A Comprehensive Account of the Breeding Systems of the Fire Ant Solenopsis invicta

When animals reproduce in social groups, the potential for conflict and cooperation is shaped by the number of reproductive individuals (breeders), their relatedness to one another, and division of reproduction among them. These features comprise species' "breeding systems." Despite their importance, breeding systems are poorly characterized in most social animals, and detailed accounts for single species are rare. Here, we comprehensively characterize the breeding systems of the fire ant Solenopsis invicta, an invasive species in which a large genetic element (supergene) determines whether a colony has a single queen (monogyne social form) or multiple queens (polygyne form). Colonies of the monogyne form are simple families, and the breeding system is correspondingly straightforward. The breeding system of the polygyne form is complex, with many features still not well characterized. We conducted a large longitudinal experiment tracking parentage, relatedness, and supergene genotype in laboratory-reared polygyne colonies. Along with reanalyzed data from previous studies, we show that colony queen number is highly variable, queens generally mate once, nestmate breeders (queens and their mates) generally are unrelated, and reproductive skew is pervasive, especially for parentage of sexual daughters. Uncommon instances of polyandry occur when a queen remates after initially mating with a male bearing the Sb supergene haplotype (associated with small size and low sperm counts). Paternity skew is pronounced and stable, with Sb sperm contributing to a minority of offspring (particularly sexual daughters) of polyandrous queens. The supergene thus not only determines colony queen number, it broadly affects the breeding system, impacting colony kin structure and setting the stage for conflict and cooperation in the colony. This study can serve as a template for studies of the constellation of factors that affect group genetic structure in other social animals.