Revealing the genomic innovations during evolution of holometaboly

一些进化创新为一个支系打开了全新的机会，促进了它的辐射。因此，进化生物学中的一个基本问题是，这些关键创新是如何进化的，是什么基因组变化推动了它们的出现。昆虫中最成功的创新之一是导致辐射的全变态生命周期，这种辐射占所有现存节肢动物物种的70%。与半代谢若虫不同的是，全代谢幼虫与成虫有很大的不同，允许它利用不同的生态位并专门化，例如生长和繁殖。最终，成虫的形态在蛹阶段的戏剧性重建过程中形成。什么基因参与了这一关键创新的进化，以及它们是如何影响发育过程的，这仍然是一个谜。真核基因组的注释缺乏它们的测序和组装。例如，2021年11月，在NCBI的749种昆虫中，只有198种在脚手架水平上进行了组装，其中只有198种有存放的注释。此外，大多数基因组一次只有一个被注释，基因结构预测的错误在比较分析中是必然的，因为它们通常关注相关物种之间的差异。同时，密切相关基因组的爆炸性增长允许利用新的方法来利用深度多基因组比对来使其注释更加准确和一致。在此，我们建议增强生物信息学工具以实现一致和准确的比较基因组注释。我们将把这些增强的方法应用于数百个昆虫基因组，在本SPP中测序或以其他方式获得。这一努力将为蛋白质编码基因的比较研究创造可能最大的昆虫基因组注释资源。在这个项目中，我们将挖掘资源，以确定在全代谢出现期间发生了重大变化的编码基因。从这个集合中，我们将系统地确定所选择的全息代谢特定发育过程所需的所有功能基因，即幼虫和蛹的表皮形态和幼虫的大脑发育。最后，我们将对其中几个基因进行深入的功能分析。我们的努力将创建一个超越该项目的基因组比较资源，将导致与昆虫关键创新相关的蛋白质编码基因变化的全基因组视角，并将确定参与全代谢发育的新调控因子的功能。

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.