Department of Entomology, University of California Riverside, Riverside, CA, USA.
Department of Evolution, Ecology, and Organismal Biology, University of California Riverside, Riverside, CA, USA.
Mol Ecol. 2021 Dec;30(23):6246-6258. doi: 10.1111/mec.16196. Epub 2021 Oct 8.
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.
超级基因座是基因组中抑制功能突变之间重组的区域，有助于多种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级基因座似乎都很年轻，只存在于一个或少数几个密切相关的物种中。在这里，我们研究了一个包含古老超级基因座的染色体是如何在大约 3000 万年（Ma）的时间里进化的。Formica 超级基因座是至少五个物种中蚁后数量变异的基础。我们扩展了之前对这条染色体上序列分歧的分析，涵盖了跨越 Formica 系统发育的大约 90 个物种。在非重组区域，基因敲除包含 22 个单核苷酸多态性（SNP），这些 SNP 在分化的欧洲 Formica 物种的两种替代超级基因座单倍型之间始终存在差异，我们表明这些相同的 SNP 存在于大多数 Formica 分支中。在这些分支中，包括一个早期分化的近北极 Formica 分支，在 knockout 处具有替代基因型的个体在这条染色体的其他部分也表现出更高的分化。我们沿着这条染色体识别出存在于多个 Formica 分支中的 SNP 热点，以检测可能有助于遗传多态性出现和维持的基因。最后，我们根据这些基因在单倍体雄性基因组中的明显杂合性，推断出一个单倍型上的三个基因重复。这项研究加强了证据表明，这个超级基因座起源于 Formica 进化的早期，并且在这个受到强烈抑制重组的大片区中，只有少数几个位点保留了在当代 Formica 谱系中分化强烈的等位基因。
