Dual origins for neural cells during development of the Clytia planula larva

Adult hydrozoan cnidarians undergo extensive tissue turnover, generating neural cell types including nematocytes (stinging cells) from interstitial stem cells (i-cells) expressing stemness proteins such as Piwi and Nanos. The contribution of i-cells during embryogenesis, however, has been unclear. Here we address the origin of neural cells during development of the Clytia hemisphaerica ‘planula’ larva. Marker gene in situ hybridisation revealed that Piwi/Nanos1-expressing cells within the presumptive endoderm of the early gastrula generate a substantial pool of nematoblasts, some of which migrate and differentiate into the planula ectoderm. Neurogenic transcription factor expression showed a markedly distinct pattern, predominantly in a basal layer of the aboral/lateral ectoderm during gastrula stages. Embryo bisection and lineage tracing experiments confirmed that neurosensory and secretory cell types derive from gastrula ectoderm, while nematocytes and at least some ganglionic cells derive from i-cells. Knockdown and inhibitor treatments revealed steps of both neurogenesis and nematogenesis regulated by Wnt-β-catenin. We conclude that two distinct neurogenesis pathways operate in parallel during Clytia embryogenesis, one involving aboral ectoderm delamination, and one generating mainly nematocytes from i-cell-like precursors.