Global allele polymorphism indicates a high rate of allele genesis at a locus under balancing selection

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 thecomplementary sex determiner(csd) of the Asian honeybee (Apis cerana), sampled from across its range. Honeybees are haplodiploid; hemizygotes atcsddevelop as males and heterozygotes as females, while homozygosity is lethal. Thus,csdis under strong negative frequency-dependent selection because rare alleles are less likely to end up in the lethal homozygous form. We find that inA. cerana, as in otherApis, just a few amino acid differences betweencsdalleles 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 mostcsdalleles (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 theircsdalleles. In all, the geographic patterns ofcsddiversity inA. ceranaindicate 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.

Automated summary

The study found that in the complementary sex determiner gene of the Asian honeybee, just a few amino acid differences can affect female development, while most alleles are detected in only one sample location, indicating high variation and balancing selection lead to the exceptionally high polymorphism in this locus.