Data from: Genetic architecture of isolation between two species of Silene with sex chromosomes and Haldane's rule

Examination of the genetic architecture of hybrid breakdown can provide insight into the genetic mechanisms of commonly observed isolating phenomena such as Haldane’s rule. We used line-cross analysis to dissect the genetic architecture of divergence between two plant species that exhibit Haldane’s rule for male sterility and rarity, Silene latifolia and Silene diclinis. We made 15 types of crosses, including reciprocal F1, F2, backcrosses, and later-generation crosses, grew the seeds to flowering, and measured the number of viable ovules, proportion of viable pollen, and sex ratio. Typically, Haldane’s rule for male rarity in XY animal hybrids is explained by interactions involving recessive X-linked alleles that are deleterious when hemizygous (dominance theory), while sterility is explained by rapid evolution of spermatogenesis genes (faster-male evolution). In contrast, we found that the genetic mechanisms underlying Haldane’s rule between the two Silene species did not follow these conventions. Dominance theory was sufficient to explain male sterility, but male rarity likely involved faster-male evolution. We also found an effect of the neo-sex chromosomes of S. diclinis on the extreme rarity of some hybrid males. Our findings suggest that the genetic architecture of Haldane’s rule in dioecious plants may differ from those commonly found in animals.

解析杂交衰败的遗传架构，可为霍尔丹法则（Haldane’s rule）这类常见生殖隔离现象的遗传机制提供重要研究视角。本研究以表现出雄性不育与雄性稀有性霍尔丹法则的两种植物物种——宽叶蝇子草（Silene latifolia）与二性蝇子草（Silene diclinis）——为研究对象，采用品系杂交分析法（line-cross analysis）解析二者的分化遗传架构。我们构建了15类杂交组合，涵盖正反交F1、F2、回交以及后续世代杂交，将种子培育至开花期，并测定了可育胚珠数量、可育花粉比例以及性比。通常情况下，XY型动物杂种中雄性稀有性的霍尔丹法则，可通过涉及隐性X连锁等位基因的互作机制解释——这类等位基因在半合子状态下会产生有害效应（显性学说）；而雄性不育则可由精子发生基因的快速演化（雄性快速演化假说）加以阐释。与之形成鲜明对比的是，本研究发现这两种蝇子草物种间霍尔丹法则的遗传机制并未遵循上述经典范式。显性学说足以解释雄性不育现象，但雄性稀有性大概率与雄性快速演化相关。我们还观测到，二性蝇子草的新性染色体（neo-sex chromosomes）对部分杂交雄性的极端稀有性存在显著影响。本研究结果表明，雌雄异株植物中霍尔丹法则的遗传架构，或与动物中普遍观测到的遗传模式存在显著差异。