Skip to main content
SpringerLink
Log in

Transgenerational Impact of Environmental Change

  • Chapter
  • First Online:
Reproductive Sciences in Animal Conservation

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1200))

Abstract

The ability to adapt to changing environmental conditions is critical for any species to survive. Many environmental changes occur too rapidly for an organism’s genome to adapt in time. Accordingly, being able to modify either its own phenotype, or the phenotype of its offspring to better suit future anticipated environmental conditions could afford an organism a significant advantage. However, a range of animal models and human epidemiological data sets are now showing that environmental factors such as changes in the quality or quantity of an individual’s diet, temperature, stress or exposure to pollutants can all adversely affect the quality of parental gametes, the development of the preimplantation embryo and the health and wellbeing of offspring over multiple generations. This chapter will examine transgenerational effects of both maternal and paternal environmental factors on offspring development and wellbeing in both human and animal model studies. Changes in the epigenetic status of either parental or grand-parental gametes provide one candidate mechanism through which the impacts of environmental experience can be passed from one generation to another. This chapter will therefore also focus on the impact of parental and grand-parental diet on epigenetic transgenerational inheritance and offspring phenotype.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
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

  • Aiken CE, Ozanne SE. Transgenerational developmental programming. Hum Reprod Update. 2014;20(1):63–75.

    Article  PubMed  Google Scholar 

  • Aiken CE, Tarry-Adkins JL, Ozanne SE. Transgenerational effects of maternal diet on metabolic and reproductive ageing. Mamm Genome. 2016;27(7–8):430–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alwasel SH, Harrath A, Aljarallah JS, Abotalib Z, Osmond C, Al Omar SY, et al. Intergenerational effects of in utero exposure to Ramadan in Tunisia. Am J Hum Biol. 2013;25(3):341–3.

    Article  CAS  PubMed  Google Scholar 

  • Ashworth CJ, Toma LM, Hunter MG. Nutritional effects on oocyte and embryo development in mammals: implications for reproductive efficiency and environmental sustainability. Philos Trans R Soc Lond B Biol Sci. 2009;364(1534):3351–61.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bannister AJ, Kouzarides T. Regulation of chromatin by histone modifications. Cell Res. 2011;21(3):381–95.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barker DJ, Osmond C. Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet. 1986;1(8489):1077–81.

    Article  CAS  PubMed  Google Scholar 

  • Barker DJ, Osmond C, Golding J, Kuh D, Wadsworth ME. Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. BMJ. 1989;298(6673):564–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Battisti DS, Naylor RL. Historical warnings of future food insecurity with unprecedented seasonal heat. Science. 2009;323(5911):240–4.

    Article  CAS  PubMed  Google Scholar 

  • Bényei B, Gáspárdy A, Cseh S. Effect of the El Niño phenomenon on the ovarian responsiveness and embryo production of donor cows. Acta Vet Hung. 2003;51(2):209–18.

    Article  PubMed  Google Scholar 

  • Benyshek DC, Johnston CS, Martin JF. Glucose metabolism is altered in the adequately-nourished grand-offspring (F-3 generation) of rats malnourished during gestation and perinatal life. Diabetologia. 2006;49(5):1117–9.

    Article  CAS  PubMed  Google Scholar 

  • Berghof TV, Parmentier HK, Lammers A. Transgenerational epigenetic effects on innate immunity in broilers: an underestimated field to be explored? Poult Sci. 2013;92(11):2904–13.

    Article  CAS  PubMed  Google Scholar 

  • Bird A. DNA methylation patterns and epigenetic memory. Genes Dev. 2002;16(1):6–21.

    Article  CAS  PubMed  Google Scholar 

  • Bloch Qazi MC, Miller PB, Poeschel PM, Phan MH, Thayer JL, Medrano CL. Transgenerational effects of maternal and grandmaternal age on offspring viability and performance in Drosophila melanogaster. J Insect Physiol. 2017;100:43–52.

    Article  CAS  PubMed  Google Scholar 

  • Braunschweig M, Jagannathan V, Gutzwiller A, Bee G. Investigations on transgenerational epigenetic response down the male line in F2 pigs. PLoS One. 2012;7(2):e30583.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bromfield JJ. A role for seminal plasma in modulating pregnancy outcomes in domestic species. Reproduction. 2016;152(6):R223–R32.

    Article  CAS  PubMed  Google Scholar 

  • Bromfield JJ, Schjenken JE, Chin PY, Care AS, Jasper MJ, Robertson SA. Maternal tract factors contribute to paternal seminal fluid impact on metabolic phenotype in offspring. Proc Natl Acad Sci U S A. 2014;111(6):2200–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brookheart RT, Duncan JG. Drosophila melanogaster: an emerging model of transgenerational effects of maternal obesity. Mol Cell Endocrinol. 2016;435:20–8.

    Article  CAS  PubMed  Google Scholar 

  • Buschbeck M, Hake SB. Variants of core histones and their roles in cell fate decisions, development and cancer. Nat Rev Mol Cell Biol. 2017;18(5):299–314.

    Article  CAS  PubMed  Google Scholar 

  • Caballero I, Parrilla I, Alminana C, del Olmo D, Roca J, Martinez EA, et al. Seminal plasma proteins as modulators of the sperm function and their application in sperm biotechnologies. Reprod Domest Anim. 2012;47(Suppl 3):12–21.

    Article  PubMed  Google Scholar 

  • Camargo M, Intasqui P, Bertolla RP. Understanding the seminal plasma proteome and its role in male fertility. Basic Clin Androl. 2018;28:6.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cantone I, Fisher AG. Epigenetic programming and reprogramming during development. Nat Struct Mol Biol. 2013;20(3):282–9.

    Article  CAS  PubMed  Google Scholar 

  • Carre J, Gatimel N, Moreau J, Parinaud J, Leandri R. Influence of air quality on the results of in vitro fertilization attempts: a retrospective study. Eur J Obstet Gynecol Reprod Biol. 2017;210:116–22.

    Article  CAS  PubMed  Google Scholar 

  • Cavalli G, Paro R. The Drosophila Fab-7 chromosomal element conveys epigenetic inheritance during mitosis and meiosis. Cell. 1998;93(4):505–18.

    Article  CAS  PubMed  Google Scholar 

  • Chen M, Wu L, Zhao J, Wu F, Davies MJ, Wittert GA, et al. Altered glucose metabolism in mouse and humans conceived by IVF. Diabetes. 2014;63(10):3189–98.

    Article  CAS  PubMed  Google Scholar 

  • Chen Q, Yan M, Cao Z, Li X, Zhang Y, Shi J, et al. Sperm tsRNAs contribute to intergenerational inheritance of an acquired metabolic disorder. Science. 2016a;351(6271):397–400.

    Article  CAS  PubMed  Google Scholar 

  • Chen Q, Yan W, Duan E. Epigenetic inheritance of acquired traits through sperm RNAs and sperm RNA modifications. Nat Rev Genet. 2016b;17(12):733–43.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christidis N, Jones GS, Stott PA. Dramatically increasing chance of extremely hot summers since the 2003 European heatwave. Nat Clim Change. 2015;5(1):46–50.

    Article  Google Scholar 

  • Colaco S, Sakkas D. Paternal factors contributing to embryo quality. J Assist Reprod Genet. 2018;35:1–16.

    Article  Google Scholar 

  • Cooney CA, Dave AA, Wolff GL. Maternal methyl supplements in mice affect epigenetic variation and DNA methylation of offspring. J Nutr. 2002;132(8 Suppl):2393S–400S.

    Article  CAS  PubMed  Google Scholar 

  • Cox LA, Nijland MJ, Gilbert JS, Schlabritz-Loutsevitch NE, Hubbard GB, McDonald TJ, et al. Effect of 30 per cent maternal nutrient restriction from 0.16 to 0.5 gestation on fetal baboon kidney gene expression. J Physiol. 2006;572(Pt 1):67–85.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cropley JE, Eaton SA, Aiken A, Young PE, Giannoulatou E, Ho JWK, et al. Male-lineage transmission of an acquired metabolic phenotype induced by grand-paternal obesity. Mol Metab. 2016;5(8):699–708.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dawson MA, Kouzarides T. Cancer epigenetics: from mechanism to therapy. Cell. 2012;150(1):12–27.

    Article  CAS  PubMed  Google Scholar 

  • Daxinger L, Whitelaw E. Transgenerational epigenetic inheritance: more questions than answers. Genome Res. 2010;20(12):1623–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Desai M, Jellyman JK, Ross MG. Epigenomics, gestational programming and risk of metabolic syndrome. Int J Obes (Lond). 2015;39(4):633–41.

    Article  CAS  Google Scholar 

  • Donkin I, Barres R. Sperm epigenetics and influence of environmental factors. Mol Metab. 2018;14:1–11.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du Q, Hosoda H, Umekawa T, Kinouchi T, Ito N, Miyazato M, et al. Postnatal weight gain induced by overfeeding pups and maternal high-fat diet during the lactation period modulates glucose metabolism and the production of pancreatic and gastrointestinal peptides. Peptides. 2015;70:23–31.

    Article  CAS  PubMed  Google Scholar 

  • Duhl DM, Vrieling H, Miller KA, Wolff GL, Barsh GS. Neomorphic agouti mutations in obese yellow mice. Nat Genet. 1994;8(1):59–65.

    Article  CAS  PubMed  Google Scholar 

  • Dumoulin JC, Land JA, Van Montfoort AP, Nelissen EC, Coonen E, Derhaag JG, et al. Effect of in vitro culture of human embryos on birthweight of newborns. Hum Reprod. 2010;25(3):605–12.

    Article  PubMed  Google Scholar 

  • Dunn GA, Bale TL. Maternal high-fat diet effects on third-generation female body size via the paternal lineage. Endocrinology. 2011;152(6):2228–36.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feeney A, Nilsson E, Skinner MK. Epigenetics and transgenerational inheritance in domesticated farm animals. J Anim Sci Biotechnol. 2014;5(1):48.

    Article  PubMed  PubMed Central  Google Scholar 

  • Feuer SK, Liu X, Donjacour A, Lin W, Simbulan RK, Giritharan G, et al. Use of a mouse in vitro fertilization model to understand the developmental origins of health and disease hypothesis. Endocrinology. 2014;155(5):1956–69.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fleming TP, Velazquez MA, Eckert JJ. Embryos, DOHaD and David Barker. J Dev Orig Health Dis. 2015;6(5):377–83.

    Article  CAS  PubMed  Google Scholar 

  • Fleming TP, Watkins AJ, Velazquez MA, Mathers JC, Prentice AM, Stephenson J, et al. Origins of lifetime health around the time of conception: causes and consequences. Lancet. 2018;391(10132):1842–52.

    Article  PubMed  PubMed Central  Google Scholar 

  • Frantz ED, Aguila MB, Pinheiro-Mulder Ada R, Mandarim-de-Lacerda CA. Transgenerational endocrine pancreatic adaptation in mice from maternal protein restriction in utero. Mech Ageing Dev. 2011;132(3):110–6.

    Article  CAS  PubMed  Google Scholar 

  • Fullston T, Ohlsson Teague EM, Palmer NO, DeBlasio MJ, Mitchell M, Corbett M, et al. Paternal obesity initiates metabolic disturbances in two generations of mice with incomplete penetrance to the F2 generation and alters the transcriptional profile of testis and sperm microRNA content. FASEB J. 2013;27(10):4226–43.

    Article  CAS  PubMed  Google Scholar 

  • Gapp K, Jawaid A, Sarkies P, Bohacek J, Pelczar P, Prados J, et al. Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice. Nat Neurosci. 2014;17(5):667–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gienapp P, Teplitsky C, Alho JS, Mills JA, Merila J. Climate change and evolution: disentangling environmental and genetic responses. Mol Ecol. 2008;17(1):167–78.

    Article  CAS  PubMed  Google Scholar 

  • Gluckman PD, Hanson MA. Living with the past: evolution, development, and patterns of disease. Science. 2004;305(5691):1733–6.

    Article  CAS  PubMed  Google Scholar 

  • Godfrey KM, Lillycrop KA, Burdge GC, Gluckman PD, Hanson MA. Epigenetic mechanisms and the mismatch concept of the developmental origins of health and disease. Pediatr Res. 2007;61(5 Pt 2):5R–10R.

    Article  PubMed  Google Scholar 

  • Hammoud SS, Nix DA, Zhang H, Purwar J, Carrell DT, Cairns BR. Distinctive chromatin in human sperm packages genes for embryo development. Nature. 2009;460(7254):473–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hanson MA, Gluckman PD. Developmental origins of health and disease: new insights. Basic Clin Pharmacol Toxicol. 2008;102(2):90–3.

    Article  CAS  PubMed  Google Scholar 

  • Hanson MA, Gluckman PD. Early developmental conditioning of later health and disease: physiology or pathophysiology? Physiol Rev. 2014;94(4):1027–76.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heard E, Martienssen RA. Transgenerational epigenetic inheritance: myths and mechanisms. Cell. 2014;157(1):95–109.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heindel JJ. The developmental basis of disease: update on environmental exposures and animal models. Basic Clin Pharmacol Toxicol. 2018; https://doi.org/10.1111/bcpt.13118.

    Article  CAS  Google Scholar 

  • Hoffman DJ, Reynolds RM, Hardy DB. Developmental origins of health and disease: current knowledge and potential mechanisms. Nutr Rev. 2017;75(12):951–70.

    Article  PubMed  Google Scholar 

  • Jafaroghli M, Abdi-Benemar H, Zamiri MJ, Khalili B, Farshad A, Shadparvar AA. Effects of dietary n-3 fatty acids and vitamin C on semen characteristics, lipid composition of sperm and blood metabolites in fat-tailed Moghani rams. Anim Reprod Sci. 2014;147(1-2):17–24.

    Article  CAS  PubMed  Google Scholar 

  • Jenkins TG, Aston KI, Meyer T, Carrell DT. The sperm epigenome, male aging, and potential effects on the embryo. Adv Exp Med Biol. 2015;868:81–93.

    Article  PubMed  Google Scholar 

  • Jirtle RL, Skinner MK. Environmental epigenomics and disease susceptibility. Nat Rev Genet. 2007;8(4):253–62.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan IY, Dekou V, Douglas G, Jensen R, Hanson MA, Poston L, et al. A high-fat diet during rat pregnancy or suckling induces cardiovascular dysfunction in adult offspring. Am J Physiol Regul Integr Comp Physiol. 2005;288(1):R127–33.

    Article  CAS  PubMed  Google Scholar 

  • Klonoff-Cohen HS, Savitz DA, Cefalo RC, McCann MF. An epidemiologic study of contraception and preeclampsia. JAMA. 1989;262(22):3143–7.

    Article  CAS  PubMed  Google Scholar 

  • Klosin A, Casas E, Hidalgo-Carcedo C, Vavouri T, Lehner B. Transgenerational transmission of environmental information in C. elegans. Science. 2017;356(6335):320–3.

    Article  CAS  PubMed  Google Scholar 

  • Knecht AL, Truong L, Marvel SW, Reif DM, Garcia A, Lu C, et al. Transgenerational inheritance of neurobehavioral and physiological deficits from developmental exposure to benzo[a]pyrene in zebrafish. Toxicol Appl Pharmacol. 2017;329:148–57.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kort HI, Massey JB, Elsner CW, Mitchell-Leef D, Shapiro DB, Witt MA, et al. Impact of body mass index values on sperm quantity and quality. J Androl. 2006;27(3):450–2.

    Article  PubMed  Google Scholar 

  • Lambrot R, Xu C, Saint-Phar S, Chountalos G, Cohen T, Paquet M, et al. Low paternal dietary folate alters the mouse sperm epigenome and is associated with negative pregnancy outcomes. Nat Commun. 2013;4:2889.

    Article  CAS  PubMed  Google Scholar 

  • Langley SC, Jackson AA. Increased systolic blood pressure in adult rats induced by fetal exposure to maternal low protein diets. Clin Sci (Lond). 1994;86(2):217–22. Discussion 121.

    Article  CAS  Google Scholar 

  • Lang-Mladek C, Popova O, Kiok K, Berlinger M, Rakic B, Aufsatz W, et al. Transgenerational inheritance and resetting of stress-induced loss of epigenetic gene silencing in Arabidopsis. Mol Plant. 2010;3(3):594–602.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lea RG, Amezaga MR, Loup B, Mandon-Pepin B, Stefansdottir A, Filis P, et al. The fetal ovary exhibits temporal sensitivity to a ‘real-life’ mixture of environmental chemicals. Sci Rep. 2016a;6:22279.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lea RG, Byers AS, Sumner RN, Rhind SM, Zhang Z, Freeman SL, et al. Environmental chemicals impact dog semen quality in vitro and may be associated with a temporal decline in sperm motility and increased cryptorchidism. Sci Rep. 2016b;6:31281.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee JH, Friso S, Choi SW. Epigenetic mechanisms underlying the link between non-alcoholic fatty liver diseases and nutrition. Nutrients. 2014;6(8):3303–25.

    Article  PubMed  PubMed Central  Google Scholar 

  • Li J, Na L, Ma H, Zhang Z, Li T, Lin L, et al. Multigenerational effects of parental prenatal exposure to famine on adult offspring cognitive function. Sci Rep. 2015;5:13792.

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu L, Wylie RC, Andrews LG, Tollefsbol TO. Aging, cancer and nutrition: the DNA methylation connection. Mech Ageing Dev. 2003;124(10–12):989–98.

    Article  CAS  PubMed  Google Scholar 

  • Lucas ES, Watkins AJ. The long-term effects of the periconceptional period on embryo epigenetic profile and phenotype; the paternal role and his contribution, and how males can affect offspring’s phenotype/epigenetic profile. Adv Exp Med Biol. 2017;1014:137–54.

    Article  CAS  PubMed  Google Scholar 

  • Maurice C, Kaczmarczyk M, Cote N, Tremblay Y, Kimmins S, Bailey JL. Prenatal exposure to an environmentally relevant mixture of Canadian Arctic contaminants decreases male reproductive function in an aging rat model. J Dev Orig Health Dis. 2018;9(5):511–8.

    Article  CAS  PubMed  Google Scholar 

  • McCoy CR, Jackson NL, Brewer RL, Moughnyeh MM, Smith DL, Jr., Clinton SM. A paternal methyl donor depleted diet leads to increased anxiety- and depression-like behavior in adult rat offspring. Biosci Rep 2018;38(4).

    Article  PubMed  PubMed Central  Google Scholar 

  • McPherson NO, Fullston T, Kang WX, Sandeman LY, Corbett MA, Owens JA, et al. Paternal under-nutrition programs metabolic syndrome in offspring which can be reversed by antioxidant/vitamin food fortification in fathers. Sci Rep. 2016;6:27010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meister TA, Rimoldi SF, Soria R, von Arx R, Messerli FH, Sartori C, et al. Association of assisted reproductive technologies with arterial hypertension during adolescence. J Am Coll Cardiol. 2018;72(11):1267–74.

    Article  PubMed  Google Scholar 

  • Messerschmidt DM. Should I stay or should I go: protection and maintenance of DNA methylation at imprinted genes. Epigenetics. 2012;7(9):969–75.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mima M, Greenwald D, Ohlander S. Environmental toxins and male fertility. Curr Urol Rep. 2018;19(7):50.

    Article  PubMed  Google Scholar 

  • Moallem U, Neta N, Zeron Y, Zachut M, Roth Z. Dietary alpha-linolenic acid from flaxseed oil or eicosapentaenoic and docosahexaenoic acids from fish oil differentially alter fatty acid composition and characteristics of fresh and frozen-thawed bull semen. Theriogenology. 2015;83(7):1110–20.

    Article  CAS  PubMed  Google Scholar 

  • Molaro A, Hodges E, Fang F, Song Q, McCombie WR, Hannon GJ, et al. Sperm methylation profiles reveal features of epigenetic inheritance and evolution in primates. Cell. 2011;146(6):1029–41.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murdoch BM, Murdoch GK, Greenwood S, McKay S. Nutritional influence on epigenetic marks and effect on livestock production. Front Genet. 2016;7:182.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Murrin CM, Kelly GE, Tremblay RE, Kelleher CC. Body mass index and height over three generations: evidence from the lifeways cross-generational cohort study. BMC Public Health. 2012;12:81.

    Article  PubMed  PubMed Central  Google Scholar 

  • Nestler EJ. Transgenerational epigenetic contributions to stress responses: fact or fiction? PLoS Biol. 2016;14(3):e1002426.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nilsson EE, Sadler-Riggleman I, Skinner MK. Environmentally induced epigenetic transgenerational inheritance of disease. Environ Epigenet. 2018;4(2):dvy016.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Osgerby JC, Wathes DC, Howard D, Gadd TS. The effect of maternal undernutrition on ovine fetal growth. J Endocrinol. 2002;173(1):131–41.

    Article  CAS  PubMed  Google Scholar 

  • Ost A, Lempradl A, Casas E, Weigert M, Tiko T, Deniz M, et al. Paternal diet defines offspring chromatin state and intergenerational obesity. Cell. 2014;159(6):1352–64.

    Article  PubMed  CAS  Google Scholar 

  • Otero-Ferrer F, Izquierdo M, Fazeli A, Holt WV. Embryonic developmental plasticity in the long-snouted seahorse (Hippocampus reidi, Ginsburg 1933) in relation to parental preconception diet. Reprod Fertil Dev. 2016;28(7):1020–8.

    Article  CAS  PubMed  Google Scholar 

  • Painter RC, Osmond C, Gluckman P, Hanson M, Phillips DI, Roseboom TJ. Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life. BJOG. 2008;115(10):1243–9.

    Article  CAS  PubMed  Google Scholar 

  • Paulson RJ, Comizzoli P. Addressing challenges in developing and implementing successful in vitro fertilization in endangered species: an opportunity for humanity to “give back”. Fertil Steril. 2018;109(3):418–9.

    Article  PubMed  Google Scholar 

  • Peitz B, Olds-Clarke P. Effects of seminal vesicle removal on fertility and uterine sperm motility in the house mouse. Biol Reprod. 1986;35(3):608–17.

    Article  CAS  PubMed  Google Scholar 

  • Pembrey M, Saffery R, Bygren LO, Network in Epigenetic Epidemiology, Network in Epigenetic Epidemiology. Human transgenerational responses to early-life experience: potential impact on development, health and biomedical research. J Med Genet. 2014;51(9):563–72.

    Article  PubMed  Google Scholar 

  • Pentinat T, Ramon-Krauel M, Cebria J, Diaz R, Jimenez-Chillaron JC. Transgenerational inheritance of glucose intolerance in a mouse model of neonatal overnutrition. Endocrinology. 2010;151(12):5617–23.

    Article  CAS  PubMed  Google Scholar 

  • Pisani LF, Antonini S, Pocar P, Ferrari S, Brevini TA, Rhind SM, et al. Effects of pre-mating nutrition on mRNA levels of developmentally relevant genes in sheep oocytes and granulosa cells. Reproduction. 2008;136(3):303–12.

    Article  CAS  PubMed  Google Scholar 

  • Ponting CP, Oliver PL, Reik W. Evolution and functions of long noncoding RNAs. Cell. 2009;136(4):629–41.

    Article  CAS  PubMed  Google Scholar 

  • Radford EJ, Ito M, Shi H, Corish JA, Yamazawa K, Isganaitis E, et al. In utero effects. In utero undernourishment perturbs the adult sperm methylome and intergenerational metabolism. Science. 2014;345(6198):1255903.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rattan S, Zhou C, Chiang C, Mahalingam S, Brehm E, Flaws JA. Exposure to endocrine disruptors during adulthood: consequences for female fertility. J Endocrinol. 2017;233(3):R109–R29.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ravelli AC, van der Meulen JH, Michels RP, Osmond C, Barker DJ, Hales CN, et al. Glucose tolerance in adults after prenatal exposure to famine. Lancet. 1998;351(9097):173–7.

    Article  CAS  PubMed  Google Scholar 

  • Rehman S, Usman Z, Rehman S, AlDraihem M, Rehman N, Rehman I, et al. Endocrine disrupting chemicals and impact on male reproductive health. Transl Androl Urol. 2018;7(3):490–503.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rexhaj E, Paoloni-Giacobino A, Rimoldi SF, Fuster DG, Anderegg M, Somm E, et al. Mice generated by in vitro fertilization exhibit vascular dysfunction and shortened life span. J Clin Invest. 2013;123(12):5052–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robertson SA, Sharkey DJ. Seminal fluid and fertility in women. Fertil Steril. 2016;106(3):511–9.

    Article  PubMed  Google Scholar 

  • Robertson SA, Chin PY, Schjenken JE, Thompson JG. Female tract cytokines and developmental programming in embryos. Adv Exp Med Biol. 2015;843:173–213.

    Article  CAS  PubMed  Google Scholar 

  • Robillard PY, Hulsey TC, Perianin J, Janky E, Miri EH, Papiernik E. Association of pregnancy-induced hypertension with duration of sexual cohabitation before conception. Lancet. 1994;344(8928):973–5.

    Article  CAS  PubMed  Google Scholar 

  • Rodgers AB, Morgan CP, Bronson SL, Revello S, Bale TL. Paternal stress exposure alters sperm microRNA content and reprograms offspring HPA stress axis regulation. J Neurosci. 2013;33(21):9003–12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodgers AB, Morgan CP, Leu NA, Bale TL. Transgenerational epigenetic programming via sperm microRNA recapitulates effects of paternal stress. Proc Natl Acad Sci U S A. 2015;112(44):13699–704.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rooke JA, Sinclair AG, Edwards SA. Feeding tuna oil to the sow at different times during pregnancy has different effects on piglet long-chain polyunsaturated fatty acid composition at birth and subsequent growth. Br J Nutr. 2001;86(1):21–30.

    Article  CAS  PubMed  Google Scholar 

  • Roseboom TJ, van der Meulen JH, Osmond C, Barker DJ, Ravelli AC, Bleker OP. Plasma lipid profiles in adults after prenatal exposure to the Dutch famine. Am J Clin Nutr. 2000a;72(5):1101–6.

    Article  CAS  PubMed  Google Scholar 

  • Roseboom TJ, van der Meulen JH, Osmond C, Barker DJ, Ravelli AC, Schroeder-Tanka JM, et al. Coronary heart disease after prenatal exposure to the Dutch famine, 1944-45. Heart. 2000b;84(6):595–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rousseau-Ralliard D, Couturier-Tarrade A, Thieme R, Brat R, Rolland A, Boileau P, et al. A short periconceptional exposure to maternal type-1 diabetes is sufficient to disrupt the feto-placental phenotype in a rabbit model. Mol Cell Endocrinol. 2019;480:42–53.

    Article  CAS  PubMed  Google Scholar 

  • Saben JL, Boudoures AL, Asghar Z, Thompson A, Drury A, Zhang W, et al. Maternal metabolic syndrome programs mitochondrial dysfunction via germline changes across three generations. Cell Rep. 2016;16(1):1–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sarkar M, Baffy G. Perinatal programming of adolescent nonalcoholic fatty liver disease: a case for gender inequality? Hepatology. 2018;67(1):7–9.

    Article  PubMed  Google Scholar 

  • Schagdarsurengin U, Steger K. Epigenetics in male reproduction: effect of paternal diet on sperm quality and offspring health. Nat Rev Urol. 2016;13(10):584–95.

    Article  CAS  PubMed  Google Scholar 

  • Schmidt S, Hommel A, Gawlik V, Augustin R, Junicke N, Florian S, et al. Essential role of glucose transporter GLUT3 for post-implantation embryonic development. J Endocrinol. 2009;200(1):23–33.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schübeler D. Function and information content of DNA methylation. Nature. 2015;517(7534):321–6.

    Article  PubMed  CAS  Google Scholar 

  • Schuster A, Skinner MK, Yan W. Ancestral vinclozolin exposure alters the epigenetic transgenerational inheritance of sperm small noncoding RNAs. Environ Epigenet. 2016;2(1)

    Article  PubMed  PubMed Central  Google Scholar 

  • Segovia SA, Vickers MH, Zhang XD, Gray C, Reynolds CM. Maternal supplementation with conjugated linoleic acid in the setting of diet-induced obesity normalises the inflammatory phenotype in mothers and reverses metabolic dysfunction and impaired insulin sensitivity in offspring. J Nutr Biochem. 2015;26(12):1448–57.

    Article  CAS  PubMed  Google Scholar 

  • Sinclair KD, Watkins AJ. Parental diet, pregnancy outcomes and offspring health: metabolic determinants in developing oocytes and embryos. Reprod Fertil Dev. 2014;26(1):99–114.

    Article  CAS  Google Scholar 

  • Sinclair KD, Allegrucci C, Singh R, Gardner DS, Sebastian S, Bispham J, et al. DNA methylation, insulin resistance, and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status. Proc Natl Acad Sci U S A. 2007;104(49):19351–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sokol RZ, Kraft P, Fowler IM, Mamet R, Kim E, Berhane KT. Exposure to environmental ozone alters semen quality. Environ Health Perspect. 2006;114(3):360–5.

    Article  CAS  PubMed  Google Scholar 

  • Tsuduki T, Kitano Y, Honma T, Kijima R, Ikeda I. High dietary fat intake during lactation promotes development of diet-induced obesity in male offspring of mice. J Nutr Sci Vitaminol (Tokyo). 2013;59(5):384–92.

    Article  CAS  Google Scholar 

  • Veenendaal MV, Painter RC, de Rooij SR, Bossuyt PM, van der Post JA, Gluckman PD, et al. Transgenerational effects of prenatal exposure to the 1944-45 Dutch famine. BJOG. 2013;120(5):548–53.

    Article  CAS  PubMed  Google Scholar 

  • Volkova K, Reyhanian Caspillo N, Porseryd T, Hallgren S, Dinnetz P, Olsen H, et al. Transgenerational effects of 17alpha-ethinyl estradiol on anxiety behavior in the guppy, Poecilia reticulata. Gen Comp Endocrinol. 2015;223:66–72.

    Article  CAS  PubMed  Google Scholar 

  • Walker DM, Gore AC. Epigenetic impacts of endocrine disruptors in the brain. Front Neuroendocrinol. 2017;44:1–26.

    Article  CAS  PubMed  Google Scholar 

  • Watkins AJ, Sinclair KD. Paternal low protein diet affects adult offspring cardiovascular and metabolic function in mice. Am J Physiol Heart Circ Physiol. 2014;306(10):H1444–52.

    Article  CAS  PubMed  Google Scholar 

  • Watkins AJ, Wilkins A, Cunningham C, Perry VH, Seet MJ, Osmond C, et al. Low protein diet fed exclusively during mouse oocyte maturation leads to behavioural and cardiovascular abnormalities in offspring. J Physiol. 2008;586(8):2231–44.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watkins AJ, Sirovica S, Stokes B, Isaacs M, Addison O, Martin RA. Paternal low protein diet programs preimplantation embryo gene expression, fetal growth and skeletal development in mice. Biochim Biophys Acta. 2017;1863(6):1371–81.

    Article  CAS  Google Scholar 

  • Watkins AJ, Dias I, Tsuro H, Allen D, Emes RD, Moreton J, et al. Paternal diet programs offspring health through sperm- and seminal plasma-specific pathways in mice. Proc Natl Acad Sci U S A. 2018;115(40):10064–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wolff GL, Kodell RL, Moore SR, Cooney CA. Maternal epigenetics and methyl supplements affect agouti gene expression in Avy/a mice. FASEB J. 1998;12(11):949–57.

    Article  CAS  PubMed  Google Scholar 

  • Xia B, de Belle JS. Transgenerational programming of longevity and reproduction by post-eclosion dietary manipulation in Drosophila. Aging (Albany NY). 2016;8(5):1115–34.

    Article  Google Scholar 

  • Xin F, Susiarjo M, Bartolomei MS. Multigenerational and transgenerational effects of endocrine disrupting chemicals: a role for altered epigenetic regulation? Semin Cell Dev Biol. 2015;43:66–75.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yeung EH, Druschel C. Cardiometabolic health of children conceived by assisted reproductive technologies. Fertil Steril. 2013;99(2):318–26.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zama AM, Uzumcu M. Epigenetic effects of endocrine-disrupting chemicals on female reproduction: an ovarian perspective. Front Neuroendocrinol. 2010;31(4):420–39.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zandstra H, Brentjens L, Spauwen B, Touwslager RNH, Bons JAP, Mulder AL, et al. Association of culture medium with growth, weight and cardiovascular development of IVF children at the age of 9 years. Hum Reprod. 2018;33(9):1645–56.

    Article  CAS  PubMed  Google Scholar 

  • Zhou Y, Zhu H, Wu HY, Jin LY, Chen B, Pang HY, et al. Diet-induced paternal obesity impairs cognitive function in offspring by mediating epigenetic modifications in spermatozoa. Obesity (Silver Spring). 2018;26(11):1749–57.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Dr Watkins and his research are supported by the Biotechnology and Biological Sciences Research Council (BBSRC) under grant number BB/R003556/1.

Author information

Authors and Affiliations

  1. Division of Child Health, Obstetrics and Gynaecology, Faculty of Medicine, University of Nottingham, Nottingham, UK

    Hannah L. Morgan & Adam J. Watkins

Authors
  1. Hannah L. Morgan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Adam J. Watkins
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Adam J. Watkins .

Editor information

Editors and Affiliations

  1. Smithsonian Conservation Biology Institute, National Zoological Park, Washington, DC, USA

    Pierre Comizzoli

  2. Smithsonian Conservation Biology Institute, National Zoological Park, Front Royal, VA, USA

    Janine L. Brown

  3. Academic Unit of Reproductive and Developmental Medicine, The University of Sheffield, Sheffield, UK

    William V. Holt

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Morgan, H.L., Watkins, A.J. (2019). Transgenerational Impact of Environmental Change. In: Comizzoli, P., Brown, J., Holt, W. (eds) Reproductive Sciences in Animal Conservation. Advances in Experimental Medicine and Biology, vol 1200. Springer, Cham. https://doi.org/10.1007/978-3-030-23633-5_4

Download citation

Publish with us

Policies and ethics

Search

Navigation