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Vertebrate reproductive science and technology
RESEARCH ARTICLE (Open Access)

Peri-conception and first trimester diet modifies reproductive development in bulls

K. J. Copping A F , M. D. Ruiz-Diaz B F , C. S. Rutland B , N. P. Mongan B , M. J. Callaghan C , I. C. McMillen D , R. J. Rodgers A and V. E. A. Perry B E
+ Author Affiliations
- Author Affiliations

A Robinson Research Institute, The University of Adelaide, Adelaide, SA 5005, Australia.

B School of Veterinary Medicine and Science, University of Nottingham, Sutton Bonington, Leicestershire, LE12 5RD, UK.

C Ridley Agriproducts, Suite 4 Level 1, 49 Sherwood Road, Toowong, Qld 4066, Australia.

D The Chancellery, University of Newcastle, Callaghan, NSW 2308, Australia.

E Corresponding author. Email: viv.perry@nottingham.ac.uk

F Denotes joint first authorship.

Reproduction, Fertility and Development 30(5) 703-720 https://doi.org/10.1071/RD17102
Submitted: 17 March 2017  Accepted: 19 September 2017   Published: 16 November 2017

Journal compilation © CSIRO 2018 Open Access CC BY-NC-ND

Abstract

Nutritional perturbation during gestation alters male reproductive development in rodents and sheep. In cattle both the developmental trajectory of the feto–placental unit and its response to dietary perturbations is dissimilar to that of these species. This study examined the effects of dietary protein perturbation during the peri-conception and first trimester periods upon reproductive development in bulls. Nulliparous heifers (n = 360) were individually fed a high- or low-protein diet (HPeri and LPeri) from 60 days before conception. From 24 until 98 days post conception, half of each treatment group changed to the alternative post-conception high- or low-protein diet (HPost and LPost) yielding four treatment groups in a 2 × 2 factorial design. A subset of male fetuses (n = 25) was excised at 98 days post conception and fetal testis development was assessed. Reproductive development of singleton male progeny (n = 40) was assessed until slaughter at 598 days of age, when adult testicular cytology was evaluated. Low peri-conception diet delayed reproductive development: sperm quality was lowered during pubertal development with a concomitant delay in reaching puberty. These effects were subsequent to lower FSH concentrations at 330 and 438 days of age. In the fetus, the low peri-conception diet increased the proportion of seminiferous tubules and decreased blood vessel area in the testis, whereas low first trimester diet increased blood vessel number in the adult testis. We conclude that maternal dietary protein perturbation during conception and early gestation may alter male testis development and delay puberty in bulls.

Additional keywords: fetal programming, morphology, puberty, testis.


References

Abd-Elmaksoud, A. (2005) ‘Morphological, Glycohistochemical, and Immunohistochemical Studies on the Embryonic and Adult Bovine Testis’. (LMU München: Munich.)

Andrade, L. P., Rhind, S. M., Rae, M. T., Kyle, C. E., Jowett, J., and Lea, R. G. (2013). Maternal undernutrition does not alter Sertoli cell numbers or the expression of key developmental markers in the mid-gestation ovine fetal testis. J. Negat. Results Biomed. 12, 2.
Maternal undernutrition does not alter Sertoli cell numbers or the expression of key developmental markers in the mid-gestation ovine fetal testis.Crossref | GoogleScholarGoogle Scholar |

Aponte, P. M., de Rooij, D. G., and Bastidas, P. (2005). Testicular development in Brahman bulls. Theriogenology 64, 1440–1455.
Testicular development in Brahman bulls.Crossref | GoogleScholarGoogle Scholar |

Ashworth, C. J., Toma, L. M., and Hunter, M. G. (2009). Nutritional effects on oocyte and embryo development in mammals: implications for reproductive efficiency and environmental sustainability. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364, 3351–3361.
Nutritional effects on oocyte and embryo development in mammals: implications for reproductive efficiency and environmental sustainability.Crossref | GoogleScholarGoogle Scholar |

Atkinson, S., and Adams, N. R. (1988). Adrenal glands alter the concentration of oestradiol-17 beta and its receptor in the uterus of ovariectomized ewes. J. Endocrinol. 118, 375–380.
Adrenal glands alter the concentration of oestradiol-17 beta and its receptor in the uterus of ovariectomized ewes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXlt1aksLg%3D&md5=60d69a394e57ebc7df0501258d94b3d8CAS |

Bagu, E. T., Cook, S., Gratton, C. L., and Rawlings, N. C. (2006). Postnatal changes in testicular gonadotropin receptors, serum gonadotropin, and testosterone concentrations and functional development of the testes in bulls. Reproduction 132, 403–411.
Postnatal changes in testicular gonadotropin receptors, serum gonadotropin, and testosterone concentrations and functional development of the testes in bulls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFCgt7%2FO&md5=04eecf36536d30f435cc1ee70aac61a2CAS |

Barb, C. R., and Kraeling, R. R. (2004). Role of leptin in the regulation of gonadotropin secretion in farm animals. Anim. Reprod. Sci. 82–83, 155–167.
Role of leptin in the regulation of gonadotropin secretion in farm animals.Crossref | GoogleScholarGoogle Scholar |

Barth, A. D., and Bowman, P. A. (1994). The sequential appearance of sperm abnormalities after scrotal insulation or dexamethasone treatment in bulls. Can. Vet. J. 35, 93–102.
| 1:STN:280:DyaK2czkvFaksQ%3D%3D&md5=eacbdc29c6436d328e0977b9329e166bCAS |

Barth, A. D., and Oko, R. J. (1989) ‘Abnormal Morphology of Bovine Spermatozoa’. 1st edn. (Iowa State University Press: Ames, IA, USA.)

Barth, A. D., and Ominski, K. H. (2000). The relationship between scrotal circumference at weaning and at one year of age in beef bulls. Can. Vet. J. 41, 541–546.
| 1:STN:280:DC%2BD3cvhvVGqsA%3D%3D&md5=d18dc5c3826279ea10e82dfd9860027bCAS |

Barth, A. D., Brito, L. F., and Kastelic, J. P. (2008). The effect of nutrition on sexual development of bulls. Theriogenology 70, 485–494.
The effect of nutrition on sexual development of bulls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnvVOksL8%3D&md5=6264dbbf9ad79413c2da1b92e340b591CAS |

Beggs, D. S., Bertram, J., Chenoweth, P. J., Entwistle, K., Fordyce, G., Johnston, H., Johnston, P., McGowan, M. R., Niethe, G., Norman, S., and Perry, V. E. A. (2013) ‘Veterinary Bull Breeding Soundness Evaluation’. (Australian Cattle Veterinarians: Brisbane.)

Bielli, A., Pérez, R., Pedrana, G., Milton, J. T. B., Lopez, Á., Blackberry, M. A., Duncombe, G., Rodriguez-Martinez, H., and Martin, G. B. (2002). Low maternal nutrition during pregnancy reduces the number of Sertoli cells in the newborn lamb. Reprod. Fertil. Dev. 14, 333–337.
Low maternal nutrition during pregnancy reduces the number of Sertoli cells in the newborn lamb.Crossref | GoogleScholarGoogle Scholar |

Blache, D., Tellam, R. L., Chagas, L. M., Blackberry, M. A., Vercoe, P. E., and Martin, G. B. (2000). Level of nutrition affects leptin concentrations in plasma and cerebrospinal fluid in sheep. J. Endocrinol. 165, 625–637.
Level of nutrition affects leptin concentrations in plasma and cerebrospinal fluid in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktl2qtrw%3D&md5=c8bb440f4c797d5a5f8b657b5f8714b3CAS |

Blache, D., Zhang, S., and Martin, G. B. (2003) Fertility in males: modulators of the acute effects of nutrition on the reproductive axis of male sheep. In ‘Reproduction in Domestic Ruminants V’. (Eds B. K. Campbell, R. Webb, H. Dobson and C. Doberska.) pp. 387–402. (Society for Reproduction and Fertility: Cambridge.)

Bortolussi, G., McIvor, J. G., Hodgkinson, J. J., Coffey, S. G., and Holmes, C. R. (2005). The northern Australian beef industry, a snapshot. 2. Breeding herd performance and management. Aust. J. Exp. Agric. 45, 1075–1091.
The northern Australian beef industry, a snapshot. 2. Breeding herd performance and management.Crossref | GoogleScholarGoogle Scholar |

Breier, B. H., Gallaher, B. W., and Gluckman, P. D. (1991). Radioimmunoassay for insulin-like growth factor-1: solutions to some potential problems and pitfalls. J. Endocrinol. 128, 347–357.
Radioimmunoassay for insulin-like growth factor-1: solutions to some potential problems and pitfalls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXhtFGiur8%3D&md5=f23a3f7c2247861de37a614d568bceeaCAS |

Brito, L. F., Silva, A. E., Unanian, M. M., Dode, M. A., Barbosa, R. T., and Kastelic, J. P. (2004). Sexual development in early- and late-maturing Bos indicus and Bos indicus × Bos taurus crossbred bulls in Brazil. Theriogenology 62, 1198–1217.
Sexual development in early- and late-maturing Bos indicus and Bos indicus × Bos taurus crossbred bulls in Brazil.Crossref | GoogleScholarGoogle Scholar |

Brito, L., Barth, A., Rawlings, N., Wilde, R., Crews, D., Mir, P., and Kastelic, J. (2007a). Circulating metabolic hormones during the peripubertal period and their association with testicular development in bulls. Reprod. Domest. Anim. 42, 502–508.
Circulating metabolic hormones during the peripubertal period and their association with testicular development in bulls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFKntLjN&md5=868826449a8b7fc58d162d75daab893bCAS |

Brito, L. F., Barth, A. D., Rawlings, N. C., Wilde, R. E., Crews, D. H., Boisclair, Y. R., Ehrhardt, R. A., and Kastelic, J. P. (2007b). Effect of feed restriction during calfhood on serum concentrations of metabolic hormones, gonadotropins, testosterone, and on sexual development in bulls. Reproduction 134, 171–181.
Effect of feed restriction during calfhood on serum concentrations of metabolic hormones, gonadotropins, testosterone, and on sexual development in bulls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpvFGisL8%3D&md5=7434793710ed9c1bdb59cedc91751668CAS |

Brito, L. F., Barth, A. D., Rawlings, N. C., Wilde, R. E., Crews, D. H., Mir, P. S., and Kastelic, J. P. (2007c). Effect of improved nutrition during calfhood on serum metabolic hormones, gonadotropins, and testosterone concentrations, and on testicular development in bulls. Domest. Anim. Endocrinol. 33, 460–469.
Effect of improved nutrition during calfhood on serum metabolic hormones, gonadotropins, and testosterone concentrations, and on testicular development in bulls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFenu73E&md5=d6726d87cf5457169e8a5b81b58fa216CAS |

Brito, L. F., Barth, A. D., Rawlings, N. C., Wilde, R. E., Crews, D. H., Mir, P. S., and Kastelic, J. P. (2007d). Effect of nutrition during calfhood and peripubertal period on serum metabolic hormones, gonadotropins and testosterone concentrations, and on sexual development in bulls. Domest. Anim. Endocrinol. 33, 1–18.
Effect of nutrition during calfhood and peripubertal period on serum metabolic hormones, gonadotropins and testosterone concentrations, and on sexual development in bulls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmtVGhu74%3D&md5=838aa9d47f553e921ff66bcd33494babCAS |

Burns, B. M., Fordyce, G., and Holroyd, R. G. (2010). A review of factors that impact on the capacity of beef cattle females to conceive, maintain a pregnancy and wean a calf – implications for reproductive efficiency in northern Australia. Anim. Reprod. Sci. 122, 1–22.
A review of factors that impact on the capacity of beef cattle females to conceive, maintain a pregnancy and wean a calf – implications for reproductive efficiency in northern Australia.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cfotFWnsA%3D%3D&md5=30dfc179d97e374b347d0e38e597ed4aCAS |

Burns, B. M., Corbet, N. J., Corbet, D. H., Crisp, J. M., Venus, B. K., Johnston, D. J., Li, Y., McGowan, M. R., and Holroyd, R. G. (2013). Male traits and herd reproductive capability in tropical beef cattle. 1. Experimental design and animal measures. Anim. Prod. Sci. 53, 87–100.
Male traits and herd reproductive capability in tropical beef cattle. 1. Experimental design and animal measures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXns12jsA%3D%3D&md5=fe4ca858268dd42d043380f468c49e05CAS |

Callaghan, M. J., McAuliffe, P., Rodgers, R. J., Hernandez-Medrano, J., and Perry, V. E. (2016). Subacute ruminal acidosis reduces sperm quality in beef bulls. J. Anim. Sci. 94, 3215–3228.
Subacute ruminal acidosis reduces sperm quality in beef bulls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhvVylt7fO&md5=19aa20511839f587e3c5ef7d0858dba3CAS |

Chagas, L. M., Gore, P. J. S., Meier, S., Macdonald, K. A., and Verkerk, G. A. (2007). Effect of monopropylene glycol on luteinizing hormone, metabolites, and postpartum anovulatory intervals in primiparous dairy cows. J. Dairy Sci. 90, 1168–1175.
Effect of monopropylene glycol on luteinizing hormone, metabolites, and postpartum anovulatory intervals in primiparous dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXitlWntLk%3D&md5=775d71a4fde63283a1e4fb62233d0e0cCAS |

Chase, C. C. J., Chenoweth, P. J., Larsen, R. E., Hammond, A. C., Olson, T. A., West, R. L., and Johnson, D. D. (2001). Growth, puberty, and carcass characteristics of Brahman-, Senepol-, and Tuli-sired F-1 Angus bulls. J. Anim. Sci. 79, 2006–2015.
Growth, puberty, and carcass characteristics of Brahman-, Senepol-, and Tuli-sired F-1 Angus bulls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmtFalsb8%3D&md5=bc6c03b70e7a85402cec9579d981f489CAS |

Chavatte-Palmer, P., Dupont, C., Debus, N., and Camous, S. (2014). Nutritional programming and the reproductive function of the offspring. Anim. Prod. Sci. 54, 1166–1176.
Nutritional programming and the reproductive function of the offspring.Crossref | GoogleScholarGoogle Scholar |

Copping, K. J., Hoare, A., Callaghan, M., McMillen, I. C., Rodgers, R. J., and Perry, V. E. A. (2014). Fetal programming in 2-year-old calving heifers: peri-conception and first trimester protein restriction alters fetal growth in a gender-specific manner. Anim. Prod. Sci. 54, 1333–1337.
Fetal programming in 2-year-old calving heifers: peri-conception and first trimester protein restriction alters fetal growth in a gender-specific manner.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtlaktLnP&md5=67f5ddbb0bf064f0e48884743e8ac3c9CAS |

Corbet, N. J., Burns, B. M., Johnston, D. J., Wolcott, M. L., Corbet, D. H., Venus, B. K., Li, Y., McGowan, M. R., and Holroyd, R. G. (2013). Male traits and herd reproductive capability in tropical beef cattle. 2. Genetic parameters of bull traits. Anim. Prod. Sci. 53, 101–113.
Male traits and herd reproductive capability in tropical beef cattle. 2. Genetic parameters of bull traits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXns12jtg%3D%3D&md5=69fb8deca5691ccb5eb879d8e7c4d85dCAS |

Da Silva, P., Aitken, R. P., Rhind, S. M., Racey, P. A., and Wallace, J. M. (2001). Influence of placentally mediated fetal growth restriction on the onset of puberty in male and female lambs. Reproduction 122, 375–383.
Influence of placentally mediated fetal growth restriction on the onset of puberty in male and female lambs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXntVGksLY%3D&md5=202df959223f9b13cab399913dcde5dcCAS |

Da Silva, P., Aitken, R. P., Rhind, S. M., Racey, P. A., and Wallace, J. M. (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=e73873dc961a5ea9fde813cbc27fdc48CAS |

Dupont, C., Cordier, A. G., Junien, C., Mandon-Pepin, B., Levy, R., and 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=03e798dbcd50d526125043beab544a58CAS |

Edwards, L. J., and McMillen, I. C. (2002). Impact of maternal undernutrition during the periconceptional period, fetal number, and fetal sex on the development of the hypothalamo–pituitary adrenal axis in sheep during late gestation. Biol. Reprod. 66, 1562–1569.
Impact of maternal undernutrition during the periconceptional period, fetal number, and fetal sex on the development of the hypothalamo–pituitary adrenal axis in sheep during late gestation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjtFWnsLY%3D&md5=9b313af949889ebb8305e46892d4a077CAS |

Entwistle, K. W., and Fordyce, G. (2003) ‘Evaluating and Reporting Bull Fertility’. (Australian Association of Cattle Veterinarians: Eight Mile Plains, Qld, Australia)

Evans, A. C. O., Davies, F. J., Nasser, L. F., Bowman, P., and Rawlings, N. C. (1995). Differences in early patterns of gonadotrophin secretion between early and late maturing bulls, and changes in semen characteristics at puberty. Theriogenology 43, 569–578.
Differences in early patterns of gonadotrophin secretion between early and late maturing bulls, and changes in semen characteristics at puberty.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXksVOgtr4%3D&md5=21091a25524d94fde6a5b491f493f7d8CAS |

Evans, A. C., Pierson, R. A., Garcia, A., McDougall, L. M., Hrudka, F., and Rawlings, N. C. (1996). Changes in circulating hormone concentrations, testes histology and testes ultrasonography during sexual maturation in beef bulls. Theriogenology 46, 345–357.
Changes in circulating hormone concentrations, testes histology and testes ultrasonography during sexual maturation in beef bulls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XlsVShsb4%3D&md5=4ea10e470a39272450be8c623f3472eeCAS |

Fair, T. (2010). Mammalian oocyte development: checkpoints for competence. Reprod. Fertil. Dev. 22, 13–20.
Mammalian oocyte development: checkpoints for competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitlagurg%3D&md5=9b3fe3fd237a07bd06aefffc4b1264ecCAS |

Fields, M. J., Hentges, J. F., and Cornelisse, K. W. (1982). Aspects of the sexual development of Brahman versus Angus bulls in Florida. Theriogenology 18, 17–31.
Aspects of the sexual development of Brahman versus Angus bulls in Florida.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283pvVCqtA%3D%3D&md5=513070772562310c8242fb8fc73290b8CAS |

Fordyce, G., Entwistle, K., Norman, S., Perry, V., Gardiner, B., and Fordyce, P. (2006). Standardising bull breeding soundness evaluations and reporting in Australia. Theriogenology 66, 1140–1148.
Standardising bull breeding soundness evaluations and reporting in Australia.Crossref | GoogleScholarGoogle Scholar |

Freer, M. (2007) ‘Nutrient Requirements of Domesticated Ruminants’. (CSIRO Publishing: Collingwood, Vic., Australia.)

Gardner, D. S., Van Bon, B. W., Dandrea, J., Goddard, P. J., May, S. F., Wilson, V., Stephenson, T., and Symonds, M. E. (2006). Effect of periconceptional undernutrition and gender on hypothalamic–pituitary–adrenal axis function in young adult sheep. J. Endocrinol. 190, 203–212.
Effect of periconceptional undernutrition and gender on hypothalamic–pituitary–adrenal axis function in young adult sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xpt1Wjtrc%3D&md5=9cd58d3c31009894cc15b93fde2306b7CAS |

Godinho, H., Cardoso, M., and Nogueria, J. (1973). Patterns of parenchymal ramification of the testicular artery in some ruminants. Anat. Anz. 133, 118–124.
| 1:STN:280:DyaE3s3htF2jsg%3D%3D&md5=7bb725642510bd79b23a5799e1377d76CAS |

Griswold, M. D., and McLean, D. J. (2006) The Sertoli cell. In ‘Knobil and Neill’s Physiology of Reproduction.’ (Ed. J. D. Neill.) pp. 949–975. (Elsevier: New York.)

Grover, A., Smith, C. E., Gregory, M., Cyr, D. G., Sairam, M. R., and Hermo, L. (2005). Effects of FSH receptor deletion on epididymal tubules and sperm morphology, numbers, and motility. Mol. Reprod. Dev. 72, 135–144.
Effects of FSH receptor deletion on epididymal tubules and sperm morphology, numbers, and motility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXnt1ygu7w%3D&md5=8aca452e6bc5c5208dbab48cf2915fd2CAS |

Hernandez-Medrano, J. H., Copping, K. J., Hoare, A., Wapanaar, W., Grivell, R., Kuchel, T., Miguel-Pacheco, G., McMillen, I. C., Rodgers, R. J., and Perry, V. E. (2015). Gestational dietary protein is associated with sex specific decrease in blood flow, fetal heart growth and post-natal blood pressure of progeny. PLoS One 10, e0125694.
Gestational dietary protein is associated with sex specific decrease in blood flow, fetal heart growth and post-natal blood pressure of progeny.Crossref | GoogleScholarGoogle Scholar |

Holroyd, R. G., Doogan, V. J., DeFaveri, J., Fordyce, G., McGowane, M. R., Bertram, J. D., Vankang, D. M., Fitzpatrick, L. A., Jayawardhanai, G. A., and Miller, R. G. (2002). Bull selection and use in northern Australia 4. Calf output and predictors of fertility of bulls in multiple-sire herds. Anim. Reprod. Sci. 71, 67–79.
Bull selection and use in northern Australia 4. Calf output and predictors of fertility of bulls in multiple-sire herds.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD383kvFSrtw%3D%3D&md5=2f09a9b085dbafc60fb901f00108edd5CAS |

Hopper, R. M. (2014) ‘Bovine Reproduction’. 1st edn. (John Wiley & Sons, Inc.: Ames, IA, USA.)

Jégou, B. (1992). The Sertoli cell in vivo and in vitro. Cell Biol. Toxicol. 8, 49–54.
The Sertoli cell in vivo and in vitro.Crossref | GoogleScholarGoogle Scholar |

Kaneko, H., Noguchi, J., Kikuchi, K., Akagi, S., Shimada, A., Taya, K., Watanabe, G., and Hasegawa, Y. (2001). Production and endocrine role of inhibin during the early development of bull calves. Biol. Reprod. 65, 209–215.
Production and endocrine role of inhibin during the early development of bull calves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkslWhtbk%3D&md5=2780502270000498a3856c4987c672a3CAS |

Klonisch, T., Fowler, P. A., and Hombach-Klonisch, S. (2004). Molecular and genetic regulation of testis descent and external genitalia development. Dev. Biol. 270, 1–18.
Molecular and genetic regulation of testis descent and external genitalia development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjsl2gt7w%3D&md5=d7683271608743f6d4b02fb868e67500CAS |

Knight, P. G., Muttukrishna, S., and Groome, N. P. (1996). Development and application of a two-site enzyme immunoassay for the determination of ‘total’ activin-A concentrations in serum and follicular fluid. J. Endocrinol. 148, 267–279.
Development and application of a two-site enzyme immunoassay for the determination of ‘total’ activin-A concentrations in serum and follicular fluid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XhtVCrsrg%3D&md5=c2fcf3f024e28b1b5903af4db4491212CAS |

Kotsampasi, B., Balaskas, C., Papadomichelakis, G., and Chadio, S. E. (2009). Reduced Sertoli cell number and altered pituitary responsiveness in male lambs undernourished in utero. Anim. Reprod. Sci. 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=de3622544aa6b3e3b1bbcf7e009f1fe7CAS |

Lunstra, D. D., and Echternkamp, S. E. (1982). Puberty in beef bulls: acrosome morphology and semen quality in bulls of different breeds. J. Anim. Sci. 55, 638–648.
Puberty in beef bulls: acrosome morphology and semen quality in bulls of different breeds.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3s%2FjtVGmuw%3D%3D&md5=a48d3563465d1d464b47f262eaffff22CAS |

Lunstra, D. D., Ford, J. J., and Echternkamp, S. E. (1978). Puberty in beef bulls: hormone concentrations, growth, testicular development, sperm production and sexual aggressiveness in bulls of different breeds. J. Anim. Sci. 46, 1054–1062.
Puberty in beef bulls: hormone concentrations, growth, testicular development, sperm production and sexual aggressiveness in bulls of different breeds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXksVSjsLo%3D&md5=ca757ca7cf56c1c555b1db753f209656CAS |

Mather, J. P., Woodruff, T. K., and Krummen, L. A. (1992). Paracrine regulation of reproductive function by inhibin and activin. Proc. Soc. Exp. Biol. Med. 201, 1–15.
Paracrine regulation of reproductive function by inhibin and activin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XmtVGgsrk%3D&md5=af91bbc4ffbbd2aeca9860dadcc3637fCAS |

Matsuzaki, S., Uenoyama, Y., Okuda, K., Watanabe, G., Kitamura, N., Taya, K., and Yamada, J. (2000). Age-related changes in the serum levels of inhibin, FSH, LH and testosterone in Holstein bulls. J. Reprod. Dev. 46, 245–248.
Age-related changes in the serum levels of inhibin, FSH, LH and testosterone in Holstein bulls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnvV2qs7Y%3D&md5=6a219055bd631145633c1ed58d8b65a6CAS |

Mayhew, T. M. (1991). The new stereological methods for interpreting functional morphology from slices of cells and organs. Exp. Physiol. 76, 639–665.
The new stereological methods for interpreting functional morphology from slices of cells and organs.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK38%2FnsFanuw%3D%3D&md5=ce3f3db4ebb723b787039eb326183483CAS |

Mayhew, T. M. (2011). Mapping the distributions and quantifying the labelling intensities of cell compartments by immunoelectron microscopy: progress towards a coherent set of methods. J. Anat. 219, 647–660.
Mapping the distributions and quantifying the labelling intensities of cell compartments by immunoelectron microscopy: progress towards a coherent set of methods.Crossref | GoogleScholarGoogle Scholar |

McAuliffe, P., Johnston, H., Johnston, P., and Perry, V. (2010). ‘Electroejaculators, Morphology and Microscopes’. (The Australian Cattle Veterinarians: Eight Mile Plains, Qld, Australia.)

McLachlan, R. I., Robertson, D. M., Burger, H. G., and de Kretser, D. M. (1986). The radioimmunoassay of bovine and human follicular fluid and serum inhibin. Mol. Cell. Endocrinol. 46, 175–185.
The radioimmunoassay of bovine and human follicular fluid and serum inhibin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XkvFWnu70%3D&md5=eb5b4c922c03f405a111d963d42d3496CAS |

McMillen, I. C., and Robinson, J. S. (2005). Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol. Rev. 85, 571–633.
Developmental origins of the metabolic syndrome: prediction, plasticity, and programming.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjt12lsLw%3D&md5=5055c371085737e166335faf9a33ad88CAS |

McMillen, I. C., MacLaughlin, S. M., Muhlhausler, B. S., Gentili, S., Duffield, J. L., and Morrison, J. L. (2008). Developmental origins of adult health and disease: the role of periconceptional and foetal nutrition. Basic Clin. Pharmacol. Toxicol. 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=b7850b6d0c8bf0859b90d5316f1a8bb1CAS |

Micke, G. C., Sullivan, T. M., Gatford, K. L., Owens, J. A., and Perry, V. E. (2010). Nutrient intake in the bovine during early and mid-gestation causes sex-specific changes in progeny plasma IGF-I, liveweight, height and carcass traits. Anim. Reprod. Sci. 121, 208–217.
Nutrient intake in the bovine during early and mid-gestation causes sex-specific changes in progeny plasma IGF-I, liveweight, height and carcass traits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtV2hsrrE&md5=287a6ca6c483242f79fd844dd68220ebCAS |

Micke, G. C., Sullivan, T. M., McMillen, I. C., Gentili, S., and Perry, V. E. (2011). Heifer nutrient intake during early- and mid-gestation programs adult offspring adiposity and mRNA expression of growth-related genes in adipose depots. Reproduction 141, 697–706.
Heifer nutrient intake during early- and mid-gestation programs adult offspring adiposity and mRNA expression of growth-related genes in adipose depots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmvFCis78%3D&md5=bb9ea69900d59ce658310aea77e13159CAS |

Micke, G. C., Sullivan, T. M., Kennaway, D. J., Hernandez-Medrano, J., and Perry, V. E. (2015). Maternal endocrine adaptation throughout pregnancy to nutrient manipulation: consequences for sexually dimorphic programming of thyroid hormones and development of their progeny. Theriogenology 83, 604–615.
Maternal endocrine adaptation throughout pregnancy to nutrient manipulation: consequences for sexually dimorphic programming of thyroid hormones and development of their progeny.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvFKmsb7F&md5=d3e50885502b4ac3571c7f15064574f7CAS |

Mossa, F., Carter, F., Walsh, S. W., Kenny, D. A., Smith, G. W., Ireland, J. L. H., Hildebrandt, T. B., Lonergan, P., Ireland, J. J., and Evans, A. C. O. (2013). Maternal undernutrition in cows impairs ovarian and cardiovascular systems in their offspring. Biol. Reprod. 88, 92.
Maternal undernutrition in cows impairs ovarian and cardiovascular systems in their offspring.Crossref | GoogleScholarGoogle Scholar |

Mossa, F., Walsh, S. W., Ireland, J. J., and Evans, A. C. O. (2015). Early nutritional programming and progeny performance: is reproductive success already set at birth? Anim. Front. 5, 18–24.
Early nutritional programming and progeny performance: is reproductive success already set at birth?Crossref | GoogleScholarGoogle Scholar |

Moura, A. A., and Erickson, B. H. (1997). Age-related changes in peripheral hormone concentrations and their relationships with testis size and number of Sertoli and germ cells in yearling beef bulls. J. Reprod. Fertil. 111, 183–190.
Age-related changes in peripheral hormone concentrations and their relationships with testis size and number of Sertoli and germ cells in yearling beef bulls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlsFelsQ%3D%3D&md5=b8b5753c1f0010bfee2096c0a7eabf22CAS |

Norman, M. (1963). Dry season protein and energy supplements for beef cattle on native pastures at Katherine, N.T. Aust. J. Exp. Agric. 3, 280–283.
Dry season protein and energy supplements for beef cattle on native pastures at Katherine, N.T.Crossref | GoogleScholarGoogle Scholar |

O’Shaughnessy, P. J. (2014). Hormonal control of germ cell development and spermatogenesis. Semin. Cell Dev. Biol. 29, 55–65.
Hormonal control of germ cell development and spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXksFWms7g%3D&md5=f9b16f9cc07a8569d214d3e35d2d7e12CAS |

O’Shaughnessy, P. J., and Fowler, P. A. (2011). Endocrinology of the mammalian fetal testis. Reproduction 141, 37–46.
Endocrinology of the mammalian fetal testis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXisVehs78%3D&md5=3114961b9b2fda2755c3a78d26a263e2CAS |

Perry, V. E. A., Munro, R. K., Chenoweth, P. J., Bodero, D. A. V., and Post, T. B. (1990). Relationships among bovine male and female reproductive traits. Aust. Vet. J. 67, 4–5.
Relationships among bovine male and female reproductive traits.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3c3ktFWjtA%3D%3D&md5=03e9d8e9daba7a4d8aca1e2a0dad866aCAS |

Perry, V. E. A., Chenoweth, P. J., Post, T. B., and Munro, R. K. (1991). Patterns of development of gonads, sex-drive and hormonal responses in tropical beef bulls. Theriogenology 35, 473–486.
Patterns of development of gonads, sex-drive and hormonal responses in tropical beef bulls.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283pvFKrsg%3D%3D&md5=a7388be421dfe4d0ec34744f9842307cCAS |

Polguj, M., Wysiadecki, G., Podgorski, M., Szymanski, J., Olbrych, K., Olewnik, L., and Topol, M. (2015). Morphological variations of intra-testicular arterial vasculature in bovine testis – a corrosion casting study. BMC Vet. Res. 11, 263.
Morphological variations of intra-testicular arterial vasculature in bovine testis – a corrosion casting study.Crossref | GoogleScholarGoogle Scholar |

Rae, M. T., Kyle, C. E., Miller, D. W., Hammond, A. J., Brooks, A. N., and Rhind, S. M. (2002). The effects of undernutrition, in utero, on reproductive function in adult male and female sheep. Anim. Reprod. Sci. 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=e1326288eed29faa7518bc0ba8274fb8CAS |

Rawlings, N. C., Fletcher, P. W., Henricks, D. M., and Hill, J. R. (1978). Plasma luteinizing hormone (LH) and testosterone levels during sexual maturation in beef bull calves Biol. Reprod. 19, 1108–1112.
Plasma luteinizing hormone (LH) and testosterone levels during sexual maturation in beef bull calvesCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXhtFyrurk%3D&md5=b010b4e2a8e4c90b198816eb0cedf8adCAS |

Rawlings, N., Evans, A. C., Chandolia, R. K., and Bagu, E. T. (2008). Sexual maturation in the bull. Reprod. Domest. Anim. 43, 295–301.
Sexual maturation in the bull.Crossref | GoogleScholarGoogle Scholar |

Rey, R., and Josso, N. (1996). Regulation of testicular anti-Müllerian hormone secretion. Eur. J. Endocrinol. 135, 144–152.
Regulation of testicular anti-Müllerian hormone secretion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XlsVOgs78%3D&md5=e3120b84a730c337f9a85fb875777bb1CAS |

Rey, R., Lukas-Croisier, C., Lasala, C., and Bedecarrás, P. (2003). AMH/MIS: what we know already about the gene, the protein and its regulation. Mol. Cell. Endocrinol. 211, 21–31.
AMH/MIS: what we know already about the gene, the protein and its regulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXptlOrsL0%3D&md5=410d951d8fbaaae8e2c8c5278ab5fc01CAS |

Robertson, D. M., Foulds, L. M., Prisk, M., and Hedger, M. P. (1992). Inhibin/activin β-subunit monomer: isolation and characterization. Endocrinology 130, 1680–1687.
| 1:CAS:528:DyaK38Xhs1Kmt74%3D&md5=e0ad7d7e4e4047077a9e91478110675bCAS |

Rodríguez-González, G. L., Reyes-Castro, L. A., Vega, C. C., Boeck, L., Ibáñez, C., Nathanielsz, P. W., Larrea, F., and Zambrano, E. (2014). Accelerated aging of reproductive capacity in male rat offspring of protein-restricted mothers is associated with increased testicular and sperm oxidative stress. Age (Dordr.) 36, 9721.
Accelerated aging of reproductive capacity in male rat offspring of protein-restricted mothers is associated with increased testicular and sperm oxidative stress.Crossref | GoogleScholarGoogle Scholar |

Ross, D. G., Bowles, J., Hope, M., Lehnert, S., and Koopman, P. (2009). Profiles of gonadal gene expression in the developing bovine embryo. Sex Dev. 3, 273–283.
Profiles of gonadal gene expression in the developing bovine embryo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFaqtrvE&md5=e56c0a4177f1613a0dcfb62c72dceb5aCAS |

Rota, A., Ballarin, C., Vigier, B., Cozzi, B., and Rey, R. (2002). Age dependent changes in plasma anti-Müllerian hormone concentrations in the bovine male, female, and freemartin from birth to puberty: relationship between testosterone production and influence on sex differentiation. Gen. Comp. Endocrinol. 129, 39–44.
Age dependent changes in plasma anti-Müllerian hormone concentrations in the bovine male, female, and freemartin from birth to puberty: relationship between testosterone production and influence on sex differentiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XotFGhu7k%3D&md5=2657c64742f35cc76a95b87cf3ca6339CAS |

Sharpe, R. M., McKinnell, C., Kivlin, C., and Fisher, J. S. (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=25d41a1e73758453519bbf502574169cCAS |

Sinclair, K. D., Rutherford, K. M., Wallace, J. M., Brameld, J. M., Stoger, R., Alberio, R., Sweetman, D., Gardner, D. S., Perry, V. E., Adam, C. L., Ashworth, C. J., Robinson, J. E., and Dwyer, C. M. (2016). Epigenetics and developmental programming of welfare and production traits in farm animals. Reprod. Fertil. Dev. 28, 1443–1478.
Epigenetics and developmental programming of welfare and production traits in farm animals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xhtl2msbbK&md5=159023c5e0742ac0b883c533fd076ecaCAS |

Spencer, T. E., and Hansen, T. R. (2015). Implantation and establishment of pregnancy in ruminants. In ‘Regulation of Implantation and Establishment of Pregnancy in Mammals: Tribute to 45-Year Anniversary of Roger V. Short’s “Maternal Recognition of Pregnancy”. Advances in Anatomy, Embryology and Cell Biology 216’. (Eds R. D. Geisert and F. W. Bazer.) pp. 105–135. (Springer International Publishing: Cham.)

Sullivan, T. M., Micke, G. C., Greer, R. M., Irving-Rodgers, H. F., Rodgers, R. J., and Perry, V. E. (2009a). Dietary manipulation of Bos indicus × heifers during gestation affects the reproductive development of their heifer calves. Reprod. Fertil. Dev. 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=8aa8f27b90f08b628438cebda4c281c3CAS |

Sullivan, T. M., Micke, G. C., Magalhaes, R. S., Phillips, N. J., and Perry, V. E. (2009b). Dietary protein during gestation affects placental development in heifers. Theriogenology 72, 427–438.
Dietary protein during gestation affects placental development in heifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptl2nsr4%3D&md5=2d4ebbf970e29b7bb7bdb6dfedd4e7a5CAS |

Sullivan, T. M., Micke, G. C., Greer, R. M., and Perry, V. E. (2010). Dietary manipulation of Bos indicus × heifers during gestation affects the prepubertal reproductive development of their bull calves. Anim. Reprod. Sci. 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=cbca06ba06ba451ccfef1c0878eef75eCAS |

Toledo, F. C., Perobelli, J. E., Pedrosa, F. P., Anselmo-Franci, J. A., and Kempinas, W. D. (2011). In utero protein restriction causes growth delay and alters sperm parameters in adult male rats. Reprod. Biol. Endocrinol. 9, 94.
In utero protein restriction causes growth delay and alters sperm parameters in adult male rats.Crossref | GoogleScholarGoogle Scholar |

Vergouwen, R. P. F. A., Jacobs, S. G. P. M., Huiskamp, R., Davids, J. A. G., and de Rooij, D. G. (1991). Proliferative activity of gonocytes, Sertoli cells and interstitial cells during testicular development in mice. J. Reprod. Fertil. 93, 233–243.
Proliferative activity of gonocytes, Sertoli cells and interstitial cells during testicular development in mice.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK38%2FhsFSmsg%3D%3D&md5=65fb9defd824e3e32adf2e130bc90eb3CAS |

Wathes, D. C., and Wooding, F. B. (1980). An electron microscope study of implantation in the cow. Am. J. Anat. 159, 285–306.
An electron microscope study of implantation in the cow.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3M7ls12qtQ%3D%3D&md5=a3b840d281483722bcaa31212873f42aCAS |

Wolf, F. R., Almquist, J. O., and Hale, E. B. (1965). Prepubertal behavior and pubertal characteristics of beef bulls on high nutrient allowance. J. Anim. Sci. 24, 761–765.
Prepubertal behavior and pubertal characteristics of beef bulls on high nutrient allowance.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaF2M7hvVequw%3D%3D&md5=f1d1aba1de0516dc222e5be700ad2d20CAS |

Wooding, F. B. P., and Flint, A. P. F. (1994). Placentation. In ‘Marshall’s Physiology of Reproduction’. 4th edn. (Ed. G. E. Lamming.) pp. 233–460. (Chapman & Hall: London.)

Wrobel, K. H. (2000). Prespermatogenesis and spermatogoniogenesis in the bovine testis. Anat. Embryol. (Berl.) 202, 209–222.
Prespermatogenesis and spermatogoniogenesis in the bovine testis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3cvksVKhsg%3D%3D&md5=89bb62e82940ab6e65864eb6942af187CAS |

Wrobel, K.-H., Sinowatz, F., and Mademann, R. (1981). Intratubular topography in the bovine testis. Cell Tissue Res. 217, 289–310.
Intratubular topography in the bovine testis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3M3htVWmuw%3D%3D&md5=258c982bb2dd59d8ea1a44a00c213679CAS |

Yilmaz, A., Davis, M. E., and Simmen, R. C. (2006). Analysis of female reproductive traits in Angus beef cattle divergently selected for blood serum insulin-like growth factor I concentration. Theriogenology 65, 1180–1190.
Analysis of female reproductive traits in Angus beef cattle divergently selected for blood serum insulin-like growth factor I concentration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XitVKjsrw%3D&md5=8eb9363c56f1e949d958a550faf47854CAS |

Zambrano, E., Rodriguez-Gonzalez, G. L., Guzman, C., Garcia-Becerra, R., Boeck, L., Diaz, L., Menjivar, M., Larrea, F., and Nathanielsz, P. W. (2005). A maternal low protein diet during pregnancy and lactation in the rat impairs male reproductive development. J. Physiol. 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=211834c81ec652953060c6ea7a310692CAS |

Zieba, D. A., Amstalden, M., and Williams, G. L. (2005). Regulatory roles of leptin in reproduction and metabolism: a comparative review. Domest. Anim. Endocrinol. 29, 166–185.
Regulatory roles of leptin in reproduction and metabolism: a comparative review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXltVehu70%3D&md5=5a6fc0a29aebb59852835d4c972ce253CAS |