Supergenes, regions of the genome with suppressed recombination between sets of functional mutations, contribute to the evolution of complex phenotypes in diverse systems. Excluding sex chromosomes, most supergenes discovered so far appear to be young, being found in one species or a few closely related species. Here, we investigate how a chromosome harbouring an ancient supergene has evolved over about 30 million years (Ma). The Formica supergene underlies variation in colony queen number in at least five species. We expand previous analyses of sequence divergence on this chromosome to encompass about 90 species spanning the Formica phylogeny. Within the nonrecombining region, the gene knockout contains 22 single nucleotide polymorphisms (SNPs) that are consistently differentiated between two alternative supergene haplotypes in divergent European Formica species, and we show that these same SNPs are present in most Formica clades. In these clades, including an early diverging Nearctic Formica clade, individuals with alternative genotypes at knockout also have higher differentiation in other portions of this chromosome. We identify hotspots of SNPs along this chromosome that are present in multiple Formica clades to detect genes that may have contributed to the emergence and maintenance of the genetic polymorphism. Finally, we infer three gene duplications on one haplotype, based on apparent heterozygosity within these genes in the genomes of haploid males. This study strengthens the evidence that this supergene originated early in the evolution of Formica and that just a few loci in this large region of suppressed recombination retain strongly differentiated alleles across contemporary Formica lineages.

中文翻译：

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古代社会超基因中多态性的维持

超基因是基因组中功能突变组之间重组受到抑制的区域，有助于不同系统中复杂表型的进化。除性染色体外，迄今为止发现的大多数超基因似乎都是年轻的，存在于一个物种或少数几个密切相关的物种中。在这里，我们研究了含有古老超基因的染色体是如何在大约 3000 万年 (Ma) 中进化的。福米卡超基因是至少五个物种中蜂王数量变化的基础。我们扩展了先前对该染色体上序列差异的分析，以涵盖跨越Formica系统发育的约 90 个物种。在非重组区域内，基因敲除包含 22 个单核苷酸多态性 (SNP)，这些单核苷酸多态性 (SNP) 在不同的欧洲Formica物种中始终区分两种替代超基因单倍型，我们表明这些相同的 SNP 存在于大多数Formica进化枝中。在这些进化枝中，包括早期发散的 Nearctic Formica进化枝，在敲除时具有替代基因型的个体在该染色体的其他部分也具有更高的分化。我们确定了存在于多个福米卡中的这条染色体上的 SNP 热点进化枝来检测可能有助于遗传多态性的出现和维持的基因。最后，我们根据单倍体雄性基因组中这些基因的明显杂合性推断出一种单倍型的三个基因重复。这项研究加强了这种超基因起源于福米卡进化早期的证据，并且在这个抑制重组的大区域中只有少数基因座在当代福米卡谱系中保留了强烈分化的等位基因。