When selection favours rare alleles over common ones (balancing selection in the form of negative frequency-dependent selection), a locus may maintain a large number of alleles, each at similar frequency. To better understand how allelic richness is generated and maintained at such loci, we assessed 201 sequences of the complementary sex determiner ( csd ) of the Asian honeybee ( Apis cerana ), sampled from across its range. Honeybees are haplodiploid; hemizygotes at csd develop as males and heterozygotes as females, while homozygosity is lethal. Thus, csd is under strong negative frequency-dependent selection because rare alleles are less likely to end up in the lethal homozygous form. We find that in A. cerana , as in other Apis , just a few amino acid differences between csd alleles in the hypervariable region are sufficient to trigger female development. We then show that while allelic lineages are spread across geographical regions, allelic differentiation is high between populations, with most csd alleles (86.3%) detected in only one sample location. Furthermore, nucleotide diversity in the hypervariable region indicates an excess of recently arisen alleles, possibly associated with population expansion across Asia since the last glacial maximum. Only the newly invasive populations of the Austral-Pacific share most of their csd alleles. In all, the geographic patterns of csd diversity in A. cerana indicate that high mutation rates and balancing selection act together to produce high rates of allele genesis and turnover at the honeybee sex locus, which in turn leads to its exceptionally high local and global polymorphism.

中文翻译：

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全局等位基因多态性表明在平衡选择下的基因座处等位基因发生率很高

When selection favours rare alleles over common ones (balancing selection in the form of negative frequency-dependent selection), a locus may maintain a large number of alleles, each at similar frequency. 为了更好地了解等位基因丰富度是如何在这些基因座上产生和维持的，我们评估了亚洲蜜蜂 (Apis cerana) 的 201 个互补性别决定子 (csd) 序列，这些序列是从其范围内取样的。蜜蜂是单倍体；csd 的半合子发育为雄性，杂合子发育为雌性，而纯合子是致命的。因此， csd 处于强烈的负频率依赖性选择之下，因为稀有等位基因不太可能以致命的纯合形式结束。我们发现，在 A. cerana 中，与在其他蜜蜂中一样，高变区 csd 等位基因之间的几个氨基酸差异足以引发女性发育。然后我们表明，虽然等位基因谱系分布在各个地理区域，但群体之间的等位基因分化程度很高，大多数 csd 等位基因 (86.3%) 仅在一个样本位置检测到。此外，高变区的核苷酸多样性表明最近出现的等位基因过多，这可能与自上一次冰期最大值以来整个亚洲的人口扩张有关。只有南太平洋新入侵的种群共享大部分 csd 等位基因。总之，A. cerana 中 csd 多样性的地理模式表明，高突变率和平衡选择共同作用，在蜜蜂性位点产生高等位基因发生率和周转率，