Stepwise evolution of a butterfly supergene via duplication and inversion

Supergenes maintain adaptive clusters of alleles in the face of genetic mixing. Although usually attributed to inversions, supergenes can be complex, and reconstructing the precise processes that led to recombination suppression and their timing is challenging. We investigated the origin of the BC supergene, which controls variation in warning colouration in the African Monarch butterfly, Danaus chrysippus. By generating chromosome-scale assemblies for all three alleles, we identified multiple structural differences. Most strikingly, we find that a region of >1 million bp underwent several segmental duplications at least 7.5 million years ago. The resulting duplicated fragments appear to have triggered four inversions in surrounding parts of the chromosome, resulting in stepwise growth of the region of suppressed recombination. Phylogenies for the inversions are incongruent with the species tree, and suggest that structural polymorphisms have persisted for at least 4.1 million years....

超基因（supergenes）可在基因混合的背景下维持等位基因的适应性聚类。尽管超基因通常被归因于染色体倒位，但其结构往往较为复杂，且重构导致重组抑制的精确过程及其发生时间颇具挑战。我们针对BC超基因（BC supergene）的起源展开了研究，该超基因可调控非洲帝王蝶（Danaus chrysippus）的警戒色变异。通过对全部三种等位基因构建染色体级别的基因组组装序列，我们鉴定出了多种结构差异。最引人注目的是，一段长度超过100万碱基对的区域在至少750万年前发生了多次片段重复。由此产生的重复片段似乎触发了染色体周边区域的四次倒位，进而使得重组抑制区域逐步扩张。这些倒位的系统发育树与物种树并不一致，表明结构多态性至少已存续了410万年……