Formica cinerea ants- ddRAD-seq data

Models of both sex chromosome evolution and the genetic basis of local adaptation suggest that selection acts to lock beneficial combinations of alleles together in regions of reduced or suppressed recombination. Autosomal supergenes, regions of the genome containing multiple alleles that are inherited as single unit, provide an opportunity to investigate predictions of both classes of models. We tested this premise in a Formica ant species wherein we identified four supergene haplotypes on chromosome 3 underlying colony social organization and sex ratio. Remarkably, we discovered a novel rearranged supergene variant (9r) on chromosome 9 underlying queen miniaturization. The 9r is tightly linked to one of the haplotypes (P2) on chromosome 3, found predominantly in multi-queen (polygyne) colonies. We suggest that queen miniaturization is strongly disfavored in the single queen (monogyne) background, and thus socially antagonistic. As such, divergent selection experienced by ants living in alternative social environments (monogyne and polygyne) may have contributed to the emergence of a genetic polymorphism on chromosome 9 and associated queen size dimorphism. Consequently, an ancestral polygyne-associated haplotype may have expanded to include the polymorphism on chromosome 9, resulting in a larger region of suppressed recombination spanning two chromosomes. This process is analogous to the formation of neo-sex chromosomes and consistent with models of expanding regions of suppressed recombination. We also propose that miniaturized queens, 16-20% smaller than queens without 9r, could be incipient intraspecific social parasites.