Register      Login
Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
REVIEW

Nutritional programming and the reproductive function of the offspring

P. Chavatte-Palmer A B C G , C. Dupont A B , N. Debus D E F and S. Camous A B
+ Author Affiliations
- Author Affiliations

A INRA, UMR1198 Biologie du Développement et Reproduction, F-78350 Jouy en Josas, France.

B ENVA, F-94700 Maisons-Alfort, France.

C PremUp Foundation, 4 Avenue de l’Observatoire, 75004 Paris, France.

D INRA, UMR868 Systèmes d’Elevage Méditerranéens et Tropicaux, F-34060 Montpellier, France.

E Montpellier SupAgro, F-34060 Montpellier, France.

F CIRAD, F-34060 Montpellier, France.

G Corresponding author. Email: pascale.chavatte@jouy.inra.fr

Animal Production Science 54(9) 1166-1176 https://doi.org/10.1071/AN14470
Submitted: 3 April 2014  Accepted: 5 June 2014   Published: 24 July 2014

Abstract

There is ample evidence on the importance of maternal nutrition during pregnancy on fetal and offspring development. In ruminant females, the pool of oocytes is complete and definitive before birth, based on the resting reserve of primordial follicles established during fetal life, which represent the lifespan supply for the female’s fertilisable oocytes, whereas in males, although the production of spermatozoa is a continuous process throughout post-pubertal life. Sertoli cells, which play a central role in the development of a functional testis, proliferate during pre- and post-natal life, coordinating testicular development. Both male and female fertility may, therefore, be affected by the maternal environment, but studies on the effects of developmental nutritional conditions on reproductive function and fertility, both in males and females, are relatively scarce. In humans, intrauterine growth retardation has been associated with abnormal ovarian development, characterised by a decreased volume of primordial follicles in the ovarian cortical tissue in girls, and a higher incidence of cryptorchidism in boys, with subsequent low sperm counts in adulthood. Age at puberty and gonadotropin and inhibin B plasma concentrations are also affected. Animal studies suggest both in males and females that maternal undernutrition during pregnancy may affect pituitary response to GnRH and gonadal development and function, depending on the timing and magnitude of the undernutrition. Excess nutrition, which is often associated with intrauterine growth retardation in domestic species, induces effects on the onset of puberty and both testicular and ovarian function, maybe through the observed reduction in fetal growth. This review addresses the influence of maternal nutrition on offspring reproductive function using examples in humans and animals, with particular focus on ruminants.

Additional keywords: animal breeding, DOHAD, fertility, gametes, ovary, testes.


References

Abecia JA, Casao A, Pascual-Alonso M, Lobón S, Aguayo-Ulloa LA, Meikle A, Forcada F, Sosa C, Marín RH, Silva MA, Maria GA (2014) The effect of periconceptional undernutrition of sheep on the cognitive/emotional response and oocyte quality of offspring at 30 days of age. Journal of Developmental Origins of Health and Disease 5, 79–87.

Ahsan U, Kamran Z, Raza I, Ahmad S, Babar W, Riaz MH, Iqbal Z (2014) Role of selenium in male reproduction: a review. Animal Reproduction Science 146, 55–62.
Role of selenium in male reproduction: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXktVWhtrY%3D&md5=eebe2b99d7d9e00c8e0eeeeb1bc9b830CAS | 24613013PubMed |

Aiken CE, Tarry-Adkins JL, Ozanne SE (2013) Suboptimal nutrition in utero causes DNA damage and accelerated aging of the female reproductive tract. The FASEB Journal 27, 3959–3965.
Suboptimal nutrition in utero causes DNA damage and accelerated aging of the female reproductive tract.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1Sqt7fF&md5=0675bc18ae0c83ba8aa61b4f2a35c4fdCAS |

Bach A (2012) Nourishing and managing the dam and postnatal calf for optimal lactation, reproduction, and immunity. Journal of Animal Science 90, 1835–1845.
Nourishing and managing the dam and postnatal calf for optimal lactation, reproduction, and immunity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XpsFWgsbo%3D&md5=49eb92403c39a8110182def16917ba44CAS | 21926322PubMed |

Baillet A, Mandon-Pepin B (2012) Mammalian ovary differentiation – a focus on female meiosis. Molecular and Cellular Endocrinology 356, 13–23.
Mammalian ovary differentiation – a focus on female meiosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xls1ehsbk%3D&md5=cca6bcb59abe9b681cc5495d5f032e76CAS | 21964319PubMed |

Barker DJ (1992) The fetal origins of diseases of old age. European Journal of Clinical Nutrition 46, S3–S9.

Behrens A, Georgiev A, Carraro M (2010) Future impacts of climate change across Europe. CEPS Working Document No. 324. Available at http://www.ceps.eu. [Verified 2 July 2014]

Berends LM, Fernandez-Twinn DS, Martin-Gronert MS, Cripps RL, Ozanne SE (2013) Catch-up growth following intra-uterine growth-restriction programmes an insulin-resistant phenotype in adipose tissue. International Journal of Obesity 37, 1051–1057.
Catch-up growth following intra-uterine growth-restriction programmes an insulin-resistant phenotype in adipose tissue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1CktrnN&md5=ff5ddec9725c40aa3df2aa925fe642d7CAS | 23229735PubMed |

Bernal AB, Vickers MH, Hampton MB, Poynton RA, Sloboda DM (2010) Maternal undernutrition significantly impacts ovarian follicle number and increases ovarian oxidative stress in adult rat offspring. PLoS ONE 5, e15558
Maternal undernutrition significantly impacts ovarian follicle number and increases ovarian oxidative stress in adult rat offspring.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhs1Wiu7vO&md5=2b0c3865583369bad2b14314409229aeCAS | 21179452PubMed |

Bielli A, Katz H, Pedrana G, Gastel MT, Moraña A, Castrillejo A, Lundeheim N, Forsberg M, Rodriguez-Martinez H (2001) Nutritional management during fetal and postnatal life, and the influence on testicular stereology and Sertoli cell numbers in Corriedale ram lambs. Small Ruminant Research 40, 63–71.
Nutritional management during fetal and postnatal life, and the influence on testicular stereology and Sertoli cell numbers in Corriedale ram lambs.Crossref | GoogleScholarGoogle Scholar | 11259877PubMed |

Bielli A, Perez R, Pedrana G, Milton JTB, Lopez A, Blackberry MA, Duncombe G, Rodriguez-Martinez H, Martin GB (2002) Low maternal nutrition during pregnancy reduces the number of Sertoli cells in the newborn lamb. Reproduction, Fertility and Development 14, 333–337.
Low maternal nutrition during pregnancy reduces the number of Sertoli cells in the newborn lamb.Crossref | GoogleScholarGoogle Scholar |

Borwick SC, Rhind SM, McMillen SR, Racey PA (1997) Effect of undernutrition of ewes from the time of mating on fetal ovarian development in mid gestation. Reproduction, Fertility and Development 9, 711–715.
Effect of undernutrition of ewes from the time of mating on fetal ovarian development in mid gestation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1c3osV2nuw%3D%3D&md5=39949386eccb8b1c52ff7b04376f6e21CAS |

Borwick SC, Rae MT, Brooks J, McNeilly AS, Racey PA, Rhind SM (2003) Undernutrition of ewe lambs in utero and in early post-natal life does not affect hypothalamic–pituitary function in adulthood. Animal Reproduction Science 77, 61–70.
Undernutrition of ewe lambs in utero and in early post-natal life does not affect hypothalamic–pituitary function in adulthood.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXitlGiu7c%3D&md5=3a053a99875b226fc33271a6439fd927CAS | 12654528PubMed |

Bourc’his D, Proudhon C (2008) Sexual dimorphism in parental imprint ontogeny and contribution to embryonic development. Molecular and Cellular Endocrinology 282, 87–94.
Sexual dimorphism in parental imprint ontogeny and contribution to embryonic development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXitVegtLs%3D&md5=cf42373b31168e71d383bed2f10bd9c7CAS | 18178305PubMed |

Casellas J, Caja G (2014) Fetal programming by co-twin rivalry in sheep. Journal of Animal Science 92, 64–71.
Fetal programming by co-twin rivalry in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXht12nt7o%3D&md5=5543699f105141ea061add39b0fc3674CAS | 24243893PubMed |

Cetin I, Berti C, Calabrese S (2010) Role of micronutrients in the periconceptional period. Human Reproduction Update 16, 80–95.
Role of micronutrients in the periconceptional period.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFOht7rK&md5=660fa50940759b4e899698562442e3a0CAS | 19567449PubMed |

Chadio S, Kotsampasi B (2014) The role of early life nutrition in programming of reproductive function. Journal of Developmental Origins of Health and Disease 5, 2–15.
The role of early life nutrition in programming of reproductive function.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2cjkvFOisA%3D%3D&md5=6c7e5a3563e2f71ab86c206c2eb6fd47CAS | 24847686PubMed |

Connor KL, Vickers MH, Beltrand J, Meaney MJ, Sloboda DM (2012) Nature, nurture or nutrition? Impact of maternal nutrition on maternal care, offspring development and reproductive function. The Journal of Physiology 590, 2167–2180.

Da Silva P, Aitken RP, Rhind SM, Racey PA, Wallace JM (2001) Influence of placentally-mediated foetal growth restriction on the onset of puberty in male and female lambs. Reproduction 122, 375–383.
Influence of placentally-mediated foetal growth restriction on the onset of puberty in male and female lambs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXntVGksLY%3D&md5=5eeaf2cafd76bb88a4eca81c84904951CAS | 11597303PubMed |

Da Silva P, Aitken RP, Rhind SM, Racey PA, Wallace JM (2002) Impact of maternal nutrition during pregnancy on pituitary gonadotrophin gene expression and ovarian development in growth-restricted and normally grown late gestation sheep fetuses. Reproduction 123, 769–777.
Impact of maternal nutrition during pregnancy on pituitary gonadotrophin gene expression and ovarian development in growth-restricted and normally grown late gestation sheep fetuses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XkvVCiur8%3D&md5=543be32440a11cc979b802083b7002ceCAS | 12052231PubMed |

Da Silva P, Aitken RP, Rhind SM, Racey PA, Wallace JM (2003) Effect of maternal overnutrition during pregnancy on pituitary gonadotrophin gene expression and gonadal morphology in female and male foetal sheep at day 103 of gestation. Placenta 24, 248–257.
Effect of maternal overnutrition during pregnancy on pituitary gonadotrophin gene expression and gonadal morphology in female and male foetal sheep at day 103 of gestation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXptlOltA%3D%3D&md5=f6d47adcaa0976fc98dbb25785a6dc51CAS | 12566252PubMed |

Daniel-Carlier N, Harscoet E, Thepot D, Auguste A, Pailhoux E, Jolivet G (2013) Gonad differentiation in the rabbit: evidence of species-specific features. PLoS ONE 8, e60451
Gonad differentiation in the rabbit: evidence of species-specific features.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmtlSmsbw%3D&md5=9c903ae1b1fe529958a961cabd3af7baCAS | 23593221PubMed |

Debus N, Chavatte-Palmer P, Viudes G, Camous S, Roséfort A, Hassoun P (2012) Maternal periconceptional undernutrition in Merinos d’Arles sheep: 1. Effects on pregnancy and reproduction results of mothers and offspring growth performances. Theriogenology 77, 1453–1465.
Maternal periconceptional undernutrition in Merinos d’Arles sheep: 1. Effects on pregnancy and reproduction results of mothers and offspring growth performances.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjvVems74%3D&md5=da79f194f3dd75380dd13cdfdaae9d45CAS | 22326588PubMed |

Deligeorgis SG, Chadio S, Menegatos J (1996) Pituitary responsiveness to GnRH in lambs undernourished during fetal life. Animal Reproduction Science 43, 113–121.
Pituitary responsiveness to GnRH in lambs undernourished during fetal life.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XksF2htrY%3D&md5=8fc8afc91f44142de8bc1031a56280f9CAS |

Díaz-García C, Estella C, Perales-Puchalt A, Simon C (2011) Reproductive medicine and inheritance of infertility by offspring: the role of fetal programming. Fertility and Sterility 96, 536–545.
Reproductive medicine and inheritance of infertility by offspring: the role of fetal programming.Crossref | GoogleScholarGoogle Scholar | 21794856PubMed |

Dupont C, Cordier A-G, Junien C, Mandon-Pepin B, Lévy R, Chavatte-Palmer P (2012) Maternal environment and the reproductive function of the offspring. Theriogenology 78, 1405–1414.
Maternal environment and the reproductive function of the offspring.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38bhs1emug%3D%3D&md5=dae884c5be86752f97ed2e08361cb8dcCAS | 22925651PubMed |

Dupont C, Ralliard-Rousseau D, Tarrade A, Faure C, Dahirel M, Sion B, Brugnon F, Levy R, Chavatte-Palmer P (2014) Impact of maternal hyperlipidic hypercholesterolemic diet on male reproductive organs and testosterone concentration in rabbits. Journal of Developmental Origins of Health and Disease 5, 183–188.

Evans AC, Mossa F, Walsh SW, Scheetz D, Jimenez-Krassel F, Ireland JL, Smith GW, Ireland JJ (2012) Effects of maternal environment during gestation on ovarian folliculogenesis and consequences for fertility in bovine offspring. Reproduction in Domestic Animals 47, 31–37.
Effects of maternal environment during gestation on ovarian folliculogenesis and consequences for fertility in bovine offspring.Crossref | GoogleScholarGoogle Scholar | 22827347PubMed |

Gabory A, Attig L, Junien C (2011) Developmental programming and epigenetics. The American Journal of Clinical Nutrition 94, 1943S–1952S.
Developmental programming and epigenetics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFOhtr3I&md5=cac9ec53f801440e878df919c52748e6CAS | 22049164PubMed |

Gardner DS, Ozanne S, Sinclair AJ (2009) Effect of the early-life nutritional environment on fecundity and fertility of mammals. Philosophical Transactions of the Royal Society. B 364, 3419–3427.
Effect of the early-life nutritional environment on fecundity and fertility of mammals.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1MnpsFalsA%3D%3D&md5=2bfba18d9cacd43312119e5c90bc73f3CAS |

Genovese P, Núñez M, Pombo C, Bielli A (2009) Undernutrition during foetal and post-natal life affects testicular structure and reduces the number of Sertoli cells in the adult rat. Reproduction in Domestic Animals 45, 233–236.
Undernutrition during foetal and post-natal life affects testicular structure and reduces the number of Sertoli cells in the adult rat.Crossref | GoogleScholarGoogle Scholar | 19281598PubMed |

Gluckman PD, Hanson MA, Beedle AS, Spencer HG (2008) Predictive adaptive responses in perspective. Trends in Endocrinology and Metabolism 19, 109–110.
Predictive adaptive responses in perspective.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlslWku7Y%3D&md5=d3bb5015dd1fb83008bf93855cf067e0CAS | 18328727PubMed |

Grazul-Bilska AT, Caton JS, Arndt W, Burchill K, Thorson C, Borowczyk E, Bilski JJ, Redmer DA, Reynolds LP, Vonnahme KA (2009) Cellular proliferation and vascularization in ovine fetal ovaries: effects of undernutrition and selenium in maternal diet. Reproduction 137, 699–707.
Cellular proliferation and vascularization in ovine fetal ovaries: effects of undernutrition and selenium in maternal diet.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosl2ntbo%3D&md5=ae484e8e5fb68a486f1492c3a9a69682CAS | 19129369PubMed |

Grazul-Bilska AT, Vonnahme KA, Bilski JJ, Borowczyk E, Soni D, Mikkelson B, Johnson ML, Reynolds LP, Redmer DA, Caton JS (2011) Expression of gap junctional connexin proteins in ovine fetal ovaries: effects of maternal diet. Domestic Animal Endocrinology 41, 185–194.
Expression of gap junctional connexin proteins in ovine fetal ovaries: effects of maternal diet.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1ymsr3P&md5=b43cf936e8c89846c24c51122a97e1f0CAS | 21820266PubMed |

Hales CN, Barker DJ (1992) Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 35, 595–601.
Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK38zlsVyhuw%3D%3D&md5=d9bd2290652e9c216eb2a7c248a2f490CAS | 1644236PubMed |

Hutt K, McLaughlin E, Holland M (2006) Primordial follicle activation and follicular development in the juvenile rabbit ovary. Cell and Tissue Research 326, 809–822.
Primordial follicle activation and follicular development in the juvenile rabbit ovary.Crossref | GoogleScholarGoogle Scholar | 16830146PubMed |

Jaquiery AL, Oliver MH, Bloomfield FH, Connor KL, Challis JR, Harding JE (2006) Fetal exposure to excess glucocorticoid is unlikely to explain the effects of periconceptional undernutrition in sheep. The Journal of Physiology 572, 109–118.

Kenyon PR (2008) A review of in-utero environmental effects in sheep production. Proceedings of the New Zealand Society of Animal Production 68, 142–155.

Kenyon PR, Blair HT (2014) Foetal programming in sheep – effects on production. Small Ruminant Research 118, 16–30.
Foetal programming in sheep – effects on production.Crossref | GoogleScholarGoogle Scholar |

Khireddine B, Grimard B, Ponter AA, Ponsart C, Boudjenah H, Mialot JP, Sauvant D, Humblot P (1998) Influence of flushing on LH secretion, follicular growth and the response to estrus synchronisation treatment in suckled beef cows. Theriogenology 49, 1409–1423.
Influence of flushing on LH secretion, follicular growth and the response to estrus synchronisation treatment in suckled beef cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjsVOru70%3D&md5=bc174d477988031c773a87617ff21361CAS | 10732077PubMed |

Kotsampasi B, Balaskas C, Papadomichelakis G, Chadio SE (2009a) Reduced Sertoli cell number and altered pituitary responsiveness in male lambs undernourished in utero. Animal Reproduction Science 114, 135–147.
Reduced Sertoli cell number and altered pituitary responsiveness in male lambs undernourished in utero.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXms1yqu7c%3D&md5=4149ddf75bba2e24481ccd59ae80432cCAS | 18814977PubMed |

Kotsampasi B, Chadio S, Papadomichelakis G, Deligeorgis S, Kalogiannis D, Menegatos I, Zervas G (2009b) Effects of maternal undernutrition on the hypothalamic–pituitary-gonadal axis function in female sheep offspring. Reproduction in Domestic Animals 44, 677–684.
Effects of maternal undernutrition on the hypothalamic–pituitary-gonadal axis function in female sheep offspring.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVaiurbM&md5=8e9868200651c5801828ebd7aaec1bc1CAS | 19642222PubMed |

Leveillé P, Tarrade A, Dupont C, Larcher T, Dahirel M, Poumerol E, Cordier A-G, Picone O, Mandon-Pepin B, Jolivet G, Lévy R, Chavatte-Palmer P (2014) Maternal high fat diet induces follicular atresia but does not affect fertility in adult rabbit offspring. Journal of Developmental Origins of Health and Disease 5, 88–97.

Logue DN, Mayne CS (2014) Welfare-positive management and nutrition for the dairy herd: a European perspective. Veterinary Journal 199, 31–38.
Welfare-positive management and nutrition for the dairy herd: a European perspective.Crossref | GoogleScholarGoogle Scholar |

Magre S, Vigier B (2001) Développement et différentiation sexuelle de l’appareil génital. In ‘La reproduction chez les mammifères et chez l’homme’. (Eds C Thibault, M-C Levasseur) pp. 235–255. (Ellipses: Paris)

McMillen IC, MacLaughlin SM, Muhlhausler BS, Gentili S, Duffield JL, Morrison JL (2008) Developmental origins of adult health and disease: the role of periconceptional and foetal nutrition. Basic & Clinical Pharmacology & Toxicology 102, 82–89.
Developmental origins of adult health and disease: the role of periconceptional and foetal nutrition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhvF2gsrg%3D&md5=3cbe2925ef2ce494c282640ba37f92eaCAS |

Meikle D, Westberg M (2001) Maternal nutrition and reproduction of daughters in wild house mice (Mus musculus). Journal of Reproduction and Fertility 122, 437–442.
Maternal nutrition and reproduction of daughters in wild house mice (Mus musculus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXntVGksbo%3D&md5=10efabc0965128d56b870a778855ba2eCAS |

Mirbahai L, Chipman JK (2014) Epigenetic memory of environmental organisms: a reflection of lifetime stressor exposures. Mutation Research/Genetic Toxicology and Environmental Mutagenesis 764–765, 10–17.
Epigenetic memory of environmental organisms: a reflection of lifetime stressor exposures.Crossref | GoogleScholarGoogle Scholar |

Mossa F, Carter F, Walsh SW, Kenny DA, Smith GW, Ireland JL, Hildebrandt TB, Lonergan P, Ireland JJ, Evans AC (2013) Maternal undernutrition in cows impairs ovarian and cardiovascular systems in their offspring. Biology of Reproduction 88, 92
Maternal undernutrition in cows impairs ovarian and cardiovascular systems in their offspring.Crossref | GoogleScholarGoogle Scholar | 23426432PubMed |

Muñoz C, Carson AF, McCoy MA, Dawson LER, Wylie ARG, Gordon AW (2009) Effects of plane of nutrition of ewes in early and mid-pregnancy on performance of the offspring: female reproduction and male carcass characteristics. Journal of Animal Science 87, 3647–3655.
Effects of plane of nutrition of ewes in early and mid-pregnancy on performance of the offspring: female reproduction and male carcass characteristics.Crossref | GoogleScholarGoogle Scholar | 19648487PubMed |

Parr RA, Williams AH, Campbell IP, Witcombe GF, Roberts AM (1986) Low nutrition of ewes in early-pregnancy and the residual effect on the offspring. The Journal of Agricultural Science 106, 81–87.
Low nutrition of ewes in early-pregnancy and the residual effect on the offspring.Crossref | GoogleScholarGoogle Scholar |

Rae MT, Palassio S, Kyle CE, Brooks AN, Lea RG, Miller DW, Rhind SM (2001) Effect of maternal undernutrition during pregnancy on early ovarian development and subsequent follicular development in sheep fetuses. Journal of Reproduction and Fertility 122, 915–922.
Effect of maternal undernutrition during pregnancy on early ovarian development and subsequent follicular development in sheep fetuses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhvVWisw%3D%3D&md5=4f971a6a28e06aac686d13412e3e8a44CAS |

Rae MT, Kyle CE, Miller DW, Hammond AJ, Brooks AN, Rhind SM (2002a) The effects of undernutrition, in utero, on reproductive function in adult male and female sheep. Animal Reproduction Science 72, 63–71.
The effects of undernutrition, in utero, on reproductive function in adult male and female sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XltFahsLw%3D&md5=d674bc593c7bd90cf9feaf4ca1c4ad4fCAS | 12106966PubMed |

Rae MT, Rhind SM, Fowler PA, Miller DW, Kyle CE, Brooks AN (2002b) Effect of maternal undernutrition on fetal testicular steroidogenesis during the CNS androgen-responsive period in male sheep fetuses. Reproduction 124, 33–39.
Effect of maternal undernutrition on fetal testicular steroidogenesis during the CNS androgen-responsive period in male sheep fetuses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmtFaks7s%3D&md5=7aca6b0aae44057a801b830a4dd4c2e5CAS | 12090916PubMed |

Reik W (2007) Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 447, 425–432.
Stability and flexibility of epigenetic gene regulation in mammalian development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlsFOgs7w%3D&md5=72cf9d003ff2544677a391f30bb5ba1aCAS | 17522676PubMed |

Rey R (2003) Regulation of spermatogenesis. Endocrine Development 5, 38–55.
Regulation of spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtVKgsr8%3D&md5=cd9db759336c451de63978e672faf1b3CAS | 12629891PubMed |

Roberts RM, Smith GW, Bazer FW, Cibelli J, Seidel GE, Bauman DE, Reynolds LP, Ireland JJ (2009) Farm animal research in crisis. Science 324, 468–469.
Farm animal research in crisis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltlGrtr8%3D&md5=a8ff630bf94ab84050656dce6eb64d9eCAS | 19390030PubMed |

Roséfort A, Debus N, Viudes G, Camous S, Pailhoux E, Hassoun P, Chavatte-Palmer P (2010) Effect of maternal periconceptional undernutrition on male offspring physiology and testicular development. Reproduction, Fertility and Development 23, 219
Effect of maternal periconceptional undernutrition on male offspring physiology and testicular development.Crossref | GoogleScholarGoogle Scholar |

Scaramuzzi RJ, Campbell BK, Downing JA, Kendall NR, Khalid M, Munoz-Gutierrez M, Somchit A (2006) A review of the effects of supplementary nutrition in the ewe on the concentrations of reproductive and metabolic hormones and the mechanisms that regulate folliculogenesis and ovulation rate. Reproduction, Nutrition, Development 46, 339–354.
A review of the effects of supplementary nutrition in the ewe on the concentrations of reproductive and metabolic hormones and the mechanisms that regulate folliculogenesis and ovulation rate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVOnsrzF&md5=53d39a334cce89e5723a5b6fed301638CAS | 16824444PubMed |

Sharpe RM, McKinnell C, Kivlin C, Fisher JS (2003) Proliferation and functional maturation of Sertoli cells, and their relevance to disorders of testis function in adulthood. Reproduction 125, 769–784.
Proliferation and functional maturation of Sertoli cells, and their relevance to disorders of testis function in adulthood.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXltFelt7c%3D&md5=4687cf993ff3d02c3591c414dfd602d8CAS | 12773099PubMed |

Shi L, Yue W, Zhang C, Ren Y, Zhu X, Wang Q, Liguang S, Lei F (2010) Effects of maternal and dietary selenium (Se-enriched yeast) on oxidative status in testis and apoptosis of germ cells during spermatogenesis of their offspring in goats. Animal Reproduction Science 119, 212–218.
Effects of maternal and dietary selenium (Se-enriched yeast) on oxidative status in testis and apoptosis of germ cells during spermatogenesis of their offspring in goats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktVaitro%3D&md5=cb12bb5c9b3acf3b68048015875ea890CAS | 20226605PubMed |

Sinclair KD, Allegrucci C, Singh R, Gardner DS, Sebastian S, Bispham J, Thurston A, Huntley JF, Rees WD, Maloney CA, Lea RG, Craigon J, McEvoy TG, Young LE (2007) DNA methylation, insulin resistance, and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status. Proceedings of the National Academy of Sciences, USA 104, 19 351–19 356.
DNA methylation, insulin resistance, and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXisVOjug%3D%3D&md5=1f16b3517e66eb803954c31112a07376CAS |

Sloboda DM, Howie GJ, Pleasants A, Gluckman PD, Vickers MH (2009) Pre- and postnatal nutritional histories influence reproductive maturation and ovarian function in the rat. PLoS ONE 4, e6744
Pre- and postnatal nutritional histories influence reproductive maturation and ovarian function in the rat.Crossref | GoogleScholarGoogle Scholar | 19707592PubMed |

Sofikitis N, Giotitsas N, Tsounapi P, Baltogiannis D, Giannakis D, Pardalidis N (2008) Hormonal regulation of spermatogenesis and spermiogenesis. The Journal of Steroid Biochemistry and Molecular Biology 109, 323–330.
Hormonal regulation of spermatogenesis and spermiogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmsVeitLc%3D&md5=cccd1e76dadf86f5c6ed24813423b86dCAS | 18400489PubMed |

Sullivan TM, Micke GC, Greer RM, Irving-Rodgers HF, Rodgers RJ, Perry VEA (2009) Dietary manipulation of Bos indicus × heifers during gestation affects the reproductive development of their heifer calves. Reproduction, Fertility and Development 21, 773–784.
Dietary manipulation of Bos indicus × heifers during gestation affects the reproductive development of their heifer calves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnvVOhu7Y%3D&md5=2fda8282cdff577396eddbdd4e7367f8CAS |

Sullivan TM, Micke GC, Gree RM, Perry VEA (2010) Dietary manipulation of Bos indicus × heifers during gestation affects the prepubertal reproductive development of their bull calves. Animal Reproduction Science 118, 131–139.
Dietary manipulation of Bos indicus × heifers during gestation affects the prepubertal reproductive development of their bull calves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVGltbo%3D&md5=ae5995937971721538e027f76723602fCAS | 19671489PubMed |

Watanabe T, Ebara S, Kimura S, Maeda K, Watanabe Y, Watanabe H, Kasai S, Nakano Y (2007) Maternal vitamin B12 deficiency affects spermatogenesis at the embryonic and immature stages in rats. Congenital Anomalies 47, 9–15.
Maternal vitamin B12 deficiency affects spermatogenesis at the embryonic and immature stages in rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkvVWrtLw%3D&md5=15d5059e76338c4bcc9461afb8dd1967CAS | 17300685PubMed |

Wolff GL, Kodell RL, Moore SR, Cooney CA (1998) Maternal epigenetics and methyl supplements affect agouti gene expression in Avy/a mice. The FASEB Journal 12, 949–957.

Zambrano E, Rodríguez-González GL, Guzmán C, García-Becerra R, Boeck L, Díaz L, Menjivar M, Larrea F, Nathanielsz PW (2005) A maternal low protein diet during pregnancy and lactation in the rat impairs male reproductive development. The Journal of Physiology 563, 275–284.
A maternal low protein diet during pregnancy and lactation in the rat impairs male reproductive development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXitVSnuro%3D&md5=538e518221b2f7a17c4f6c7899b9ed3fCAS | 15611025PubMed |

Zambrano E, Guzman C, Rodriguez-Gonzalez GL, Durand-Carbajal M, Nathanielsz PW (2014) Fetal programming of sexual development and reproductive function. Molecular and Cellular Endocrinology 382, 538–549.
Fetal programming of sexual development and reproductive function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFelu7nM&md5=d3425dc3845c9dd793591c55b4779f39CAS | 24045010PubMed |