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As steroids and steroid-like compounds accumulate in the environment, it has become important to understand how low-dose exposure affects reproductive function. Ovary-intact sheep were used in a multigenerational study, to determine whether chronic exposure to low levels of estrogen disrupts reproductive function and behavior. We assessed parameters of reproductive performance in control and postnatally estradiol-treated females (Generation 1, G1), and their offspring (Generation 2, G2). In the G1 animals, 17beta-estradiol (E) was administered continuously from 4 wk of age at two doses via subcutaneous implants (ultralow E [<1 pg/ml in circulation, n = 8] or low E [1-3 pg/ml, n = 8]). Both doses delayed puberty; low E also produced pronounced prepubertal and seasonal anestrus hypogonadotropism, and delayed the onset of the second breeding season. All G1 animals conceived and produced offspring (G2), the treatment of which resulted from continuous maternal exposure during pregnancy and lactation. Behavioral observations of G2 females revealed that low prenatal E modestly masculinized play behavior and increased the frequency of attempts to displace competitors relative to ultralow E and control animals. The timing and magnitude of the LH surge also differed in prepubertal low prenatal E females relative to the controls, although these differences were not evident when retested at one year of age. These findings support the hypothesis that chronic exposure to physiologic amounts of exogenous estrogens has multigenerational effects on behavior and neuroendocrine function. Despite these disruptive steroid actions, ovarian cyclicity and fertility are not invariably compromised, pointing to an impressive resiliency of the reproductive axis to insult by exogenous estrogenic compounds.

Previous studies of the gray short-tailed opossum have shown that ovarian activity and estrus are induced by male pheromones, but we recently documented urogenital sinus (UGS) estrus in postlactational females despite their isolation from the male stimuli known to be associated with induced estrus. Body weights and UGS smears were collected after removal of pups in midlactation (19-37 days postpartum), after weaning (55-61 days postpartum), or after pheromone exposure. Estradiol was measured by RIA in plasma samples collected from dams during lactation, after separation from pups, and at estrus. Average days to UGS estrus from pup removal or initial pheromone exposure differed (P<0.05) only between the midlactation and pheromone exposure groups. Postlactational females showed a decrease in body weight from the time of pup removal or weaning to estrus, which contrasts with the increase seen in pheromonally stimulated females. Plasma estradiol was elevated at estrus in all groups, and females that were paired with males at postlactational estrus mated and produced litters. This study demonstrates that gray short-tailed opossums consistently experience estrus within 2 wk of weaning their young and that postlactational estrus appears to be hormonally and behaviorally equivalent to estrus induced by direct exposure to male pheromones.

Estrus is induced in female gray short-tailed opossums (Monodelphis domestica) by exposure to male chemical signals (pheromones). Isolated females remain anestrous, but direct exposure to a male or his scent-marked cage induces estrus within 4-6 days. The objective of this study was to investigate the importance of the vomeronasal organ in detection of and response to estrus-inducing pheromones. The vomeronasal organ was surgically removed through the palate from 8 females (VNX); 5 females (SHAM) underwent sham surgeries in which the vomeronasal organ was exposed but not removed. After a 10-day recovery period, females were placed into male scent-marked cages. Body weight and urogenital sinus cytology were monitored throughout the experiment. All females were anesthetized and perfused with 4% paraformaldehyde 12-13 days after initial pheromone exposure. Vomeronasal organ ablation was evaluated histologically in decalcified snouts. In addition, deafferentation of the accessory olfactory bulb was confirmed by use of a lectin stain specific for the vomeronasal nerve and the glomerular layer of the bulb. All females classified as completely VNX (n = 5) remained anestrous throughout the pheromonal exposure. Incompletely VNX females (n = 2) and all SHAM animals exhibited estrus within 7 days of pheromone stimulation. At perfusion, the mean uterine weight (280.71 +/- 95.6 mg/85 g BW) of SHAM females was greater (p < 0.05) than that of unresponsive, VNX females (133.33 +/- 31.14 mg/85 g). This study demonstrates that the vomeronasal organ is an essential component for transduction of male pheromones required for induction of estrus in a marsupial species.