Department of Cell Biology, Duke University Medical Center, Durham, NC 27701, USA.
Department of Ecology, Faculty of Science Charles University, Viničná 7, Praha 2 12844, Czech Republic.
Curr Biol. 2023 Jul 24;33(14):3017-3023.e2. doi: 10.1016/j.cub.2023.06.008. Epub 2023 Jun 23.
In many reptile species, gonadal sex is affected by environmental temperature during a critical period of embryonic development-a process known as temperature-dependent sex determination (TSD). The oviparous red-eared slider turtle, Trachemys scripta, has a warm-female/cool-male TSD system and is among the best-studied members of this group. When incubated at low temperatures, the somatic cells of the bipotential gonad differentiate into Sertoli cells, the support cells of the testis, whereas at high temperatures, they differentiate into granulosa cells, the support cells of the ovary. Here, we report the unexpected finding that temperature independently affects the number of primordial germ cells (GCs) in the embryonic gonad at a time before somatic cell differentiation has initiated. Specifically, embryos incubated at higher, female-inducing temperatures have more GCs than those incubated at the male-inducing temperature. Furthermore, elimination of GCs in embryos incubating at intermediate temperatures results in a strong shift toward male-biased sex ratios. This is the first evidence that temperature affects GC number and the first evidence that GC number influences sex determination in amniotes. This observation has two important implications. First, it supports a new model in which temperature can impact sex determination in incremental ways through multiple cell types. Second, the findings have important implications for a major unresolved question in the fields of ecology and evolutionary biology-the adaptive significance of TSD. We suggest that linking high GC number with female development improves female reproductive potential and provides an adaptive advantage for TSD.
在许多爬行动物物种中，性腺性别受胚胎发育关键期环境温度的影响，这一过程被称为温度依赖型性别决定（TSD）。卵生的红耳滑龟（Trachemys scripta）具有暖-雌性/冷-雄性 TSD 系统，是该类群中研究最多的物种之一。当在低温下孵化时，双能性腺的体细胞分化为睾丸的支持细胞——支持细胞，而在高温下，它们分化为卵巢的支持细胞——颗粒细胞。在这里，我们报告了一个意外的发现，即在体细胞分化开始之前，温度独立地影响胚胎性腺中原始生殖细胞（GCs）的数量。具体来说，在诱导雌性的较高温度下孵化的胚胎比在诱导雄性的温度下孵化的胚胎具有更多的 GCs。此外，在中间温度下孵化的胚胎中消除 GCs 会导致性别比例向雄性偏斜的强烈转变。这是温度影响 GC 数量的第一个证据，也是 GC 数量影响羊膜动物性别决定的第一个证据。这一观察结果有两个重要的含义。首先，它支持了一个新的模型，即温度可以通过多种细胞类型以渐进的方式影响性别决定。其次，这些发现对生态学和进化生物学领域一个未解决的重大问题具有重要意义——TSD 的适应意义。我们认为，将高 GC 数量与雌性发育联系起来可以提高雌性的生殖潜力，并为 TSD 提供适应优势。
