Sequential origin of an alternative colony founding strategy driven by two supergenes in Temnothorax ants
In social insects, the transition from solitary colony founding to cooperative strategies, where multiple queens reproduce within the same colony, has evolved repeatedly. Such transitions on colony organization are often accompanied by reductions in queen body size and alternative dispersal tactics. The most striking extremes are microgynes, worker-sized queens that have lost the ability to disperse and establish new colonies independently and instead reproduce only through reintegration into established nests. The evolutionary processes leading to this strategy arises remain poorly understood. Here, we investigate the North American ant Temnothorax rugatulus, which exhibits polymorphism in colony founding strategy: large, dispersing macrogynes and miniaturized microgynes that forgo dispersal to rejoin their natal colony. We identify two distinct extensive nonrecombining genomic regions that govern these alternative strategies. A 9.3 Mb region on chromosome 2 determines polygyny, while a 7.0 Mb region on chromosome 8 underlies queen miniaturization. Divergence dating shows that the supergene controlling queen-number polymorphism predates that of queen-size dimorphism, supporting that the evolution of polygyny provided the conditions for the emergence of microgyny. These findings reveal a stepwise evolutionary trajectory in which successive genomic rearrangements drove the turnover of colony founding strategies.