A Mitogenome-Based Phylogenetic Framework for Mantidae (Mantodea: Mantoidea): Systematic Implications and Spatio-Temporal Dynamics

Mantidae exhibits the most extensive adaptive radiation within the order Mantodea; however, studies elucidating their internal phylogenetic relationships and spatio-temporal diversification patterns remain scarce. This study aims to resolve the long-standing taxonomic uncertainties within Mantidae by testing the hypothesis that the polyphyletic nature of several subfamilies—specifically Tenoderinae and Hierodulinae—is linked to an incomplete understanding of their mitochondrial genomic evolution. To address this, we assembled 16 complete Mantodea mitochondrial genomes, including seven representatives of the tribe Archimantini (Mantidae: Hierodulinae). Of these, 10 mitogenomes conform to the ancestral insect mitochondrial gene order proposed by Cameron and colleagues, but six mitochondrial gene orders do not conform to the ancestral insect mitochondrial gene order. We identified typical mantodean mitochondrial rearrangement patterns in three species, characterized by gene duplications within the trnA-trnR-trnN-trnS-trnE-trnF and CR-trnI-trnQ-trnM-trnM-ND2 gene cluster. Phylogenetic analyses corroborate the monophyly of Orthoderinae, Mantinae, Choeradodinae, Vatinae, and Archimantini within Mantidae; conversely, Tenoderinae and Hierodulinae are resolved as polyphyletic assemblages. Divergence time estimation indicates that the split between extant Mantodea and Blattodea occurred during the Middle Permian (275.4 Ma, 95% HPD: 207.07–329.09 Ma). Mantidae originated during the Late Cretaceous (87.83 Ma, 95% HPD: 58.89–118.23 Ma), with the diversification of most subfamilies of Mantidae occurring during the Late Cretaceous (80.48 Ma; 95% HPD: 54.86–106.41 Ma). Historical biogeographic analysis and the estimated divergence times suggests that the common ancestor of Mantidae originated within Gondwana during the Late Cretaceous. Ancestral range reconstructions identify Australasia realms and Neotropical realms as the most probable center of origination for Mantidae and achieved a global distribution by expanding along the trans-Antarctic route and leveraging the ‘Indian Ark’ effect.