The transition to flying insects: lessons from evo-devo and fossils

Insects are the only arthropod group to achieve powered flight, which facilitated their explosive radiation on land. It remains a significant challenge to understand the evolutionary transition from nonflying (apterygote) to flying (pterygote) insects due to the large gap in the fossil record. Under such a situation, ontogenic information has historically been used to compensate for fossil evidence. Recent evo-devo studies support and refine a paleontology-based classical hypothesis that an ancestral exite incorporated into the body wall contributed to the origin of insect wings. The modern hypothesis locates an ancestral precoxa leg segment with an exite within the hexapod lateral tergum, reframing the long-standing debate on the insect wing origin. A current focus is on the contributions of the incorporated exite homolog and surrounding tissues, such as the pleuron and the medial bona fide tergum, to wing evolution. In parallel, recent analyses of Paleozoic fossils have confirmed thoracic and abdominal lateral body outgrowths as transitional wing precursors and suggested their possible role as respiratory organs in aquatic or semiaquatic environments. These recent studies have revised our understanding of the transition to flying insects. This review highlights recent progress in both evo-devo and paleontology, and discusses future challenges, including the evolution of metamorphic development. • A paleontology-based hypothesis about the wing origin from an incorporated leg segment is reconsidered by evo-devo studies. • Lateral outgrowths, derived from tergum or tergum + pleuron, on the prothorax and abdominal segments I-IX in Palaeodictyoptera, were confirmed as wing homologs. • Precursors of wings might be evolved in an aquatic/semiaquatic environment from an ancestral type of gills (plate gills). • Thoracic wing pads in Paleozoic Palaeodictyoptera were presumably movable in late nymphs, although fixed in early instars. • Postembryonic metamorphic development has facilitated evolution of novelties including wings in insects.