The spectacular success of eusocial insects can be attributed to their sophisticated cooperation, yet cooperation is conspicuously absent during colony foundation when queens are alone. Selection against this solitary stage has led to a dramatically different strategy in thousands of eusocial insect species in which colonies are started by groups of nestmates and the benefits of sociality are retained continuously. Dependent colony foundation (DCF) evolved recurrently multiple times across the ants, bees, and wasps, though its prevalence in termites remains unclear. We review adaptations at both the colony level (reproductive investment shifts from sexuals to workers) and the individual level (wingless queens evolve in ants), and other consequences for life history (invasiveness, parasite transmission). Although few studies have focused on DCF, the accumulated data from anecdotal reports, supported by indirect information including morphology, population genetics, and colony demographics, make it clear that this strategy is more diverse and widespread than is usually recognized.

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Many ants have independently evolved castes with novel morphology as well as function, such as soldiers and permanently wingless (ergatoid) queens. We present a conceptual model, based on modularity in morphology and development, in which evolutionary innovation is facilitated by the ancestral ant polyphenism of winged queens and wingless workers. We suggest that novel castes evolved from rare intercastes, anomalous mosaics of winged queens and workers, erratically produced by colonies through environmental or genetic perturbations. The colonial environment is highly accommodating and buffers viable intercastes from individual selection. Their cost is limited because they are diluted by the large number of nestmates, yet some can bring disproportionate benefits to their colonies in the context of defense or reproduction (e.g., wingless intercastes able to mate). Useful intercastes will increase in frequency as their morphology is stabilized through genetic accommodation. We show that both soldiers and ergatoid queens are mosaics of winged queens and workers, and they are strikingly similar to some intercastes. Modularity and developmental plasticity together with winged/wingless polyphenism thus allow for the production of highly variable mosaic intercastes, and colonies incubate the advantageous mosaics.