Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Testicular parameters and spermatogenesis in different birthweight boars

P. A. Auler A , G. H. F. A. Moreira B , C. O. Hogg C , C. J. Ashworth C , F. P. Bortolozzo D , H. Chiarini-Garcia A and F. R. C. L. Almeida A E

A Biological Sciences Institute, Federal University of Minas Gerais, Av. Antônio Carlos 6627, 31.270-901, Belo Horizonte, MG, Brazil.

B Veterinary School, Federal University of Minas Gerais, Av. Antônio Carlos 6627, 31.270-901, Belo Horizonte, MG, Brazil.

C The Roslin Institute and Royal (Dyck) School of Veterinary Studies, University of Edinburgh, Easter Bush, Midlothian, EH25 9RG, UK.

D Faculty of Veterinary, Federal University of Rio Grande do Sul, Av. Bento Gonçalves 9090, 91.540-000, Porto Alegre, RS, Brazil.

E Corresponding author. Email: falmeida@icb.ufmg.br

Reproduction, Fertility and Development - https://doi.org/10.1071/RD16164
Submitted: 20 April 2016  Accepted: 23 August 2016   Published online: 28 September 2016

Abstract

The present study investigated the effect of birthweight on testicular development and spermatogenesis in boars. Twenty-four pairs of littermate boars were selected: one piglet with the highest birthweight (HW) and the other with the lowest birthweight (LW) within the litter. Two subsets of 12 pairs of male littermates from each birthweight group were obtained after selection: one subset was orchiectomised at 8 days and the other at 8 months of age. HW boars had higher body and testicular weights at both ages (P < 0.05). Testosterone concentrations and the relative expression of 17α-hydroxylase in the testis were similar between birthweight groups. Birthweight affected somatic and germ cell numbers in the neonatal testis, which were higher in HW boars (P < 0.05). Moreover, a significant reduction in the number of pachytene spermatocytes and round spermatids was observed in LW boars (P < 0.05) at 8 months of age, which caused a decrease in the total number of elongated spermatids and daily sperm production (P < 0.05). Hence, HW boars have the potential to produce more spermatozoa and consequently more semen doses per ejaculate, and would be very valuable to an industry that relies on AI.

Additional keyword: testis.


References

Abercrombie, M. (1946). Estimation of nuclear populations from microtome sections. Anat. Rec. 94, 239–247.
Estimation of nuclear populations from microtome sections.CrossRef | 1:STN:280:DyaH28%2FjtlOisQ%3D%3D&md5=036a771ddd37ccb6809e10e110874a57CAS | 21015608PubMed | open url image1

Almeida, F. R. C. L., Alvarenga, A. L. N., Foxcroft, G. R., and Chiarini-Garcia, H. (2009). Birth weight implications for reproductive parameters in boars. In ADSA-CSAS-ASAS Joint Annual Meeting, Montreal. J. Anim. Sci. 87, 195. open url image1

Alvarenga, A. L. N., Chiarini-Garcia, H., Cardeal, P. C., Moreira, L. P., Foxcroft, G. R., Fontes, D. O., and Almeida, F. R. C. L. (2013). Intra-uterine growth retardation affects birthweight and postnatal development in pigs, impairing muscle accretion, duodenal mucosa morphology and carcass traits. Reprod. Fertil. Dev. 25, 387–395.
Intra-uterine growth retardation affects birthweight and postnatal development in pigs, impairing muscle accretion, duodenal mucosa morphology and carcass traits.CrossRef | 1:STN:280:DC%2BC38bos1Gltg%3D%3D&md5=b36e842f49762f7584cc29197bb92b1aCAS | open url image1

Amann, R. P., and Almquist, J. O. (1962). Reproductive capacity of dairy bulls. VIII. Direct and indirect measurement of testicular sperm production. J. Dairy Sci. 45, 774–781.
Reproductive capacity of dairy bulls. VIII. Direct and indirect measurement of testicular sperm production.CrossRef | open url image1

Ashworth, C. J., Hogg, C. O., Hoeks, C. W. F., Donald, R. D., Duncan, W. C., Lawrence, A. B., and Rutherford, K. M. D. (2011). Pre-natal social stress and post-natal pain affect the developing pig reproductive axis. Reproduction 142, 907–914.
Pre-natal social stress and post-natal pain affect the developing pig reproductive axis.CrossRef | 1:CAS:528:DC%2BC3MXhs1GqtLbL&md5=c51a0e1e3a6c7436a3f96e8e3cc09405CAS | 21984747PubMed | open url image1

Beaulieu, A. D., Aalhus, J. L., Williams, N. H., and Patience, J. F. (2010). Impact of piglet birth weight, birth order, and litter size on subsequent growth performance, carcass quality, muscle composition, and eating quality of pork. J. Anim. Sci. 88, 2767–2778.
Impact of piglet birth weight, birth order, and litter size on subsequent growth performance, carcass quality, muscle composition, and eating quality of pork.CrossRef | 1:CAS:528:DC%2BC3cXpvVOrt7o%3D&md5=c8229f42a2fb4fdd49395d76981446c4CAS | 20418451PubMed | open url image1

Chiarini-Garcia, H., Parreira, G. G., and Almeida, F. R. C. L. (2011). Glycolmethacrylate embedding for improved morphological, morphometrical and immunohistochemical investigations under light microscopy: testes as a model. In ‘Light Microscopy: Methods and Protocols’. (Eds H. Chiarini-Garcia and R. C. N. Melo.) pp. 3–18. (Humana Press: Totowa, NJ.)

Drumond, A. L., Meistrich, M. L., and Chiarini-Garcia, H. (2011a). Spermatogonial morphology and kinetics during testis development in mice: a high-resolution light microscopy approach. Reproduction 142, 145–155.
Spermatogonial morphology and kinetics during testis development in mice: a high-resolution light microscopy approach.CrossRef | 1:CAS:528:DC%2BC3MXhtFSqu7zL&md5=5fc6cf8e1b0483c96c67359ef7d6db51CAS | 21521798PubMed | open url image1

Drumond, A. L., Weng, C. C., Wang, G., Chiarini-Garcia, H., Eras-Garcia, L., and Meistrich, M. L. (2011b). Effects of multiple doses of cyclophosphamide on mouse testes: accessing the germ cells lost, and the functional damage of stem cells. Reprod. Toxicol. 32, 395–406.
Effects of multiple doses of cyclophosphamide on mouse testes: accessing the germ cells lost, and the functional damage of stem cells.CrossRef | 1:CAS:528:DC%2BC3MXhsFegtrnL&md5=a1c53cff15ce9e8ed70d6ae59940d6c2CAS | 22001253PubMed | open url image1

Foxcroft, G. R., Dixon, W. T., Novak, S., Outman, C. T., Town, S. C., and Vinsky, M. D. (2006). The biological basis for prenatal programming of postnatal performance in pigs. J. Anim. Sci. 84, E105–E112.
The biological basis for prenatal programming of postnatal performance in pigs.CrossRef | 16582081PubMed | open url image1

França, L. R., and Cardoso, F. M. (1998). Duration of spermatogenesis and sperm transit time through the epididymis in the Piau boar. Tissue Cell 30, 573–582.
Duration of spermatogenesis and sperm transit time through the epididymis in the Piau boar.CrossRef | 9839480PubMed | open url image1

França, L. R., and Russell, L. D. (1998).The testis of domestic mammals. In ‘Male Reproduction: A Multidisciplinary Overview’. (Eds F. Martinez-Garcia and J. Regadera.) pp. 198–219. (Churchill Communications: Madrid.)

França, L. R., Avelar, G. F., and Almeida, F. F. L. (2005). Spermatogenesis and sperm transit through the epididymis in mammals with emphasis on pigs. Theriogenology 63, 300–318.
Spermatogenesis and sperm transit through the epididymis in mammals with emphasis on pigs.CrossRef | 15626401PubMed | open url image1

Gondret, F., Lefaucheur, L., Juin, H., Louveau, I., and Lebret, B. (2006). Low birth weight is associated with enlarged muscle fiber area and impaired meat tenderness of the longissimus muscle in pigs. J. Anim. Sci. 84, 93–103.
Low birth weight is associated with enlarged muscle fiber area and impaired meat tenderness of the longissimus muscle in pigs.CrossRef | 1:CAS:528:DC%2BD28XjvFynuw%3D%3D&md5=f4c7f99088484b9b1e87961a5b881712CAS | 16361495PubMed | open url image1

Hernandez, S. C., Hogg, C. O., Billion, Y., Sanchez, M., Bidanel, J., Haley, C. S., Archibald, A. L., and Ashworth, C. J. (2013). Secreted phosphoprotein I expression in endometrium and placental tissues of hyperprolific Large White and Meishan gilts. Biol. Reprod. 88, 120.
Secreted phosphoprotein I expression in endometrium and placental tissues of hyperprolific Large White and Meishan gilts.CrossRef | 23575146PubMed | open url image1

Knox, R. V. (2014). Impact of swine reproductive technologies on pig and global food production. In ‘Current and Future Reproductive Technologies and World Food Production’. (Eds G.C. Lamb and N. DiLorenzo.) pp. 131–160 (Springer: New York.)

Knox, R. V. (2016). Artificial insemination in pigs today. Theriogenology 85, 83–93.
Artificial insemination in pigs today.CrossRef | 1:STN:280:DC%2BC287gvFSjtA%3D%3D&md5=dab4fd2f3e556913f52d5c8f3ba233f5CAS | 26253434PubMed | open url image1

Lin, Y., Cheng, X., Sutovsky, P., Wu, D., Che, L. Q., Fang, Z. F., Xu, S. Y., Ren, B., and Dong, H. J. (2015). Effect of intra-uterine growth restriction on long-term fertility in boars. Reprod. Fertil. Dev. , .
Effect of intra-uterine growth restriction on long-term fertility in boars.CrossRef | 26293651PubMed | open url image1

Majdic, G., Sharpe, R. M., O’Shaughnessey, P. J., and Saunders, P. T. (1996). Expression of cytochrome P450 17alpha-hydroxylase/C17–20 lyase in the fetal rat testis is reduced my maternal exposure to exogenous estrogens. Endocrinology 137, 1063–1070.
| 1:CAS:528:DyaK28Xht1Kju74%3D&md5=acdd59d4024a35d73eb72a926262da01CAS | 8603575PubMed | open url image1

Martin-Gronert, M. S., and Ozanne, S. E. (2006). Maternal nutrition during pregnancy and health of the offspring. Biochem. Soc. Trans. 34, 779–782.
Maternal nutrition during pregnancy and health of the offspring.CrossRef | 1:CAS:528:DC%2BD28XhtFWnsLbM&md5=700139c956581674bfc8d06fa59b3f3cCAS | 17052196PubMed | open url image1

Melo, M. C., Almeida, F. R. C. L., Caldeira-Brant, A. L., Parreira, G. G., and Chiarini-Garcia, H. (2014). Spermatogenesis recovery in protein-restricted rats subjected to a normal protein diet after weaning. Reprod. Fertil. Dev. 26, 787–796.
Spermatogenesis recovery in protein-restricted rats subjected to a normal protein diet after weaning.CrossRef | 1:CAS:528:DC%2BC2cXhtFynsbjJ&md5=33871a83f190e8bb12c7883150f1fa12CAS | 23743013PubMed | open url image1

Nygard, A. B., Jorgensen, C. B., Cirera, S., and Fredholm, M. (2007). Selection of reference genes for gene expression studies in pig tissues using SYBR green qPCR. BMC Mol. Biol. 8, 67–72.
Selection of reference genes for gene expression studies in pig tissues using SYBR green qPCR.CrossRef | 17697375PubMed | open url image1

Okwun, O. E., Igboeli, G., Ford, J. J., Lunstra, D. D., and Johnson, L. (1996). Number and function of Sertoli cells, number and yield of spermatogonia, and daily sperm production in three breeds of boar. J. Reprod. Fertil. 107, 137–149.
Number and function of Sertoli cells, number and yield of spermatogonia, and daily sperm production in three breeds of boar.CrossRef | 1:CAS:528:DyaK28XmtFOlurY%3D&md5=b5a09bcc7fced0008bf8c3b6175ea68fCAS | 8699427PubMed | open url image1

Orth, J. M., Gunsalus, G. L., and Lamperti, A. A. (1988). Evidence from Sertoli cell-depleted rats indicates that spermatid number in adults depends on numbers of Sertoli cells produced during perinatal development. Endocrinology 122, 787–794.
Evidence from Sertoli cell-depleted rats indicates that spermatid number in adults depends on numbers of Sertoli cells produced during perinatal development.CrossRef | 1:STN:280:DyaL1c7jslWgug%3D%3D&md5=468d1f95fd07c28764e1a4502c85b3aaCAS | 3125042PubMed | open url image1

Pacek, M., and Walter, J. C. (2004). A requirement for MCM7 and Cdc45 in chromosome unwinding during eukaryotic DNA replication. EMBO J. 23, 3667–3676.
A requirement for MCM7 and Cdc45 in chromosome unwinding during eukaryotic DNA replication.CrossRef | 1:CAS:528:DC%2BD2cXnsFajsLg%3D&md5=e2608f602484c6c4d12b0ced58bfb351CAS | 15329670PubMed | open url image1

Père, M. C., and Etienne, M. (2000). Uterine blood flow in sows: effects of pregnancy stage and litter size. Reprod. Nutr. Dev. 40, 369–382.
Uterine blood flow in sows: effects of pregnancy stage and litter size.CrossRef | 11081664PubMed | open url image1

Ren, D., Xing, Y., Lin, M., Wu, Y., Li, K., Li, W., Yang, S., Guo, T., Ren, J., Ma, J., Lan, L., and Huang, L. (2009). Evaluations of boar gonad development, spermatogenesis with regard to semen characteristics, libido and serum testosterone levels based on Large White Duroc × Chinese Erhualian crossbred boars. Reprod. Domest. Anim. 44, 913–919.
Evaluations of boar gonad development, spermatogenesis with regard to semen characteristics, libido and serum testosterone levels based on Large White Duroc × Chinese Erhualian crossbred boars.CrossRef | 1:CAS:528:DC%2BD1MXhs1Sjt7zO&md5=2e00cb63d09641e58e724a0600834f33CAS | 19000221PubMed | open url image1

Russell, L. D., and Peterson, R. N. (1984). Determination of the elongate spermatid–Sertoli cell ratio in various mammals. J. Reprod. Fertil. 70, 635–641.
Determination of the elongate spermatid–Sertoli cell ratio in various mammals.CrossRef | 1:STN:280:DyaL2c7jvVCisg%3D%3D&md5=fe0f2ba9386dcadb43a181cd6a467485CAS | 6366223PubMed | open url image1

Smit, M. N., Spencer, J. D., Almeida, F. R. C. L., Patterson, J. L., Chiarini-Garcia, H., Dyck, M. K., and Foxcroft, G. R. (2013). Consequences of a low litter birth weight phenotype for postnatal lean growth performance and neonatal testicular morphology in the pig. Animal 7, 1681–1689.
Consequences of a low litter birth weight phenotype for postnatal lean growth performance and neonatal testicular morphology in the pig.CrossRef | 1:STN:280:DC%2BC3sjnslyrtw%3D%3D&md5=9af1db00edb6f0eddbd8352f8dc2ad04CAS | 23822933PubMed | open url image1

Town, S. C., Putman, C. T., Turchinsky, N. J., Dixon, W. T., and Foxcroft, G. R. (2004). Number of conceptuses in utero affects porcine fetal muscle. Reproduction 128, 443–454.
Number of conceptuses in utero affects porcine fetal muscle.CrossRef | 1:CAS:528:DC%2BD2cXptlGjsLs%3D&md5=88118e79bdc59fe68f1e23a9987a0622CAS | 15454639PubMed | open url image1

Turner, A. S., and McIlwaith, C. W. (2002). ‘Técnicas cirúrgicas em animais de grande porte.’ (Roca: São Paulo.)

Waberski, D., Petrunlina, A. M., and Topfer-Petersen, E. (2008). Can external quality control improve pig AI efficiency? Theriogenology 70, 1346–1351.
Can external quality control improve pig AI efficiency?CrossRef | 1:STN:280:DC%2BD1cnmvVOjtw%3D%3D&md5=2f9f5fe6470a84c7c929407fa24c0355CAS | 18656253PubMed | open url image1

Wu, G., Bazer, F. W., Cudd, T. A., Meininger, C. J., and Spencer, T. E. (2004). Maternal nutrition and fetal development. J. Nutr. 134, 2169–2172.
| 1:CAS:528:DC%2BD2cXns1ejtLg%3D&md5=830f920e01e8bc296e2691d9eb4f9323CAS | 15333699PubMed | open url image1

Wu, G., Bazer, F. W., Wallace, J. M., and Spencer, T. E. (2006). Intrauterine growth retardation: implications for the animal sciences. J. Anim. Sci. 84, 2316–2337.
Intrauterine growth retardation: implications for the animal sciences.CrossRef | 1:CAS:528:DC%2BD28XovFGktLs%3D&md5=b593f5476e5a12e92c091576679dd13eCAS | 16908634PubMed | open url image1



Export Citation Cited By (1)