisms have been proposed as a mediator of both these within- and across-generation effects, and there is increasing evidence to support the role of environmentally induced changes in DNA methylation, posttranslational histone modifications, and noncoding RNAs in predicting these outcomes. Advances in our understanding of these molecular modifications contribute to increasingly nuanced perspectives on plasticity and transmission of phenotypes across generations. A challenge that emerges from this research is in how we integrate these “new” perspectives with traditional views of development, reproduction, and inheritance. This paper will highlight evidence suggestive of an epigenetic impact of the environment on mothers, fathers, and their offspring, and illustrate the importance of considering the dynamic nature of reproduction and development and inclusive views of inheritance within the evolving field of behavioral and environmental epigenetics.

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Special Section Articles
Information
Development and Psychopathology , Volume 28 , Special Issue 4pt2: Epigenetics: Development, Psychopathology, Resilience, and Preventive Intervention , November 2016 , pp. 1219 - 1228
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Copyright © Cambridge University Press 2016 

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References

Alter, M. D., Gilani, A. I., Champagne, F. A., Curley, J. P., Turner, J. B., & Hen, R. (2009). Paternal transmission of complex phenotypes in inbred mice. Biological Psychiatry, 66, 1061–1066.Google Scholar
Anway, M. D., Cupp, A. S., Uzumcu, M., & Skinner, M. K. (2005). Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science, 308, 1466–1469.Google Scholar
Anway, M. D., & Skinner, M. K. (2006). Epigenetic transgenerational actions of endocrine disruptors. Endocrinology 147(Suppl. 6), S43–S49.CrossRefGoogle ScholarPubMed
Arnold, K. E., Gilbert, L., Gormen, H. E., Griffiths, K. J., Adam, A., & Nager, R. G. (2016). Paternal attractiveness and the effects of differential allocation of parental investment. Animal Behaviour, 113, 69–78.Google Scholar
Bagot, R. C., Zhang, T. Y., Wen, X., Nguyen, T. T., Nguyen, H. B., Diorio, J., et al. (2012). Variations in postnatal maternal care and the epigenetic regulation of metabotropic glutamate receptor 1 expression and shippocampal function in the rat. Proceedings of the National Academy of Sciences, 109(Suppl. 2), 17200–17207.Google Scholar
Barski, A., Cuddapah, S., Cui, K., Roh, T. Y., Schones, D. E., Wang, Z., et al. (2007). High-resolution profiling of histone methylations in the human genome. Cell, 129, 823–837.CrossRefGoogle ScholarPubMed
Bartolomei, M. S., & Ferguson-Smith, A. C. (2011). Mammalian genomic imprinting. Cold Spring Harbor Perspectives in Biology, 3, a002592.CrossRefGoogle ScholarPubMed
Benoit, D., & Parker, K. C. (1994). Stability and transmission of attachment across three generations. Child Development, 65, 1444–1456.CrossRefGoogle ScholarPubMed
Berman, C. (1990). Intergenerational transmission of maternal rejection rates among free-ranging rheus monkeys on Cayo Santiago. Animal Behavior, 44, 247–258.Google Scholar
Biniszkiewicz, D., Gribnau, J., Ramsahoye, B., Gaudet, F., Eggan, K., Humpherys, D., et al. (2002). Dnmt1 overexpression causes genomic hypermethylation, loss of imprinting, and embryonic lethality. Molecular and Cellular Biology, 22, 2124–2135.CrossRefGoogle ScholarPubMed
Boccia, M. L., & Pedersen, C. A. (2001). Brief vs. long maternal separations in infancy: Contrasting relationships with adult maternal behavior and lactation levels of aggression and anxiety. Psychoneuroendocrinology , 26, 657–672.Google Scholar
Braun, K., & Champagne, F. A. (2014). Paternal influences on offspring development: Behavioural and epigenetic pathways. Journal of Neuroendocrinology, 26, 697–706.Google Scholar
Burley, N. (1988). The differential-allocation hypothesis—An experimental test. American Naturalist, 132, 611–628.Google Scholar
Casas-Agustench, P., Fernandes, F. S., Tavares do Carmo, M. G., Visioli, F., Herrera, E., & Davalos, A. (2015). Consumption of distinct dietary lipids during early pregnancy differentially modulates the expression of microRNAs in mothers and offspring. PLOS ONE, 10, e0117858.Google Scholar
Champagne, F. A., & Meaney, M. J. (2006). Stress during gestation alters postpartum maternal care and the development of the offspring in a rodent model. Biological Psychiatry, 59, 1227–1235.Google Scholar
Champagne, F. A., & Meaney, M. J. (2007). Transgenerational effects of social environment on variations in maternal care and behavioral response to novelty. Behavioral Neuroscience, 121, 1353–1363.CrossRefGoogle ScholarPubMed
Champagne, F. A., Weaver, I. C., Diorio, J., Dymov, S., Szyf, M., & Meaney, M. J. (2006). Maternal care associated with methylation of the estrogen receptor-alpha1b promoter and estrogen receptor-alpha expression in the medial preoptic area of female offspring. Endocrinology, 147, 2909–2915.Google Scholar
Champagne, F. A., Weaver, I. C., Diorio, J., Sharma, S., & Meaney, M. J. (2003). Natural variations in maternal care are associated with estrogen receptor alpha expression and estrogen sensitivity in the medial preoptic area. Endocrinology, 144, 4720–4724.CrossRefGoogle ScholarPubMed
Crews, D., Gore, A. C., Hsu, T. S., Dangleben, N. L., Spinetta, M., Schallert, T., et al. (2007). Transgenerational epigenetic imprints on mate preference. Proceedings of the National Academy of Sciences, 104, 5942–5946.CrossRefGoogle ScholarPubMed
Curley, J. P., Davidson, S., Bateson, P., & Champagne, F. A. (2009). Social enrichment during postnatal development induces transgenerational effects on emotional and reproductive behavior in mice. Frontiers in Behavioral Neuroscience, 3, 25.Google Scholar
Danchin, E., Charmantier, A., Champagne, F. A., Mesoudi, A., Pujol, B., & Blanchet, S. (2011). Beyond DNA: Integrating inclusive inheritance into an extended theory of evolution. Nature Reviews Genetics, 12, 475–486.Google Scholar
Davis, E. P., & Sandman, C. A. (2012). Prenatal psychobiological predictors of anxiety risk in preadolescent children. Psychoneuroendocrinology, 37, 1224–1233.CrossRefGoogle ScholarPubMed
de Castro Barbosa, T., Ingerslev, L. R., Alm, P. S., Versteyhe, S., Massart, J., Rasmussen, M., et al. (2016). High-fat diet reprograms the epigenome of rat spermatozoa and transgenerationally affects metabolism of the offspring. Molecular Metabolism, 5, 184–197.Google Scholar
de Waal, E., Vrooman, L. A., Fischer, E., Ord, T., Mainigi, M. A., Coutifaris, C., et al. (2015). The cumulative effect of assisted reproduction procedures on placental development and epigenetic perturbations in a mouse model. Human Molecular Genetics, 24, 6975–6985.Google Scholar
de Waal, E., Yamazaki, Y., Ingale, P., Bartolomei, M. S., Yanagimachi, R., & McCarrey, J. R. (2012). Gonadotropin stimulation contributes to an increased incidence of epimutations in ICSI-derived mice. Human Molecular Genetics, 21, 4460–4472.Google Scholar
Dias, B. G., & Ressler, K. J. (2014). Parental olfactory experience influences behavior and neural structure in subsequent generations. Nature Neuroscience, 17, 89–96.Google Scholar
Dietz, D. M., Laplant, Q., Watts, E. L., Hodes, G. E., Russo, S. J., Feng, J., et al. (2011). Paternal transmission of stress-induced pathologies. Biological Psychiatry, 70, 408–414.Google Scholar
Dunn, G. A., & Bale, T. L. (2009). Maternal high-fat diet promotes body length increases and insulin insensitivity in second-generation mice. Endocrinology, 150, 4999–5009.CrossRefGoogle ScholarPubMed
Dunn, G. A., & Bale, T. L. (2011). Maternal high-fat diet effects on third-generation female body size via the paternal lineage. Endocrinology, 152, 2228–2236.Google Scholar
El Hajj, N., & Haaf, T. (2013). Epigenetic disturbances in in vitro cultured gametes and embryos: Implications for human assisted reproduction. Fertility and Sterility, 99, 632–641.Google Scholar
Fortier, A. L., Lopes, F. L., Darricarrere, N., Martel, J., & Trasler, J. M. (2008). Superovulation alters the expression of imprinted genes in the midgestation mouse placenta. Human Molecular Genetics, 17, 1653–1665.Google Scholar
Franklin, T. B., Russig, H., Weiss, I. C., Graff, J., Linder, N., Michalon, A., et al. (2010). Epigenetic transmission of the impact of early stress across generations. Biological Psychiatry, 68, 408–415.CrossRefGoogle Scholar
Gabory, A., Ferry, L., Fajardy, I., Jouneau, L., Gothie, J. D., Vige, A., et al. (2012). Maternal diets trigger sex-specific divergent trajectories of gene expression and epigenetic systems in mouse placenta. PLOS ONE, 7, e47986.Google Scholar
Gapp, K., Jawaid, A., Sarkies, P., Bohacek, J., Pelczar, P., Prados, J., et al. (2014). Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice. Nature Neuroscience, 17, 667–669.Google Scholar
Gely-Pernot, A., Hao, C., Becker, E., Stuparevic, I., Kervarrec, C., Chalmel, F., et al. (2015). The epigenetic processes of meiosis in male mice are broadly affected by the widely used herbicide atrazine. BMC Genomics, 16, 885.Google Scholar
Gleason, E. D., & Marler, C. A. (2013). Non-genomic transmission of paternal behaviour between fathers and sons in the monogamous and biparental California mouse. Proceedings of the Royal Society B: Biological Sciences, 280, 20130824.CrossRefGoogle ScholarPubMed
Gubernick, D. J., & Alberts, J. R. (1983). Maternal licking of young: Resource exchange and proximate controls. Physiology & Behavior, 31, 593–601.Google Scholar
Haig, D. (1993). Genetic conflicts in human pregnancy. Quarterly Review of Biology, 68, 495–532.Google Scholar
Harold, G. T., Leve, L. D., Barrett, D., Elam, K., Neiderhiser, J. M., Natsuaki, M. N., et al. (2013). Biological and rearing mother influences on child ADHD symptoms: Revisiting the developmental interface between nature and nurture. Journal of Child Psychology and Psychiatry, 54, 1038–1046.CrossRefGoogle ScholarPubMed
Harris, W. E., & Uller, T. (2009). Reproductive investment when mate quality varies: Differential allocation versus reproductive compensation. Philosophical Transactions of the Royal Society B: Biological Sciences, 364, 1039–1048.CrossRefGoogle ScholarPubMed
Himes, K. P., Koppes, E., & Chaillet, J. R. (2013). Generalized disruption of inherited genomic imprints leads to wide-ranging placental defects and dysregulated fetal growth. Developmental Biology, 373, 72–82.Google Scholar
Howerton, C. L., Morgan, C. P., Fischer, D. B., & Bale, T. L. (2013). O-GlcNAc transferase (OGT) as a placental biomarker of maternal stress and reprogramming of CNS gene transcription in development. Proceedings of the National Academy of Sciences, 110, 5169–5174.Google Scholar
Huffman, S. R., Pak, Y., & Rivera, R. M. (2015). Superovulation induces alterations in the epigenome of zygotes, and results in differences in gene expression at the blastocyst stage in mice. Molecular Reproduction and Development, 82, 207–217.Google Scholar
Isles, A. R., & Holland, A. J. (2005). Imprinted genes and mother–offspring interactions. Early Human Development, 81, 73–77.CrossRefGoogle ScholarPubMed
Ivy, A. S., Brunson, K. L., Sandman, C., & Baram, T. Z. (2008). Dysfunctional nurturing behavior in rat dams with limited access to nesting material: A clinically relevant model for early-life stress. Neuroscience, 154, 1132–1142.Google Scholar
Jablonka, E., & Lamb, M. J. (2002). The changing concept of epigenetics. Annals of the New York Academy of Sciences, 981, 82–96.Google Scholar
Jensen Pena, C., Monk, C., & Champagne, F. A. (2012). Epigenetic effects of prenatal stress on 11beta-hydroxysteroid dehydrogenase-2 in the placenta and fetal brain. PLOS ONE, 7, e39791.Google Scholar
Jenuwein, T., & Allis, C. D. (2001). Translating the histone code. Science, 293, 1074–1080.CrossRefGoogle ScholarPubMed
Jones, P. A., & Taylor, S. M. (1980). Cellular differentiation, cytidine analogs and DNA methylation. Cell, 20, 85–93.Google Scholar
Kaati, G., Bygren, L. O., Pembrey, M., & Sjostrom, M. (2007). Transgenerational response to nutrition, early life circumstances and longevity. European Journal of Human Genetics, 15, 784–790.Google Scholar
Kember, R. L., Dempster, E. L., Lee, T. H., Schalkwyk, L. C., Mill, J., & Fernandes, C. (2012). Maternal separation is associated with strain-specific responses to stress and epigenetic alterations to Nr3c1, Avp, and Nr4a1 in mouse. Brain and Behavior, 2, 455–467.CrossRefGoogle Scholar
Keverne, B. (2009). Monoallelic gene expression and mammalian evolution. Bioessays, 31, 1318–1326.Google Scholar
Kumar, N., Leverence, J., Bick, D., & Sampath, V. (2012). Ontogeny of growth-regulating genes in the placenta. Placenta, 33, 94–99.CrossRefGoogle ScholarPubMed
Kundakovic, M., Gudsnuk, K., Franks, B., Madrid, J., Miller, R. L., Perera, F. P., et al. (2013). Sex-specific epigenetic disruption and behavioral changes following low-dose in utero bisphenol A exposure. Proceedings of the National Academy of Sciences, 110, 9956–9961.Google Scholar
Kundakovic, M., Gudsnuk, K., Herbstman, J. B., Tang, D., Perera, F. P., & Champagne, F. A. (2015). DNA methylation of BDNF as a biomarker of early-life adversity. Proceedings of the National Academy of Sciences, 112, 6807–6813.CrossRefGoogle ScholarPubMed
Kundakovic, M., Lim, S., Gudsnuk, K., & Champagne, F. A. (2013). Sex-specific and strain-dependent effects of early life adversity on behavioral and epigenetic outcomes. Frontiers in Psychiatry, 4, 78.Google Scholar
Laland, K. N., Uller, T., Feldman, M. W., Sterelny, K., Muller, G. B., Moczek, A., et al. (2015). The extended evolutionary synthesis: Its structure, assumptions and predictions. Proceedings of the Royal Society B: Biological Sciences, 282, 20151019.Google Scholar
Lamarck, J.-B. (1809). Philosophie zoologique. Paris: Museum d'Histoire Naturelle.Google Scholar
Laprise, S. L. (2009). Implications of epigenetics and genomic imprinting in assisted reproductive technologies. Molecular Reproduction and Development, 76, 1006–1018.CrossRefGoogle ScholarPubMed
Liang, M., Zhong, J., Liu, H. X., Lopatina, O., Nakada, R., Yamauchi, A. M., et al. (2014). Pairmate-dependent pup retrieval as parental behavior in male mice. Frontiers in Neuroscience, 8, 186.Google Scholar
Libhaber, N., & Eilam, D. (2002). Social vole parents force their mates to baby-sit. Developmental Psychobiology, 41, 236–240.Google Scholar
Limbourg, T., Mateman, A. C., & Lessells, C. M. (2013). Opposite differential allocation by males and females of the same species. Biology Letters, 9, 20120835.Google Scholar
Liu, H. X., Lopatina, O., Higashida, C., Fujimoto, H., Akther, S., Inzhutova, A., et al. (2013). Displays of paternal mouse pup retrieval following communicative interaction with maternal mates. Nature Communications, 4, 1346.Google Scholar
Mashoodh, R., Franks, B., Curley, J. P., & Champagne, F. A. (2012). Paternal social enrichment effects on maternal behavior and offspring growth. Proceedings of the National Academy of Sciences, 109(Suppl. 2), 17232–17238.Google Scholar
McGhee, K. E., & Bell, A. M. (2014). Paternal care in a fish: Epigenetics and fitness enhancing effects on offspring anxiety. Proceedings of the Royal Society B: Biological Sciences, 281, 20141146.Google Scholar
McGowan, P. O., Suderman, M., Sasaki, A., Huang, T. C., Hallett, M., Meaney, M. J., et al. (2011). Broad epigenetic signature of maternal care in the brain of adult rats. PLOS ONE, 6, e14739.Google Scholar
McMinn, J., Wei, M., Schupf, N., Cusmai, J., Johnson, E. B., Smith, A. C., et al. (2006). Unbalanced placental expression of imprinted genes in human intrauterine growth restriction. Placenta, 27, 540–549.Google Scholar
Meaney, M. J. (2001). Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annual Reviews of Neuroscience, 24, 1161–1192.CrossRefGoogle Scholar
Miller, L., Kramer, R., Warner, V., Wickramaratne, P., & Weissman, M. (1997). Intergenerational transmission of parental bonding among women. Journal of the American Academy of Child & Adolescent Psychiatry, 36, 1134–1139.Google Scholar
Monk, C., Feng, T., Lee, S., Krupska, I., Champagne, F. A., & Tycko, B. (2016). Distress during pregnancy: Epigenetic regulation of placenta glucocorticoid-related genes and fetal neurobehavior. American Journal of Psychiatry. Advance online publication.Google Scholar
Monk, C., Spicer, J., & Champagne, F. A. (2012). Linking prenatal maternal adversity to developmental outcomes in infants: The role of epigenetic pathways. Development and Psychopathology, 24, 1361–1376.Google Scholar
Moore, C. L., & Morelli, G. A. (1979). Mother rats interact differently with male and female offspring. Journal of Comparative and Physiological Psychology, 93, 677–684.Google Scholar
Murgatroyd, C., Patchev, A. V., Wu, Y., Micale, V., Bockmuhl, Y., Fischer, D., et al. (2009). Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nature Neuroscience, 12, 1559–1566.CrossRefGoogle ScholarPubMed
Naguib, M., & Nemitz, A. (2007). Living with the past: Nutritional stress in juvenile males has immediate effects on their plumage ornaments and on adult attractiveness in zebra finches. PLOS ONE, 2, e901.CrossRefGoogle ScholarPubMed
Numan, M. (2007). Motivational systems and the neural circuitry of maternal behavior in the rat. Developmental Psychobiology, 49, 12–21.CrossRefGoogle ScholarPubMed
Ogawa, S., Eng, V., Taylor, J., Lubahn, D. B., Korach, K. S., & Pfaff, D. W. (1998). Roles of estrogen receptor-alpha gene expression in reproduction-related behaviors in female mice. Endocrinology, 139, 5070–5081.Google Scholar
Oquendo, M. A., Ellis, S. P., Chesin, M. S., Birmaher, B., Zelazny, J., Tin, A., et al. (2013). Familial transmission of parental mood disorders: Unipolar and bipolar disorders in offspring. Bipolar Disorders, 15, 764–773.Google Scholar
Pena, C. J., & Champagne, F. A. (2015). Neonatal overexpression of estrogen receptor-alpha alters midbrain dopamine neuron development and reverses the effects of low maternal care in female offspring. Developmental Neurobiology, 75, 1114–1124.Google Scholar
Pena, C. J., Neugut, Y. D., & Champagne, F. A. (2013). Developmental timing of the effects of maternal care on gene expression and epigenetic regulation of hormone receptor levels in female rats. Endocrinology, 154, 4340–4351.Google Scholar
Pusalkar, M., Suri, D., Kelkar, A., Bhattacharya, A., Galande, S., & Vaidya, V. A. (2016). Early stress evokes dysregulation of histone modifiers in the medial prefrontal cortex across the life span. Developmental Psychobiology, 58, 198–210.CrossRefGoogle ScholarPubMed
Razin, A. (1998). CpG methylation, chromatin structure and gene silencing—A three-way connection. EMBO Journal, 17, 4905–4908.Google Scholar
Reik, W., Constancia, M., Fowden, A., Anderson, N., Dean, W., Ferguson-Smith, A., et al. (2003). Regulation of supply and demand for maternal nutrients in mammals by imprinted genes. Journal of Physiology, 547(Pt. 1), 35–44.Google Scholar
Ribeiro, A. C., Musatov, S., Shteyler, A., Simanduyev, S., Arrieta-Cruz, I., Ogawa, S., et al. (2012). siRNA silencing of estrogen receptor expression specifically in medial preoptic area neurons abolishes maternal care in female mice. Proceedings of the National Academy of Sciences, 109, 16324–16329.Google Scholar
Rodgers, A. B., Morgan, C. P., Leu, N. A., & Bale, T. L. (2015). Transgenerational epigenetic programming via sperm microRNA recapitulates effects of paternal stress. Proceedings of the National Academy of Sciences, 112, 13699–13704.Google Scholar
Roth, T. L., Lubin, F. D., Funk, A. J., & Sweatt, J. D. (2009). Lasting epigenetic influence of early-life adversity on the BDNF gene. Biological Psychiatry, 65, 760–769.Google Scholar
Sable, P., Randhir, K., Kale, A., Chavan-Gautam, P., & Joshi, S. (2015). Maternal micronutrients and brain global methylation patterns in the offspring. Nutritional Neuroscience, 18, 30–36.Google Scholar
Sato, F., Tsuchiya, S., Meltzer, S. J., & Shimizu, K. (2011). MicroRNAs and epigenetics. FEBS Journal, 278, 1598–1609.Google Scholar
Schmauss, C., Lee-McDermott, Z., & Medina, L. R. (2014). Trans-generational effects of early life stress: The role of maternal behavior. Scientific Reports, 4, 4873.Google Scholar
Schroeder, D. I., Blair, J. D., Lott, P., Yu, H. O., Hong, D., Crary, F., et al. (2013). The human placenta methylome. Proceedings of the National Academy of Sciences, 110, 6037–6042.Google Scholar
Seo, M. K., Ly, N. N., Lee, C. H., Cho, H. Y., Choi, C. M., Nhu, L. H., et al. (2016). Early life stress increases stress vulnerability through BDNF gene epigenetic changes in the rat hippocampus. Neuropharmacology, 105, 388–397.Google Scholar
Skinner, M. K. (2015). Environmental epigenetics and a unified theory of the molecular aspects of evolution: A neo-Lamarckian concept that facilitates neo-Darwinian evolution. Genome Biology and Evolution, 7, 1296–1302.Google Scholar
Stern, J. M. (1997). Offspring-induced nurturance: Animal–human parallels. Developmental Psychobiology, 31, 19–37.Google Scholar
Stolzenberg, D. S., & Numan, M. (2011). Hypothalamic interaction with the mesolimbic DA system in the control of the maternal and sexual behaviors in rats. Neuroscience & Biobehavioral Reviews, 35, 826–847.Google Scholar
Susiarjo, M., Sasson, I., Mesaros, C., & Bartolomei, M. S. (2013). Bisphenol a exposure disrupts genomic imprinting in the mouse. PLOS Genetics, 9, e1003401.Google Scholar
Suter, M. A., Ma, J., Vuguin, P. M., Hartil, K., Fiallo, A., Harris, R. A., et al. (2014). In utero exposure to a maternal high-fat diet alters the epigenetic histone code in a murine model. American Journal of Obstetrics and Gynecology, 210, e1–e11.Google Scholar
Svare, B., Kinsley, C. H., Mann, M. A., & Broida, J. (1984). Infanticide: Accounting for genetic variation in mice. Physiology & Behavior, 33, 137–152.Google Scholar
Vassoler, F. M., White, S. L., Schmidt, H. D., Sadri-Vakili, G., & Pierce, R. C. (2013). Epigenetic inheritance of a cocaine-resistance phenotype. Nature Neuroscience, 16, 42–47.CrossRefGoogle ScholarPubMed
Waddington, C. H. (1942). The epigenotype. Endeavour, 1, 18–20.Google Scholar
Watson, J. B., Mednick, S. A., Huttunen, M., & Wang, X. (1999). Prenatal teratogens and the development of adult mental illness. Development and Psychopathology, 11, 457–466.Google Scholar
Weaver, I. C., Cervoni, N., Champagne, F. A., D'Alessio, A. C., Sharma, S., Seckl, J. R., et al. (2004). Epigenetic programming by maternal behavior. Nature Neuroscience, 7, 847–854.Google Scholar
Weaver, I. C., Meaney, M. J., & Szyf, M. (2006). Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood. Proceedings of the National Academy of Sciences, 103, 3480–3485.Google Scholar
Welshons, W. V., Nagel, S. C., & vom Saal, F. S. (2006). Large effects from small exposures: III. Endocrine mechanisms mediating effects of bisphenol A at levels of human exposure. Endocrinology, 147(Suppl. 6), S56–S69.Google Scholar
West-Eberhard, M. J. (2014). Darwin's forgotten idea: The social essence of sexual selection. Neuroscience & Biobehavioral Reviews, 46(Pt. 4), 501–508.Google Scholar
Wilkinson, L. S., Davies, W., & Isles, A. R. (2007). Genomic imprinting effects on brain development and function. Nature Reviews Neuroscience, 8, 832–843.Google Scholar
Woodroffe, R., & Vincent, A. (1994). Mother's little helpers: Patterns of male care in mammals. Trends in Ecology and Evolution, 9, 294–297.Google Scholar
Yehuda, R., Daskalakis, N. P., Bierer, L. M., Bader, H. N., Klengel, T., Holsboer, F., et al. (2015). Holocaust exposure induced intergenerational effects on FKBP5 methylation. Biological Psychiatry.Google Scholar
Zamudio, N. M., Chong, S., & O'Bryan, M. K. (2008). Epigenetic regulation in male germ cells. Reproduction, 136, 131–146.Google Scholar
Zhang, T. Y., Hellstrom, I. C., Bagot, R. C., Wen, X., Diorio, J., & Meaney, M. J. (2010). Maternal care and DNA methylation of a glutamic acid decarboxylase 1 promoter in rat hippocampus. Journal of Neuroscience, 30, 13130–13137.Google Scholar