Evolution of supergenes: lessons from social chromosomes

Supergenes are large genomic regions that determine complex polymorphic traits. The most well known example are sex chromosomes. A large portion of the X and Y chromosomes do not recombine, which allows them to diverge and evolve sex-specific traits. In general, supergenes allow for the evolution of a diverse range of complex traits, including floral morphology in primroses, mimetic wing patterns in butterflies, and morphs with distinct reproductive strategies in birds and lizards. All these examples constitute complex traits of high fitness impact.

In social insects such as ants, the social structure and mode of colony reproduction have great ecological and evolutionary consequences. "Social chromosomes" harbor supergenes that determine colony structure in socially polymorphic species, which form either monogyne (headed by a single queen) or polygyne colonies (with multiple queens). Such supergenes were discovered in diverse ant species, suggesting multiple independent evolutionary origins. We discovered a novel supergene in the desert ant Cataglyphis niger, representing a fourth independent origin. Comparative analyses of the four systems reveal general patterns of social supergene evolution, as well as striking variations that may reflect differences in life history and ecology among ant lineages. Interestingly, two of the previously described supergenes act as selfish genetic elements, employing two different mechanisms of action. In the Cataglyphis supergene, we found an unexpected mode of apparently strict maternal inheritance, which may be related to selfish evolution. We are investigating the mechanism responsible for this pattern, including potential mito-nuclear incompatibility.