Linked supergenes underlie split sex ratio and social organization in an ant

Abstract

Sexually reproducing organisms usually invest equally in male and female offspring. Deviations from this pattern have led researchers to new discoveries in the study of parent-offspring conflict, genomic conflict, and cooperation. Some social insect species exhibit the unusual population-level pattern of split sex ratio, wherein some colonies specialize in the production of future queens and others specialize in the production of males. Theoretical work focused on the relatedness asymmetries emerging from haplodiploid inheritance, whereby queens are equally related to daughters and sons, but their daughter workers are more closely related to sisters than to brothers, led to a series of testable predictions and spawned many empirical studies of this phenomenon. However, not all empirical systems follow predicted patterns, so questions remain about how split sex ratio emerges. Here, we sequence the genomes of 138 Formica glacialis workers from 34 male-producing and 34 gyne-producing colonies to determine whether split sex ratio is under genetic control. We identify a supergene spanning 5.5 Mbp that is closely associated with sex allocation in this system. Strikingly, this supergene is adjacent to another supergene spanning 5 Mbp that is associated with variation in colony queen number. We identify a similar pattern in a second related species, Formica podzolica. The discovery that split sex ratio is determined, at least in part, by a supergene in two species opens a new line of research on the evolutionary drivers of split sex ratio. Significance Statement Some social insects exhibit split sex ratio, wherein some colonies produce future queens and others produce males. This phenomenon spawned many influential theoretical studies and empirical tests, both of which have advanced our understanding of parent-offspring conflicts and cooperation. However, some empirical systems did not follow theoretical predictions, indicating that researchers lack a comprehensive understanding of the drivers of split sex ratio. Here, we show that split sex ratio is associated with a large genomic region in two ant species. The discovery of a genetic basis for sex allocation in ants provides a novel explanation for this phenomenon, particularly in systems where empirical observations deviate from theoretical predictions.