Sea spider body patterning during ontogeny and regeneration

Chelicerata is a diverse arthropod lineage, best known for its terrestrial representatives (spiders, scorpions, and kin). The impressive evolutionary success of chelicerates was accompanied by a considerable morphological diversification of their segmented bodies. While evolutionary- developmental research (evo-devo) has made significant progress in unravelling the molecular- developmental basis of body plan evolution across the animal kingdom, studies in chelicerates are limited to few representatives (mainly spiders and harvestmen) and critically lack data on early branching representatives, such as the bizarre sea spiders. In contrast to most of their chelicerate kin, sea spiders never transitioned from water to land and their life cycle includes a minute hatching larva, which may resemble an ancestral feature of arthropod development. Hence, pycnogonid evo-devo holds great potential to reveal ancestral principles of chelicerate development. Beyond this, the only recently discovered ability of sea spiders to regenerate part of their main body axis after traumatic injury may likewise represent an ancestral arthropod trait, but awaits detailed study at the molecular and cell type levels. This project will characterize major events in the development of the sea spider body plan, including the establishment of the main body axes in embryos, the formation of body segments from the hatching larva to the adult, the subsequent differentiation of body segments/regions into different functional units, and the development of sea spider-specific morphological traits (such as their highly specialized ovigeral legs). This will be complemented by regeneration experiments, to permit comparison of the processes underlying normal development with those acting during regeneration. To achieve these aims, developmental gene expression studies will be performed on the sea spider Pycnogonum litorale, with a focus on conserved gene regulatory networks and signaling pathways underlying arthropod axis patterning and segmentation, as well as Hox genes, as major players in segment identity specification. This will provide crucial data points for comparison with land-living chelicerates and other arthropod groups, to test the plausibility of current scenarios on the evolution of chelicerate body patterning. In addition to gene expression studies, cell division assays and single-cell RNA-sequencing will be employed in regeneration studies. This synergistic combination of established techniques with single-cell RNA-sequencing will help to decipher sea spider regeneration at the cell level and yield first insights into the cell division dynamics of the regeneration-related cell types. These novel data will enable comparison with other animal groups that boast similarly good or even better regenerative abilities and thereby contribute to a vibrant research field seeking to extract common principles of regeneration across the entire animal kingdom.