Sequential origin of an alternative colony founding strategy driven by two supergenes in Temnothorax ants

Abstract

Recent discoveries reveal that many complex intraspecific polymorphisms are shaped by a single supergene that maintains coadapted genetic variants through suppressed recombination. Here, we show that in the ant Temnothorax rugatulus, an extreme reproductive polymorphism is instead governed by two independent genomic rearrangements that arose sequentially on different chromosomes. Colonies of this species contain either a single large dispersing queen or multiple queens, including extremely miniaturized microgynes that cannot establish new colonies on their own and reproduce only by joining established multiple-queen colonies. Using chromosome-scale assemblies and population genomic data, we identify two genomic rearrangements, 9.3 and 7.0 Mb in size, that jointly determine these strategies. Divergence dating shows that the supergene underlying colony social structure arose first, creating the conditions for the subsequent emergence of a miniaturization supergene. These findings demonstrate that complex adaptive strategies can be assembled stepwise through the sequential origin of multiple supergenes.