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）之间的演化过渡始终是学界的一大未解谜题。在脊椎动物中，个体性别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），二是胚胎孵化温度驱动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过渡。尽管性别决定机制具有这种演化可塑性，但从基因型性别决定（即从雄性异配性别系统XX/XY，或雌性异配性别系统ZZ/ZW）向温度依赖型性别决定的过渡仍是一个演化难题：这类过渡似乎需要跨越一道适应度低谷，而该低谷源于携带退化性染色体的纯合基因型（即YY或WW个体）的存活能力显著下降。此外，学界尚不明确替代性性别决定形式（如混合型性别决定）能否在漫长的演化时间尺度上持续存在。此前有研究指出，若温度依赖型性逆转（如XX雄性或XY雌性）具有不对称性，即仅发生在同配性别个体中，那么从GSD向TSD的演化过渡会相对容易。然而，直到近年，学界才提出了能够解释这类不对称性逆转的性别决定机制模型。本研究证实，在符合现实的性别决定系统中，针对温度依赖型性别决定的选择压力可轻松驱动从GSD向TSD的演化过渡，且无需产生YY或WW个体。在XX/XY性别决定系统中，仅部分XX个体发生性逆转（由雌性转为雄性）；随着XX个体间的交配，Y染色体（或Y等位基因）会逐渐从种群中消失。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发现的全新演化稳定状态——混合型性别决定系统。本研究阐明了性别决定机制演化的具体路径与最终结局，解决了长期困扰学界的两大性别决定机制演化难题。