Department of Biology, Harrisonburg, James Madison University, VA, United States.
Department of Cellular and Molecular Biology, University of Wisconsin, Madison, WI, United States.
Front Endocrinol (Lausanne). 2023 Mar 13;14:1135535. doi: 10.3389/fendo.2023.1135535. eCollection 2023.
Sex steroid hormones are powerful regulators of reproductive behavior and physiology in vertebrates, and steroidogenesis has distinct sex- and season-specific patterns ultimately dictated by the expression of key enzymes. Most comparative endocrinology studies, however, focus only on circulating levels of sex steroids to determine their temporal association with life-history events in what are termed associated reproductive patterns. The red-sided garter snake () is a notable exception; this species exhibits maximal sex behavior decoupled from maximal sex steroid production and gametogenesis in what is termed a dissociated reproductive pattern. And while this is true for male red-sided garter snakes and their production of testosterone, females have maximal estradiol production during peak breeding (spring) but only immediately after mating. Here, we demonstrate that expression of ovarian aromatase (conversion of androgens to estrogens) matches the established seasonal hormone pattern in females. Additionally, steroidogenic gene expression in the ovary is broadly reduced if not suppressed compared to the testis throughout the active year. Bizarrely, male red-sided garter snakes demonstrate an unexplained pattern of steroidogenic gene expression in the testis. StAR (import of cholesterol to steroidogenesis) is maximally expressed in spring, yet Hsd17b3 expression (conversion of androstenedione to testosterone) is highest in summer, with the latter matching the established summer peak in male testosterone. The function of elevated StAR in spring is unknown, but our results suggest a decoupling between maximal StAR expression and testosterone biosynthesis (Hsd17b3 expression). We also purport that the reproductive pattern binary should be reassessed given its lack of fit for many vertebrate species that demonstrate seasonal, mixed patterns of (a)synchrony between circulating sex hormones and reproductive behavior.
性甾体激素是脊椎动物生殖行为和生理学的强有力调节剂，类固醇生成具有明显的性别和季节性特定模式，最终由关键酶的表达决定。然而，大多数比较内分泌学研究仅关注循环中的性激素水平，以确定它们与所谓的相关生殖模式中生命史事件的时间关联。红边束带蛇 () 是一个显著的例外；这种物种表现出最大的性行为，与最大的性激素产生和配子发生分离，这被称为分离的生殖模式。虽然这对于雄性红边束带蛇及其睾丸酮的产生是正确的，但雌性在高峰期繁殖（春季）时具有最大的雌二醇产生，但仅在交配后立即产生。在这里，我们证明卵巢芳香酶的表达（将雄激素转化为雌激素）与雌性的季节性激素模式相符。此外，与睾丸相比，卵巢中的类固醇生成基因表达在整个活跃年内广泛降低，如果不是被抑制的话。奇怪的是，雄性红边束带蛇的睾丸中表现出一种无法解释的类固醇生成基因表达模式。StAR（胆固醇向类固醇生成的输入）在春季表达最高，而 Hsd17b3 表达（雄烯二酮向睾丸酮的转化）在夏季最高，后者与雄性睾丸酮的夏季高峰相匹配。春季高 StAR 的功能尚不清楚，但我们的结果表明，最大 StAR 表达与睾丸酮生物合成（Hsd17b3 表达）之间存在解耦。我们还声称，鉴于缺乏适应许多表现出循环性激素和生殖行为之间同步季节性混合模式的脊椎动物物种，生殖模式二元性应重新评估。
