Data from: Male spiders control offspring sex ratio through greater production of female-determining sperm

Sex allocation theory predicts that when sons and daughters have different reproductive values, parents should adjust offspring sex ratio towards the sex with the higher fitness return. Haplo-diploid species directly control offspring sex ratio, but species with chromosomal sex determination (CSD) were presumed to be constrained by Mendelian segregation. There is now increasing evidence that CSD species can adjust sex ratio strategically, but the underlying mechanism is not well understood. One hypothesis states that adaptive control is more likely to evolve in the heterogametic sex through a bias in gamete production. We investigated this hypothesis in males as the heterogametic sex in two social spider species that consistently show adaptive female biased sex ratio and in one subsocial species that is characterised by equal sex ratio. We quantified the production of male (0) and female (X) determining sperm cells using flow cytometry, and show that males of social species produce significantly more X-carrying sperm than 0-sperm, on average 70%. This is consistent with the production of more daughters. Males of the subsocial species produced a significantly lower bias of 54% X-carrying sperm. We also investigated whether inter-genomic conflict between hosts and their endosymbionts may explain female bias. Next generation sequencing showed that five common genera of bacterial endosymbionts known to affect sex ratio are largely absent, ruling out that endosymbiont bacteria bias sex ratio in social spiders. Our study provides evidence for paternal control over sex allocation through biased gamete production as a mechanism by which the heterogametic sex in CSD species adaptively adjust offspring sex ratio.

性分配理论（Sex allocation theory）预测，当子代雄性与雌性具备不同的繁殖价值时，双亲应调整子代性比，以偏向能带来更高适合度收益的性别。单倍二倍体物种可直接调控子代性比，但此前学界认为染色体性别决定（chromosomal sex determination, CSD）物种会受孟德尔分离定律的约束。当前越来越多的证据表明，CSD物种可适应性地调整性比，但其背后的分子机制仍未得到充分阐明。其中一项假说提出，异配性别可通过配子产生偏倚，更易演化出适应性的性别分配调控能力。本研究以异配性别雄性为研究对象，针对两种始终表现出适应性雌性偏向性比的社会性蜘蛛物种，以及一种以均等性比为特征的亚社会性物种展开了探究。我们借助流式细胞术（flow cytometry）定量检测了决定雄性（标记为0）与雌性（标记为X）的精子细胞占比，结果显示：社会性蜘蛛物种的雄性产生的携带X的精子占比显著高于携带0的精子，平均占比达70%，这与其产生更多雌性子代的表型相符。而亚社会性物种的雄性产生的携带X的精子偏倚显著更低，仅为54%。我们还探究了宿主与其内共生体之间的基因组间冲突是否能够解释雌性偏向性比的现象。下一代测序（next generation sequencing）结果显示，五种已知会影响性比的常见细菌内共生体属群在样本中基本缺失，由此排除了内共生细菌导致社会性蜘蛛性比偏倚的可能性。本研究提供了直接证据，证明CSD物种的异配性别可通过配子产生偏倚，由父本调控性分配，以此适应性地调整子代性比。