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INTRODUCTION
Secondary sexual signals (coloration, morphology, scents) mostly
serve as honest indicators of an individual’s genetic sex and potential
mate quality. Many vertebrate secondary sexual signals are directly
controlled by sex steroid hormones, which can reinforce their value
as honest signals because primary sex steroids, such as testosterone
and 17-estradiol, exhibit sexually dimorphic patterns that correlate
with an individual’s genetic sex and quality/health. Such signals can
be expressed seasonally (e.g. breeding plumage, skin coloration) or
for the duration of the annual cycle (e.g. electric waveforms) and are
often subject to modulation and/or regulation by sex steroids.
Sexual signals and the sensory systems required for their
perception (visual, auditory, olfactory) are directly influenced by
sex steroid hormones during development. Key experiments done
by Phoenix et al. demonstrated that sex steroids are crucial for
guiding the organization of neural centers controlling sex-specific
behavior and that the presence of those same sex steroids or others
are necessary later in life to activate sexual behavior controlled by
these centers (Phoenix et al., 1959). Their results established that
sex steroids have two major effects in vertebrate reproduction:
permanent (organizational) and reversible (activational). Although
this generalized verbal model has been adjusted to accommodate
other, more complicated pathways through which sex hormones act
(e.g. Moore et al., 1998), the concept of activational/organizational
effects of steroids generally fits most systems and has repeatedly
passed experimental tests [reviewed extensively in a special issue
of Hormones and Behavior (Wallen, 2009)].
Organizational and activational effects of steroids on sexual
signals (e.g. behavior, coloration) have been demonstrated in
numerous vertebrate groups. For testing organizational effects,
individuals or whole clusters of offspring are exposed either in utero
or at birth to exogenous sex steroids and then followed into
adulthood to examine the effects of treatment on specific secondary
sexual signals. Largely, these experiments study changes in
behaviors and their neurological centers following steroid treatment
[e.g. singing behavior in zebra finches, Taeniopygia guttata (Gurney
and Konishi, 1980) and courtship behavior in Japanese quail,
Coturnix japonica (Adkins, 1979)]. Activational effects of steroid
hormones on secondary sexual signals, however, focus on the signals
themselves and how they respond to steroid treatment over smaller
windows of time, typically in adults. The activation of conspicuous
and/or powerful sexual signals by primary sex steroids is present
in all vertebrate groups [e.g. fish (Liley and Stacey, 1983),
amphibians (Kelley and Pfaff, 1976), reptiles (Cooper et al., 1987),
birds (van Oordt and Junge, 1934) and mammals (Carlisle et al.,
1981)].
The Journal of Experimental Biology 215, 723-730
© 2012. Published by The Company of Biologists Ltd
doi:10.1242/jeb.064923
RESEARCH ARTICLE
How to make a sexy snake: estrogen activation of female sex pheromone in male
red-sided garter snakes
M. Rockwell Parker* and Robert T. Mason
Department of Zoology, Oregon State University, 3029 Cordley Hall, Corvallis, OR 97331, USA
*Author for correspondence at present address: Monell Chemical Senses Center, 3500 Market Street, Philadelphia, PA 19104, USA
(rparker@monell.org)
Accepted 15 November 2011
SUMMARY
Vertebrates indicate their genetic sex to conspecifics using secondary sexual signals, and signal expression is often activated by
sex hormones. Among vertebrate signaling modalities, the least is known about how hormones influence chemical signaling. Our
study species, the red-sided garter snake (Thamnophis sirtalis parietalis), is a model vertebrate for studying hormonal control of
chemical signals because males completely rely on the female sex pheromone to identify potential mates among thousands of
individuals. How sex hormones can influence the expression of this crucial sexual signal is largely unknown. We created two
groups of experimental males for the first experiment: Sham (blank implants) and E2 (17-estradiol implants). E2 males were
vigorously courted by wild males in outdoor bioassays, and in a Y-maze E2 pheromone trails were chosen by wild males over
those of small females and were indistinguishable from large female trails. Biochemically, the E2 pheromone blend was similar to
that of large females, and it differed significantly from Shams. For the second experiment, we implanted males with 17-estradiol
in 2007 but removed the implants the following year (2008; Removal). That same year, we implanted a new group of males with
estrogen implants (Implant). Removal males were courted by wild males in 2008 (implant intact) but not in 2009 (removed). Total
pheromone quantity and quality increased following estrogen treatment, and estrogen removal re-established male-typical
pheromone blends. Thus, we have shown that estrogen activates the production of female pheromone in adult red-sided garter
snakes. This is the first known study to quantify both behavioral and biochemical responses in chemical signaling following sex
steroid treatment of reptiles in the activation/organization context. We propose that the homogametic sex (ZZ, male) may possess
the same targets for activation of sexual signal production, and the absence of the activator (17-estradiol in this case) underlies
expression of the male phenotype.
Key words: activation, pheromone, chemical ecology, endocrinology, reproduction, snake.
THEJOURNALOFEXPERIMENTALBIOLOGY