A critique of the evidence on the importance of steroid feedback to seasonal changes in gonadotrophin secretion.

Abstract

Casual observation of farm animals immediately points to some basic differences in their reproductive function; namely, some species (sheep and horses) have distinct breeding seasons while others (cows and pigs) do not. The seasonal nature of reproduction in the former is not only of immense practical importance to the agricultural industry but is also of considerable theoretical interest to the reproductive endocrinologist. The demonstration that photoperiod is the primary environmental cue controlling reproduction in sheep (Yeates, 1949; Hafez, 1952) raises several intriguing questions including: How does the sheep measure the length of the day? How is photoperiodic information transferred from the photoreceptor to the hypothalamo— hypophysial axis? What changes in the hypothalamo—hypophysial axis determine the reproductive capacity of the gonads? In this paper we will concentrate on the last question. In both the ram (Pelletier & Ortavant, 1975b; Lincoln & Short, 1980) and the ewe (Legan, Karsch & Foster, 1977), photoperiodically controlled changes in the system governing the tonic mode of gonadotrophin secretion appear to be responsible for the seasonal transitions between reproductive activity and quiescence. During the breeding season tonic gonadotrophin secretion is high; in the non-breeding season it is low. In the male, these changes most probably provide a direct drive to the seasonal fluctuations in testicular function. In the female, however, the changes in tonic gonadotrophin secretion must operate via the luteinizing hormone (LH) surge system to cause the termination and re-initiation of oestrous cycles. More specifically, it has been proposed that oestrous cycles can occur only when tonic secretion of LH is sufficient to stimulate an oestradiol rise which is needed to induce the preovulatory LH surge. Ovarian cycles cease when tonic LH secretion is low because levels of the gonadotrophin are insufficient to produce the oestradiol signal for the LH surge (Legan et al., 1977). Details of this hypothesis and supporting evidence have been described by Legan & Karsch (1979) and Goodman & Karsch (1980). Although seasonal changes in tonic gonadotrophin secretion appear to be a critical element in both sexes, there is not general agreement as to how they are produced. In the ewe, the seasonal variation in tonic LH secretion is thought to reflect a change in responsiveness to the inhibitory feedback action of oestradiol. In the breeding season oestradiol is a weak inhibitory steroid whereas in anoestrus it is extremely potent in this regard (Legan et al., 1977). In contrast, it has been proposed that seasonal changes in LH secretion in the ram may not require sex-steroid feedback (Lincoln & Short, 1980). This question regarding the importance of sex-steroid feedback is not confined to the sheep. Indeed, it has been raised for numerous other seasonal breeders particularly birds (Follett, 1978) and hamsters (Turek & Campbell, 1979). Our interest in the importance of steroid feedback has arisen, in part, because the question of steroid dependency touches upon the fundamental mechanisms underlying the photoperiodic