Effects of castration and androgen replacement on male courtship behavior in the red-sided garter snake (Thamnophis sirtalis parietalis)

Camazine, Brian; Garstka, William R.; Tokarz, Richard R.; Crews, David

doi:10.1016/0018-506x(80)90025-2

Cited by 78 publications

(53 citation statements)

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“…Woolley et al, 2004). For example, initial studies of male red-sided garter snakes demonstrated that androgen concentrations were basal during winter dormancy and spring emergence (Camazine et al, 1980;Crews, 1984). Subsequent studies showed that androgen concentrations were elevated upon spring emergence and rapidly declined over the mating season Moore et al, 2000).…”

Section: Sex Steroid Hormone and Corticosterone Profilesmentioning

confidence: 99%

“…Snakes are refractory to warm temperatures and require a period of low temperature conditions for more than 4 weeks to initiate sexual behavior (Camazine et al, 1980;Garstka et al, 1982;Bona-Gallo and Licht, 1983). Reproductive behavior of red-sided garter snakes is also independent of changes in photoperiodic conditions (Nelson et al, 1987;Whittier et al, 1987a).…”

Section: Introductionmentioning

confidence: 99%

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

Lutterschmidt

Mason

2009

Journal of Experimental Biology

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SUMMARYWe investigated the mechanisms by which temperature induces seasonal reproductive behavior in red-sided garter snakes (Thamnophis sirtalis parietalis). Specifically, we addressed whether elevated temperatures during winter dormancy influence (1) diel melatonin and corticosterone rhythms; (2) sex steroid hormone and corticosterone profiles; and (3) the expression of reproductive behavior following emergence. Elevated hibernation temperatures (i.e. 10°C versus 5°C) significantly increased overall melatonin and decreased corticosterone concentrations of snakes. The temperature-induced differences in melatonin rhythms between the 5°C and 10°C treatment groups persisted even after both groups were again acclimated to 10°C, indicating that cold temperature exposure has a lasting influence on melatonin rhythms. Elevated hibernation temperatures also significantly altered androgen and corticosterone profiles of snakes, providing a potential mechanism to explain reported annual variation in steroid hormones. Although previous studies indicate that male red-sided garter snakes exhibit a dissociated reproductive strategy, we demonstrate the presence of intersexual variation in sex steroid hormone profiles, as estradiol concentrations of female snakes increased significantly prior to spring mating activity. Importantly, the percentage change in body mass did not differ significantly between snakes in the hibernation treatments, indicating that the observed changes in hormone profiles are indeed temperature induced and not simply an indirect result of significant changes in the energy balance of snakes. Finally, in males maintained at 10°C during winter dormancy the onset of courtship behavior following emergence was delayed. Our results suggest that environmental temperatures induce reproductive behavior, in part, via changes in diel melatonin and/or corticosterone rhythms in this seasonally breeding reptile.

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Section: Sex Steroid Hormone and Corticosterone Profilesmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

Lutterschmidt

Mason

2009

Journal of Experimental Biology

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“…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.…”

Section: Introductionmentioning

confidence: 99%

“…There is a much greater chance of accepting a false positive (type I error) in a sequential testing design compared to the more commonly used simultaneous testing design (in which different groups are treated at the same time). Our subsequent studies (8)(9)(10)(11)(12)(13) in which the latter design was used revealed that male garter snakes can exhibit courtship behavior in the absence of androgen. The present study thus incorporates both the sequential and simultaneous testing designs.…”

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confidence: 99%

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

Crews

1991

Proc. Natl. Acad. Sci. U.S.A.

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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...

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“…For example, evolution can result in changes in the hormone-dependent behaviours that may not be initially predicted by ecological or evolutionary perspectives. Testosterone may be critical for the expression of sexual behaviour in one species, such as laboratory rats [63], but not in another, such as red-sided garter snakes (Thamnophis sirtalis [64]). Similarly, work in evolutionary developmental biology has shown gene expression underlying traits with the same adaptive function may, or may not, be the same.…”

Section: Review Levels Of Analysis S a Macdougall-shackleton 2079mentioning

confidence: 99%

The levels of analysis revisited

MacDougall‐Shackleton

2011

Phil. Trans. R. Soc. B

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The term levels of analysis has been used in several ways: to distinguish between ultimate and proximate levels, to categorize different kinds of research questions and to differentiate levels of reductionism. Because questions regarding ultimate function and proximate mechanisms are logically distinct, I suggest that distinguishing between these two levels is the best use of the term. Integrating across levels in research has potential risks, but many benefits. Consideration at one level can help generate novel hypotheses at the other, define categories of behaviour and set criteria that must be addressed. Taking an adaptationist stance thus strengthens research on proximate mechanisms. Similarly, it is critical for researchers studying adaptation and function to have detailed knowledge of proximate mechanisms that may constrain or modulate evolutionary processes. Despite the benefits of integrating across ultimate and proximate levels, failure to clearly identify levels of analysis, and whether or not hypotheses are exclusive alternatives, can create false debates. Such non-alternative hypotheses may occur between or within levels, and are not limited to integrative approaches. In this review, I survey different uses of the term levels of analysis and the benefits of integration, and highlight examples of false debate within and between levels. The best integrative biology reciprocally uses ultimate and proximate hypotheses to generate a more complete understanding of behaviour.

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Effects of castration and androgen replacement on male courtship behavior in the red-sided garter snake (Thamnophis sirtalis parietalis)

Cited by 78 publications

References 35 publications

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

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

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

The levels of analysis revisited

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