Beyond queen number: two supergenes coordinate dispersal, mating, and colony founding in the ant Formica cinerea

Abstract

Reproductive success often depends on coordinated combinations of morphology, dispersal ability, and mating behavior. Supergenes, genomic regions of suppressed recombination, allow such combinations to be inherited by offspring as a single unit. In ants, independently evolved supergenes control colony queen number, yet few studies have investigated their joint influence on morphology, mating, and colony-founding in sexuals. Formica cinerea provides a unique opportunity to address this question because it harbors two supergenes that together produce three queen and male morphs: large monogyne, large polygyne, and small polygyne. Here we show that these supergenes jointly shape an integrated suite of traits across the reproductive cycle. Wing area was primarily associated with the chromosome 3 supergene, with monogyne individuals having larger wings than polygyne individuals. Thorax volume was associated with the chromosome 9 supergene, with small polygyne individuals having reduced thorax volume regardless of social origin. Mating was assortative for both supergenes in large morphs but random in small polygyne queens. Independent colony founding was almost exclusively performed by large monogyne queens; initial egg production was unaffected by mate genotype. These findings show that the two supergenes jointly coordinate dispersal morphology, mate choice, and colony-founding into coherent reproductive strategies, preventing maladaptive intermediate phenotypes.