The placenta provides a maternal-fetal exchange interface that maximizes the diffusion of gases, nutrients, and wastes. However, the placenta also may permit diffusion of lipid-soluble steroid hormones that influence processes such as sex-specific fetal development and maternal pregnancy maintenance. In mammals, placental steroid metabolism contributes to regulation of maternal and fetal hormone levels. Such mechanisms may be less highly developed in species that have recently evolved placentation, such as many reptiles. We therefore chose to investigate placental metabolism of steroids in the viviparous lizard Sceloporus jarrovi. In vitro tissue incubations tested the abilities of the chorioallantoic placenta to clear progesterone and corticosterone by converting them to other metabolites and to synthesize progesterone. Placental tissue rapidly cleared progesterone and corticosterone added to the incubation media, indicating that the tissue had converted the steroids to other products. Placental tissue also synthesized substantial concentrations of progesterone from the prohormone pregnenolone. Thus, even in a species with a simple, recently evolved placenta, steroid metabolism appears to be highly developed and could be critical for regulation of maternal and fetal hormone levels. This finding suggests that placental hormone metabolism may be critical to the successful evolution of placentation.
In most species, plasma levels of baseline glucocorticoids such as corticosterone (B) have a circadian rhythm. This rhythm can be entrained by both photoperiod and food intake and is related to aspects of energy intake and metabolism. Marine iguanas (Amblyrhynchus cristatus) offer a unique opportunity to better understand the relative importance of the light:dark cycle versus food intake in influencing the rhythm in baseline B in a natural system. Compared to other species, food intake is not as strictly determined by the phase of the light:dark cycle. Animals feed in the intertidal zone so feeding activity is heavily influenced by the tidal cycle. We measured baseline plasma B levels in free-living iguanas over several 24-h periods that varied in the timing of low tide/foraging activity. We found that baseline B levels were higher during the day relative to night. However, when low tide occurred during the day, baseline B levels dropped coincident with the timing of low tide. Whether the baseline B rhythm (including the drop during foraging) is an endogenous rhythm with a circatidal component, or is simply a result of feeding and associated physiological changes needs to be tested. Together, these data suggest that the baseline B rhythm in marine iguanas is influenced by the tidal cycle/food intake as well as the light:dark cycle.
During development, sex steroids are important in establishing differences between males and females. However, sex steroids also are involved in the development and maintenance of individual differences in morphology and behavior within each sex. As adults, male tree lizards (Urosaurus ornatus) exhibit alternative reproductive tactics correlated with dewlap (throat fan) coloration. Males with orange-blue dewlaps are aggressive and territorial, whereas males with orange dewlaps are less aggressive and employ a satellite strategy. Dewlap coloration develops within the first 90 days after hatching and remains fixed throughout life. Recent work demonstrates that individual males differ in progesterone and testosterone secretion during development, suggesting that these hormones regulate the development of alternative male phenotypes. The current work uses in vitro incubation of adrenal and gonadal tissues to identify the source of progesterone and testosterone during the period of male differentiation and to follow ontogenetic changes in hormone release. The results indicate that, in all developmental stages sampled, adrenal incubations primarily contain progesterone and corticosterone whereas gonadal incubations contain primarily testosterone. These data indicate that the hatchling adrenal is the primary source of progesterone during early post-hatching development. Since progesterone has been demonstrated to play a role in the establishment of individual differences in morphology and behavior in male tree lizards, our results suggest that the hatchling adrenal gland plays an important role in post-hatching development of alternative male phenotypes.
We investigated maternal-fetal hormone transfer in the mountain spiny lizard, Sceloporus jarrovi, a viviparous species with a simple chorioallantoic placenta. In one experiment, we examined the effect of elevated maternal progesterone on fetal and yolk hormone levels. Progesterone implants increased maternal progesterone nearly 100-fold; however, the resulting increase in fetal and yolk progesterone was only about 2% of that seen in mothers, providing evidence that the placenta buffers hormone diffusion. In addition, some effects of progesterone treatment differed between male and female fetuses, suggesting that this buffering may differ between the sexes. In a second experiment, we examined the relationship between maternal and fetal hormone levels in viviparous versus oviparous species. We measured endogenous progesterone, testosterone, estradiol, and corticosterone levels in pregnant S. jarrovi and their fetuses and neonates, and in gravid S. graciosus (an oviparous congener) and their fetuses and hatchlings. No clear relationship was identified between maternal and fetal or hatchling S. graciosus hormone levels. However, the data for S. jarrovi suggest that maternal hormones may inhibit perinatal hormone secretion. These findings indicate that, despite the relatively recent evolutionary origin and simple structure of the S. jarrovi placenta, mechanisms for placental mediation of the maternal-fetal endocrine relationship have evolved. Although the placenta appears to buffer hormone transport, maternal hormones can affect fetal and yolk hormone levels, suggesting that disruption of endocrine regulation could be a physiological cost of the evolution of viviparity.