Effects of birthweight on reproductive system development and onset of puberty in gilts
F. R. C. L. Almeida A D , B. Laurenssen B , L. X. Pereira A , K. J. Teerds C and N. M. Soede BA Department of Morphology, Federal University of Minas Gerais, Belo Horizonte, MG 31.270-901, Brazil.
B Adaptation Physiology Group, Department of Animal Sciences, Wageningen University, P.O. Box 338, 6700 AH, Wageningen, The Netherlands.
C Human and Animal Physiology Group, Department of Animal Sciences, Wageningen University, P.O. Box 338, 6700 AH, Wageningen, The Netherlands.
D Corresponding author. Email: falmeida@icb.ufmg.br
Reproduction, Fertility and Development 29(2) 254-261 https://doi.org/10.1071/RD15036
Submitted: 24 January 2015 Accepted: 19 June 2015 Published: 16 July 2015
Abstract
The aim of the present study was to investigate the effects of birthweight on bodyweight development, development of the genital tract, onset of puberty and their associations with insulin-like growth factor (IGF) 1 and leptin concentrations. Pairs of littermate gilts from 51 litters were selected: one piglet with the highest birthweight (HW; 1.5 ± 0.2 kg) and the other with the lowest birthweight (LW; 1.0 ± 0.2 kg). Gilt pairs were killed at either fixed ages (80.8 ± 1.2 days; AG; 16 pairs), fixed bodyweight (35.2 ± 1.4 kg; WG; 16 pairs) or after first oestrus (EG; 19 pairs). In the AG group, HW gilts were 5.6 kg heavier at the time of death than LW gilts. In the WG group, LW gilts were 5.9 days older at the time of death (P < 0.05). There were no significant differences in the number or size of total antral follicles or in the follicle population among birthweight classes. Age at puberty was similar between the HW and LW gilts, but bodyweight at time of death was greater for HW gilts (P < 0.05). Birthweight did not affect the development of the genital tract, ovulation rate or hormone plasma concentrations. These results suggest that birthweight does not affect the development of the genital tract before puberty and puberty onset.
Additional keywords: genital tract, insulin-like growth factor 1, leptin, ovary.
References
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 | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38bos1Gltg%3D%3D&md5=cdb6e0d567e053b7ce47fc499a683574CAS |
Amaral Filha, W. S., Bernardi, M. L., Wentz, I., and Bortolozzo, F. P. (2010). Reproductive performance of gilts according to growth rate and backfat thickness at mating. Anim. Reprod. Sci. 121, 139–144.
| Reproductive performance of gilts according to growth rate and backfat thickness at mating.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cnotVygtg%3D%3D&md5=7e7d81b41b5fc9ed15c03188ec757f09CAS | 20641148PubMed |
Barb, C. R., Hausman, G. J., and Lents, C. A. (2008). Energy metabolism and leptin: effects on neuroendocrine regulation of reproduction in the gilt and sow. Reprod. Domest. Anim. 43, 324–330.
| Energy metabolism and leptin: effects on neuroendocrine regulation of reproduction in the gilt and sow.Crossref | GoogleScholarGoogle Scholar | 18638142PubMed |
Beardsall, K., Vanhaesebrouck, S., Frystyk, J., Ogilvy-Stuar, A. L., Vanhole, C., van Weissenbruch, M., Midgley, P., Thio, M., Cornette, L., Gill, B., Ossuetta, I., Iglesias, I., Theyskens, C., de Jong, M., Ahluwalia, J. S., de Zegher, F., Dunger, D. B., NIRTURE Study Group (2014). Relationship between insulin-like growth factor I levels, early insulin treatment, and clinical outcomes of very low birth weight infants. J. Pediatr. 164, 1038–1044.e1.
| Relationship between insulin-like growth factor I levels, early insulin treatment, and clinical outcomes of very low birth weight infants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitleltLo%3D&md5=9675844775b1eec2d33741b2a9838babCAS | 24518169PubMed |
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 | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpvVOrt7o%3D&md5=e37387ad442e09cd071835bfc759427bCAS | 20418451PubMed |
Bee, G. (2004). Effect of early gestation feeding, birth weight, and gender of progeny on muscle fiber characteristics of pigs at slaughter. J. Anim. Sci. 82, 826–836.
| 1:CAS:528:DC%2BD2cXhvVCku7g%3D&md5=3b8e8546af8ccd2c4e55f7f6c9f0c500CAS | 15032440PubMed |
Beltranena, E., Aherne, F. X., Foxcroft, G. R., and Kirkwood, R. N. (1991). Effects of pre- and postpubertal feeding on production traits at first and second estrus in gilts. J. Anim. Sci. 69, 886–893.
| 1:STN:280:DyaK3M3os1Wnsg%3D%3D&md5=b0b60ac1e74abb9c952480810e7f2968CAS | 2061258PubMed |
Booth, P. J., Cosgrove, J. R., and Foxcroft, G. R. (1996). Endocrine and metabolic responses to realimentation in feed-restricted prepubertal gilts: associations among gonadotropins, metabolic hormones, glucose, and utero-ovarian development. J. Anim. Sci. 74, 840–848.
| 1:CAS:528:DyaK28XitlCiur8%3D&md5=19092e43c75c3bde33de9f41c8bd4264CAS | 8728006PubMed |
Bortolozzo, F. P., Bernardi, M. L., Kummer, R., and Wentz, I. (2009). Growth, body state and breeding performance in gilts and primiparous sows. Soc. Reprod. Fertil. Suppl. 66, 281–291.
| 1:STN:280:DC%2BD1MjgvFaktA%3D%3D&md5=c555ead241a32691e37f05316ff49e6aCAS | 19848294PubMed |
Da Silva, P., Aitken, R. P., Rhind, S. M., Racey, P. A., and Wallace, J. M. (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=1d627c207f7bf79414f7ee0c0512a3e8CAS | 12052231PubMed |
Da Silva-Buttkus, P., van den Hurk, R., teVelde, E. R., and Taverne, M. A. (2003). Ovarian development in intrauterine growth-retarded and normally developed piglets originating from the same litter. Reproduction 126, 249–258.
| Ovarian development in intrauterine growth-retarded and normally developed piglets originating from the same litter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntFyjtrs%3D&md5=6a4c886fb072a8db4bae5b98a6fe4b05CAS | 12887281PubMed |
da Silva Faria, T. S., Ramos, C. F., and Sampaio, F. J. B. (2004). Puberty onset in the female offspring of rats submitted to protein or energy restricted diet during lactation. J. Nutr. Biochem. 15, 123–127.
| Puberty onset in the female offspring of rats submitted to protein or energy restricted diet during lactation.Crossref | GoogleScholarGoogle Scholar |
De Bruin, J. P., Nikkels, P. G. J., van Haaften, M., Looman, C. W. N., and teVelde, E. R. (2001). Morphometry of human ovaries in normal and growth-restricted fetuses. Early Hum. Dev. 60, 179–192.
| Morphometry of human ovaries in normal and growth-restricted fetuses.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3M7isF2htA%3D%3D&md5=e552ee7bdb00706451eedacc5ef85411CAS | 11146237PubMed |
Dyce, K. M., Sack, W. O., and Wensing, C. J. G. (2009). ‘Textbook of Veterinary Anatomy’, 4th edn. (Saunders Elsevier: St. Louis, MO).
Dyck, G. W., and Swierstra, E. E. (1983). Growth of the reproductive tract of the gilt from birth to puberty. Can. J. Anim. Sci. 63, 81–87.
| Growth of the reproductive tract of the gilt from birth to puberty.Crossref | GoogleScholarGoogle Scholar |
Evans, F. D., Cristopherson, R. J., and Aherne, F. X. (1988). Comparative physiological development of the reproductive and adrenal axis of the gilt from weaning to puberty. Can. J. Anim. Sci. 68, 1113–1119.
| Comparative physiological development of the reproductive and adrenal axis of the gilt from weaning to puberty.Crossref | GoogleScholarGoogle Scholar |
Foxcroft, G. R., Dixon, W. T., Dyck, M. K., Novak, S., Harding, J. C., and Almeida, F. R. C. L. (2009). Prenatal programming of postnatal development in the pig. Soc. Reprod. Fertil. Suppl. 66, 213–231.
| 1:STN:280:DC%2BD1MjgvFaksA%3D%3D&md5=9130035af6c7ca8b8e2402a89b978dc4CAS | 19848290PubMed |
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.
| 1:CAS:528:DC%2BD28XjvFynuw%3D%3D&md5=d5dd4c4d62069b8f8568f7855d4d79eeCAS | 16361495PubMed |
Grazul-Bilska, A. T., Neville, T. L., Borowczyk, E., Sharma, A., Reynolds, L. P., Caton, J. S., Redmer, D. A., and Vonnahme, K. A. (2014). Ovarian and uterine characteristics and onset of puberty in adolescent offspring: effects of maternal diet and selenium supplementation in sheep. Theriogenology 81, 887–895.
| Ovarian and uterine characteristics and onset of puberty in adolescent offspring: effects of maternal diet and selenium supplementation in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXislOitbc%3D&md5=ec4993e097ad155b1f07500b1dbf26b8CAS | 24534339PubMed |
Gregoraszczuk, E. Ł., Ptak, A., Wojciechowicz, T., and Nowak, K. (2007). Action of IGF-I on expression of the long form of the leptin receptor (ObRb) in the prepubertal period and throughout the estrous cycle in the mature pig ovary. J. Reprod. Dev. 53, 289–295.
| Action of IGF-I on expression of the long form of the leptin receptor (ObRb) in the prepubertal period and throughout the estrous cycle in the mature pig ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlslOjsLg%3D&md5=a36beb94be6973d132576dd65baab834CAS | 17139134PubMed |
Hausman, G. J., Barb, C. R., and Lents, C. A. (2012). Leptin and reproductive function. Biochimie 94, 2075–2081.
| Leptin and reproductive function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XktlGksbk%3D&md5=c4b5d141d78203611d049d0a9500ca65CAS | 22980196PubMed |
Holt, R. I. (2002). Fetal programming of the growth hormone–insulin-like growth factor axis. Trends Endocrinol. Metab. 13, 392–397.
| Fetal programming of the growth hormone–insulin-like growth factor axis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnsVShsr8%3D&md5=ff2833a575cdc200ff3c908bb2e89f14CAS | 12367821PubMed |
Kotsampasi, B., Chadio, S., Papadomichelakis, G., Deligeorgis, S., Kalogiannis, D., Menegatos, I., and Zervas, G. (2009). Effects of maternal undernutrition on the hypothalamic–pituitary–gonadal axis function in female sheep offspring. Reprod. Domest. Anim. 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=cd252fdcd88b772ba16e68d386218191CAS | 19642222PubMed |
Kummer, R., Bernardi, M. L., Schenkel, A. C., Amaral Filha, W. S., Wentz, I., and Bortolozzo, F. P. (2009). Reproductive performance of gilts with similar age but with different growth rate at the onset of puberty stimulation. Reprod. Domest. Anim. 44, 255–259.
| Reproductive performance of gilts with similar age but with different growth rate at the onset of puberty stimulation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M3jsVGqsg%3D%3D&md5=7b7e835eeb1236add483ecb8e4d406cdCAS | 18694424PubMed |
Lamberson, W. R., Sterle, J. A., and Matteri, R. L. (1996). Relationships of serum insulin-like growth factor II concentrations to growth, compositional, and reproductive traits of swine. J. Anim. Sci. 74, 1753–1756.
| 1:CAS:528:DyaK28XltVSgtbg%3D&md5=d972b1b81fbb02bb3df9068aafa0e1d8CAS | 8856427PubMed |
Louveau, I., and Bonneau, M. (1996). Effect of a growth hormone infusion on plasma insulin-like growth factor-I in Meishan and Large White pigs. Reprod. Nutr. Dev. 36, 301–310.
| Effect of a growth hormone infusion on plasma insulin-like growth factor-I in Meishan and Large White pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XltFKqtb8%3D&md5=7dba666c0d0ed88c6df0e4be860b59e9CAS | 8766734PubMed |
Miller, D. W., Blache, D., Boukhliq, R., Curlewis, J. D., and Martin, G. B. (1998). Central metabolic messengers and the effects of nutrition on gonadotrophin secretion in sheep. J. Reprod. Fertil. 112, 347–356.
| Central metabolic messengers and the effects of nutrition on gonadotrophin secretion in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXktVensLc%3D&md5=987834539fbf69d1a40f82e865184691CAS | 9640274PubMed |
Moreira, F., Corcini, C. D., Mondadori, R. G., Gevehr-Fernandes, C., Mendes, F. F., Araújo, G., Lucia, E. G., and Jr, T. (2013). Leptin and mitogen-activated protein kinase (MAPK) in oocytes of sows and gilts. Anim. Reprod. Sci. 139, 89–94.
| Leptin and mitogen-activated protein kinase (MAPK) in oocytes of sows and gilts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmtlGhsL0%3D&md5=e4413b795aaa9e2910383ff2792118e9CAS | 23602489PubMed |
Picton, H. M. (2001). Activation of follicle development: the primordial follicle. Theriogenology 55, 1193–1210.
| Activation of follicle development: the primordial follicle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjsFSju7c%3D&md5=414f2c2b36a02c5cc59ba071f65c11efCAS | 11327680PubMed |
Poore, K. R., and Fowden, A. L. (2004). The effects of birth weight and postnatal growth patterns on fat depth and plasma leptin concentrations in juvenile and adult pigs. J. Physiol. 558, 295–304.
| The effects of birth weight and postnatal growth patterns on fat depth and plasma leptin concentrations in juvenile and adult pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtFWhtrk%3D&md5=b95a8ea8b1e61190a1de88b9883d2c9cCAS | 15121800PubMed |
Quesnel, H., Pasquier, A., Mounier, A. M., Louveau, I., and Prunier, A. (1998). Influence of feed restriction in primiparous lactating sows on body condition and metabolic parameters. Reprod. Nutr. Dev. 38, 261–274.
| Influence of feed restriction in primiparous lactating sows on body condition and metabolic parameters.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK1czmtFOnsQ%3D%3D&md5=3541d4020e59e07d738b90f1e3b583aeCAS | 9698277PubMed |
Richards, J. S. (2001). Perspective: the ovarian follicle – a perspective in 2001. Endocrinology 142, 2184–2193.
| 1:CAS:528:DC%2BD3MXjvFGgtbk%3D&md5=b9d9d85651dcd045a8caa8f7a97e5040CAS | 11356661PubMed |
SAS Institute Inc (2001). ‘Statistical Analysis System User’s Guide: Statistics. SAS for Windows, Version 8.2.’ (SAS Institute, Inc.: Cary, NC.)
Slot, K. A., Kastelijn, J., Bachelot, A., Kelly, P. A., Binart, N., and Teerds, K. J. (2006). Reduced recruitment and survival of primordial and growing follicles in GH receptor-deficient mice. Reproduction 131, 525–532.
| Reduced recruitment and survival of primordial and growing follicles in GH receptor-deficient mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjs12jsLo%3D&md5=35031cc37c138e405d0973f50b33afcbCAS | 16514195PubMed |
Snyder, J. L., Clapper, J. A., Roberts, A. J., Sanson, D. W., Hamernik, D. L., and Moss, G. E. (1999). Insulin-like growth factor-I, insulin-like growth factor-binding proteins, and gonadotropins in the hypothalamic–pituitary axis and serum of nutrient-restricted ewes. Biol. Reprod. 61, 219–224.
| Insulin-like growth factor-I, insulin-like growth factor-binding proteins, and gonadotropins in the hypothalamic–pituitary axis and serum of nutrient-restricted ewes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXktFKgu7o%3D&md5=9e230d01b6d774736d978ecbc78fcd3aCAS | 10377052PubMed |
Tilly, J. L. (2003). Ovarian follicle counts: not as simple as 1, 2, 3. Reprod. Biol. Endocrinol. 1, 11–14.
| Ovarian follicle counts: not as simple as 1, 2, 3.Crossref | GoogleScholarGoogle Scholar | 12646064PubMed |
Zak, L. J., Cosgrove, J. R., Aherne, F. X., and Foxcroft, G. R. (1997). Pattern of feed intake and associated metabolic and endocrine changes differentially affect postweaning fertility in primiparous lactating sows. J. Anim. Sci. 75, 208–216.
| 1:CAS:528:DyaK2sXhtVGkur0%3D&md5=0a82a8a4368877a19edd71bd2a93eeaaCAS | 9027568PubMed |