The Effect of Daylength on Pituitary FSH and LH and Gonadal Development of Snowshoe Hares
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1 BIOLOGY OF REPRODUCTION 6, (1972) The Effect of Daylength on Pituitary FSH and LH and Gonadal Development of Snowshoe Hares 1 G. J. DAVIS AND R. K. MEYER Department of Zoology and (lie Endocrinology-Reproductive Physiology Program, The University of Wisconsin, Madison, Wisconsin Received August 26, 1971 The effect of daylength on gonadal development and pituitary LH and FSH in snowshoe hares collected in the field and maintained on simulated natural light was studied. Snowshoe hares were live trapped near Rochester, Alberta, Canada, and either were returned to the University of Wisconsin, Madison, or were killed in the field where pituitary glands, reproductive tracts, and serum were collected. In nature, prior to the breeding season, gonads develop as a function of daylength. The relationship is significantly less with the on- Set of breeding season as the testes approach their maximal size. After the summer solstice, the gonads begin a seasonal regression as a function of decreasing daylength. In both field-captured and laboratory-maintained hares pituitary gonadotropins as measured by using modifications of Parlow OAAD and Steelman and Pohley HCG augmentation method for LH and FSH, respectively, were positively correlated with gonadal development. Animals maintained on long day photoperiod from the summer solstice through September 1 maintained gonadal development and high pituitary hormone levels. It was therefore concluded that in the showshoe hare, gonadal development and therefore the breeding season is primarily controlled by gonadotropins which, in turn, are regulated by photoperiod. INTRODUCTION This paper demonstrates that the stimulus ultimately controlling the breeding season in snowshoe hares (Lepus americanus) is a function of daylength which regulates gonadotropin production and thus controls gonadal development. Marshall and Bowden (1934) demonstrated that although extra light could hasten the onset of estrus in the ferret (Putorius vulgaris) light was not a prerequisite for normal sexual maturation, since animals kept in constant darkness came into estrus at approximately the same time as those in natural lighting. White-crowned sparrows (Zonotrichia leucophrys) appear to have an absolute light requirement for seasonal gonad growth (Farner, 1961); however, sexual development in prairie dogs (Cynomys ludouicianus), another annual breeder, seems to be entirely unaffected by environmental lighting (Foreman, 1962). These observations indicate that there is wide variation among species in the extent to which cyclic gonadal function is regulated by environmental lighting. Marshall (1942) was the first to emphasize the dependence of the breeding season in many species on environmental factors. He also suggested that these factors exert an effect by nervous stimulation of the secretion of pituitary gonadotropic hormones, primarily FSH. MATERIAL AND METHODS 1 This investigation was supported by Public Health Service Training Grant No. 2-TOl-HD and 05, from the National Institute of Child Health and Human Development and The Ford Foundation, Giant No A. Field Data Snowshoe hares were collected near Rochester, Alberta, Canada, at various times throughout the year between 1961 and 1970; however, most collections Copyright 1972 by the Society for the Study of Reproduction 264
2 GONADAL DEVELOPMENT OF SNOWSHOE HARES 265 were made in December, April, June, July, and August. The snowshoe hares were removed from the traps and transported to the field laboratory where they were given a number, sexed, weighed, and examined for ectoparasites and body scars. After this initial processing, the hare was sacrificed by cervical dislocation; the pituitary and adrenal glands were removed and immediately frozen; and the internal organs (liver, spleen, and heart) and testes were removed and weighed. The frozen tissues were later returned to the Univet sity of Wisconsin and sorted as to age and capture date. The pituitary glands were later bioassayed for FSH and LH. Laboratory Data Snowshoe hares were live trapped near Rochester, Alberta, Can. and returned to the University of Wisconsin. Additional hares were raised in captivity. Antmals were caged individually and maintained on a simulated natural light regimen at a temperature of 70-75F. The longest day was June 21(17.2 hr light) and shortest was December 21 (6.8 hr light). Rabbit pellets and water were provided ad libitum with carrots and lettuce provided twice weekly. Five males were selected from the colony every 45 days for 1 year and ml of blood were collected by cardiac puncture from each hare after which each was immediately sacrificed by cervical dislocation; and the anterior pituitary and adrenal glands were removed and weighed to the nearest 0.1 mg. The blood samples were allowed to clot at room temperature and later centrifuged at 2000 rpm in a refrigerated centrifuge. Approximately 20 ml from each hare and all tissues were stored in individual plastic vials at - 15C until the time of bioassay. Bioassay The LH of individual pituitaries was determined by the Bogdanove and Gay (1967) modification of the ovarian ascorbic acid depletion assay (OAAD) (Parlow, 1961). Every assay was conducted with an ovine (NIH-LH-S14) and a domestic rabbit reference preparation at 3 dose levels in the manner previously described (Davis and Meyer, 1971). FSH was estimated by Johnson and Naqvi s (1970) modification of the ovarian augmentation assay (Steelman and Pohley, 1953). This modification required only 2 injections of test material augmented with 50 LU of HCG into 24-day-old Holtzman rats which were autopsied 54 hr after the initial injection. The assays were designed as 2 dose assays with 5 rats/dose. Because the FSH bioassays were not sensitive enough to detect FSH from individual glands, the 5 pituitary glands in each experimental group were pooled. At approximately 9:00 PM on the evening before the FSH and LH bioassays were done, the frozen pituitaries were removed from the freezer and homogenized individually in physiological saline. Preparations of test material for 2 LH assays were made from each pituitary; the remainder of the pituitary was pooled with other pituitaries of the same group and used for the FSH assays. Significance levels between means were determined by Student-Newman-Keuls multiple range test (Sokal and Rohlf, 1969). Regression analysis for testis weights on daylength was computed by the least squares method using the University of Wisconsin Computer Center s STEPREGAN I STATJOB program. (Table 1). RESULTS Gonadotropins and Testis Weight Male snowshoe hares maintained in the laboratory or collected in the field show an increase in pituitary FSH and LH at the onset of the breeding season. FSH reaches a peak by the middle of the breeding season and LH at the end (Fig. 1). Both FSH and LH return to prebreeding season levels by Sept. Hares collected in the field did appear to have less pituitary FSH than the animals maintained in the laboratory (Fig. 1A and B). Testis weights in both the laboratory and field animals were closely related with pituitary FSH (r = 0.841) (Fig. 1A and B). January testis weights of laboratory males were substantially greater than field collected males (Fig. IA and B). Testis Weight and Day!ength Testes from 623 snowshoe hares were collected and weighed between 1961 and A regression line of testis weight on daylength was fitted to the data (N = 119) collected between the shortest day of the year and the beginning of the breeding season (Fig. 2, Line A). This regression has a significant slope with no significant variation from this regression indicating a positive relationship between daylength and testis weight
3 266 DAVIS AND MEYER -.4 I.. I- 0. >..4 I- = I.. 0. B. B ) F M A U 40, s 20 LH A A 5. 0 B FIELD J F MA U J J AS 0 BREEDING x (0 8 SEASON FIG. 1. Pituitary LH, FSH, and testis weight of snowshoe hares at various times throughout the year: (A) data obtained at 45 day intervals from hares maintained in the laboratory. (8)1970 field data from hares collected near Rochester, Alberta, Can. (LH = mean of 5 determinations ±si; FSH = 1 determination of 5 with 95% confidence limits; and testis wt = mean of 5). ILK 10 e d I- A second regression line was fitted to the data (N = 167) collected between the beginning of the breeding season and the summer solstice (Fig. 2, Line B). The slope of regression B is significantly different from the slope of regression A, as well as from zero (Table 1); thus indicating the testis responds more rapidly to increasing daylength prior to the breeding season (Slope A) than during the first half of the breeding season (Slope B). A third regression line was fitted to the data (N = 288) collected between the summer solstice and the birth of the last litter (Fig. 2, Line C). The slope of regression C is significantly different from the slopes of regression A or B (p < 0.01) and indicates that testes rapidly decrease in weight with decreasing daylength (Slope C). From Sept. 1 through the shortest day of the year, the testes are completely regressed, thus no relationship exists between testis weight and daylength. Gonadotropins, Testis Weight, and Daylength The importance of daylength in maintaining snowshoe hares in reproductive condition was examined in this manner. On June BREEDING SEASON I J F M I M lull A $ B HOURS OF DAYLIGHT FIG. 2. Linear regressions of testis weight on daylength: Regression A is calculated from data collected prior to the breeding season; regression B is calculated from data collected from the start of the breeding season to the summer solstice (SS); regression C is calculated from data collected from the SS through the end of the breeding season for snowshoe hares collected near Rochester, Alberta, Can. between 1961 and VE = vernal equinox; AE = autumnal equinox. SS A1E
4 GONADAL DEVELOPMENT OF SNOWSHOE HARES 267 TABLE I SUMMARY OF ANALYSIS OF VARIANCE FOR REGRESSIONS Line Source of variation df Mean square F ratio Significance level A Linear regression <0.001 Residual from regression Controls B Linear regression <0.02 Residual from regression C Linear regression <0.001 Residual from regression TABLE 2 FSH, LH AND PITUITARY WEIGHT OF SNOWSHOE HARES MAINTAINED ON A 17 hr LIGHT-7 hr DARK PHOTOPERIOD Group No. of Pituitary Mean FSH LH (big/pit; (date of an- vt (mg; testis wt (95% CL) ±SE) autopsy) imals ±SE) (g; ±se) (June Serum LH (ng/ml; 21) ± ± ± ± 3.2 ( ) Simulated natural light (Sept. 1) ± ± ± ± 2.4 ( ) Long daylight (Sept. 1) ± ± ± ± when natural daylength was 17.2 hr, 15 male snowshoe hares were selected from the laboratory colony. Five were autopsied immediately and the pituitary glands, testes, and blood were collected. Five were placed on a simulated natural light regimen and 5 on long daylight. Both groups were autopsied on Sept. 1. Simulated natural light resulted in a significant decrease in pituitary LU and FSH, serum LH and testis weight when compared to the June 21 controls (Table 2). In the group maintained on long day light, the decrease in hormone levels and testis weight was significantly retarded (Table 2). DISCUSSION Snowshoe hares near Rochester, Alberta, Can., mate initially in early April with the birth of the fourth litter occurring in early August (Meslow and Keith, 1968). Gonadal ( ) development begins in the winter and reaches a maximum in June followed by a steady decrease or regression (Figs. 1 and 2). A similar pattern of gonadal development is reported for hares in Ontario (MacLulich, 1937). The breeding season is followed by 4 months of complete inactivity of the reproductive tract in both males and females. In upper Michigan (Bookhout, 1965) the snowshoe hare begins the annual recrudescence in the winter as in Alberta, but the testis reaches peak weight in May and then begins the annual regression 1 month earlier than in Alberta. Maximum testis weight in Alberta (54#{176} N latitude) is over 8 g but only 6 g in upper Michigan (46#{176} N latitude). This variation in testis weight in the 2 studies could be due to the difference in latitude as Moreau et a!. (1947) noted in some avian species. The annual variation in gonadal ±SE)
5 268 DAVIS AND MEYER size was correlated with latitude with the northern avian species showing a much greater difference between maximum and minimum testis dimensions. How the breeding seasons in these 2 separate geographic locations are regulated remains unanswered. Since the early work on snowshoe hare coat color (Lyman, 1943) and reproduction (Severaid, 1942) daylength has been considered the obvious proximal factor regulating the seasonal changes in the reproductive cycle of the hare. Our observation that hares maintained on simulated natural light have an annual gonadal cycle similar to the naturally occurring animals lends additional support to this earlier assumption. Prior to the breeding season testis weight is a positive linear function of increasing daylength (Fig. 2). For example, the testis would be expected to increase 18 mg for a I mm increase in daylength or on Feb. 14 when daylength increases 4 mm over the previous day, a testis should increase in weight approximately 72 mg. Between the start of the breeding season and the summer solstice, the regression of testis weight on daylength has a lesser slope with greater variance than prior to the breeding season indicating light is not as important in determining testis weight. This difference in the function of light could come from at least 2 sources. First, perhaps at the start of the breeding season when the testis reaches approximately 6 g, a given light stimulus is not as effective in promoting testicular growth as it was when the testis was smaller. Secondly, the hares may not respond the same to a daylength over 12 hr as they did for a daylength of less than 12 hr. The latter suggestion seems unlikely since above an undetermined threshold of light duration the manner in which the light ratio is increased does not seem to be significant (Bissonette, 1938; Hammond, 1954). A daylength which was effective in maintaining testis weight prior to the summer solstice was ineffective after the longest day of the year. After the summer solstice, a third regression shows testis weight is a linear function of decreasing daylength. For example, the testis would be expected to decrease 38.4 mg for every minute decrease in daylength, or in July a change of 3.1 mm in daylength would result in a testis weight decrease of 119 mg. Lyman (1943) suggests that it may not be daylength which controls testis development and regression but whether the daylength is increasing or decreasing. In view of our results, this may be true because testes started to increase as soon as the daylength started to increase and regression began as daylength decreased. Since the early pioneer experiments of Rowan (1926) much photo-experimentation has taken place (see reviews by Farner, 1964; Wolfson, 1959; Follett and Farner, 1966). It is now well established that in many north temperate species a response to daylength variation has been evolved as the outstanding stimulator of the hypothalamicpituitary axis controlling gametogenesis. Snowshoe hares show a seasonal increase in pituitary gonadotropins, which begins in the winter and increases to a peak by midsummer before decreasing (Fig. 1). The pituitary content of gonadotropins is thought to be a function of light as it occurs in nature and in the simulated laboratory conditions. Seasonal development of the reproductive function in the hare is more closely correlated with seasonal variation in the pituitary content of FSH than LU (Fig. 1), suggesting that FSH controls gonadal development in the male hare. Therefore, seasonal regression of the testis is a result of decreasing daylength, an absence of stimuli to the hypothalamic-pituitary axis to synthesize and release FSH. It is equally true in other species that under the influence of long days the gonads spontaneously regress as gonadotropin secretion from the anterior pituitary diminishes and imposes a period of sexual quiescence
6 GONADAL DEVELOPMENT OF SNOWSHOE HARES 269 (Benoit et al., 1950; Greeley and Meyer, 1953; Lofts and Marshall, 1958). Previous work in our laboratory indicates that during the quiescent period of the sexual cycle in snowshoe hares the pituitary is not releasing gonadotropin. Therefore, we believe that seasonal regression and recrudescence of the testis in the hare is a direct function of gonadotropin release, primarily FSH, which is controlled by daylength mediated through the hypothalamus. REFERENCES ALLANSON, M., HILL, R. T., AND PARKES, A. 5. (1934). Induction of fertility and pregnancy in anoestrous ferret. Proc. Roy. Soc., Ser. B, 115, BENOIT, J., ASSENMACHER, 1., AND WALTER, F. X. (1950). Responses du mechanisme gonado-stimulant a leclairement artificiel et la prehypophyse aux castrations bilaterale et unilaterale, chez 1e canard domestique male, au cours de la periode de regression testiculaire saisonniere. C. R. Soc. Biol. 144, BISSONETTE, T. H. (1938). Influence of light on the hypophysis. Endocrinology 22, BOGDANOVE, E. M., AND GAY, V. L. (1967). Enhancement of the ovarian ascorbic acid depletion response during estrogen prolonged pseudopregnancy. An improved bioassay for LH. Endocrinology 81, BOOKI-tOUT, T. A. (1965). Breeding biology of snowshoe hares in Michigan s Upper peninsula. J. Wild!. Manage. 29, DAVIS, G. J., AND MEYER, R. K. (1971). FSH and LH in snowshoe hares during the increasing phase of the 10-year cycle, unpublished data. FARNER, D. 5. (1961). Comparative physiology: photoperiodicity. Annit. Rev. Physiol. 23, FARNER, D. S. (1964). The photoperiodic control of reproductive cycles in birds. Amer. Sci. 52, FOLLETr, B. K., AND FARNER, D. S. (1966). The effectsof the daily photoperiod on gonadal growth, neurohypophysial hormone content and neurosecretion in hypothalamo-hypophysial system of the Japanese quail (Coturnix coturnix japonica). Geit. Comp. Endocrinol. 7, FOREMAN, D. (1962). The normal reproductive cycle of the prairie dog and the effect of light. Aizat. Rec. 121, GREELEY, F., AND MEYER, R. K. (1953). Seasonal variation in testis-stimulating activity of male pheasant pituitary glands. Auk 70, HAMMOND, J., JR. (1954). Light regulation of hormone secretion. Vitam. Horm. (New York) 12, JOHNSON, D. C., AND NAQVI, R. H. (1970). A simplified augmented ovarian weight assay for folliclestimulating hormone. Proc. Soc. Exp. Biol. Med. 133, LOFTS, B., AND MARSHALL, A. J. (1958). An investigation of the refractory period of reproduction in male birds by means of exogenous prolactin and follicle stimulating hormones. J. Endocrinol. 17, LYMAN, C. P. (1943). Control of coat color in the varying hare, Lepus americanus. Bull. Miis. Comp. Zoo!., Harvard Univ. 93, MACLULICH, D. A. (1937). Fluctuations in the numbers of the varying hare (Lepus americaiu,s). Univ. Toronto Stud., Biol. Ser. 43, 136. MARSHALL, F. H. A. (1942). Exteroceptive factors in sexual periodicity. Biol. Rev. Cambridge P/id. Soc. 17, MARSHALL, F. H. A., AND BOWDEN, F. P. (1934). The effect of irradiation with different wavelengths on the oestrous cycle of ferrets, with remarks on the factors controlling sexual periodicity. J. Exp. Biol. 11, MARSHALL, F. H. A., AND BOWDEN, F. P. (1936). Further effects of irradiation on oestrous cycle of ferret. J. Exp. Biol. 13, MESLow, E. C., AND KEITH, L. B. (1968). Demographic parameters of a snowshoe hare population. J. Wild!. Manage. 32, M0REAu, R. E., WILK, A. L., AND ROWAN, W. (1947). The moult and gonad cycles of three species of birds at five degrees south of the equator. Proc. Zoo!. Soc. London 117, PARLOW. A. F. (1961). Human Pituitary Gonadotropins (A. Albert, ed), p Thomas, Springfield, IL. ROWAN, W. (1926). On photoperiodism, reproductive periodicity and annual migration of birds and certain fishes. Proc. Boston Soc. Nat. Hist. 38, SEVERAID, J. H. (1942). The snowshoe hare, its life history and artificialpropagation. Maine Dept. Inland Fisheries Game. 95 pp. SOKAL, R. R., AND ROHLF, F. J. (1969). Biometry. p Freeman, San Francisco. STEELMAN, S. L., AND POHLEY, F. M. (1953). Assay of the folliclestimulating hormone based on the augmentation with human chorionic gonadotropin. Endocrinology 53, WOLFSON, A. (1959). Role of light and darkness in the regulation of spring migration and reproductive cycles in birds. Iii Photoperiodism and Related Phenomena in Plants and Animals. (R. B. Withrow, ed), pp Amer. Ass. Advan. Sci., Washington, D.C.
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