Trans-seasonal action of androgen in the control of spring courtship behavior in male red-sided garter snakes.

Abstract

Gonadal steroids have traditionally been found to have short-term effects on the mating behavior of adult vertebrates, such that increased steroid hormone levels influence behavior over the course of a few days. Long-term effects also have been observed in which embryonic exposure to steroid hormone influences the sexual behavior of adults. The generality of the paradigms that have resulted from this work must be viewed with caution as all of the species studied exhibit a particular reproductive pattern. Here it is shown that in the adult red-sided garter snake, the seasonal androgen peak in the summer has a delayed action (8 months) on the male's readiness to court the next spring following emergence from hibernation. This suggests that the interval between the exposure to and the effects of steroid hormones in adult vertebrates may range from short latencies to long latencies and that the present dichotomy of organizing (permanent) versus activating (transient) effects of steroid hormones may not apply in certain instances.Originally gonadal steroids were thought to act in vertebrates both early during specific periods of development and later in adulthood. The initial effects on the brain were believed to be permanent (organizational) and the latter effects were thought to be transient (activational) (1). More recent formulations (2-4) recognize that these are not sharp boundaries and that cyclic hormone-induced structural changes can occur in the adult brain in seasonally breeding species, a process referred to as seasonal activation (5, 6). However, in all species so studied there always is a close temporal association between gonadal activity and mating behavior (7). In the red-sided garter snake (Thamnophis sirtalis parietalis), testicular growth occurs only after the brief spring mating season has ended and circulating androgens do not play a role in activating courtship behavior in the spring (8)(9)(10)(11)(12)(13). Testicular androgens appear instead to organize the nervous system during the summer such that the male will respond to the appropriate stimuli the following spring. The long latency (8 months) between the androgen exposure in the summer and the consequent behavioral response the following spring suggests that a hormone-mediated organization of the brain is occurring on a seasonal basis, a process that can be regarded as seasonal organization.Fifteen years ago, I authored the first experiment on the hormonal control of sexual behavior in red-sided garter snakes (14). This initial investigation suggested that the hormonal control of sexual behaviors followed the accepted vertebrate paradigm: estrogen controlled the attractivity of females and androgen activated the courtship responses of males. While the first conclusion has withstood the test of time, the second has not. Because of the few animals available, a sequential testing design was used in that study whereby individual male garter snakes were tested behaviorally and then given androgen during a period that, as we later learne...

Effects of ovariectomy and estrogen replacement on attractivity and receptivity in the red-sided garter snake (Thamnophis sirtalis parietalis)

“…This restriction does not appear to be necessary in female snakes unless the low level of estrogen remaining in ovariectomized animals is sufficient to induce genomic, long-term changes. An alternative mechanism may be that of "gene memory", where estrogen can exert long-term effects on the genome that persist in the absence of the steroid and then elicit a more rapid response when the stimulus is re-instated (Burch and Evans 1986;Hache et al 1987;Crews 1991;Pfaff et al 1994).…”

“…However, although independent of androgenic modulation of courtship behavior in the relative short term (i.e. 1 2 years), males do require periodic exposure to testosterone (T) for the continued seasonal expression of behavior (Crews 1991). For example, males that have been gonadectomized 3~4 years no longer exhibit courtship behavior even after exposure to hibernation conditions.…”

“…For example, males that have been gonadectomized 3~4 years no longer exhibit courtship behavior even after exposure to hibernation conditions. If, however, longterm castrates are implanted with T the summer before hibernation, they will court upon emergence (Crews 1991). Therefore, some exposure to testosterone is necessary to maintain the seasonal expression of sexual behavior, but the short-term activation of courtship appears dependent on the males experiencing a certain temperature regimen.…”

Endocrine mechanisms mediating temperature-induced reproductive behavior in red-sided garter snakes (Thamnophis sirtalis parietalis)

“…Crews and Garstka, 1982). In this dissociated breeder, reproductive behavior does not coincide with peak gonadal activity (Crews, 1984;Crews, 1991;Crews et al, 1984). Rather, mating occurs while plasma sex steroid concentrations are declining, gonads are regressed, and glucocorticoid levels are high (Aleksiuk and Gregory, 1974;Crews 1984;Crews et al, 1984;Whittier et al, 1987b).…”

Sexual Behavior and 2-Deoxyglucose Uptake in Male Red-Sided Gaiter Snakes <i>(Thamnophis sirtalis parietalis)</i>

“…In male garter snakes, courtship behavior in the spring occurs when the levels of circulating sex hormones are low; testicular growth docs not occur until the summer, long after all sexual activity has ceased [Crews et al. 1984;Crews, 1990], Recently it has been shown that the testosterone surge associated with testicular recrudescence in the summer effects brain activity such that males respond appropriately to attractive females on emer gence from hibernation the following sping [Crews, 1991). If sexual behavior can be dissociated from gonadal activity, can the brain areas known to be involved in the control of sexual behavior (data from species with an associated reproductive pattern) be similarly dissociated?…”