Ancient but dynamic: structural expansion, massive gene duplication, and transposable element colonization in a supergene controlling ant social organization

Supergenes are clusters of linked loci that underlie complex alternative phenotypes, such as colony social organization in ants. In many species of the genus Formica, a 30 million-year-old supergene determines whether colonies have one queen (monogyny) or multiple queens (polygyny), yet the detailed architecture of this genetic polymorphism remains poorly known. Here we investigate the structural and functional evolution of the supergene haplotypes controlling alternative social forms in Formica selysi. The comparison of chromosomal-level genome assemblies for each social form reveals a 13.8 Mbp long rearranged supergene comprising three large inversions and a transposition, resulting in reduced recombination and high differentiation between haplotypes. The rearranged, derived polygynous haplotype has accumulated transposable elements (TEs) and gene duplicates. It also exhibits haplotype-specific gene expression and gene specialization. Notably, the Formica genus shows a large expansion of the Ubiquitin Conjugation Factor E4 B gene family, which is significantly enriched in the supergene. Despite its ancient origin, the supergene shows sparse signs of degeneration and little accumulation of deleterious variations. Overall, our results demonstrate that the supergene haplotype associated with multi-queen colonies has undergone enrichment of lineage-specialized single- and multi-copy genes with haplotype-specific expression patterns that likely contribute to the phenotype. A combination of relaxed and purifying selection allowed gene duplicates and TEs to accumulate, but prevented the accumulation of deleterious mutations, which helps to explain the long-term persistence of this large social supergene.