Data from: Novel evolutionary pathways of sex-determining mechanisms

Evolutionary transitions between sex-determining mechanisms (SDMs) are an enigma. Among vertebrates, individual sex (male or female) is primarily determined by either genes (genotypic sex determination, GSD) or embryonic incubation temperature (temperature-dependent sex determination, TSD), and these mechanisms have undergone repeated evolutionary transitions. Despite this evolutionary lability, transitions from GSD (i.e. from male heterogamety, XX/XY, or female heterogamety, ZZ/ZW) to TSD are an evolutionary conundrum, as they appear to require crossing a fitness valley arising from the production of genotypes with reduced viability owing to being homogametic for degenerated sex chromosomes (YY or WW individuals). Moreover, it is unclear whether alternative (e.g. mixed) forms of sex-determination can persist across evolutionary time. It has previously been suggested that transitions would be easy if temperature-dependent sex-reversal (e.g. XX male or XY female) were asymmetrical, occurring only in the homogametic sex. However, only recently has a mechanistic model of sex determination emerged that may allow such asymmetrical sex-reversal. We demonstrate that selection for TSD in a realistic sex-determining system can readily drive evolutionary transitions from GSD to TSD that do not require the production of YY or WW individuals. In XX /XY systems, sex-reversal (female to male) occurs in a portion of the XX individuals only, leading to the loss of the Y allele (or chromosome) from the population as XX individuals mate with each other. The outcome is a population of XX individuals whose sex is determined by incubation temperature (TSD). Moreover, our model reveals a novel evolutionarily stable state representing a mixed-mechanism system that has not been revealed by previous approaches. This study solves two long-standing puzzles of the evolution of sex-determining mechanisms by illuminating the evolutionary pathways and endpoints.

性别决定机制（sex-determining mechanisms, SDMs）之间的演化转变一直是学界的未解之谜。在脊椎动物中，个体性别（雄性或雌性）主要由两类因素决定：一是基因调控的基因型性别决定（genotypic sex determination, GSD），二是胚胎孵化温度介导的温度依赖型性别决定（temperature-dependent sex determination, TSD），且这类性别决定机制已多次发生演化转变。尽管存在这种演化可塑性，但从GSD（即从雄性异配性别XX/XY系统，或雌性异配性别ZZ/ZW系统）向TSD的演化转变仍是一道演化难题：这一过程似乎需要跨越一个适合度低谷，该低谷源于携带退化性染色体的纯合子个体（YY或WW个体）生存力降低的基因型的产生。此外，目前学界尚不清楚替代性性别决定形式（如混合型性别决定系统）能否在演化时间尺度上持续存续。此前有研究提出，若温度依赖的性反转（如XX雄性或XY雌性）具有不对称性，仅发生在纯合子性别中，那么这类演化转变会更容易实现。然而，直到近期，学界才提出了能够解释这类不对称性反转的性别决定机制模型。我们的研究表明，在符合现实的性别决定系统中，针对TSD的选择可轻易驱动从GSD向TSD的演化转变，且无需产生YY或WW个体。在XX/XY系统中，仅部分XX个体发生性反转（雌性转为雄性），随着XX个体间的交配，Y等位基因（或Y染色体）会从种群中逐渐丢失。最终种群将全部由XX个体组成，其性别由孵化温度决定（即TSD）。此外，我们的模型还揭示了一种此前未被过往研究发现的、全新的演化稳定状态——混合型性别决定系统。本研究阐明了性别决定机制演化的路径与终点，解决了该领域两个长期存在的经典谜题。