Does social antagonism facilitate supergene expansion? A novel region of suppressed recombination in a 4-haplotype supergene system.

Abstract

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. Drawing inspiration from such models, we apply similar logic to investigate whether an autosomal supergene underlying colony social organization in ants expanded to include "socially antagonistic" alleles. 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. Significance statementWhen sets of gene variants work well together, selection may lead to a reduction in recombination between them. Here, we discover a novel supergene region on chromosome 9 that controls a previously undescribed queen size polymorphism in Formica cinerea ants. The haplotype that is found in small queens, 9r, is tightly linked to a supergene haplotype on chromosome 3 that is found in multi-queen colonies. We propose that the region of suppressed recombination expanded to include both chromosome 3 and chromosome 9 because small queens could be successful in the multi-queen but not in the single-queen environment.