Phylogenomics insights into the evolution of pronotal leaf mimicry in Hierodulinae (Mantodea: Mantidae)

Abstract

The evolutionary relationships within the mantid subfamily Hierodulinae remain contentious, particularly concerning the morphological diversity and classification of species with leaf-like pronotum, which are broad and flattened thoracic structures. Traditionally regarded as a defining characteristic of the genus Rhombodera, specifically as a specialized pronotal trait, mitochondrial phylogenomics has cast doubt on this assumption, suggesting potential homoplasy. In this study, we generated 30 high-quality transcriptomes of Hierodulinae and established the first Mantodea-specific orthologous database (Mantodea_odb) to identify universal single-copy orthologues (USCOs) for phylogenomic inference. By integrating genomic and transcriptomic data, we reconstructed well-supported phylogenetic trees using both maximum likelihood and coalescent-based approaches, which provided the framework to assess evolutionary patterns of morphological traits. Divergence time estimation and ancestral state reconstruction suggested that the leaf-like pronotum evolved independently on multiple occasions within Hierodulinae, corresponding temporally to the late Paleogene to early Neogene (Oligocene-Miocene transition, ca. 20–23 Ma). Notably, our molecular phylogeny exhibits a strong correlation with distinct clades delineated by male genital morphology, thereby resolving longstanding taxonomic inconsistencies. These findings reveal decoupled evolutionary patterns between homoplastic pronotal traits and conserved genital morphology in Hierodulinae, showcasing how phylogenomics can discriminate between convergent and conserved traits.