NEW Projects in the second funding phase
Core-project 2: Functional annotation of genomic innovations in a densely populated clade with deep learning
This project aims to develop a sustainable, integrated annotation pipeline for gene prediction, with a strong emphasis on newly emerging genes, providing a core resource for GEvol projects. By adapting and expanding existing workflows, the project will enable high-quality annotation using advanced tools such as BRAKER and Tiberius.
A key focus is the prediction of newly emerging genes, addressing a major challenge in evolutionary genomics. Bulk genomic and transcriptomic data will be processed through a Snakemake-based pipeline, supporting both existing annotations and de novo genome annotation. To enhance predictions, the project will refine a UTR annotation pipeline based on RNA-Seq/IsoSeq data, generating critical training data for deep learning.
Tiberius will be expanded with a UTR model and adapted for de novo gene prediction through modifications to its loss function, supervised learning on a "de novo gene set," and RNA-Seq/IsoSeq-based noise reduction. The possible integration of Clamsa to generate base-wise prediction so signals of de novo genes will also be evaluated.
The final pipeline will integrate Tiberius into workflows for large-scale genome-wide annotation, including functional annotation via FANTASIA to uncover the evolutionary roles of predicted genes. Significant GPU resources and an experienced postdoc will be essential for implementation.
This project will deliver a scalable, reusable infrastructure for gene annotation, supporting GEvol and advancing evolutionary genomics research.
Project Team
Co-option of sex determination and differentiation pathways in caste differentiation in ants
Major evolutionary transitions are key events in evolutionary history leading to an increase in the complexity of life. Following the major transition to sexual reproduction, sex determination and differentiation pathways evolved which encode sex-specific phenotypes from the same genome; the same mechanisms have been shown to modulate alternative phenotypes within sexes in some species. We hypothesize that due to their prominent role in the regulation of phenotypic variation, sex differentiation mechanisms have been co-opted in the major transition to superorganismality in ants, explaining the modular development of fertile queens and non-reproductive workers. Support for this idea comes from our model species Cardiocondyla obscurior, as well as from other social Hymenoptera. In C. obscurior embryos with known sex and caste, many microRNAs and mRNAs with sex-biased expression are expressed in a caste-biased manner, similar to previous findings showing caste-specific differential splicing of genes expressed in a sex-biased manner in final stage larvae. Using a comparative approach, we will investigate the evolution of co-option of sex differentiation mechanisms in caste differentiation in three ant species with obligately sterile workers, Cardiocondyla obscurior, Solenopsis invicta and Pheidole pallidula. These three species belong to the largest ant subfamily, the Myrmicinae, and each represents one of the three most diverse taxa within the subfamily (Crematogastrini, Solenopsidini, Attini), thus covering substantial phylogenetic breadth. This will be complemented with a functional, experimental approach using RNAi knockdowns of doublesex in the lab model C. obscurior. Our project will assess the molecular mechanisms underlying sex and caste differentiation across the entire course of ant development, thus providing the opportunity to study the evolution of regulatory mechanisms acting in both processes. Together, the results from this project will contribute basic knowledge about the mechanistic links between two major evolutionary transitions.
Project Team
Dramatic genome rearrangements in Cardiocondyla
We are currently comparing genome architecture in Cardiocondyla and several other ant species as part of the first phase of GEvol. Our analyses revealed extreme degrees of genome rearrangements with a nearly complete decay of macro- and micro-synteny in Cardiocondyla. Similar “chromosomal tectonic shifts” have recently been described in other animal lineages where they are suggested to be associated with fundamental shifts in life history and ecology, such as the transition from marine to terrestrial habitats in annelids. At first glance, there is no such fundamental transition apparent in Cardiocondyla ants, who form inconspicuous colonies that look very much like colonies of other ants. However, the males of Cardiocondyla are indeed unique among ants in that they have evolved into so-called ergatoid fighter males. Unlike males of other ants, the males of Cardiocondyla show physiological, developmental, morphological and
behavioral specializations (e.g. accelerated development, life-long spermatogenesis, enlarged mandibles) to monopolize reproduction within the colony, often by killing rival males. To explore whether this remarkable evolutionary transition in male life history is associated with the extensive reorganization of the genome in this genus, we propose to (1) combine gene co-expression and ATACseq to reconstruct ergatoid male specific gene regulatory networks, (2) use microCT scanning to characterize the micromorphology of the ergatoid male syndrome, and (3) use in situ hybridization and RNAi to identify key genes driving the developmental canalization towards the ergatoid phenotype across multiple species of Cardiocondyla.
Project Team
Beyond averages: the evolution of transcriptional variability and its role in adaptation and evolutionary innovation
The study of gene expression evolution and how it relates to speciation and adaptation is usually focused on differences in mean expression values between species. However, there is growing evidence that not only mean expression values but also expression variability, the spread of individual expression values around the group average, is an important gene property which is genetically regulated and plays an important role in adaptation to new environments. The molecular and evolutionary constraints on the degree of expression variance per gene have been explored at the population level. In this project, we will take a phylogenetic approach to study how expression variance evolves in the Drosophila clade, and what are the potential implications for adaptation, de-novo gene evolution, and gene regulatory network evolution. For this, we focus on six Drosophila species spanning 3-40 M years of divergence. For each species we collect RNAseq data for different inbred lines (different genotypes), as well as for multiple individuals per inbred line (same genotype) to be able to model transcriptional variance at the species level, as well as transcriptional noise for each genotype, respectively. With a focus on gene regulatory networks, we will develop stochastic models for the evolution of transcriptional variance across the Drosophila phylogeny and ask 1) what is the type of selection shaping its evolution, and 2) what are the associated molecular and regulatory network changes that drive such evolution. This project will combine experimental, bioinformatics, and theoretical approaches to tackle these questions.
Project Team
FOrmidablE - Function, Origin and Evolution of peptides in venoms of formicine ants
Venomous animals and the venoms they wield as a biochemical weapon for foraging and defense are a remarkable example of repeated evolution that can be used to study processes of adaptive evolution using comparative approaches. Species of the insect order Hymenoptera, including wasps, bees, and ants, are equipped with venoms that in most cases contain proteins and peptides as the principle active compounds.
More than 50 years ago, a peptide fraction was discovered in the highly acidic, formic acid containing venoms of non-stinging ants of the subfamily Formicinae. Whilst recent work has revealed that formic acid serves not only as a chemical weapon but also plays a role in cognition and immune defence, up till now, the identities, functions, and evolutionary origins of these peptides have never been addressed. In preliminary work, we recently discovered several peptides in venoms of Camponotus (carpenter ants), which appear to be unique to the Formicinae ant subfamily.
The aim of the present proposal is to 1) thoroughly investigate the content of venom peptides in additional Formicine species to uncover novel peptides and their genes, 2) to comprehensively study the diversity and evolution of these novel venom peptide gene families across all available formicine genomes including outgroup genomes of Myrmicinea and other Hymenoptera, and 3) to investigate their function using bioassays. To achieve this aim, we will combine organismic, comparative genomic and transcriptomic as well as analytical chemistry know-how and methods in this interdisciplinary proposal.
This study will thus provide a hitherto unprecedented insight into venoms and evolutionary novel venom peptides of ants from the subfamily Formicinae. Additionally, results of this study will add to the expanding knowledge on molecular mechanisms underlying the origin, evolution, regulation and function of diverse animal venom systems
Project Team
Gene regulatory mechanisms underlying the expression of social behaviour in two distinct beetle clades
Although sociality is rare in insects, various social lifestyles have arisen sporadically across a broad range of taxa. The simplest form, subsociality, in which only some form of parental care exists, has evolved independently in at least 13 insect orders. However, transitions from subsociality to the most advanced level, obligate eusociality, are extremely rare. This transition from brood care to colonies with reproductive division of labour and overlapping adult generations has only occurred in 3 insect orders: Multiple times in Hymenoptera (ants, some bees and wasps), once in Blattodea (termites) and once in Coleoptera (ambrosia beetle).
In the first phase of the SPP-Gevol this project investigated the genomic mechanisms linked to the multiple origins of sub-sociality in beetles, as well as those associated with the rare advancements to higher forms of sociality. Ten new genomes were sequenced to uncover gene family expansions and contractions associated with the various social forms. To identify genes associated with social behaviour, we sequenced transcriptomes from head and fatbody tissue of five carrion and five weevil adult female beetles before and during three distinct social phases: (i) early pre-hatching care, (ii) late pre-hatching care and (iii) post-hatching care. We were able to find distinct changes in gene expression levels following the transition from the solitary to the social phase and between successive social phases. Gene expression patterns associated with social behaviour are species-specific and closely resemble ecological and behavioural factors during the reproduction of each species.
For the second phase, we now propose to make use the newly generated genome resources as a backbone and go one step further to investigate the regulatory machinery involved in the expression of social behaviour. We will use the same set of beetle species across the sociality gradient as in phase one. We will again collect samples from the different care-taking time points, and also experimentally manipulate the expression of female social behaviour in species where this behaviour can be induced or inhibited. We will use species with fixed social behaviour and non-social behaviour as the extremes and outgroups. We will obtain brain transcriptomes to investigate gene expression patterns and complement those with information on a suit of epigenetic factors putatively involved in regulating this behaviour. These will include cPG methylation (enzyme-seq), histone acetylation (H3K27ac; CUT&TAG), and two histone methylation marks (H3K27me, H3K4me; CUT&TAG)
Project Team
Genetic and genomic structural evolution underlying feeding ecology transitions in the Hemiptera
The Hemiptera are the largest order of hemimetabolous insects, comprising many species of agricultural and medical importance. Their evolutionary history includes repeated, often convergent shifts in feeding strategies, with lineages adapting to plant feeding (phytophagy) or predation, including blood feeding. Within the seed bug family (Lygaeidae), recent dietary adaptations span from monophagous (feeding on a single plant species) to generalist (feeding on many plant types) strategies.
Feeding is a key trait for connecting genomic changes to phenotypic outcomes. The recent expansion of genomic resources in Hemiptera presents an opportunity to study the genetic and genomic basis of diversification and convergent feeding strategies at an unprecedented scale. Hemiptera are still underrepresented in comparative genomics and offer distinctive features for study, including high rates of intron gain and turnover, as well as varied feeding ecologies.
This project integrates expertise in algorithm development, comparative genomics, and Hemiptera biology to conduct multi-scale, multi-modal analyses of the evolution of metabolic and regulatory pathways related to feeding. We will examine whether species regulate feeding behavior by adjusting gene expression or by deploying different subsets of their gene repertoire. By compiling advanced genomic datasets—including curated gene sets for metabolism—we will identify the global set of feeding-related genes. Tracing orthologs across hundreds of species will reveal their evolutionary trajectories within a broad Hemiptera pan-genomic framework, situating our findings on the model species Oncopeltus fasciatus. Gene expression profiling across species with varying dietary specializations—both in the wild and in experimentally tractable systems—will clarify how regulatory changes underlie dietary adaptation.
We will investigate the relative roles of gene duplication and alternative splicing in protein functional diversification. Using innovative approaches linking intron-exon structures to 3D protein folding, we aim to identify structural impacts of transcript diversity. Key candidate genes emerging from these analyses will be functionally tested and integrated into broader metabolic and regulatory networks.
We will also trace the taxonomic origin of feeding-related genes to construct a holo-genome perspective on feeding biology. This includes exploring microbial genomic bycatch data to test hypotheses about metabolic complementation between insect hosts and their microbiomes.
Ultimately, our work will illuminate how feeding-related genomic strategies have evolved across Hemiptera, and how these strategies compare both within the order and with other insect taxa that have converged on similar diets.
Project Team
GEvol-Defence – Evolution of a novel cellular defence via horizontal gene transfer in leaf beetles
The evolutionary success of insects lies in their versatile defence systems against pathogens and predators. Insects’ cellular defence is mostly mediated by hemocytes, a group of cells that are important for immunity and toxin production. Although evidence suggests rapid evolution of hemocytes, the genomic mechanisms remain elusive. Our recent Colorado potato beetles (CPB, Leptinotarsa decemlineata) expression atlas showed that three recently duplicated genes, which originated from horizontal gene transfer from bacterial at the basal branch of leave beetles, were specifically expressed in CPB hemocytes, suggesting that horizontal gene transfer (HGT) can contribute to the evolution of novel defences in the beetles. Here, we aim to illustrate how these HGT genes evolve and contribute to novel cellular defences in beetles. We will first peform single-cell RNA- and ATAC-sequencing to identify in which hemocytes are these HGT genes expressed and evovled among six beetle species, using Tribolium castaneum as an outgroup where we recently fully characterized hemocytes on a morphological and genetic level. Then, we will perform RNA interference to investigate the cellular defence functions of these HGT genes in two leaf beetles. Third, we will reconstruct the evolutionary history of the HGT genes, aiming to identify the key functional motifs that contributed to the novel defence function in beetles. We will further test the predicted evolutionary changes and their functions by expressing them in Drosophila melanogaster. By integrating state-of-the-art genomic and molecular tools, this project will provide new insights into how HGT genes can be recruited into existing signaling networks and contribute to novel defences in insects.
Project Team
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