Larval development in the apodid sea cucumber Chiridota gigas, with a focus on coelom development and the serotonergic nervous system during metamorphosis

Abstract

A unifying feature of echinoderm larvae is the development of a left anterior coelom, which consists of an undivided left axocoel and hydrocoel. Although the axocoel is a key deuterostome trait, the presence of this coelom in holothurians has been the subject of debate. Here, we focus on the development of the coelom in a basal holothuroid, the apodid Chiridota gigas (F. Chiridotidae). The dorsal pore and dorsal duct develop first, just after gastrulation, followed by expansion into an axohydrocoel in the auricularia. The left somatocoel was first evident adjacent to the stomach ~30 days post-fertilization. The axohydrocoel differentiated into two distinct parts: the hydrocoel adjacent to the stomach, and a thin-walled axocoel that was mid-dorsal between the hydrocoel and the dorsal pore. This left axocoel extended to both the anterior and posterior but did not cross the larval midline. Out-folding of the hydrocoel to form the primary tentacles was first observed at 58 days. Transition to a doliolaria with four-rings was rapid (24 hr) and similar to the transition in other holothurians, with the hydrocoel encircling the esophagus. This transition involved a posterior shift of elements of the auricularia ciliary band and associated nervous system. The ciliary band of the auricularia was rearranged to form transverse bands of the doliolaria larva, and at the same time, the serotonergic cells and fibers that had been at the anterior end moved with the portions of the ciliary band with which they were associated. These serotonergic cells and fibers were still present in the pentactula. The first pentactula was observed at 66 days. Coelom development in C. gigas showed two differences from that in other holothurians, including the development of the left axocoel and the extension of the anterior coelom into the preoral lobe. Description of the full larval development in C. gigas also revealed highly variable morphology in the late auricularia stage, which may aid in identifying apodid holothurians from plankton samples.