Data from: Multiple large inversions and breakpoint rewiring of gene expression in the evolution of the fire ant social supergene

Supergenes consist of co-adapted loci that segregate together and are associated with adaptive traits. In the fire ant Solenopsis invicta, two ‘social’ supergene variants regulate differences in colony queen number and other traits. Suppressed recombination in this system is maintained, in part, by a >9 Mb inversion, but the supergene is larger. Has the supergene in S. invicta undergone multiple large inversions? The initial gene content of the inverted allele of a supergene would be the same as that of the wild-type allele. So, how did the inversion increase in frequency? To address these questions, we cloned one extreme breakpoint in the fire ant supergene. In doing so, we found a second large (>800 Kb) rearrangement. Furthermore, we determined the temporal order of the two big inversions based on the translocation pattern of a third small fragment. Because the S. invicta supergene lacks evolutionary strata, our finding of multiple inversions may support an introgression model of the supergene. Finally, we showed that one of the inversions swapped the promoter of a breakpoint-adjacent gene, which might have conferred a selective advantage relative to the non-inverted allele. Our findings provide a rare example of gene alterations arising directly from an inversion event.

超基因（supergene）由共分离且与适应性性状相关的共适应基因座（co-adapted loci）构成。在红火蚁（Solenopsis invicta）中，两种“社会性”超基因变体可调控蚁群蚁后数量等性状的差异。该系统中的重组抑制（suppressed recombination）部分由一段长度超过9兆碱基（Mb）的倒位维持，但超基因的实际长度更长。红火蚁的超基因是否经历过多次大型倒位？超基因倒位等位基因的初始基因组成与野生型等位基因一致，那么倒位是如何实现频率提升的？为解答上述问题，我们克隆了红火蚁超基因的一个极端断点，并在此过程中发现了第二个大型（>800千碱基Kb）重排事件。此外，我们通过第三个小片段的易位模式（translocation pattern）确定了这两次大型倒位的时间顺序。由于红火蚁超基因不存在进化层（evolutionary strata），我们发现的多次倒位现象或可支持超基因的渐渗模型（introgression model）。最后，我们证实其中一次倒位替换了断点邻近基因（breakpoint-adjacent gene）的启动子（promoter），这可能使该等位基因相较于非倒位等位基因获得了选择优势（selective advantage）。本研究结果为直接由倒位事件引发基因改变的案例提供了罕见例证。