ConvergeAnt · Uncovering the genomic underpinnings of the convergent evolution of a major social trait

Uncovering the genomic underpinnings of the convergent evolution of a major social trait

Ant colonies consist of specialised individuals performing distinct tasks, such that queens and males reproduce, while the workers care for the queen’s offspring, forage and defend the colony. The ancestral ant colony most certainly comprised a single queen and highly related workers. Over time, however, the more than 20,000 described extant ant species have evolved a remarkable diversity of social lifestyles and today occupy most terrestrial habitats. The sophisticated social structures of ant colonies largely depend on a fundamental trait that varies broadly across species: the number of reproductive queens in a colony. Notably, socially polymorphic species such as the red imported fire ant Solenopsis invicta have evolved the capability of founding colonies with either one or multiple reproductive queens. Colony queen number correlates with several other traits. For example, multiple-queen colonies have longer lifespans and queens with smaller body size and decreased fecundity relative to single-queen colonies. Previous work revealed that a supergene – a set of tightly linked genes inherited as a unit – controls the stable polymorphism in queen number in S. invicta. Yet, it remains unclear how supergenes might have shaped the evolution of other socially polymorphic ant species. The overall objectives of the project were to trace the evolutionary origin of genetic features underlying the polymorphism in queen number across ant species, evaluate changes in gene family size and content across such species and identify convergent patterns of selection on coding sequences. The prevalent understanding of social organisation in ants postulated that environmental factors control the number of queens in a colony. Limited genomic research, however, previously revealed that certain ant species independently evolved supergenes controlling the polymorphism in queen number. For example, colonies of S. invicta with a single queen include members carrying only the Social B (SB) supergene haplotype on the ‘social chromosome’ (chromosome 16). Colonies of S. invicta with multiple queens, however, contain the alternative Sb haplotype in heterozygous (SB/Sb) queens and workers. In this MSCA-IF project, we conducted a comparative genomic study to reveal the origin and evolution of the fire ant supergene. Specifically, we applied population genetics and phylogenetic methods to reveal the origin and subsequent evolution of a supergene across multiple species of Solenopsis fire ants, assess whether specific gene families consistently associate with supergene haplotypes and identify patterns of positive selection. Challenging previous studies, the findings of this study revealed that the supergene variant Sb originated in S. invicta and then introgressed into other Solenopsis species.

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