Joan M. Whittier

Plasma steroid hormone levels of female red-sided garter snakes, Thamnophis sirtalis parietalis: Relationship to mating and gestation

Plasma levels of progesterone (P), testosterone (T), estradiol (E2), and corticosterone (B) of female red-sided garter snakes were measured during the period of ovarian development. Differences in hormone levels were analyzed with respect to three factors: whether the female mated in the spring, ovarian condition, and time after emergence from hibernation. The influence of these three factors on steroid hormone levels of two groups of females were then compared. In experiment I, females were obtained in the fall, subjected to an artificial dormancy period, and placed on warm, summer-like conditions in the laboratory. In experiment II, females were collected in the spring and sampled in the field. They were held in the field on fluctuating conditions for several weeks and then returned to the laboratory for sampling during early vitellogenesis. Females in experiment I had a shortened but otherwise normal ovarian and gestational cycle, whereas females in experiment II had an ovarian and gestational cycle typical of females in the field. In spite of these differences, the steroid hormone levels in relation to the ovarian cycle were remarkably similar for the two groups of females. We confirmed that mating in the spring induces a surge in E2; E2 also was elevated in a single sample obtained from animals collected in the fall. This elevation in plasma levels of E2 in the fall occurs at a time when the majority of females have recently deposited sperm in their oviducts. Plasma levels of T, P, and B were not significantly influenced by mating. Unlike previous reports of other viviparous snakes, plasma levels of P were low and mostly nondetectable, even during late gestation. Plasma T was significantly elevated around the time of late vitellogenesis and ovulation, and there was a tendency for E2 levels to be elevated at this time. In the field, plasma B levels were initially high immediately after capture and declined with time. Plasma B was significantly elevated in all females several weeks after emergence, suggesting that levels of B may vary with other annual cycles.

Sex steroid hormones during the ovarian cycle of an all-female, parthenogenetic lizard and their correlation with pseudosexual behavior

Cnemidophorus uniparens is a unisexual lizard that reproduces by parthenogenesis. Individuals of this species display male-like and female-like copulatory behaviors during different phases of the ovarian cycle suggesting that these pseudocopulatory behaviors are hormonally activated. To learn more about both the endocrinology of parthenogenesis and the possible hormonal activation of male-like copulatory behavior in female individuals, we (1) characterized changes in plasma levels of the sex steroid hormones progesterone, 5 alpha-dihydrotestosterone, testosterone, and 17 beta-estradiol during the ovarian cycle in both free-living and captive individuals, and (2) measured sex steroid hormones in plasma collected from captive individuals immediately after they expressed male-like or female-like copulatory behavior. In general, the pattern of secretion of ovarian hormones in C. uniparens appears to be similar to that of other oviparous vertebrates with similar reproductive cycles. Estradiol is elevated only during the preovulatory phase, whereas progesterone increases slightly during vitellogenesis and then increases dramatically following ovulation. Circulating levels of androgen are very low and are generally below the sensitivity of our radioimmunoassay at all stages of the ovarian cycle. The hormonal correlates of female-like copulatory behavior suggest that, as in other vertebrates, female receptivity is activated by a synergism of estradiol and progesterone. There is no evidence that the hormonal cycle has been altered to produce elevated levels of androgens during the phase of the cycle when male-like behavior is expressed. Rather it seems more likely that the central nervous system has evolved a novel response to a typical pattern of ovarian steroid hormone secretion. At present, the best hormonal correlate of male-like behavior is that changes in plasma levels of progesterone closely parallel changes in probability of expressing male-like behavior.

SEASONAL REPRODUCTION: PATTERNS AND CONTROL

The great diversity of reproductive tactics among and within vertebrate species is a testament to the many levels of biological organization at which selection acts to shape the reproductive process. In this chapter, we define seasonal reproduction as the occurrence of breeding in an individual at a specific time of year. Populations exhibit seasonal reproduction insofar as the individuals of the population breed synchronously. Seasonal reproductive cycles are not necessarily synonymous with annual reproductive cycles; for example, an individual that breeds in the spring every two or three years has a seasonal cycle, but not an annual one. Aseasonal (or nonseasonal) reproduction includes reproductive patterns in which individuals breed continuously or year around. Aseasonal reproduction may also include reproductive patterns in which individuals of species breed in response to specific yet erratic environmental cues; for example, species living in the deserts of mid-western Australia may breed only when occasional and unpredictable rains inundate an area.

Mating in the red-sided garter snake, Thamnophis sirtalis parietalis: differential effects on male and female sexual behavior

SummaryFemale red-sided garter snakes, Thamnophis sirtalis parietalis, become unattractive to most males after mating in the field and in the laboratory. Male red-sided garter snakes vary in their latencies to court attractive females following copulation, with courtship resuming in minutes to hours. Unsuccessful males in mating balls disperse from mating pairs, but are not residually inhibited from courting attractive females. These patterns of behavior indicate that males have evolved mechanisms to maximize opportunities for copulation with several females, while females mate only once per season.

Gonadotropin-releasing hormone from brains of reptiles: Turtles (Pseudemys scripta) and snakes (Thamnophis sirtalis parietalis)

Gonadotropin-releasing hormone (GnRH)-like peptides were present in whole brain extracts of turtle (Pseudemys scripta) and snake (Thamnophis sirtalis parietalis) with higher content and concentration in the turtle brain. The peptides were identified by cross-reactivity profiles with four GnRH antisera and by retention times on reverse-phase high-pressure liquid chromatography (HPLC) compared with synthetic GnRH standards. Turtle brain extracts contained two HPLC peaks that cross-reacted with GnRH antisera; these peaks eluted from the HPLC in the same positions as chicken I and II GnRH. Snake brain extracts contained only one major HPLC peak (and two minor peaks in some brains) that cross-reacted with anti-GnRH sera; the major peak eluted with the same retention time as chicken I GnRH. Mammalian, salmon, and lamprey GnRH-like peptides were not detected. In extracts from both turtle and snake brains, the cross-reactivity profile of the HPLC peaks compared with those of synthetic chicken I and II GnRH showed a similar order of sensitivity with four antisera. It is likely that chicken I and II GnRH-like peptides were present in ancestral reptiles prior to the evolution of the three living reptilian subclasses of Anapsida (turtle), Lepidosauria (snake and lizard), and Archosauria (alligator). This assertion is based on the present demonstration and work by others showing that chicken I and II GnRH-like peptides are in turtle and alligator, chicken I is in snake, and chicken II is in lizard.

Male-like behaviour in an all-female lizard: relationship to ovarian cycle

Abstract A quantitative analysis of the relationship between pseudocopulatory behaviour and the ovarian cycle in the parthenogenetic lizard Cnemidophorus uniparens indicates (1) that this behaviour is frequently and regularly expressed by captive individuals, and (2) that the sexual role, either male-like or female-like, exhibited by an animal is correlated with its ovarian state. The expression of female-like behaviour patterns was associated with and primarily limited to the vitellogenic stage of the cycle. Male-like behaviour patterns occurred most frequently during post-ovulatory stages but was not limited to these stages. Neither behavioural role was ever expressed by non-reproductive individuals. Reproductive individuals often alternated in assuming the female-like and male-like roles during the progress of the ovarian cycle. These observations suggest that pseudosexual behaviour is hormonally activated in this species. However, it also appears that the prevailing social situation is an important factor determining which behavioural role is taken. This work strengthens the hypothesis that pseudosexual behaviour in all-female lizards occurs as the result of natural selection.

Ovarian development in red-sided garter snakes, Thamnophis sirtalis parietalis: Relationship to mating

Female red-sided garter snakes (Thamnophis sirtalis parietalis) exhibit a complex array of behavioral patterns. Females may mate once, more than once, or not at all in the spring of the year, and a high percentage of females may mate in late summer before returning to winter hibernacula. The role of mating in the induction of ovarian growth in this species is complicated by this pattern of spring and late summer mating. Females hibernated in the laboratory that mate on emergence in the spring exhibit higher frequencies of ovarian recrudescence than females that do not mate when exposed to males. Yet neither male courtship nor mating in the spring is required for ovarian development. However, mated and unmated females collected in the field in the spring of the year do not differ in frequencies of ovarian recrudescence. Ovarian growth in unmated females collected in the spring parallels the incidence of mating in the previous late summer. Thus, mating may influence the initiation of ovarian growth, but the effect can occur immediately (from spring mating) or be stored over winter (from late summer mating). Large year-to-year variation in reproductive rates of female red-sided garter snakes suggests that other factors such as nutrition and stored energy reserves may modify the effects of mating on ovarian growth.

Role of progesterone in the control of female sexual receptivity in Anolis carolinensis

The synergism of progesterone (P) with estrogen (estradiol benzoate, EB) in the facilitation of receptivity in female green anole lizards (Anolis carolinensis) is independent of time since ovariectomy, but is dependent on the time interval between EB and P administration and on the time of year. There is a brief window of time during which P facilitates receptivity in females primed with a subthreshold dose of EB. Sexual receptivity is induced if the time interval between EB and P is 24 hr but not if it is 48 hr. Furthermore, female A. carolinensis appear to be more sensitive to hormone treatment during different times of the year. Ovariectomized green anole females injected with EB and P during the summer are sexually receptive, but if given the same hormone regimen during the winter, they remain unreceptive.

Environmental control of seasonal reproduction in a parthenogenetic lizard Cnemidophorus uniparens

Previous studies of the parthenogenetic whiptail lizard Cnemidophorus uniparens have provided the best evidence for an endogenous circannual rhythm of reproduction in a reptile. However, these studies were restricted to captive animals on constant photothermal conditions. We report the results of field and laboratory studies indicating that timing of reproduction is dramatically affected by seasonal temperature change. Our field data show that between-year variations in timing of breeding in natural populations are correlated with between-year variations in spring temperatures. Our laboratory data demonstrate that reproduction is delayed and synchronized by exposure to winter-like photothermal conditions. Thus, temperature appears to be the most important environmental cue regulating timing of reproduction in this species. However, the conclusion of previous studies that the natural reproductive cycle is controlled by a circannual rhythm is equivocal and requires further study.