Origin and transition of sex determination mechanisms in a gynogenetic hexaploid fish

Most vertebrates reproduce sexually, and plastic sex determination mechanisms including genotypic sex determination (GSD) and environmental sex determination (ESD) have been extensively revealed. However, why sex determination mechanisms evolve diversely and how they correlate with diverse reproduction strategies remain largely unclear. Here, we utilize the superiority of a hexaploid gibel carp (Carassius gibelio) that is able to reproduce by unisexual gynogenesis and contains a rare but diverse proportion of males to investigate these puzzles. A total of 2248 hexaploid specimens were collected from 34 geographic wild populations throughout mainland China, in which 24 populations were revealed to contain 186 males with various incidences ranging from 1.2 to 26.5%. Subsequently, the proportion of temperature-dependent sex determination (TSD) was revealed to be positively correlated to average annual temperature in wild populations, and male incidence in lab gynogenetic progenies was demonstrated to increase with the increasing of larval rearing temperature. Meanwhile, extra microchromosomes were confirmed to play genotypic male determination role as previously reported. Thereby, GSD and TSD were found to coexist in gibel carp, and the proportions of GSD were observed to be much higher than that of TSD in sympatric wild populations. Our findings uncover a potential new mechanism in the evolution of sex determination system in polyploid vertebrates with unisexual gynogenesis ability, and also reveal a possible association of sex determination mechanism transition between TSD and GSD and reproduction mode transition between unisexual gynogenesis and bisexual reproduction.

大多数脊椎动物进行有性繁殖，包括基因型性别决定（GSD）和环境型性别决定（ESD）在内的可塑性性别决定机制已被广泛揭示。然而，性别决定机制为何多样进化以及它们如何与多样的繁殖策略相关联，在很大程度上仍不清楚。在此，我们利用六倍体银鲫（Carassius gibelio）的优势来研究这些难题，银鲫能够通过单性雌核生殖繁殖，并且包含比例稀少但多样的雄性。从中国大陆的34个地理野生种群共收集了2248个六倍体样本，其中24个种群被发现含有186只雄性，其发生率在1.2%到26.5%之间不等。随后，发现温度依赖性性别决定（TSD）的比例与野生种群的年平均温度呈正相关，并且实验室雌核生殖后代中的雄性发生率被证明随着幼体饲养温度的升高而增加。同时，如先前报道的那样，额外的微染色体被证实起到基因型雄性决定作用。因此，发现GSD和TSD在银鲫中共存，并且在同域野生种群中观察到GSD的比例远高于TSD。我们的研究结果揭示了具有单性雌核生殖能力的多倍体脊椎动物性别决定系统进化中的一种潜在新机制，并且还揭示了TSD和GSD之间性别决定机制转变以及单性雌核生殖和两性繁殖之间繁殖模式转变的一种可能关联。