Climate, host-plant use and macroevolution of weevils

The role of Earths climate, host-plant associations and adaptations to chemical defense compounds in the species diversification of the weevil subfamily Ceutorhynchinae (Curculionidae, Coleoptera) a combined phylogenomic and experimental approach: About a quarter of the multicellular species on Earth are herbivorous insects, but it is still unclear how this enormous biodiversity has originated. Phylogenetic analyses have shown that the interactions of herbivorous insects with their host plants had an influence on speciation. Furthermore, it has been proposed that climate changes have determined the radiation and distribution of insect groups. In order to gain a deeper understanding of the specific impact of climate and host plant use on the radiation of herbivorous insects, it is necessary to reconstruct phylogenetic relationships and divergence times in order to estimate the impact of specific biotic factors (conservation of the host plant, host plant changes and larval host plant use) and abiotic factors (historical climate changes). This research project investigates the evolution of a subfamily of weevils (Ceutorhynchinae, Curculionidae, Coleoptera). Host plants of the Ceutorhynchinae include garlic, aconite, poppy, and ephedra. Weevils of the genus Ceutorhynchus, which alone account for about a quarter of all species of this subfamily, use exclusively crucifers such as rape and cabbage as host plants, although these plants have a highly effective chemical defense system against predators. If injured, mustard oil glycosides are degraded enzymatically to reactive mustard oils, which are toxic to herbivorous insects. Some insects have adapted to this so-called mustard oil bomb and can, for example, prevent mustard oil glycosides from being converted into toxic degradation products. The aim of the project is infer the impact both historical climate changes and specific host-plant uses on the radiation of Ceutorhynchinae. In order to gain a deeper understanding of whether and how overcoming phytochemical barriers has actually contributed to radiation, the project will investigate the detoxification mechanism of Ceutorhynchus pallidactylus to find out how these beetles disarm the mustard oil bomb. To reconstruct the phylogenetic relationships of Ceutorhynchinae and to further investigate the evolution of their detoxification mechanisms, a novel approach combining modern transcriptome data sets and classical molecular data sets is applied. The application of such a data set to evolutionary biology questions is a novelty. This work will allow drawing a detailed picture of the evolutionary history of weevil-host interactions, thus providing a stepping-stone to further elucidate insect diversity and phylogeny.

Insect-plant interactions are among the key drivers of biological diversity. From pollination and seed dispersal to herbivory and chemical defense, these interactions shape the dynamic co-evolution of both organism groups and facilitate the emergence of new ecological niches. In addition to these biotic interactions, abiotic factors - such as climatic changes or fluctuations in atmospheric oxygen levels - also play a fundamental role in species formation. In our recent FWF-project, we investigated how both biotic and abiotic factors have influenced the evolutionary history of the weevil subfamily Ceutorhynchinae (Curculionidae, Coleoptera). A central aim of the project was to analyze the functional adaptation of the cabbage stem weevil (Ceutorhynchus pallidactylus) to its crucifer host plants (Brassicaceae). This plant family employs a potent chemical defense system based on glucosinolates, whose breakdown products - are toxic to many insects. Through controlled feeding experiments, we were able to demonstrate how C. pallidactylus can partially overcome these defense compounds using glutathione S-transferases (GSTs). To further explore the molecular basis of this adaptation, we sequenced a reference genome for C. pallidactylus and annotated candidate GST genes across several weevil genomes. Comparative analyses revealed lineage-specific expansions in the GST gene family, which correlate with host plant use on Brassicaceae. Another major focus of the project was to explore the diversification patterns within the Ceutorhynchinae, based on a comprehensive phylogenomic dataset covering approximately 25% of the 1,300 described species from all major biogeographic regions. Using phylogenetic tree reconstruction and macroevolutionary modeling, we assessed the effects of historical biogeography, host plant associations, and climatic changes. Our findings suggest that the Ceutorhynchinae originated in Africa during the Late Cretaceous and subsequently spread to Europe, North America, and Southeast Asia. A marked increase in diversification rates occurred during the Middle Eocene, coinciding with the expansion of several key host plant families across the Palearctic region. Moreover, we identified host shifts to new plant families - for example, the genus Ceutorhynchus on Brassicaceae and Mogulones on Boraginaceae - as being associated with accelerated speciation rates in multiple lineages. In contrast, we found no direct evidence that Paleogene temperature shifts had a significant impact on diversification rates. We also examined how flea beetles adapted to feeding on crucifers, and the effect this had on their evolution. By analysing the relationships of over 600 flea beetle species, we were able to trace the evolution of these insects over time. Interestingly, only one group of crucifer-feeding beetles showed signs of increased diversification. This suggests that feeding on crucifers alone does not generally lead to higher speciation rates and the differences in species diversity within this group cannot be explained by the choice of host plant alone.