Revealing the genomic innovations during evolution of holometaboly

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Some evolutionary innovations open completely new opportunities to a clade, fostering its radiation. Therefore, one of the fundamental questions in evolutionary biology is, how such key innovations evolved and what genomic changes drove their emergence. One of the most successful innovations in insects is the holometabolous life cycle leading to a radiation, which comprises >70% of all extant arthropod species. In contrast to hemimetabolan nymphs, the holometabolan larva differs strongly from the adult allowing it to exploit different niches and to specialize e.g. to growth versus reproduction. Eventually, the adult’s morphology forms during a dramatic re-construction during the pupal stage. It has remained enigmatic, what genes were involved in the evolution of this key innovation and how they influence developmental processes.The annotation of eukaryotic genomes lacks behind their sequencing and assembly. For example, in November 2021 only 198 out of 749 insect species with an assembly at scaffold level at NCBI also had a deposited annotation. Further, most genomes were annotated one at a time and errors in gene structure prediction are consequential in comparative analyses as they typically focus on the differences between related species. Simultaneously, the explosive growth of closely related genomes allows to leverage new methods that exploit deep multiple genome alignments to make their annotation more accurate and consistent.Here, we propose to enhance the bioinformatics tools for consistent and accurate comparative genome annotations. We will apply these enhanced methods to hundreds of insect genomes, sequenced in this SPP or otherwise available. This effort will create the probably largest insect genome annotation resource for comparative studies of protein-coding genes. In this project, we will mine the resource to identify coding genes that have undergone impactful changes during the emergence of holometaboly. From this set, we will systematically identify all genes that are functionally required for selected holometabola-specific developmental processes, i.e. larval and pupal epidermal morphology and larval brain development. Finally, we will perform in-depth functional analyses for a few of those genes.Together, our effort will create a resource for genome comparisons beyond this project, will lead to a genome-wide view on the protein coding gene changes associated with an insect key innovation and it will identify the function of novel regulators involved in holometabolan development.