How to stay attached: Evolution and development of the plug, a transient novel tissue in ricefishes (Beloniformes: Adrianichthyidae)

• Applicant: Dr. Julia Schwarzer
• Subject Area: Evolution, Anthropology ; Evolutionary Cell and Developmental Biology (Zoology) ; Systematics and Morphology (Zoology)
• Term: since 2023
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 529550112

The origin of novelty is a substantial question in evolutionary biology. According to the Stress Induced Evolutionary Innovation (SIEI) model, novel structural components can arise from ancestral stress responses, such as modified inflammation. The extremely thick epidermis of cetaceans (whales and dolphins) and the decidual stromal cells of placental mammals are rare examples of such innovations. Another example might be the "plug" in Sulawesi ricefishes (Beloniformes: Adrianichthyidae). Female ricefishes carry fertilized eggs attached to their body by long attaching filaments that protrude from the genital pore. While most species deposit their eggs shortly after spawning (transfer brooder), in some species they stay attached until the juveniles hatch (pelvic brooder). The plug is a novel, transient tissue that forms in the female reproductive tract of pelvic brooding ricefish species around the attaching filaments and plays an important role in keeping the eggs attached. Our own data revealed that the transcriptome of the plug of the pelvic brooding species Oryzias eversi is dominated by inflammatory signaling. Further we found, based on histology, that foreign body multinucleated giant cells, a hallmark of foreign body granulomas, are present in the plug. In the proposed project we will (1) compare the different solutions towards prolonged egg carrying in ricefishes based on morphology and (2) study plug formation in O. eversi at single cell level. For the first part, we will combine µ-computed tomography, histology and immune cell staining to compare the macro- and micro-anatomy of the reproductive tract of female ricefishes (three pelvic brooding Oryzias species and two pelvic brooding Adrianichthys species at five different time points as well as two closely related transfer brooding Oryzias species). For the second part, we will combine single-cell transcriptomics and spatial transcriptomics of plug-invading and surrounding cells in O. eversi (at different time points during brooding). The data obtained will be used to map and understand the distribution and origin of cell types in the plug as well as to identify similarities and differences with granuloma formation in fish and granuloma disease in humans (e.g., tuberculosis). The results of the proposed project will provide new insights into the evolutionary pathways that explain pelvic brooding within Sulawesi ricefishes. In addition, it will reveal if the development of the plug in the Oryzias lineage is a result of inflammation-induced formation of a novel tissue and if plug formation resembles foreign body granuloma formation. If so, the ricefish plug would be the first example of a granuloma exhibiting an altered function in a non-disease context.

• DFG Programme: Research Grants