The evolutionary history of praying mantises (Dictyoptera, Mantodea)

Mantodea are among the most charismatic insects, and investigations of their evolutionary history interrogate some of their most compelling morphological traits. Despite this, studies of Mantodea systematics have often drastically changed historical perspectives about their evolutionary history, underscoring the lack of study on the group. The present account provides a comprehensive transcriptomic analysis with 51 species from 14 of the 16 established superfamilies that resolves several critical questions in mantodean phylogeny, including the relationship among the five major lineages, namely Chaeteessoidea, Mantoidoidea, Metallyticoidea, Amerimantodea and Cernomantodea. The inferred phylogeny highlights a well‐supported sister‐group relation between Chaeteessoidea and all remaining extant mantids. This placement of Chaeteessoidea implies that its unique thoracic musculature and foreleg morphology are indeed ancestral traits, which bridge cockroach‐like ancestors and derived Mantodea lineages. Our results are ambiguous about the position of Metallyticoidea in relation to Mantoidoidea, as we recover conflicting signals between the different analyses performed. Within Amerimantodea and Cernomantodea, we corroborate prior research by demonstrating the polyphyletic nature of traditional taxonomic groups and the significant role of morphological convergence in obscuring true evolutionary relationships. Divergence estimates place the split between cockroaches and praying mantises in the middle of the Permian period at ~274 ± 37 million years ago (mya), with crown‐Mantodea originating around 185 mya in the Jurassic, predating most previous estimates and suggesting a deep evolutionary history shaped by significant geological changes. In particular, the dated phylogeny and the distribution of Mantodea's major extant lineages provide additional evidence that vicariance associated with the breakup of Gondwana played a crucial role in the early diversification of the group. In summary, this study establishes a robust phylogenomic framework for Mantodea and clarifies long‐standing systematic uncertainties, providing a solid foundation for future research into praying mantises' evolution, biogeography and morphological diversification.