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Significance Polyneoptera is the only major lineage of winged insects (Pterygota) with an unresolved evolutionary history concerning important phenotypic traits like external shape, social behavior, and lifestyle. These ambiguities have far-reaching consequences for our understanding of the early evolution of winged insects. We closed this knowledge gap through large-scale phylogenomic analyses tracing traits concerning lifestyle and habitus within Polyneoptera and Pterygota. Both groups were ancestrally terrestrial in all developmental stages, implying that wings did not evolve in species living in water. All polyneopteran insects derive from a ground-dwelling insect with a largely unmodified body relative to the last common ancestor of winged insects. Intriguingly, different forms of social behavior, changes in lifestyle, and associated morphological specializations evolved multiple times within Polyneoptera.

Evolutionary history of Polyneoptera and its implications for our understanding of early winged insects