Defeminization of the reproductive response to photoperiod occurs early in prenatal development in the sheep

Abstract

Photoperiod times the transition to sexual maturity in many seasonal breeders. In male and female sheep, photoperiod influences the timing of puberty differentially. Whereas in females, age at sexual maturity is highly dependent on photoperiod, puberty in males begins at the same age regardless of day length. We have determined that this sex difference is due to the organizing action of androgens during prenatal development. In the present investigation, we studied when during gestation (term: ~150 days) androgens defeminize the reproductive response to photoperiod. We compared the age at sexual maturity in female lambs treated with testosterone prenatally from Days 30 to 76 (Early, n = 7) or 89 to 135 (Late, n = 8) to that of normal males (n = 8) and normal females (n = 7). To reveal differential responsiveness to photoperiod, all lambs were maintained from birth under constant long days (16L:8D), a treatment that inhibits puberty in normal females. The age at the pubertal LH rise was determined in a standardized experimental model (lambs gonadectomized and treated with estradiol). As expected in the long day photoperiod, only 1 of 7 normal females had a pubertal rise in LH. In contrast, all males increased LH secretion by 6.7 ± 0.6 wk. Similarly, in the Early group, a sustained increase in LH occurred in all females, but this was delayed relative to the increase in the males (16.8 ± 1.7 wk; p < 0.001). The Late group had LH patterns similar to those of the normal females, with only 3 of 8 females having sustained elevations in LH. These data suggest that a 'critical period' for the defeminization of the reproductive response to photoperiod occurs early in prenatal development. In addition, it appears that this critical period and the period for defeminization of the surge mode of gonadotropin secretion occur at similar stages in development. When challenged with an acute increase in estradiol, all normal and Late androgenized females responded with an LH surge. In contrast, none of the males and only 1 of 7 Early females produced a robust response to estradiol.