Demuth Jeffery P, Wade Michael J
Indiana University, Department of Biology, 1001 East 3rd Street, Bloomington, Indiana 47405, USA.
Evolution. 2007 Mar;61(3):694-9. doi: 10.1111/j.1558-5646.2007.00049.x.
The heterogametic sex tends to be rare, absent, sterile, or deformed in F1 hybrid crosses between species, a pattern called Haldane's rule (HR). The introgression of single genes or chromosomal regions from one drosophilid species into the genetic background of another have shown that HR is most often associated with fixed genetic differences in inter-specific crosses. However, because such introgression studies have involved species diverged several hundred thousand generations from a common ancestor, it is not clear whether HR attends the speciation process or results from the accumulation of epistatically acting genes postspeciation. We report the first evidence for HR prior to speciation in crosses between two populations of the red flour beetle, Tribolium castaneum, collected 931 km apart in Colombia and Ecuador. In this cross, HR is manifested as an increase in the proportion of deformed males compared to females and the expression of HR is temperature dependent. Neither population, when crossed to a geographically distant population from Japan, exhibits HR at any rearing temperature. Using joint-scaling analysis and additional data from backcrosses and F2's, we find that the hybrid incompatibilities and the emergence of HR are concurrent processes involving interactions between X-linked and autosomal genes. However, we also find many examples of incompatibilities manifest by F2 and backcross hybrids but not by F1 hybrids and most incompatibilities are not sex different in their effects, even when they involve both X-autosomal interactions and genotype-by-environment interactions. We infer that incipient speciation in flour beetles can occur with or without HR and that significant hybrid incompatibilities result from the accumulation of epistatically acting gene differences between populations without differentially affecting the heterogametic sex in F1 hybrids. The temperature dependence of the incompatibilities supports the inference that genotype-by-environment interactions and adaptation to different environments contribute to the genetic divergence important to postzygotic reproductive isolation.
在物种间的F1杂交中，异配性别往往稀少、缺失、不育或畸形，这种模式被称为霍尔丹法则（HR）。将单个基因或染色体区域从一种果蝇物种渗入到另一种的遗传背景中，这表明HR最常与种间杂交中固定的遗传差异相关。然而，由于此类渗入研究涉及的物种与共同祖先已分化了几十万代，所以尚不清楚HR是伴随着物种形成过程出现，还是物种形成后上位作用基因积累的结果。我们报告了在红粉甲虫栗色赤拟谷盗两个种群杂交中，物种形成之前出现HR的首个证据，这两个种群分别采集于哥伦比亚和厄瓜多尔，相距931公里。在这个杂交中，HR表现为畸形雄性相对于雌性的比例增加，并且HR的表达依赖于温度。当与来自日本的地理上遥远的种群杂交时，这两个种群在任何饲养温度下都不表现出HR。通过联合尺度分析以及回交和F2的额外数据，我们发现杂种不相容性和HR的出现是同时发生的过程，涉及X连锁基因和常染色体基因之间的相互作用。然而，我们也发现许多不相容性的例子在F2和回交杂种中表现出来，但在F1杂种中未表现出来，并且大多数不相容性在影响上没有性别差异，即使它们涉及X - 常染色体相互作用和基因型 - 环境相互作用。我们推断，面粉甲虫的初始物种形成可以伴随着或不伴随着HR发生，并且显著的杂种不相容性是由于种群之间上位作用基因差异的积累导致的，而不会在F1杂种中对异配性别产生不同影响。不相容性对温度的依赖性支持了这样的推断，即基因型 - 环境相互作用以及对不同环境的适应促成了对合子后生殖隔离很重要的遗传分化。
