Effect of delayed breeding on the reproductive performance of female mice
J. J. Tarín A D , V. Gómez-Piquer A , F. Rausell A , C. Hermenegildo B and A. Cano CA Department of Functional Biology and Physical Anthropology, Faculty of Biological Sciences, University of Valencia, Burjassot, 46100 Valencia, Spain.
B Research Unit, Hospital Clínico de Valencia and Department of Physiology, University of Valencia, 46010 Valencia, Spain.
C Department of Pediatrics, Obstetrics and Gynecology, Faculty of Medicine, University of Valencia, Avda. Blasco Ibañez 17, 46010 Valencia, Spain.
D To whom correspondence should be addressed. email: tarinjj@uv.es
Reproduction, Fertility and Development 16(3) 373-378 https://doi.org/10.1071/RD03093
Submitted: 9 October 2003 Accepted: 1 April 2004 Published: 25 May 2004
Abstract
The aim of the present study was to determine, in the mouse, whether maintaining females as virgins until an advanced reproductive age was associated with decreased reproductive performance and reproductive lifespan compared with females of the same age that were first mated with males at an earlier reproductive age. Randomly selected virgin hybrid (C57BL/6JIco female × CBA/JIco male) female mice were housed individually with a randomly selected 12- to 14-week-old hybrid male either at the age of 28 weeks (normal breeding group; n = 20) or 51 weeks (delayed breeding group; n = 23) for the rest of their reproductive life. Females were checked once daily to determine the day of parturition and to record the litter size and gender of pups at birth for each consecutive litter. At weaning, offspring were weighed and killed. Delayed breeding was associated with smaller litter sizes, both at birth and at weaning, a higher bodyweight of pups at weaning, a higher percentage of litters with at least one newborn pup cannibalised, earlier cessation of female reproductive life and a higher mortality rate of dams during the breeding period. These results show that delayed breeding in the mouse is associated with decreased reproductive performance and a shorter reproductive lifespan compared with females bred at an earlier reproductive age.
Extra keywords: delayed motherhood, litter size, menopause, reproductive lifespan.
Acknowledgment
This work was supported by grant FIS 01/0138 from Instituto de Salud Carlos III, Fondo de Investigación Sanitaria, Ministerio de Sanidad y Consumo and grant BFI2003–04761 from Ministerio de Ciencia y Tecnología, co-financed by the Fondo Europeo de Desarrollo Regional (FEDER).
Abel, E. L. , Kruger, M. , and Burd, L. (2002). Effects of maternal and paternal age on Caucasian and Native American preterm births and birth weights. Am. J. Perinatol. 19, 49–54.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Alonzo, A. A. (2002). Long-term health consequences of delayed childbirth: NHANES III. Womens Health Issues 12, 37–45.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Asdell, S. A., Bogart, R., and Sperling, G. (1941).
Astolfi, P. , and Zonta, L. A. (2002). Delayed maternity and risk at delivery. Paediatr. Perinat. Epidemiol. 16, 67–72.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Clutton-Brock, T. H. , and Iason, G. R. (1986). Sex ratio variation in mammals. Q. Rev. Biol. 61, 339–374.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
de La Rochebrochard, E. , and Thonneau, P. (2002). Paternal age and maternal age are risk factors for miscarriage: results of a multicentre European study. Hum. Reprod. 17, 1649–1656.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Finn, C. A. (1963). Reproductive capacity and litter size in mice. Effect of age and environment. J. Reprod. Fertil. 6, 205–214.
Gosden, R. G. (1979). Effects of age and parity on the breeding potential of mice with one or two ovaries. J. Reprod. Fertil. 57, 477–487.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Institute of Laboratory Animal Research (1996).
James, W. H. (1987). The human sex ratio. Part 1: a review of the literature. Hum. Biol. 59, 721–752.
| PubMed |
Jones, E. C. , and Krohn, P. L. (1961). The relationship between age, numbers of oocytes and fertility in virgin and multiparous mice. J. Endocrinol. 21, 469–494.
| PubMed |
Juntunen, K. S. T. , Kvist, A. P. , and Kauppila, A. J. I. (1997). A shift from a male to a female majority in newborns with the increasing age of grand grand multiparous women. Hum. Reprod. 12, 2321–2323.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kennedy, T. G. , and Kennedy, J. P. (1972). Effects of age and parity on reproduction in young female mice. J. Reprod. Fertil. 28, 77–84.
| PubMed |
Matt, D. W. , Sarver, P. L. , and Lu, J. K. (1987). Relation of parity and estrous cyclicity to the biology of pregnancy in aging female rats. Biol. Reprod. 37, 421–430.
| PubMed |
McKenzie, F. F. (1928). Growth and reproduction in swine. Missouri Agric. Exp. Stn Res. Bull. 118, 1–67.
McNeilly, A. S. (1997). Lactation and fertility. J. Mammary Gland Biol. Neoplasia 2, 291–298.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Nass, T. E. , Lapolt, P. S. , and Lu, J. K. (1982). Effects of prolonged caging with fertile males on reproductive functions in aging female rats. Biol. Reprod. 27, 609–615.
| PubMed |
Okada, Y. (1981). The occurrence rate of neonatal anomaly depending on aging of grafted ovaries in C57BL/6J strain mice. Hokkaido Igaku Zasshi 56, 665–673.
| PubMed |
Schlager, G. , and Roderick, T. H. (1968). Secondary sex ratio in mice. J. Hered. 59, 363–365.
| PubMed |
Seoud, M. A. , Nassar, A. H. , Usta, I. M. , Melhem, Z. , Kazma, A. , and Khalil, A. M. (2002). Impact of advanced maternal age on pregnancy outcome. Am. J. Perinatol. 19, 1–8.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Shelton, M. (1959). A comparison of the population of oocytes in nulliparous and multiparous senile laboratory rats. J. Endocrinol. 18, 451–455.
| PubMed |
Tarín, J. J. , Bernabeu, R. , Baviera, A. , Bonada, M. , and Cano, A. (1995). Sex selection may be inadvertently performed in in-vitro fertilization–embryo transfer programmes. Hum. Reprod. 10, 2992–2998.
| PubMed |
Tarín, J. J. , Brines, J. , and Cano, A. (1998). Long-term effects of delayed parenthood. Hum. Reprod. 13, 2371–2376.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
te Velde, E. R. , Dorland, M. , and Broekmans, F. J. (1998). Age at menopause as a marker of reproductive ageing. Maturitas 30, 119–125.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tough, S. C. , Svenson, L. W. , Johnston, D. W. , and Schopflocher, D. (2001). Characteristics of preterm delivery and low birthweight among 113 994 infants in Alberta: 1994–1996. Can. J. Public Health 92, 276–280.
| PubMed |
Tough, S. C. , Newburn-Cook, C. , Johnston, D. W. , Svenson, L. W. , Rose, S. , and Belik, J. (2002). Delayed childbearing and its impact on population rate changes in lower birth weight, multiple birth, and preterm delivery. Pediatrics 109, 399–403.
| PubMed |
vom Saal, F. S., Finch, C. E. and Nelson, J. F. (1994). Natural history and mechanisms of reproductive rodents, and other selected vertebrates. In
Wainwright, P. E. (1997). Issues of design and analysis relating to the use of multiparous species in developmental nutritional studies. J. Nutr. 128, 661–663.
Wang, M. H. , and vom Saal, F. S. (2000). Maternal age and traits in offspring. Nature 407, 469–470.
| PubMed |
