Animals have evolved a variety of mechanisms for sex determination. About 12% of animal species employ haplodiploid sex determination: males develop parthenogenetically from unfertilised eggs and are haploid, and females from fertilised eggs and are diploid. Here we identify a new mechanism of sex determination underlying haplodiploidy in the ant Linepithema humile. A multiallelic regulatory region (Lh-CSD) acts as the primary signal of sex determination in a haplodiploid system. Heterozygous embryos at Lh-CSD develop into females while homozygotes and hemizygotes (haploid individuals) develop into males. Heterozygosity at Lh-CSD greatly increases the expression of ANTSR, an adjacent long non-coding RNA, thereby providing information on the homozygosity/heterozygosity status of Lh-CSD. Knockdown of ANTSR in female-destined embryos (i.e., Lh-CSD heterozygotes) resulted in the production of a male-specific splicing form of transformer (tra). Comparative analyses indicate that ANTSR is an ancient, yet rapidly evolving gene in Aculeata. In addition to identifying the first lncRNA acting as a master sex determination gene, this study uncovers a new regulatory mechanism based on complementarity among multiple alleles.
The lncRNA ANTSR coordinates complementary sex determination in ants.