Differential Regulation of Luteinizing Hormone and Follicle-Stimulating Hormone in Male Siberian Hamsters by Exposure to Females and Photoperiod

0013-7227/02/$15.00/0 Printed in U.S.A. Endocrinology 143(6):2178 –2188 Copyright © 2002 by The Endocrine Society Differential Regulation of Luteinizing Hormone and Follicle-Stimulating Hormone in Male Siberian Hamsters by Exposure to Females and Photoperiod SONALI ANAND, SUSAN LOSEE-OLSON, FRED W. TUREK, AND TERESA H. HORTON Department of Neurobiology and Physiology, Northwestern University, Evanston, Illinois 60208 Siberian hamsters have decreased gonadotropin levels and testis size after short-day (SD) exposure. Upon transfer from short to long days, FSH and testis weight increase rapidly, whereas LH and T remain low for much longer. We investigated whether an additional environmental stimulus, specifically a female, could trigger an earlier release of LH and whether the response to the female was dependent on photoperiod. An increase in serum LH was induced in long day (LD), but not SD, males within minutes of female exposure. The ability of SD males to secrete LH upon female exposure was regained within 4 d of photostimulation. FSH was not secreted after female exposure, but varied with photoperiod. Thus, S EASONAL CHANGES in day length are used as a proximate cue by photoperiodic species to trigger changes in reproductive activity in anticipation of changing environmental conditions. Seasonal changes in day length, however, do not predict changes in environmental conditions perfectly because other factors, such as food availability, temperature, and proximity of a mate vary acutely and less reliably than photoperiod. To compensate for variability in environmental conditions, many species use information from additional environmental signals to adjust the onset of reproduction within the time frame defined by seasonally appropriate day lengths (1– 4). Siberian hamsters (Phodopus sungorus) reproduce seasonally and are commonly used in studies to investigate the mechanism by which seasonal changes in photoperiod regulate reproductive function. Recent work from our laboratory demonstrates a dramatic difference in the secretion of the two gonadotropins, FSH and LH after photostimulation of male Siberian hamsters (5, 6). Although exposure to long days stimulates early FSH secretion, LH secretion and consequently T secretion remain low for many more days or weeks. This observation suggests that additional environmental cues may be needed to accelerate the release of LH. This differential secretion of FSH and LH may reflect the distinct roles of these hormones in testicular spermatogenesis and steroidogenesis and may provide a mechanism for the integration of multiple forms of environmental information to effect the timing of reproduction. In the laboratory, seasonal changes in reproductive activity can be simulated by manipulation of photoperiod (7–9) and melatonin (10, 11). Siberian hamsters held in a short photoperiod for several weeks after weaning have negligible Abbreviations: CST, Central standard time; 16L:8D, 16 h of light, 8 h of darkness; LD, long days; SD, short days; NMDA, N-methyl-d,l-aspartate. FSH and LH are differentially regulated by photoperiod and female exposure. In subsequent studies melatonin injections and a GnRH antagonist were used to show that photoperiod modulates the endocrine responsiveness of a male to a female via melatonin and that female-induced LH release is GnRH dependent. Collectively, these results suggest separation of gonadotropin signaling pathways by environmental stimuli and provide an excellent model to elucidate the effects of photoperiod on the processing of social and chemosensory inputs to the GnRH neurons of the hypothalamus. (Endocrinology 143: 2178 –2188, 2002) amounts of circulating gonadotropins and small testes (5, 6). After transfer from a short to a long photoperiod, FSH increases significantly within 3–5 d, peaks by the 10th day, and then decreases and plateaus to levels characteristic of a reproductively mature male (5, 6, 9). This increase in serum FSH can be blocked in part by injection of a GnRH antagonist; suggesting that secretion of FSH is partially dependent upon GnRH release (6). Testicular weight increases by the 10th day of photostimulation (5, 9) subsequent to FSH stimulation (12, 13). In contrast, despite the increase in FSH, serum LH levels either do not increase in response to photostimulation (5, 14) or increase much later than FSH (9). Correspondingly, serum T levels are low. Thus, photostimulation causes a rapid increase in serum FSH and testicular weight, but not in serum LH and T. These differences in the time course for release of FSH and LH are consistent with a model in which increasing day lengths trigger the release of FSH to promote the development of the testes, which requires several weeks to complete, in anticipation of improved environmental conditions. In contrast, the release of LH and T, which are required for the final stages of sperm maturation and regulate reproductive behaviors, may be delayed for several weeks or until additional proximate cues are present that more directly reflect environmental conditions required for successful reproduction. Given that both FSH and LH are required to induce full testicular maturation (12, 15) and the full complement of reproductive behaviors, we investigated whether an additional environmental stimulus is able to induce LH secretion in this species and whether the response to that stimulus is, in turn, dependent upon photoperiod. In several species, serum LH levels in males and females can be influenced by exposure to a prospective mate. For example, serum LH levels of male laboratory mice can be 2178 Anand et al. • Effects of Female and Photoperiod on LH and FSH increased by exposure to females (16). Similarly, the presence of an ewe facilitates an increase in plasma LH and redevelopment of testes in rams before the onset of breeding (17). An increase in serum LH and/or T in male Golden hamsters (Mesocricetus auratus) in response to female urine and vaginal secretions is well documented (16, 18 –20). Hence, we investigated whether exposure to a female would serve as an additional environmental stimulus to induce LH secretion in males. The first study reported here tested the hypothesis that presentation of a female can induce LH secretion in male Siberian hamsters and that long photoperiods provide a permissive condition enabling males to release LH upon exposure to a female. FSH levels were monitored to determine whether exposure to a female also triggered FSH release. Cortisol levels in male Siberian hamsters are known to decline upon establishment of a pair bond and to increase upon separation of the pair (21, 22). Cortisol is also elevated in Siberian hamsters housed in a short photoperiod compared with a long photoperiod (23). Because corticosteroids are known to influence the differential secretion of LH and FSH (24, 25), serum cortisol was measured when sufficient serum was available. Subsequent studies investigated wheth (...truncated)