Generational stability of epigenetic transgenerational inheritance facilitates adaptation and evolution

References

• Ayala FJ. Darwin’s explanation of design: from natural theology to natural selection. Infect, Genet Evol. 2010;10(6):839–16. doi: 10.1016/j.meegid.2009.09.014
   Web of Science ®Google Scholar
• Darwin C. On the origin of species. London: John Murray; 1859. p. 488.
   Google Scholar
• Mendel G. Versuche über pflanzen-hybriden. Verh des Naturforsch Ver in Brünn 4. 1866;3–47.
   Google Scholar
• Gayon J. From Mendel to epigenetics: history of genetics. C R Biol. 2016;339(7–8):225–230. doi: 10.1016/j.crvi.2016.05.009
   PubMed Web of Science ®Google Scholar
• Huxley J. Evolution: the modern synthesis. London: George Allen & Unwin Ltd; 1942. p. 645.
   Google Scholar
• Noble D. The illusions of the modern synthesis. Biosemiotics. 2021;14(1):5–24. doi: 10.1007/s12304-021-09405-3
   Web of Science ®Google Scholar
• Baldwin J. A new factor in evolution. Am Nat. 1896;30(354):441–451. doi: 10.1086/276408
   Google Scholar
• Crispo E. The Baldwin effect and genetic assimilation: revisiting two mechanisms of evolutionary change mediated by phenotypic plasticity. Evolution. 2007;61(11):2469–2479. doi: 10.1111/j.1558-5646.2007.00203.x
   PubMed Web of Science ®Google Scholar
• Vargas AO, Krabichler Q, Guerrero-Bosagna C. An epigenetic perspective on the midwife toad experiments of Paul Kammerer (1880–1926). J Exp Zool B Mol Dev Evol. 2017;328(1–2):179–192. doi: 10.1002/jez.b.22708
   PubMed Web of Science ®Google Scholar
• Waddington CH. Organisers and genes. Cambridge: Cambridge Univ. Press; 1940.
   Google Scholar
• Mousseau TA, Fox CW., Mousseau, Fox, editors. Maternal effects as adaptations. Oxford University Press; 1998. p. 400.
   Google Scholar
• Coe EH. A regular and continuing conversion-type phenomenon at the B locus in maize. In: Proceedings of the National Academy of Sciences of the United States of America; 1959;45( 6):828–832.
   Google Scholar
• Chandler V, Alleman M. Paramutation: epigenetic instructions passed across generations. Genetics. 2008;178(4):1839–1844. doi: 10.1093/genetics/178.4.1839
   PubMed Web of Science ®Google Scholar
• Stam M, Belele C, Ramakrishna W, et al. The regulatory regions required for B’ paramutation and expression are located far upstream of the maize b1 transcribed sequences. Genetics. 2002;162(2):917–930. doi: 10.1093/genetics/162.2.917
   PubMed Web of Science ®Google Scholar
• Laland KN, Uller T, Feldman MW, et al. The extended evolutionary synthesis: its structure, assumptions and predictions. In: Proceedings Biological sciences/The Royal Society; 2015;282( 1813):20151019.
   Google Scholar
• Skinner MK. Environmental epigenetics and a unified theory of the molecular aspects of evolution: a neo-lamarckian concept that facilitates neo-darwinian evolution. Genome Biol Evol. 2015;7(5):1296–1302. doi: 10.1093/gbe/evv073
   PubMed Web of Science ®Google Scholar
• Skinner MK. Environmental epigenetic transgenerational inheritance and somatic epigenetic mitotic stability. Epigenet: Off J DNA Methylation Soc. 2011;6(7):838–842.
   PubMed Web of Science ®Google Scholar
• Bartova E, Krejci J, Harnicarova A, et al. Histone modifications and nuclear architecture: a review. J Histochem Cytochem. 2008;56(8):711–721. doi: 10.1369/jhc.2008.951251
   PubMed Web of Science ®Google Scholar
• Yaniv M. Chromatin remodeling: from transcription to cancer. Cancer Genet. 2014;207(9):352–357. doi: 10.1016/j.cancergen.2014.03.006
   PubMed Web of Science ®Google Scholar
• Kornfeld JW, Bruning JC. Regulation of metabolism by long, non-coding RNAs. Front Genet. 2014;5:57. doi: 10.3389/fgene.2014.00057
   PubMed Web of Science ®Google Scholar
• Handy DE, Castro R, Loscalzo J. Epigenetic modifications: basic mechanisms and role in cardiovascular disease. Circulation. 2011;123(19):2145–2156. doi: 10.1161/CIRCULATIONAHA.110.956839
   PubMed Web of Science ®Google Scholar
• Singer J, Stellwagen RH, Roberts-Ems J, et al. 5-methylcytosine content of rat hepatoma DNA substituted with bromodeoxyuridine. J Biol Chem. 1977;252(15):5509–5513. doi: 10.1016/S0021-9258(19)63380-6
   PubMed Web of Science ®Google Scholar
• Bird A, Taggart M, Frommer M, et al. A fraction of the mouse genome that is derived from islands of nonmethylated, CpG-rich DNA. Cell. 1985;40(1):91–99. doi: 10.1016/0092-8674(85)90312-5
   PubMed Web of Science ®Google Scholar
• Moore LD, Le T, Fan G. DNA methylation and its basic function. Neuropsychopharmacology. 2013;38(1):23–38. doi: 10.1038/npp.2012.112
   PubMed Web of Science ®Google Scholar
• Nilsson EE, Ben Maamar M, Skinner MK. Role of epigenetic transgenerational inheritance in generational toxicology. Environ Epigenet. 2022;8(1):dvac001, 1–9. doi: 10.1093/eep/dvac001
   Web of Science ®Google Scholar
• Skinner MK, Nilsson EE. Role of environmentally induced epigenetic transgenerational inheritance in evolutionary biology: unified evolution theory. Environ Epigenet. 2021;7(1): dvab012, 1–12. doi: 10.1093/eep/dvab012
   Web of Science ®Google Scholar
• Ben Maamar M, Wang Y, Nilsson EE, et al. Transgenerational sperm DMRs escape DNA methylation erasure during embryonic development and epigenetic inheritance. Environ Epigenet. 2023;9(1):dvad003, 1–15. doi: 10.1093/eep/dvad003
   Web of Science ®Google Scholar
• Boulias K, Greer EL. Biological roles of adenine methylation in RNA. Nat Rev Genet. 2023;24(3):143–160. doi: 10.1038/s41576-022-00534-0
   PubMed Web of Science ®Google Scholar
• Haussmann IU, Bodi Z, Sanchez-Moran E, et al. m6A potentiates sxl alternative pre-mRNA splicing for robust drosophila sex determination. Nature. 2016;540(7632):301–304. doi: 10.1038/nature20577
   PubMed Web of Science ®Google Scholar
• Turner BM. Histone acetylation as an epigenetic determinant of long-term transcriptional competence. Cell Mol Life Sci. 1998;54(1):21–31. doi: 10.1007/s000180050122
   PubMed Web of Science ®Google Scholar
• Rothbart SB, Strahl BD. Interpreting the language of histone and DNA modifications. Biochim Biophys Acta. 2014;1839(8):627–643. doi: 10.1016/j.bbagrm.2014.03.001
   PubMed Web of Science ®Google Scholar
• Taylor BC, Young NL. Combinations of histone post-translational modifications. Biochem J. 2021;478(3):511–532. doi: 10.1042/BCJ20200170
   PubMed Web of Science ®Google Scholar
• Zaib S, Rana N, Khan I. Histone modifications and their role in Epigenetics of cancer. Curr Med Chem. 2022;29(14):2399–2411. doi: 10.2174/0929867328666211108105214
   PubMed Web of Science ®Google Scholar
• Grewal SIS. The molecular basis of heterochromatin assembly and epigenetic inheritance. Mol Cell. 2023;83(11):1767–1785. doi: 10.1016/j.molcel.2023.04.020
   PubMed Web of Science ®Google Scholar
• Larriba E, Del Mazo J. Role of non-coding RNAs in the transgenerational epigenetic transmission of the effects of reprotoxicants. Int J Mol Sci. 2016;17(4):452. doi: 10.3390/ijms17040452
   PubMed Web of Science ®Google Scholar
• Cayir A. Environmental exposures and RNA N6-methyladenosine modified long non-coding RNAs. Crit Rev Toxicol. 2020;50(8):641–649. doi: 10.1080/10408444.2020.1812511
   PubMed Web of Science ®Google Scholar
• Yue Y, Liu J, He C. RNA N6-methyladenosine methylation in post-transcriptional gene expression regulation. Genes Dev. 2015;29(13):1343–1355. doi: 10.1101/gad.262766.115
   PubMed Web of Science ®Google Scholar
• Fu Y, Dominissini D, Rechavi G, et al. Gene expression regulation mediated through reversible m6A RNA methylation. Nat Rev Genet. 2014;15(5):293–306. doi: 10.1038/nrg3724
   PubMed Web of Science ®Google Scholar
• Kusmartsev V, Drozdz M, Schuster-Bockler B, et al. Cytosine methylation affects the mutability of neighboring nucleotides in germline and Soma. Genetics. 2020;214(4):809–823. doi: 10.1534/genetics.120.303028
   PubMed Web of Science ®Google Scholar
• Ben Maamar M, Nilsson E, Sadler-Riggleman I, et al. Developmental origins of transgenerational sperm DNA methylation epimutations following ancestral DDT exposure. Dev. Biol. 2019;445(2):280–293. doi: 10.1016/j.ydbio.2018.11.016
   PubMed Web of Science ®Google Scholar
• Skinner MK, Guerrero-Bosagna C, Haque MM. Environmentally induced epigenetic transgenerational inheritance of sperm epimutations promote genetic mutations. Epigenet: Off J DNA Methylation Soc. 2015;10(8):762–771. doi: 10.1080/15592294.2015.1062207
   PubMed Web of Science ®Google Scholar
• Feng W, Li Y, Kratsios P. Emerging roles for hox proteins in the last steps of neuronal development in worms, flies, and mice. Front Neurosci. 2021;15:801791. doi: 10.3389/fnins.2021.801791
   PubMed Web of Science ®Google Scholar
• Vergeer P, Wagemaker NC, Ouborg NJ. Evidence for an epigenetic role in inbreeding depression. Biol Lett. 2012;8(5):798–801. doi: 10.1098/rsbl.2012.0494
   PubMed Web of Science ®Google Scholar
• Pennisi E. European society for evolutionary biology meeting. Epigenetics linked to inbreeding depression. Science. 2011;333(6049):1563. doi: 10.1126/science.333.6049.1563
   PubMed Web of Science ®Google Scholar
• Han T, Wang F, Song Q, et al. An epigenetic basis of inbreeding depression in maize. Sci Adv. 2021;7(35):eabg5442. doi: 10.1126/sciadv.abg5442
   PubMed Web of Science ®Google Scholar
• Dapp M, Reinders J, Bediee A, et al. Heterosis and inbreeding depression of epigenetic Arabidopsis hybrids. Nat Plants. 2015;1(7):15092. doi: 10.1038/nplants.2015.92
   PubMed Web of Science ®Google Scholar
• Venney CJ, Johansson ML, Heath DD. Inbreeding effects on gene-specific DNA methylation among tissues of chinook salmon. Mol Ecol. 2016;25(18):4521–4533. doi: 10.1111/mec.13777
   PubMed Web of Science ®Google Scholar
• Cheptou PO, Donohue K. Epigenetics as a new avenue for the role of inbreeding depression in evolutionary ecology. Heredity (Edinb). 2013;110(3):205–206. doi: 10.1038/hdy.2012.66
   PubMed Web of Science ®Google Scholar
• Deepashree S, Shivanandappa T, Ramesh SR. Is longevity a heritable trait? Evidence for non-genomic influence from an extended longevity phenotype of drosophila melanogaster. Curr Aging Sci. 2018;11(1):24–32. doi: 10.2174/1874609810666170615120942
   PubMedGoogle Scholar
• Legoff L, D’Cruz SC, Lebosq M, et al. Developmental exposure to chlordecone induces transgenerational effects in somatic prostate tissue which are associated with epigenetic histone trimethylation changes. Environ Int. 2021;152:106472. doi: 10.1016/j.envint.2021.106472
   PubMed Web of Science ®Google Scholar
• Wilhelm D, Palmer S, Koopman P. Sex determination and gonadal development in mammals. Physiol Rev. 2007;87(1):1–28. doi: 10.1152/physrev.00009.2006
   PubMed Web of Science ®Google Scholar
• Nilsson E, Sadler-Riggleman I, Skinner MK, et al. Environmentally induced epigenetic transgenerational inheritance of disease. Environ Epigenet. 2018;4(2):1–13, dvy016. doi: 10.1093/eep/dvy016
   Web of Science ®Google Scholar
• Nilsson E, King SE, McBirney M, et al. Vinclozolin induced epigenetic transgenerational inheritance of pathologies and sperm epimutation biomarkers for specific diseases. PLOS ONE. 2018;13(8):1–29, e0202662. doi: 10.1371/journal.pone.0202662
   Web of Science ®Google Scholar
• Ben Maamar M, King SE, Nilsson E, et al. Epigenetic transgenerational inheritance of parent-of-origin allelic transmission of outcross pathology and sperm epimutations. Dev Biol. 2020;458(1):106–119. doi: 10.1016/j.ydbio.2019.10.030
   PubMed Web of Science ®Google Scholar
• Skinner MK, Guerrero-Bosagna C, Haque MM, et al. Epigenetics and the evolution of darwin’s finches genome biology & evolution. Genome Biol Evol. 2014;6(8):1972–1989. doi: 10.1093/gbe/evu158
   PubMed Web of Science ®Google Scholar
• McNew SM, Beck D, Sadler-Riggleman I, et al. Epigenetic variation between urban and rural populations of darwin’s finches. BMC Evol Biol. 2017;17(1):183. doi: 10.1186/s12862-017-1025-9
   PubMedGoogle Scholar
• Ashe A, Sapetschnig A, Weick EM, et al. piRNAs can trigger a multigenerational epigenetic memory in the germline of C. elegans. Cell. 2012;150(1):88–99. doi: 10.1016/j.cell.2012.06.018
   PubMed Web of Science ®Google Scholar
• Waddington CH. Canalisation of development and the inheritance of acquired characters. Nature. 1942;150(3811):563–565. doi: 10.1038/150563a0
   Google Scholar
• Kubsad D, Nilsson EE, King SE, et al. Assessment of glyphosate induced epigenetic transgenerational inheritance of pathologies and sperm epimutations: generational toxicology. Sci Rep. 2019;9(1):6372. doi: 10.1038/s41598-019-42860-0
   PubMedGoogle Scholar
• Nilsson EE, McBirney M, De Santos S, et al. Multiple generation distinct toxicant exposures induce epigenetic-transgenerational-inheritance of enhanced pathology and obesity. Environ Epigenet. 2023;9(1):dvad006, 1–19. doi: 10.1093/eep/dvad006
   Web of Science ®Google Scholar
• King SE, Nilsson E, Beck D, et al. Adipocyte epigenetic alterations and potential therapeutic targets in transgenerationally inherited lean and obese phenotypes following ancestral exposures. Adipocyte. 2019;8(1):362–378. doi: 10.1080/21623945.2019.1693747
   PubMed Web of Science ®Google Scholar
• Kabasenche WP, Skinner MK. DDT, epigenetic harm, and transgenerational environmental justice. Environmental health: a global access science source. Environ Health. 2014;13(1):62. doi: 10.1186/1476-069X-13-62
   PubMedGoogle Scholar
• Beck D, Sadler-Riggleman I, Skinner MK. Generational comparisons (F1 versus F3) of vinclozolin induced epigenetic transgenerational inheritance of sperm differential DNA methylation regions (epimutations) using MeDIP-seq. Environ Epigenet. 2017;3(3):1–12, dvx016. doi: 10.1093/eep/dvx016
   Web of Science ®Google Scholar
• Bonilla MM, Zeh JA, Zeh DW. An epigenetic resolution of the lek paradox. BioEssays: news and reviews in molecular, cellular and developmental biology. Bioessays. 2016;38(4):355–366. doi: 10.1002/bies.201500176
   PubMed Web of Science ®Google Scholar
• Hauser MT, Aufsatz W, Jonak C, et al. Transgenerational epigenetic inheritance in plants. Biochim Biophys Acta. 2011;1809(8):459–468. doi: 10.1016/j.bbagrm.2011.03.007
   PubMed Web of Science ®Google Scholar
• Gallusci P, Dai Z, Genard M, et al. Epigenetics for plant improvement: Current knowledge and modeling avenues. Trends Plant Sci. 2017;22(7):610–623. doi: 10.1016/j.tplants.2017.04.009
   PubMed Web of Science ®Google Scholar
• Diez CM, Roessler K, Gaut BS. Epigenetics and plant genome evolution. Curr Opin Plant Biol. 2014;18:1–8. doi: 10.1016/j.pbi.2013.11.017
   PubMed Web of Science ®Google Scholar
• Zhang YY, Fischer M, Colot V, et al. Epigenetic variation creates potential for evolution of plant phenotypic plasticity. New Phytol. 2013;197(1):314–322. doi: 10.1111/nph.12010
   PubMed Web of Science ®Google Scholar
• Cubas P, Vincent C, Coen E. An epigenetic mutation responsible for natural variation in floral symmetry. Nature. 1999;401(6749):157–161. doi: 10.1038/43657
   PubMed Web of Science ®Google Scholar
• Luo D, Carpenter R, Vincent C, et al. Origin of floral asymmetry in Antirrhinum. Nature. 1996;383(6603):794–799. doi: 10.1038/383794a0
   PubMed Web of Science ®Google Scholar
• Wang X, Cong R, Li A, et al. Transgenerational effects of intertidal environment on physiological phenotypes and DNA methylation in Pacific oysters. Sci Total Environ. 2023;871:162112. doi: 10.1016/j.scitotenv.2023.162112
   PubMed Web of Science ®Google Scholar
• Thorson JLM, Smithson M, Beck D, et al. Epigenetics and adaptive phenotypic variation between habitats in an asexual snail. Sci Rep. 2017;7(1):14139. doi: 10.1038/s41598-017-14673-6
   PubMedGoogle Scholar
• Thorson JLM, Smithson M, Sadler-Riggleman I, et al. Regional epigenetic variation in asexual snail populations among urban and rural lakes. Environ Epigenet. 2019;5(4):dvz020. doi: 10.1093/eep/dvz020
   PubMed Web of Science ®Google Scholar
• Kelley JL, Tobler M, Beck D, et al. Epigenetic inheritance of DNA methylation changes in fish living in hydrogen sulfide-rich springs. In: Proceedings of the National Academy of Sciences of the United States of America; 2021;118( 26):e2014929118.
   Google Scholar
• Nilsson E, Sadler-Riggleman I, Beck D, et al. Differential DNA methylation in somatic and sperm cells of hatchery versus wild (natural-origin) steelhead trout populations environmental epigenetics. Environ Epigenet. 2021;7(1):1–17, dvab002. doi: 10.1093/eep/dvab002
   Web of Science ®Google Scholar
• Moran P, Perez-Figueroa A. Methylation changes associated with early maturation stages in the Atlantic salmon. BMC Genet. 2011;12(1):86. doi: 10.1186/1471-2156-12-86
   PubMedGoogle Scholar
• Jensen N, Allen RM, Marshall DJ, et al. Adaptive maternal and paternal effects: gamete plasticity in response to parental stress. Funct Ecol. 2013;28:724–733. doi: 10.1111/1365-2435.12195
   Web of Science ®Google Scholar
• Vogt G. Facilitation of environmental adaptation and evolution by epigenetic phenotype variation: insights from clonal, invasive, polyploid, and domesticated animals. Environ Epigenet. 2017;3(1):dvx002. doi: 10.1093/eep/dvx002
   PubMedGoogle Scholar
• Carneiro VC, Lyko F. Rapid epigenetic adaptation in animals and its role in invasiveness. Integr Comp Biol. 2020;60(2):267–274. doi: 10.1093/icb/icaa023
   PubMed Web of Science ®Google Scholar
• Anway MD, Memon MA, Uzumcu M, et al. Transgenerational effect of the endocrine disruptor vinclozolin on male spermatogenesis. J Androl. 2006;27(6):868–879. doi: 10.2164/jandrol.106.000349
   PubMedGoogle Scholar
• Ng SF, Lin RC, Laybutt DR, et al. Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring. Nature. 2010;467(7318):963–966. doi: 10.1038/nature09491
   PubMed Web of Science ®Google Scholar
• Morgan HD, Sutherland HG, Martin DI, et al. Epigenetic inheritance at the agouti locus in the mouse. Nat Genet. 1999;23(3):314–318. doi: 10.1038/15490
   PubMed Web of Science ®Google Scholar
• Roseboom T, de Rooij S, Painter R. The Dutch famine and its long-term consequences for adult health. Early Hum Dev. 2006;82(8):485–491. doi: 10.1016/j.earlhumdev.2006.07.001
   PubMed Web of Science ®Google Scholar
• York G, Mick H. Last ghost of the Vietnam war. The Globe And Mail. 2008. July 12:2008.
   Google Scholar
• Hauser R, Singh NP, Chen Z, et al. Lack of an association between environmental exposure to polychlorinated biphenyls and p,p’-DDE and DNA damage in human sperm measured using the neutral comet assay. Hum Reproduction. 2003;18(12):2525–2533. doi: 10.1093/humrep/deg508
   PubMed Web of Science ®Google Scholar
• ATSDR. Agency for toxic substances and diseases registry (ATSDR)/US public health service, toxicological profile for 4, 4’-DDT, 4,4’-DDE, 44’-DDD (update). Atlanta (GA): ATSDR. 1994.
   Google Scholar
• Longnecker MP, Klebanoff MA, Zhou H, et al. Association between maternal serum concentration of the DDT metabolite DDE and preterm and small-for-gestational-age babies at birth. The Lancet. 2001;358(9276):110–114. doi: 10.1016/S0140-6736(01)05329-6
   PubMed Web of Science ®Google Scholar
• Jaga K, Brosius D. Pesticide exposure: human cancers on the horizon. Rev Environ Health. 1999;14(1):39–50. doi: 10.1515/REVEH.1999.14.1.39
   PubMedGoogle Scholar
• Mimouni NEH, Paiva I, Barbotin AL, et al. Polycystic ovary syndrome is transmitted via a transgenerational epigenetic process. Cell Metab. 2021;33(3):513–30 e8. doi: 10.1016/j.cmet.2021.01.004
   PubMed Web of Science ®Google Scholar
• Kahn LG, Philippat C, Nakayama SF, et al. Endocrine-disrupting chemicals: implications for human health. Lancet Diabetes Endocrinol. 2020;8(8):703–718. doi: 10.1016/S2213-8587(20)30129-7
   PubMed Web of Science ®Google Scholar
• Jablonka E, Raz G. Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. The Q Rev Biol. 2009;84(2):131–176. doi: 10.1086/598822
   PubMed Web of Science ®Google Scholar
• Lachmann M, Jablonka E. The inheritance of phenotypes: an adaptation to fluctuating environments. J Theor Biol. 1996;181(1):1–9. doi: 10.1006/jtbi.1996.0109
   PubMed Web of Science ®Google Scholar
• Kokko H, Heubel K. Condition-dependence, genotype-by-environment interactions and the lek paradox. Genetica. 2008;134(1):55–62. doi: 10.1007/s10709-008-9249-7
   PubMed Web of Science ®Google Scholar
• Anway MD, Cupp AS, Uzumcu M, et al. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science. 2005;308(5727):1466–1469. doi: 10.1126/science.1108190
   PubMed Web of Science ®Google Scholar
• Anway MD, Leathers C, Skinner MK. Endocrine disruptor vinclozolin induced epigenetic transgenerational adult-onset disease. Endocrinology. 2006;147(12):5515–5523. doi: 10.1210/en.2006-0640
   PubMed Web of Science ®Google Scholar
• Manikkam M, Haque MM, Guerrero-Bosagna C, et al. Pesticide methoxychlor promotes the epigenetic transgenerational inheritance of adult onset disease through the female germline. PLOS ONE. 2014;9(7):1–19, e102091. doi: 10.1371/journal.pone.0102091
   Web of Science ®Google Scholar
• Gaspari L, Paris F, Kalfa N, et al. Experimental evidence of 2,3,7,8-tetrachlordibenzo-p-dioxin (TCDD) transgenerational effects on reproductive health. Int J Mol Sci. 2021;22(16):9091. doi: 10.3390/ijms22169091
   PubMed Web of Science ®Google Scholar
• Baker TR, King-Heiden TC, Peterson RE, et al. Dioxin induction of transgenerational inheritance of disease in zebrafish. Mol Cell Endocrinol. 2014;398(1–2):36–41. doi: 10.1016/j.mce.2014.08.011
   PubMed Web of Science ®Google Scholar
• Bruner-Tran KL, Osteen KG. Developmental exposure to TCDD reduces fertility and negatively affects pregnancy outcomes across multiple generations. Reprod Toxicol. 2011;31(3):344–350. doi: 10.1016/j.reprotox.2010.10.003
   PubMed Web of Science ®Google Scholar
• Manikkam M, Tracey R, Guerrero-Bosagna C, et al. Dioxin (TCDD) induces epigenetic transgenerational inheritance of adult onset disease and sperm epimutations. PLOS ONE. 2012;7(9):1–15, e46249. doi: 10.1371/journal.pone.0046249
   Web of Science ®Google Scholar
• Manikkam M, Guerrero-Bosagna C, Tracey R, et al. Transgenerational actions of environmental compounds on reproductive disease and identification of epigenetic biomarkers of ancestral exposures. PLOS ONE. 2012;7(2):1–12, e31901. doi: 10.1371/journal.pone.0031901
   Web of Science ®Google Scholar
• Manikkam M, Tracey R, Guerrero-Bosagna C, et al. Plastics derived endocrine disruptors (BPA, DEHP and DBP) induce epigenetic transgenerational inheritance of obesity, reproductive disease and sperm epimutations. PLOS ONE. 2013;8(1):1–18, e55387. doi: 10.1371/journal.pone.0055387
   Web of Science ®Google Scholar
• Ziv-Gal A, Wang W, Zhou C, et al. The effects of in utero bisphenol a exposure on reproductive capacity in several generations of mice. Toxicol Appl Pharmacol. 2015;284(3):354–362. doi: 10.1016/j.taap.2015.03.003
   PubMed Web of Science ®Google Scholar
• Tracey R, Manikkam M, Guerrero-Bosagna C, et al. Hydrocarbons (jet fuel JP-8) induce epigenetic transgenerational inheritance of obesity, reproductive disease and sperm epimutations. Reprod Toxicol. 2013;36:104–116. doi: 10.1016/j.reprotox.2012.11.011
   PubMed Web of Science ®Google Scholar
• Gregory DJ, Kobzik L, Yang Z, et al. Transgenerational transmission of asthma risk after exposure to environmental particles during pregnancy. American Journal Of Physiology-Lung Cellular And Molecular Physiology. 2017;313(2):L395–L405. doi: 10.1152/ajplung.00035.2017
   PubMed Web of Science ®Google Scholar
• Manikkam M, Tracey R, Guerrero-Bosagna C, et al. Pesticide and insect repellent mixture (permethrin and DEET) induces epigenetic transgenerational inheritance of disease and sperm epimutations. Reprod Toxicol. 2012;34(4):708–719. doi: 10.1016/j.reprotox.2012.08.010
   PubMed Web of Science ®Google Scholar
• Blanc M, Antczak P, Cousin X, et al. The insecticide permethrin induces transgenerational behavioral changes linked to transcriptomic and epigenetic alterations in zebrafish (danio rerio). Sci Total Environ. 2021;779:146404. doi: 10.1016/j.scitotenv.2021.146404
   PubMed Web of Science ®Google Scholar
• King SE, McBirney M, Beck D, et al. Sperm epimutation biomarkers of obesity and pathologies following DDT induced epigenetic transgenerational inheritance of disease. Environ Epigenet. 2019;5(2):1–15, dvz008. doi: 10.1093/eep/dvz008
   Web of Science ®Google Scholar
• Maggio AG, Shu HT, Laufer BI, et al. Elevated exposures to persistent endocrine disrupting compounds impact the sperm methylome in regions associated with autism spectrum disorder. Front Genet. 2022;13:929471. doi: 10.3389/fgene.2022.929471
   PubMed Web of Science ®Google Scholar
• Skinner MK, Manikkam M, Tracey R, et al. Ancestral dichlorodiphenyltrichloroethane (DDT) exposure promotes epigenetic transgenerational inheritance of obesity. BMC Med. 2013;11(228):1–16. doi: 10.1186/1741-7015-11-228
   PubMedGoogle Scholar
• Salian S, Doshi T, Vanage G. Impairment in protein expression profile of testicular steroid receptor coregulators in male rat offspring perinatally exposed to bisphenol a. Life Sci. 2009;85(1–2):11–18. doi: 10.1016/j.lfs.2009.04.005
   PubMed Web of Science ®Google Scholar
• Wolstenholme JT, Edwards M, Shetty SR, et al. Gestational exposure to bisphenol a produces transgenerational changes in behaviors and gene expression. Endocrinology. 2012;153(8):3828–3838. doi: 10.1210/en.2012-1195
   PubMed Web of Science ®Google Scholar
• Doyle TJ, Bowman JL, Windell VL, et al. Transgenerational effects of Di-(2-ethylhexyl) phthalate on testicular germ cell associations and spermatogonial stem cells in mice. Biol Reprod. 2013;88(5):112. doi: 10.1095/biolreprod.112.106104
   PubMed Web of Science ®Google Scholar
• Chamorro-Garcia R, Sahu M, Abbey RJ, et al. Transgenerational inheritance of increased fat depot size, stem cell reprogramming, and hepatic steatosis elicited by prenatal exposure to the obesogen tributyltin in mice. Environ Health Perspect. 2013;121(3):359–366. doi: 10.1289/ehp.1205701
   PubMed Web of Science ®Google Scholar
• Ben Maamar M, Beck D, Nilsson EE, et al. Epigenome-wide association study for glyphosate induced transgenerational sperm DNA methylation and histone retention epigenetic biomarkers for disease. Epigenet: Off J DNA Methylation Soc. 2021;16(10):1150–1167. doi: 10.1080/15592294.2020.1853319
   PubMed Web of Science ®Google Scholar
• Golding J, Northstone K, Gregory S, et al. The anthropometry of children and adolescents may be influenced by the prenatal smoking habits of their grandmothers: a longitudinal cohort study. Am J Hum Biol. 2014;26(6):731–739. doi: 10.1002/ajhb.22594
   PubMed Web of Science ®Google Scholar
• Rehan VK, Liu J, Sakurai R, et al. Perinatal nicotine-induced transgenerational asthma. Am J Physiol Lung Cell Mol Physiol. 2013;305(7):L501–7. doi: 10.1152/ajplung.00078.2013
   PubMed Web of Science ®Google Scholar
• Zhu J, Lee KP, Spencer TJ, et al. Transgenerational transmission of hyperactivity in a mouse model of ADHD. J Neurosci. 2014;34(8):2768–2773. doi: 10.1523/JNEUROSCI.4402-13.2014
   PubMed Web of Science ®Google Scholar
• McCarthy DM, Morgan TJ Jr., Lowe SE, et al. Nicotine exposure of male mice produces behavioral impairment in multiple generations of descendants. PLOS Biol. 2018;16(10):e2006497. doi: 10.1371/journal.pbio.2006497
   PubMed Web of Science ®Google Scholar
• Govorko D, Bekdash RA, Zhang C, et al. Male germline transmits fetal alcohol adverse effect on hypothalamic proopiomelanocortin gene across generations. Biol Psychiatry. 2012;72(5):378–388. doi: 10.1016/j.biopsych.2012.04.006
   PubMed Web of Science ®Google Scholar
• Gangisetty O, Chaudhary S, Palagani A, et al. Transgenerational inheritance of fetal alcohol effects on proopiomelanocortin gene expression and methylation, cortisol response to stress, and anxiety-like behaviors in offspring for three generations in rats: evidence for male germline transmission. PLOS ONE. 2022;17(2):e0263340. doi: 10.1371/journal.pone.0263340
   PubMed Web of Science ®Google Scholar