A genome-based framework for the insect tree of life reveals the distinct biological drivers of phylogenomic conflict
Description
Understanding insect evolution requires resolving deep phylogenetic relationships and divergence times, yet conflicting hypotheses persist due to biological and methodological complexities. Here, we address this challenge by leveraging 794 high-quality genomes to reconstruct a robust, time-calibrated phylogeny of Insecta using 481 strictly defined single-copy orthologous genes, effectively minimizing the missing-data artifacts often prevalent in broad transcriptomic studies. Our analyses resolve most inter-ordinal relationships with high confidence and employ a multi-faceted framework to diagnose the nature of phylogenomic conflict at two historically contentious nodes. We provide evidence that the instability surrounding the relationships among Paraneoptera stems from a hard polytomy, consistent with an ancient rapid radiation event where dichotomous phylogenetic signal is largely absent. In contrast, the conflict regarding the placement of Strepsiptera (sister to Coleoptera) is characterized by a dominant signal competing with a significant secondary one, a pattern consistent with incomplete lineage sorting (ILS) that allows for a statistically confident resolution. Importantly, by incorporating recent critical fossil discoveries and implementing permissive minimum-age constraints, our updated divergence time estimates place the origin of winged insects in the Early Ordovician (~477 Ma), a timeline synchronous with the initial terrestrialization of early land plants. Ultimately, our study provides a rigorously updated genome-based framework for the insect tree of life and demonstrates how distinguishing between different evolutionary processes can resolve key relationships and explain sources of persistent incongruence.
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Initially, genome assemblies were obtained from InsectBase 2.0 and the NCBI Genome Database (NCBI Resource Coordinators et al. 2018; Mei et al. 2022). Detailed source information, including accession numbers and assembly versions for all genomes used in this study, is provided in Table S1 and the associated data repository. To ensure the quality and comprehensiveness of gene sets for ortholog identification, BUSCO v5.2.0 was employed to assess genome completeness (Manni et al. 2021). For this purpose, we used the Insecta official ortholog sets from OrthoDB (Insecta_odb10.2020-09-10) (Zdobnov et al. 2021). Genome assemblies were retained with BUSCO completeness scores greater than or equal to 80% for subsequent analysis. This resulted in 763 genome assemblies across 23 insect orders and 31 species from Collembola, Diplura, Branchiopoda, Multicrustacea and Oligostraca to serve as outgroups (Table S1).