Core-project: Global patterns of genomic innovations
New experimental and computational techniques provide exciting opportunities to study the evolutionary his- tory of genomes and to reconstruct the emergence of new traits from an integrated, phylogenomic perspective, way beyond the limited perspective of model species. GEvol will exploit these opportunities by connecting researchers from complementary fields, including genomics, bioinformatics, evolutionary ecology, molecu- lar evolution, and developmental biology to unravel the dynamics of major genomic innovations underlying novel traits in insects.
This project will knit together several strands of research from within the SPP and focus on the gain and loss of transcripts, genes, domains and regulatory motifs related to, e.g. sociality or mating systems; complex systems of communication and defence, developmental and morphological innovations and plasticity. The project will combine multiple genomic and other OMIC resources (e.g., genomics, transcriptomics and epigenomics), allowing for comparative evolutionary genomic studies to delineate past events, even many million years ago. We will study the roles of coding vs. regulatory changes, transposable elements, epigenetics, gene family evolution, copy number dynamics and structural genomic rearrangements.
In first place we will focus on genomic innovations, comprising the expansion or contraction of gene families, including the de novo emergence of novel genes and the prevalence and effects of gene losses. We will study the frequency at which novel protein domains are gained or lost and how they are rearranged. Through collaborations, we will develop tools for automated integration of new data from annotation pipelines with the objective to compute selection signatures across the whole
insect phylogeny and relate them to phenotypic innovations and transitions in gene regulation.
Project Team
Publications
Book chapter: Feldmeyer, Barbara; Bornberg-Bauer, Erich; Dohmen, Elias; Fouks, Bertrand; Heckenhauer, Jacqueline., Huylmans, Ann Kathrin; Jones, Alun RC; Stolle, Eckart and Harrison, Marc C, 2023
Comparative Evolutionary Genomics in Insects
Dohmen, Elias; Aubel, Margaux; Eicholt, Lars A.; Roginski, Paul; Luria, Victor; Karger, Amir; Grandchamp, Anna
DeNoFo: a file format and toolkit for standardised, comparable de novo gene annotation
In: Bioinformatics, vol. 40, iss. 10, pp. btaf539, 2025.
Grandchamp, Anna; Aubel, Margaux; Eicholt, Lars A.; Roginski, Paul; Luria, Victor; Karger, Amir; Dohmen, Elias
De Novo Gene Emergence: Summary, Classification, and Challenges of Current Methods
In: Genome Biology and Evolution, pp. evaf197, 2025.
Webserver
https://gevol-viewer.uni-muenster.de/
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
Comparative and experimental approaches to the transcriptomics and genomic regulation of eusociality in the sweat bees
Eusociality is a major evolutionary innovation that has independently evolved multiple times across the insects. Using one lineage of halictid bees (Hymenoptera: Halictini) in which eusociality has arisen once, been elaborated upon and subsequently lost repeatedly, we investigated in the preceding project of phase I of GEvol the variation in gene expression and its regulation associated with the gain and subsequent loss of eusociality. Results from this preceding project provide indirect support for the idea that the evolutionary origin of eusociality is rooted in the developmental plasticity of ancestral behavioural traits (working and reproducing), predicted to be coupled in the solitary ancestor and decoupled in the eusocial descendent. Our data suggest that the different social phenotypes that are the hallmark of eusocial systems (queens and workers) might have emerged from evolutionary changes in the way ancient genes are expressed, i.e. from changes in gene regulatory networks. In this follow-up project, we rely again on the socially variable halictid bees for a cross-species comparison of ancestrally solitary, eusocial and derived solitary species to study how shifts in gene expression that we have observed in phase I are regulated, with the aim of understanding the extent to which the origin of eusociality is ascribable to changes in regulatory mechanisms. We intend to: i) identify regulatory elements that act as regulatory switches of gene expression through the integration of deep learning approaches and multi-omics data (RNAseq, ATACseq, CUT&Tag, EMseq); ii) study how these regulatory elements evolved; and iii) investigate the extent to which conserved genes, such as developmental genes and genes involved in sex differentiation, have been co-opted for eusociality. Our proposed study will contribute to a better understanding of the genetic origins of biological novelties, of which eusociality is one of the most intriguing.
Project Team
Conflict or cooperation between transposons and their Drosophila hosts?
Telomeres, repetitive DNA at chromosome ends, protect coding DNA from the shortening of chromosomes at cell replication. In most eukaryotes, telomeres are maintained by the enzyme telomerase. Accordingly, Diptera are unusual because they have lost telomerase. Alternative telomere-maintenance strategies include, among others, telomere-specific transposable ele- ments that maintain telomeres by replication at chromosomal ends. In our project FlyInnovation, we will determine if telomere-specific transposable elements are a genomic innovation for preserving telomeres in the absence of telomerase or simply selfish genetic elements avoiding host-silencing in a genomic safe-site.
Project Team
Publications
Omole,Adekanmi Daniel; Czuppon, Pete
Maintenance of long-term transposable element activity through regulation by nonautonomous elements
In: Genetics, 2025
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
![Avatar](https://g-evol.uni-muenster.de/wp-content/uploads/2025/11/csm_Schultner.jpg")
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
Dynamics of chromosome evolution in termites: Inbreeding, translocations and sociality
Inbreeding is widespread in insects and may have negative effects on individual fitness. In social insects, only a few individuals reproduce often with related individuals. Inbreeding could thus encourage kin selection and plays a role in the evolution of eusociality. One very interesting trait that may occur due to inbreeding is the formation of ring chromosomes and chromosome chains. Ring chromosomes have been observed in male meiosis of several termite species and may increase the rate of translocations via uneven break-ups. Furthermore, this also involves the sex chromosomes and may thus enable fast evolution of sex determination. Furthermore, inbreeding may impact male and female fitness differently, as has, for example, been shown for immunity in Lepidoptera and crickets.
While the X chromosome in termites shows at least in parts homology to that of cockroaches from which termites have evolved, the Y chromosome is young and must have appeared at the base of the termites. It is likely that this new sex chromosome has evolved from a fusion or translocation, possibly as a consequence of increased inbreeding with the onset of sociality. We will investigate chromosome evolution in termites to answer questions with regard to the evolution of sociality, inbreeding, and sex determination.
Project Team
Publications
Fraser, Roxanne; Moraa, Ruth; Djolai, Annika; Meisenheimer, Nils; Laube, Sophie; Vicoso, Beatriz and Huylmans, Ann Kathrin
Recurrent sex chromosome turn-over in termites
In: Preprint
Emergence, loss and regulation of de novo genes
In recent years, a major shift has occurred in understanding how new proteins arise and gain function. Earlier research assumed that small, adaptive changes in duplicates of established genes led to the evolution of new proteins with new functions. However, recent research showed that new protein-encoding genes can arise ”de novo” from previously non-coding DNA. Although some mechanisms underlying de novo gene emer- gence are now understood, no coherent picture of how and how often novel protein coding genes arise, gain function and spread through a population is available. The aim of this project is to characterise the short and long-term evolutionary dynamics of de novo gene emergence, loss and regulation. This will be done by sequencing genomes and transcriptomes of multiple Drosophila species spanning 3–40 million years of evo- lutionary divergence, including multiple individual genomes per species. This will allow us to precisely pin down the most recent events, such as the emergence of regulatory sequences that may have triggered the expression of an intronic or intergenic region. Including longer time scales will allow us to understand how often protein coding genes are created de novo and how often they are lost – most likely because they had not assumed a sufficiently important function to be retained by selection. Bioinformatic, population genetic and experimental functional genetic analyses will be performed to expand our understanding of how genomes change over time to give rise to new molecular and phenotypic traits.
Project Team
Publications
Grandchamp, Anna; Kühl, Lucas; Lebherz, Marie; Brüggemann, Kathrin; Parsch, John; Bornberg-Bauer, Erich
Population genomics reveals mechanisms and dynamics of de novo expressed open reading frame emergence in Drosophila melanogaster
In: Genome Research, 2023.
Glaser-Schmitt; Amanda, Lebherz, Marie; Sayda, Ezgi; Bornberg-Bauer, Erich and Parsch, John
Expression of de novo open reading frames in natural populations of Drosophila melanogaster
In: Journal of Experimental Zoology Part, 2025
Grandchamp, Anna; Czuppon, Pete and Bornberg-Bauer, Erich
Quantification and modeling of turnover dynamics of de novo transcripts in Drosophila melanogaster
In: Nucleic Acids Research, 2024
Lebherz, Marie; Fouks, Bertrand; Schmidt, Julian; Bornberg-Bauer, Erich and Grandchamp, Anna
DNA Transposons favour de novo transcript emergence through enrichment of transcription factor binding motifs
In: Genome Biology and Evolution, 2024
Ravi, Bharat I.; Grandchamp, Anna and Bornberg-Bauer, Erich
How antisense transcripts can evolve to encode novel proteins
In: Nature Communications, 2024
Evolution of epigenetic regulation in beetles (Coleoptera)
Insects show a remarkable evolutionary flexibility concerning the means by which epigenetic regulation is achieved. Even within the group of beetles (Coleoptera), some species rely on CpG methylation, while other species do not seem to show any functionally relevant levels of CpG methylation. Accordingly, genes encoding DNA methyltransferases (Dnmt1 and 3 genes) have been partially (e.g., Tribolium castaneum) or completely (e.g., Dendroctonus ponderosae) lost in some beetle species. Surprisingly, knock-down of these Dnmt genes can have strong and even lethal effects, even in species lacking CpG methylation, suggesting additional func- tions of DNMTs. On the other hand, it is still unclear, which other epigenetic processes could have replaced CpG methylation in such species.
In vertebrates, histone modification plays a major role in gene regulation. Many core components of the hi- stone modification system are even conserved from animals to plants. Both, histone modification and DNA methylation are global regulators that are mechanistically similar in the sense that they give rise to marks being set along the genome but distinct with respect to their material basis. However, the combined mode of control may range from the mere coexistence to indispensable and rich crosstalk.
Our project thus has the following three main aims: (1) Understanding the evolution of epigenetic regulation systems; (2) Elucidating alternative functions of DNA methyltransferases; (3) Assessing the mutual depen- dences between DNA methylation and histone modification. We will make use of the combined power of bioinformatics, sequencing technology to analyse epigenetic processes (Methyl-Seq, Cut&Tag, RNAseq) and functional validation (RNAi) in ten beetle species. Our project addressing the surprising evolutionary flexibil- ity in something as crucial as epigenetic regulation will thus provide urgently needed basic knowledge of the evolution of epigenetic regulation systems even more generally, beyond insects.
Project Team
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Publications
Israel, Elisa; Länger, Zoe M.; Heckenhauer, Jacqueline; Kurtz, Joachim and Projaska, Sonja J.
MBD2/3 lost its methyl-CpG binding ability in multiple families of Holometabola
In: biobxiv 2025,
Länger, Zoe M.; Israel, Elisa; Engelhardt, Jan; Kalita, Agata I.; Keller Valsecchi, Claudia I.; Kurtz, Joachim and Projaska, Sonja J.
Multiomics reveal associations between CpG methylation, histone modifications and transcription in a species that has lost DNMT3, the Colorado potato beetle
In: J Exp Zool B, 2025,
Evolutionary genomics of sociality in beetles
Although sociality is rare in insects, various types of social lifestyles have evolved sporadically across a broad range of taxa. Sociality ranges from parental care of offspring in subsocial species to complex colonies with division of reproductive labour in eusocial insects, such as in ants, as well as some bees, wasps and termites. Several comparativea studies have revealed a broad range of genomic signatures related to the evolution of eusociality, especially in Hymenoptera (mainly ants and bees) and termites. However, little is known about the genomic origins of sociality in beetles or on the early transitions from solitary living to subsociality.
This is an important omission since subsociality, which occurs in at least 11 beetle families, is recognised as an important first step towards eusociality. With our project we aim to close this gap by investigating the genomic signatures related to the evolution of sociality in beetles. We put a particular focus on genomic mechanisms linked to the early stages of social evolution and aim to distinguish these molecular signals from those related to later elaborations towards eusociality.
We propose to study several species from two beetle families (carrion beetles and weevils) that cover several levels of subsociality, two origins of facultative and one origin of obligate eusociality.
With a broad range of genomic and transcriptomic analyses, we plan to infer detailed changes in genomic content, transcriptional regulation, protein evolution, and expression patterns, that are related to the tran- sitions from solitary to subsocial living and then the further elaborations towards obligate eusociality. We will support these inferences with investigations into the influence of purifying and positive selection, as well as genomic and transcriptomic upheavals caused, for instance, by transposable element activity. In the early stages of social evolution, we expect to find regulatory changes leading to the emergence of expression patterns associated with parental care. Greater adaptive changes, especially those affecting communication, nutrition, and immunity, are expected to occur along the progression towards obligate eusociality in wood- boring weevils. With genomic comparisons across all origins of insect eusociality (Hymenoptera, Isoptera and Coleoptera), we aim to identify molecular mechanisms that are universally associated with the rare evolution- ary progressions from solitary to eusocial species. Moreover, by combining these genomic and transcriptomic analyses with lab-based manipulations and RNAi experiments we aim to identify candidate gene families and networks that are integral to social behaviour. This project can bring us closer to understanding the genomic and regulatory mechanisms associated with the emergence of subsociality from solitary ancestors, and its rare advancement along the ultimate transition towards eusociality.
Project Team
Publications
A, Mikhailova; S, Rinke; MC, Harrison
Genomic signatures of eusocial evolution in insects.
In: Current Opinion in Insect Science, 2023.
T, Biswas ; H Vogel; PHW Biedermann; M Lehenberger; JK Yuvarai; MN Andersson,
Few chemoreceptor genes in the ambrosia beetle Trypodendron lineatum may reflect its specialized ecology.
In: BMC Genomics, 2024
S Rinke; PHW Biedermann; M Schebeck and MC Harrison,
Genomic Insights into the Evolution of Parental Care in Weevils
Evolution of transcriptional noise and its role in adaptation and evolutionary innovation
Transcriptional noise is understood as gene expression variation between individuals of the same genotype. However, contrary to what the term ‘noise’ might imply, it has been shown that the amount of noise is a gene property, with environment-sensing genes being noisier (i.e., more variable) across individuals, and housekeeping genes being less noisy. Such gene-level noise correlates with other gene-level properties like amount of genetic diversity, gene essentiality, and network connectivity. Taken together, this data points to the fact that transcriptional noise has been evolutionary constrained and therefore that it could play a role in adaptation to new environments. Here we aim to explore whether this is the case by focusing on six species of the Drosophila clade. Transcriptional noise has not been explored in a phylogenetic context, and we will use this set up to tackle three main questions: 1) Does gene-level expression noise evolves. 2) What are the genomic signatures that are acquired during evolution to regulate the level of transcriptional noise, in other words, how do the ‘genomic neighborhoods of robustness’ look like. And, 3) do genes with larger transcriptional noise tend to be more involved in adaptation and evolutionary innovation?
Given the fact that transcriptional noise has been understudied, there is the need to develop theoretical models for noise evolution. Based on these models we will develop data analysis methods 1) to robustly infer variance (e.g., noise) and quantify variance differences within and across species, 2) to model the role of transcriptional variance in evolutionary adaptation, and 3) to evaluate transcriptional noise driven by genetic vs non-genetic sources (i.e., within-genotype vs between-genotypes), including e.g. adaptation and the emergence of de-novo genes. On the experimental side, we will collect RNAseq data for multiple individuals of five inbred lines per species. This dataset will allow us to quantify transcriptional noise within genotype, but also across genotypes for each one of the six Drosophila species.
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 and genome duplication and phenotypic novelties – Insights from spiders and insects
Phenotypic novelties, such as the wings in insects or silk glands in spiders, facilitate adaptations to changing environments and are thus a major driver for evolutionary diversification. Expansion of genomic information by small-scale gene duplications (tandem duplications) or large-scale duplications (chromosomal or whole genome duplications) are important prerequisites for such novelties. Recent genomic analyses of different arthropod groups revealed at least one large scale duplication event at the base of the arachnopulmonates (e.g. spiders and scorpions). This finding provides a unique opportunity to compare the consequences of large-scale duplication events to small-scale duplications commonly observed in insects. Since vertebrates (that underwent several rounds of whole genome duplications), have hitherto been the only animals to study the consequences of large-scale duplication events, new genomic resources in arthropods now facilitate the comparison of large-scale duplication events across different animal groups. Duplicated genes that are bene- ficial for the organism are usually retained in the genome and subsequent diversification of gene expression and function contributes to phenotypic innovations. A systematic genome-wide analysis of gene duplications and their impact on phenotypic novelties is missing in arthropods. Therefore, we will combine comparative genomics, functional genomics and functional genetics approaches to reveal gene retention and gene loss patterns in insects and spiders and to functionally test the impact of gene duplications on phenotypic nov- elties. We will assemble and annotate high-quality reference genomes for underrepresented spider lineages and analyze them together with existing high-quality insect and chelicerate genomes. We will study intron architecture, transposable element content, chromatin accessibility and transcript expression levels to gain insights into the molecular mechanisms underlying the diversification of expression of gene duplicates. For selected gene duplicates we will analyze spatial and temporal expression in developing spider novelties like breathing organs or the silk apparatus, and the function of a subset of genes will be functionally validated via RNA interference mediated gene knock-down. Our work will provide unique insights into the extent, nature and consequences of gene and genome duplications and their importance for the evolution and diversification of phenotypic novelties.
Project Team
Publications
Janssen R, Pechmann M.
Expression of posterior Hox genes and opisthosomal appendage development in a mygalomorph spider.
In: Dev Genes Evol., 2023.
Erdogan, Dugcar E; Karimifard, Shadi; Khodadadi, Mozghan; Ling L; Linke, Luisa; Catalan, Ana; Doublet, Vincent; Glaser-Schmitt, Amanda; Niehuis, Oliver; Nowick, Katja; Soro, Antonella; Turetzek, Natascha; Feldmeyer, Barbara and Posnien, Nico.
ATAC-seq in Emerging Model Organisms: Challenges and Strategies.
In: J Exp Zool B, 2025
Munegowda, Chetan; Pechmann, Matthias; Prpic-Schäper, Nikolai-Michael and Turetzek, Natascha;
Gene and genome duplication in spiders.
In: J Exp Zool B, 2025
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
Genomic and gene regulatory basis of cuticular hydrocarbon diversification in aculeate Hymenoptera
Evolutionary innovation can result from various mechanisms from genomic to regulatory changes. Evolution- ary innovation is particularly interesting to study complex phenotypic traits that are vital for the organism, yet evolve rapidly. Cuticular hydrocarbon (CHC) profiles represent such a multifunctional trait in insects. CHCs cover the body of all terrestrial insects, protecting against water loss and carrying communicating informa- tion. CHC profiles can differ drastically between closely related species, conspecific sexes, and — in social species — between castes, suggesting a versatile underlying genetic machinery. Despite a generally good understanding of CHC biosynthesis, we still know little about the molecular mechanisms behind intra- and interspecific CHC variation and novel phenotypes. Our project aims to identify the genomic, transcriptomic, and epigenetic underpinnings of CHC diversification. We study 13 pairs of closely related yet chemically dis- tinct species that cover the major lineages of aculeate Hymenoptera (stinging wasps, ants, and bees), and also consider sex and caste differences in some of these species. We are sequencing the genomes of 13 species, and exploit available genomes where possible. Applying a cross-species comparative genomic approach, we will assess the relative importance of gene copy number variation, non-synonymous changes in coding sequences, alternative mRNA splicing, and other regulatory changes for fostering diversification of this multifunctional trait.
Project Team
Genomic evolution of underwater silk in caddisflies (Insecta: Trichoptera) and other freshwater arthropods
Aquatic insects have been neglected in genomic studies. However, they exhibit a suite of ecologically relevant key innovations and adaptive traits, the evolution and genetic background of which remain poorly understood. This project is designed to fill this gap by generating and analyzing genomic data to study the evolution of adhesive underwater silk in Trichoptera (caddisflies) and other (semi-) aquatic arthropods. Caddisflies exhibit the greatest diversity of underwater silk uses. This exciting key innovation has potentially facilitated their radiation across a multitude of different aquatic environments. Further, the unique properties of under water silk (polymerization in aquatic environment, enormous tensile strength, elasticity) makes this system interest- ing for applied sciences. Using a comparative genomics framework and targeting mechanisms such as gene family expansion, selection, presence/absence of genes and variation in gene sequences (e.g. repeat motifs in important silk gene clusters), the project aims to uncover the genomic basis of the evolution of genes and gene families encoding for silk phenotypes in Trichoptera and other freshwater arthropods. Further, by looking at different developmental stages, genetic modulation and regulation of the different properties of silk will be investigated, i.e., the role of gene expression and post-transcriptional modifications (e.g., alternative splicing) and potential methylation patterns in silk genes will be examined. Understanding the genomic evolution and molecular mechanisms of silk production will not only address questions regarding molecular adaptations responsible for the diversification in aquatic environments but also lay the foundation to gauge the potential of underwater silk for biomedical and biotechnological applications.
Project Team
Publications
Deng, X; Kuranishi BR; Pauls , Steffen U.; Frandsen, Paul B. and Heckenhauer, Jacqueline;
De novo whole genome assemblies of unusual case-making caddisflies highlight genomic convergence in the composition of the major silk gene (h-fibroin)
In: J Exp Zool B, 2025
Heckenhauer, Jacqueline., Stewart, Russel J.; Rios-Touma, Blanca; Tshering, Dorji; Frandsen, Paul B. and Pauls U., Steffen
Characterization of the primary structure of the major silk gene, h-fibroin, across caddisfly (Trichoptera) suborders
In: IScience, 2023
Heckenhauer, Jacqueline; Plotkin, David; Martinez, Jose I; Bethin, Jacob; Pauls , Steffen U.; Frandsen, Paul B. and Kawahara, Akito Y.
Genomic resources of two aquatic Lepidoptera, Elophila obliteralis and Hyposmocoma kahamanoa, reveal similarities with Trichoptera in amino acid composition of major silk genes
In: G3 (Bethesda), 2024
Frandsen, Paul B; Hotaling, Scott; Powell, Ashlyn; Heckenhauer, Jacqueline.; Kawahara, Akito Y.; Baker, Richard H.; Hayashi, Cheryl Y.; Rios-Touma, Blanca; Holzenthal, Ralph; Pauls U., Steffen and Stewart, Russel J.
Allelic resolution of insect and spider silk genes reveals hidden genetic diversity
In: PNAS, 2023
Powell, Ashlyn; Heckenhauer, Jaqueline; Pauls, Steffen U.; Ríos-Touma, Blanca; Kuranishi, Ryoichi B.; Holzenthal Ralph W.; Razuri-Gonzales, Ernesto; Bybee, Seth and Frandsen, Paul B.
Evolution of Opsin Genes in Caddisflies (Insecta: Trichoptera)
In: Genome Biology and Evolution, 2025
Sproul, John S.; Hotaling, Scott; Heckenhaauer, Jaqueline; Powell, Ashlyn; Marshall, Dez; Larracuente, Amanda M.; Kelley, Joanna L.; Pauls, Steffen U. and Frandsen, Pauls B.
600+ insect genomes reveal repetitive element dynamics and highlight biodiversity-scale repeat annotation challenges
In: Genome Research, 2023
Standring, Samantha; Heckenhauer, Jaqueline; Stewart, Russel J. and Frandsen, Paul B.
Unraveling the genetics of underwater caddisfly silk.
In: Trends in Genetics, 2025
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
ImmuNov: genomics and epigenomics of immune innovations in insects
With the project ImmuNov, my aim is to understand how novel genes, and genes with a novel function, can integrate into pre-existing highly conserved gene networks and how their expression is regulated. As a functional model, I will use the innate immune system of insects, which is both highly conserved in its core set of genes and signaling pathways, and one of the fastest evolving biological functions, displaying a high rate of gene gains and losses across the insect phylogeny. To achieve this, I will perform a screen of immune- induced gene expression across phylogenetically diverse insect species, through experimental infections with two opportunistic pathogens, to identify common sets of immune genes and novel, taxon-specific immune- induced genes. I will test the role of chromatin accessibility as an epigenomic mechanism to control the expression of immune genes in response to infections and identify the cis-regulatory elements that govern the expression pattern of immune-induced genes. Finally, I will reveal the evolutionary history of immune- induced genes and test whether taxon-specific immune genes exhibit specific epigenetic signature. The recent development in molecular and computational technologies offers the possibility to design for the first time a large-scale comparative study of immune-induced transcriptomes couple with epigenomics in a controlled fashion to identify novel genes and reveal their regulatory mechanisms. This innovative project will provide insights into fundamental functional aspects of the genomic and epigenomic basis of immune innovation in insects beyond the Drosophila model, insights which are not attainable with comparative genomics alone.
Project Team
Recurrent genomic dynamics linked to parallel evolution of secondary phytophagy in Hymenoptera
The phytophagous lifestyle is a key innovation in insects and has, evolved in only one third of all insect orders. The evolution of, phytophagy likely involves fundamental behavioural and morphological changes ac- companied by chemosensory and metabolic adaptations. To date, the genomic basis and genetic, innovations related to evolutionary dietary shifts are poorly understood. Here we focus on two monophyletic groups within the, order Hymenoptera, particularly Aculeata and Chalcidoidea, which, descend from zoophagous ancestors but exhibit repeated reversals towards secondary phytophagy. These lineages e.g., the gall-wasps and pollen- collecting bees, switched to phytophagy, while the sister lineages retained a zoophagous lifestyle. In order to contribute to our knowledge of the evolution of nutritional capabilities in insects, we propose to comparatively study the genomic architecture in representative Hymenoptera that are linked to transitions to secondary herbivory. To shed light on evolutionary processes that shaped the diversity of nutritional adap- tations in Hymenoptera we
address the following main research questions: (1) Is parallel evolution at the phenotypic level reflected by parallel genome evolution? And (2), did similar genomic innovations appear when independent lineages re- alized convergent dietary transitions? Using comparative genomics and transcriptomics we aim to uncover genomic underpinnings of macroevolutionary dietary adaptations linked to e.g., the metabolism of plant sec- ondary compounds, the composition of odorant receptors, gustatory receptor families, or carbon dioxide re- ceptor genes. Further, we will study genomic changes underlying evolutionary dietary shifts, testing the repeatability of gene gain and loss, and rapid evolution in regulatory sequences, transposable element dynam- ics, and gene copy numbers. Results will be of major interest to scientists in the fields of functional genomics, systematic biology, and protein function analysis of insects, including those insects of economic importance.
Project Team
Recurring phenotypic loss: Repeatability of genome and regulatory evolution
The loss of phenotypes represents a type of evolutionary innovation and is a widespread phenomenon. Like phenotypic gain, it can be adaptive and lead to new life histories. However, compared to phenotype gain, it is less well studied. A particularly interesting case for evolutionary studies is the repeated loss of the same phenotype in independent lineages, because this allows for investigating the repeatability, and to some extent predictability, of evolution. Here we propose to study the genomic basis of repeated phenotypic loss using pollen collecting structures as example. These structures, called scopae, have evolved in several independent bee lineages and facilitated the evolutionary success of these lineages as pollinators. As typically only fe- male bees engage in foraging, scopae are sexually dimorphic. Interestingly, scopae have been lost in more than a dozen independent lineages of kleptoparasitic bees, along with certain behaviors and pilosity. Using a genome-wide comparative approach, we aim to reveal the genomic underpinnings that lead to the repeated evolution of that loss.
To this end, we will take advantage of existing high quality bee genomes and produce another 21 new high quality bee genomes of species with critical positions in the phylogenetic tree. This will provide us with more than 100 genomes as foundation for comprehensively studying genomic differences at all levels to reveal the emergence of that phenotypic loss within a phylogenetic framework. Using forward phylogenomic genotype to phenotype mapping and comparative genomics we will investigate genomic changes associated with phe- notypic loss, in particular loss of genes and regulatory elements, including the evolution of gene families. As scopae are a sexually dimorphic trait that seems to be gained and lost dynamically during evolution, we hy- pothesize that gene regulatory changes play an important role in achieving such phenotypic plasticity that can eventually get fixed in the genome. Hence, in addition to genomes, we will also produce transcriptomes and ATAC-Seq data from six species, precisely three pairs of host and kleptoparasitic species having gained or lost scopae, respectively, from males and females during development. With this setup, we will test whether similar changes are involved in plastic as well as evolutionary loss of scopae. We will integratively analyze these new OMICs data using state-of-the-art computational methods to reveal the role of coding versus reg- ulatory changes, transposable elements in genome architecture and regulation, gene family evolution and sequence changes with a focus on gene regulatory factors. We will further study how the genomic elements and factors are interacting in regulatory networks and how these networks have changed during evolution. In addition, we will investigate shifts in selective pressures acting on coding and non-coding sequences to understand how they might have conveyed the repeated loss of scopae.
Project Team
Publications
Chen, Yao-Chung; Maupas, Arnaud; Nowick, Katja
Regulatory networks of KRAB zinc finger genes and transposable elements changed during human brain evolution and disease
In: eLife, 2025
Revealing the genomic innovations during evolution of holometaboly
Holometaboly is a key innovation within insects and led to a very successful and diverse clade, the holometabolous insects, which have conquered all habitats and include important pests and vectors. However, many aspects
of the evolution of holometaboly remain enigmatic. Do holometabolous larvae correspond to hemimetabolan embryos or nymphs? How did the simplified morphology of first instar larvae evolve? How did immature de- veloping brains become functional in first instar larvae? What is the genetic control of shifted developmental timing (heterochrony)? What genes are specifically required for metamorphosis leading to the pupa, a novel stage? Genetic studies have so far mainly relied on the fly Drosophila melanogaster, which shows a quite derived mode of metamorphosis.
We want to develop and apply a genome-wide bioinformatics approach comparing hundreds of insect genomes to identify genes that show signs of increased sequence evolution at the base of aholometabolous insects. Sub- sequently, we test the functions of the genes emerging from this analysis in the red flour beetle Tribolium castaneum, an insect with insect typical metamorphosis. This approach has become possible only recently, as a large number of high quality insect genome sequences have become available and since genome wide functional screening was established in an insect with typical metamorphosis.
Project Team
Publications
Saenko, Stepan, ; Hoff, Katharina J. and Stanke, Mario
Annotation of 200 Insect Genomes with BRAKER for Consistent Comparisons across Species
In: Preprint, 2025
The evolution of genome compartmentalization in the ant genus Cardiocondyla
Transposable elements (TEs) are major players in evolution. To advance our understanding of TEs in genome evolution, we will study evolutionary causes and consequences of extreme TE landscapes in the ant genus Cardiocondyla. The only so far studied species of this genus, the invasive C. obscurior, has evolved an extraordinary TE distribution with slowly evolving TE- poor and fast evolving TE-rich regions. By comparative genomic, population genomic and transcriptomic studies across several closely related species, we will unravel how such extreme genome architecture can evolve, how it affects genome evolutionary dynamics, and whether it can contribute to a species’ ability to adapt to changing environmental conditions. Further, by comparative analyses of ~170 genomes of ants, we will explore how TEs have impacted this large insect family and whether Cardiocondyla is indeed distinct from other ants given its remarkably unlikely genome structure. For these projects, we have already begun to develop a novel approach to identify, curate, classify, and annotate TEs across several genomes from the same clade aiming to generate high-quality TE annotations for accurate comparative studies.
Project Team
Publications
Schrader, Lukas; Rinke, Janina; Errbii, Mohammed; Teresi, Scott; van den Bos, Esther; Xiong, Zijun; Vizueta, Joel; Boomsma, Jacobus; Gadau, Jürgen and Zhang, Guojie
The impact of transposable elements on the adaptive radiation of ants.
In: submitted
Synteny-Based Identification of Genomic Innoavations in Insects
Genome architecture in insects varies notably within and between taxonomic groups in terms of size, in- tron distribution, repeat content, and patterns of ancient gene linkage structures. The relationship between these patterns of genome evolution and phenotypic and behavioral diversity of insects is, however, not well understood. Secondarily increased or reduced genomes blurs the link between organismal complexity, and non-adaptive scenarios can explain the emergence of genomic complexity through population-genetic envi- ronments. Establishing a timeline of genome changes across a gradient of evolutionary distances, linked with a functional analysis of identified novelties, is thus essential to understand how genome innovation is linked to phenotypic sophistication.
In our SPP tandem project, we propose to systematically use syntenic conservation as a means of tracking orthology, local duplications, turn-over of repetitive elements, gains and losses of protein domains and coding capacity, and the emergence and decline of non-protein-coding genes. This synteny-based approach will go beyond the construction of reliable, unambiguous genomic alignments and thus overcome existing limits in classical methods of sequence-based gene phylogenies. This will, in particular, allow to unveil the evolutionary history of DNA elements that do not have 1-1 relationships across species, and to disentangle the evolutionary history also at phylogenetic distances that are too large to allow reliable sequence alignments.
To establish a scalable approach that can address innovation across a gradient of evolutionary distances, we will take advantage of the broad taxon sampling in the insect order Diptera (true flies) and its particularly deep sampling of the family Drosophilidae. Fly evolution has been previously characterized by distinct episodes of rapid increase in taxonomic diversity, and coarse comparisons of fly genomes have suggested fly specific innovations in patterning and signaling pathways. We will present the general outline of our project and comment on first results of our approach to catalogue signatures of innovation across 250+ fly genomes.
Project Team
Publications
Käther, K., Lemke, S., Stadler, P.F.
Annotation-Free Identification of Potential Synteny Anchors.
In: Bioinformatics and Biomedical Engineering., 2023.
Remmel, Andreas; Lemke, Steffen and Stadler, Peter.F.
Transiently expressed genes with recent evolutionary origin continue to become enriched at life stage transitions of flies.
In: J Exp Zool B, 2025
The genomic basis of extreme sexual dimorphism in fireflies
Fireflies are well known for their charismatic lighted mating signals. Less known, fireflies exhibit a fascinat- ing variation in sexual dimorphism: some species show very mild sexual dimorphism whereas other species exhibit extreme sexual dimorphism. In species where extreme sexual dimorphism is present, females remain in a neotenic state with wing pads instead of fully developed wings. In some species the light organ is also sexually dimorphic, were males do not have a light organ but neotenic females do. Most importantly, this sexual dimorphism has evolved repeatedly across the firefly phylogeny.
Such strong variation in traits must be caused by underlying gene expression variation. Specifically, sexual dimorphism must be related to sex-biased gene expression. However, it is unknown how sex-biased gene expression evolves and if the same sex-biased genes are shared across the phylogeny. Furthermore, gene expression is most likely regulated by open chromatin accessibility. Nevertheless, the correlation between sex-biased open chromatin accessibility and sex-biased gene expression has not be shown previously.
In this project, we will study the evolutionary forces acting on gene expression using a phylogenetic frame- work. Only within a phylogenetic framework can we distinguish between all scenarios of gene expression evolution, for example, distinguishing directional selection from relaxed stabilizing selection. To address our questions, we will develop new methods and theory for the statistical analysis (Brownian motion and Ornstein-Uhlenbeck processes), specifically focusing on utilizing within-species variance in gene expression and sex-biased gene expression. Our novel methods will allow us to study the evolutionary forces acting on sex-biased gene expression, and if sex-biased gene expression is linked to extreme sexual dimorphism.
We will also generate the first homogeneous gene expression dataset (RNA-seq) for >10 species from at least 5 divergent genera, with multiple individuals per species and separated by body parts. Our study system, fireflies, is ideal for studying sex-biased gene expression evolution due to the repeated evolution of neoteny, but can be used as a reference and comparison to other non-sex-biased datasets too. Additionally, we will use ATAC-seq to generate chromatin accessibility data. With the ATAC-seq data, our project will produce novel insights into the correlation between gene expression evolution and chromatin accessibility evolution on a phylogenetic scale.
Taken together, our project will (a) generate a new comprehensive transcriptomic gene expression and chro- matin accessibility dataset, (b) novel methods to study gene expression and chromatin accessibility evolution for multiple species and individuals across a phylogeny, (c) advance our understanding of genome evolution with regards to the molecular mechanism underlying sexual dimorphism. This knowledge will advance our understanding which genomic elements are driving innovations in insects, such as sexual dimorphism.
Project Team
Publications
A Catalan; D Gygax; L Rodriguez-Montes; T Hinzke; K Hoff and P Duchen
Two novel genomes of fireflies with different degrees of sexual dimorphism reveal insights into sex-biased gene expression and dosage compensation.
In: Communications Biology, 2025