Variability of hair cells in the coronal organ of ascidians (Chordata, Tunicata)

Abstract

The tunicate ascidians are nonvertebrate chordates that possess mechanoreceptor cells in the coronal organ in the oral siphon, which monitor the incoming water flow. Like vertebrate hair cells, the mechanoreceptor–coronal cells are secondary sensory (axonless) cells accompanied by supporting cells and they exhibit morphological diversities of apical specialisations: they are multiciliate in ascidians of the order Enterogona, whereas they are more complex and possess one or two cilia accompanied by stereovilli, also graded in length, in ascidians of the order Pleurogona. In morphology, embryonic origin, and arrangement, coronal sensory cells closely resemble vertebrate hair cells. We describe here the coronal organs of five ascidians ( Pyura haustor (Stimpson, 1864), Pyura stolonifera (Heller, 1878), Styela gibbsii (Stimpson, 1864), Styela montereyensis (Dall, 1872), and Polyandrocarpa zorritensis (Van Name, 1931)), belonging to Pleurogona, also comprising species of one family (Pyuridae), not yet considered, and thus completing our overview of the order. Each species possesses at least two kinds of secondary sensory cells, some of them characterized by stereovilli graded in length. In some species, the coronal sensory cells exhibit secretory activity; in P. haustor, a mitotic sensory cell has also been found. We compare the coronal organ in both ascidians and with other chordate sensory organs formed of secondary sensory cells, and discuss their possible homologies.

Evolutionary diversification of secondary mechanoreceptor cells in tunicata

“…Stereovilli are linked to each other and with the cilium (where present) by fibrillar links; this forms the structural device for transduction of the stimulatory force acting on the cilium to the site of mechanosensitive ion channels. In stolidobranch ascidians, extracellular radial filaments connecting the cilium or cilia to the surrounding stereovilli have been described [3,40] though the mechanism of signal transduction is not yet known. It is noteworthy that a loose fibrillar matrix is generally present also among microvilli and cilia.…”

“…Microvilli are drawn as shorter sticks compared to stereovilli, and cilia are represented by the longest sticks. Light green: supporting and secretory cells; light yellow: secondary sensory cells (modified from [3,5,7]).…”

“…In ascidians and thaliaceans, the tunic layer envelopes the entire external animal surface including part or the inner wall of oral aperture, but the tunic ends just anterior of the position of the coronal organ so that coronal sensory cells are directly exposed to the water current [5,40,48]. This is different from what generally occurs in tunicate mechanoreceptor organs based on primary sensory cells, in which sensory elements are covered by either the outer tunic or by acellular cupulae [3,48]. …”

“…In ascidians, these cells have been hypothesised as possible homologues of vertebrate secondary sensory cells, namely the hair cells of the ear and the lateral line. In all ascidians analysed so far, sensory cells are located in the oral aperture and are arranged to form a structure called the coronal organ, which is composed of a row of cells bordering the oral tentacle surface [3]. Its role is to monitor inflowing water during the feeding process [4].…”

“…Its role is to monitor inflowing water during the feeding process [4]. Coronal sensory cells show considerable variability in different species [3,5,6], especially regarding the apical cell surface, which can exhibit one or more cilia that may be surrounded by microvilli or stereovilli of similar or different lengths. In thaliaceans, the coronal organ was described in Doliolum nationalis and Pyrosoma atlanticum , which represent the orders Doliolida and Pyrosomatida [7].…”