Single cell RNA sequencing provides clues for the developmental genetic basis of Syngnathidae’s evolutionary adaptations

Seahorses, pipefishes, and seadragons are fishes from the family
Syngnathidae that have evolved extraordinary traits including male
pregnancy, elongated snouts, loss of teeth, and dermal bony armor. The
developmental genetic and cellular changes that led to the evolution of
these traits are largely unknown. Recent syngnathid genomes revealed
suggestive gene content differences and provide the opportunity for
detailed genetic analyses. We created a single cell RNA sequencing atlas
of Gulf pipefish embryos to understand the developmental basis of four
traits: derived head shape, toothlessness, dermal armor, and male
pregnancy. We completed marker gene analyses, built genetic networks, and
examined spatial expression of select genes. We identified
osteochondrogenic mesenchymal cells in the elongating face that express
regulatory genes bmp4, sfrp1a, and prdm16. We found no evidence for tooth
primordia cells, and we observed re-deployment of osteoblast genetic
networks in developing dermal armor. Finally, we found that epidermal
cells expressed nutrient processing and environmental sensing genes,
potentially relevant for the brooding environment. The examined pipefish
evolutionary innovations are composed of recognizable cell types,
suggesting derived features originate from changes within existing gene
networks. Future work addressing syngnathid gene networks across multiple
stages and species is essential for understanding how their novelties
evolved.