However, the empirical evidence for this proposition is contentious Gray et al. A fetus growing faster in utero can be considered to have a greater effective exposure to a given insult than one that undergoes fewer cell cycles during the period of exposure. This is a major point requiring clarification via further experimental work. It is unclear whether exposure to sex steroids may have similar adverse effects. Genetic and morphological differences in development Evidence from rodent models From the earliest stages of preimplantation development, the sex of the embryo influences both growth patterns and survival. There is a marked difference in developmental programming of offspring phenotypes when measured before and after puberty.
It could therefore be postulated that all fetuses respond identically to the same insult, but the insult is buffered by the mother in a way that depends on the sex of the fetus. Developmental programming stresses are not normally applied to the fetus directly, but particularly in the case of dietary interventions are mediated by the maternal physiology. In male rats, it has also been shown that prenatal exposure to a maternal low-protein diet in rats shortens telomeres prematurely in a number of organs Tarry-Adkins et al. In view of the major temporal, spatial and biochemical differences between male and female development, both pre- and post-natally, it may be argued that the sexes should be treated by researchers as separate models. Ultrasonographic measurements of human growth in utero shows that the slower rate of growth of the female fetus becomes significant at 28 weeks of gestation and increases towards term Parker et al. In the female preimplantation embryo, there exists a period during which transcription occurs from both X chromosomes, between the start of transcription from the embryonic genome and X inactivation. This finding is consistent with the increased sensitivity of gene expression profiles in female placentas to a maternal high-fat diet Mao et al. Thus, in the bovine preimplantation embryo, before expression of any overt sex-specific morphology, survival may already be influenced in a sex-dependent manner by the interaction of genetic factors and environmental conditions. The consideration of intrauterine position applies much less frequently to larger mammal and human populations that are not litter-bearing, but the differences in physiology observed in 2M females adds weight to the hypothesis that in utero exposure to sex steroids may profoundly influence developmental programming. The decreased incidence of adverse outcomes in female fetuses compared with males could be the consequence of a greater environmental adaptability, and hence protection, by placental physiology. Fetal sex is determined by the presence or absence of a Y chromosome bearing the Sry gene. Epidemiological evidence shows that the sex difference in risk for cardiovascular disease narrows considerably after the menopause and that oophorectomy in rats can narrow this gap in incidence at an earlier age Ojeda et al. Timing of development Human males and females are known to undergo development at different rates, both in utero and post-natally up until the post-pubertal stage Pedersen , Davis et al. It is known that telomere length in both the renal cortex and the medulla of male rats is shorter than in females and that telomere shortening is associated with increased markers of cellular senescence Tarry-Adkins et al. In designing experiments, it is the goal of most researchers to use the fewest animals and least resources practicable to fully address their question. In humans, male sex is a significant risk factor for adverse motor and cognitive outcomes in premature infants and for survival in neonatal intensive care units Stevenson et al. Sex differences in temporal development have been postulated from the time of conception itself, with the proposition that human male conceptuses are more likely to result at the extremes of the fertile period James , This leads to a paucity of studies in which sexual dimorphism is built into the model, and yet this is a pertinent issue when applying the results of developmental programming studies to designing diagnostic, preventative and therapeutic measures. European women undergo menopause at a median age of 54 years Dratva et al. A further consideration in polytocous organisms is the effect of differing levels of intrauterine sex steroid exposure in the female offspring, dependent on intrauterine position. Cultured preimplantation murine male embryos show a faster rate of growth in vitro than do female embryos Valdivia et al. Sexual dimorphism is also a feature of early post-implantation growth in mammalian conceptuses Pedersen Cells derived from day There is insufficient data available to draw conclusions on whether glucose concentrations may influence development in vitro in a sex-specific manner in other species, but given the difference in the findings of bovine and murine studies, it may be expected that this will prove to be a species-specific effect. In female sheep offspring, it has been demonstrated that in utero administration of testosterone to the mother produces pancreatic dysregulation and changes in liver metabolism Hogg et al. For instance, maternal high-fat diet during pregnancy appears to directly influence placental methylation patterns only in female murine offspring Gallou-Kabani et al. There is a marked difference in developmental programming of offspring phenotypes when measured before and after puberty.
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