The loss of a supergene in obligately polygynous Formica wood ant species

Some of the most striking examples of phenotypic variation within species are controlled by supergenes. However, most research on supergenes has focused on their emergence and long-term maintenance, leaving the later stages of their life cycle largely unexplored. Specifically, what happens to a derived supergene haplotype when the trait it controls reaches fixation? Here we answer this question using the ancient supergene system of Formica ants, where (monogynous) single-queen colonies carry only the ancestral haplotype M while the derived haplotype P is exclusive to (polygynous) colonies with multiple queens. Through comparative genomics of all seven European wood ant species, we found that the P haplotype was present in only one of the three obligate polygynous species (F. polyctena). In the two others (F. aquilonia and F. paralugubris) the P haplotype was completely missing except for duplicated P-specific paralogs of two genes, Zasp52 and TTLL2, with Zasp52 being directly involved in wing muscle development. We hypothesize that these genes play a direct role in polygyny and contribute to differences in body size and/or dispersal behaviour between monogynous and polygynous queens. A complete lack of P/P genotypes among the 136 workers suggest strong selection against such genotypes. While our analyses did not reveal evidence of increased mutation load on the P, it is possible that this skew in genotype distributions is driven by a few loci with strong fitness effects. We propose that selection to escape P-associated fitness costs underlies the loss of this haplotype in obligate polygynous wood ants.