A supergene-controlling social structure in Alpine ants also affects the dispersal ability and fecundity of each sex.

Social organization, dispersal and fecundity coevolve, but whether they are genetically linked remains little known. Supergenes are prime candidates for coupling adaptive traits and mediating sex-specific trade-offs. Here, we test whether a supergene that controls social structure in Formica selysi also influences dispersal-related traits and fecundity within each sex. In this ant species, single-queen colonies contain only the ancestral supergene haplotype M and produce MM queens and M males, while multi-queen colonies contain the derived haplotype P and produce MP queens, PP queens and P males. By combining multiple experiments, we show that the M haplotype induces phenotypes with higher dispersal potential and higher fecundity in both sexes. Specifically, MM queens, MP queens and M males are more aerodynamic and more fecund than PP queens and P males, respectively. Differences between MP and PP queens from the same colonies reveal a direct genetic effect of the supergene on dispersal-related traits and fecundity. The derived haplotype P, associated with multi-queen colonies, produces queens and males with reduced dispersal abilities and lower fecundity. More broadly, similarities between the Formica and Solenopsis systems reveal that supergenes play a major role in linking behavioural, morphological and physiological traits associated with intraspecific social polymorphisms.

Cryptic recessive lethality of a supergene controlling social organization in ants.

Supergenes are clusters of linked loci that control complex phenotypes, such as alternative forms of social organization in ants. Explaining the long-term maintenance of supergenes is challenging, particularly when the derived haplotype lacks homozygous lethality and causes gene drive. In the Alpine silver ant, Formica selysi, a large and ancient social supergene with two haplotypes, M and P, controls colony social organization. Single-queen colonies only contain MM females, while multiqueen colonies contain MP and PP females. The derived P haplotype, found only in multiqueen colonies, selfishly enhances its transmission through maternal effect killing, which could have led to its fixation. A population genetic model showed that a stable social polymorphism can only be maintained under a narrow set of conditions, which includes partial assortative mating by social form (which is known to occur in the wild), and low fitness of PP queens. With a combination of field and laboratory experiments, we show that the P haplotype has deleterious effects on female fitness. The survival rate of PP queens and workers was around half that of other genotypes. Moreover, P-carrying queens had lower fertility and fecundity compared to other queens. We discuss how cryptic lethal effects of the P haplotype help stabilize this ancient polymorphism.

Winter is coming: harsh environments limit independent reproduction of cooperative-breeding queens in a socially polymorphic ant.

Cooperative breeding animals frequently inhabit harsh environments. It is widely accepted that harsh environments hinder independent reproduction, and this constraint maintains individuals in family groups. Yet the assumption that harsh ecological conditions reduce the success of members of cooperative breeding groups when breeding independently has not been experimentally tested. We addressed this shortcoming using the socially polymorphic Alpine silver ant, Formica selysi. This species has single-queen (independent breeders) and multiple-queen (cooperative breeders) colonies coexisting within populations. We placed newly mated queens emerging from each type of colony to breed alone in either a harsh or mild winter condition and recorded their brood production and survival. Queens emerging from single-queen colonies were unaffected by the winter condition and were more successful at founding a nest independently than queens from multiple-queen colonies. By contrast, queens from multiple-queen colonies had higher mortality after a harsh than after a mild winter. These results support the long-held assumption that harsh environments constrain independent reproduction of members of cooperative breeding groups.