The ultrastructure of the apical organ of the Müller's larva of the tiger flatworm Prostheceraeus crozieri

Abstract

The tiger flatworm Prostheceraeus crozieri (Polycladida) develops via an eight‐lobed, and three‐eyed planktonic Müller's larva. This larva has an apical organ, ultrastructural details of which remain elusive due to a scarcity of studies. The evolution and possible homology of the polyclad larva with other spiralian larvae is still controversial. Here, we provide ultrastructural data and three‐dimensional reconstructions of the apical organ of P. crozieri. The apical organ consists of an apical tuft complex and a dorso‐apical tuft complex. The apical tuft complex features a central tuft of five long cilia, which emerge from four or five individual cells that are themselves encircled by two anchor cells. The necks of six multibranched gland cells are sandwiched between ciliated tuft cell bodies and anchor cells. The proximal parts of the ciliated cell bodies are in contact with the lateral brain neuropil via gap junctions. Located dorsally of the apical tuft complex, the dorso‐apical tuft complex is characterized by several long cilia of sensory neurons, these emerge from an epidermal lumen and are closely associated with several gland cells that form a crescent apically around the dorsal anchor cell, and laterally touch the brain neuropil. Such ciliated sensory neurons emerging from a ciliated lumen are reminiscent of ampullary cells of mollusc and annelid larvae; a similar cell type can be found in the hoplonemertean decidula larva. We hypothesize that the ampullary‐like cells and the tuft‐forming sensory cells in the apical organs of these spiralian larvae could be homologous.

Emerging trends in the study of spiralian larvae

“…As in many other animals during the development of the anterior nervous system, the staggered expression of transcription factors like six3/6, foxQ2 and otx, and their presumed interaction with signaling pathway gradients like Wnt specify the apical organs of spiralian larvae during embryogenesis Marlow et al, 2014;Santagata et al, 2012;Vopalensky et al, 2019) (Figure 3a). The combination of embryonic data with the use of full-body serial-section transmission electron microscopy to reconstruct the neural connectome (Randel et al, 2014) and behavioral assays are fundamental to dissecting the levels of conservation of apical organs among spiralian larvae (Dittmann et al, 2023;Williams et al, 2017). Given that many of the patterns of expression and the gene regulatory networks involved in the development of anterior neural structures, including the larval apical organs, are similar across multiple bilaterian animals (Feuda & Peter, 2022;Gattoni et al, 2023), it might be that these structures are homologous across spiralians and even bilaterians.…”