© 2000, Annual Reports of the Zoological Institute RAS.


Neural complex of tunicates in relation to vertebrate hypophysis

Vladislav N. Romanov

Zoological Institute, Russian Academy of Sciences, Universitetskaya nab., 1, St. Petersburg, 199034, Russia
 

The neural gland, a part of the neural complex of tunicates, has been studied for more than 130 years. Till present, however, both the nature of this organ and its function remain unknown. Hancock (1868), who had described this organ for the first time, assumed that it was a sense organ. Later, it was called a mucous producing, digestive, excretory, chemoreceptor, or endocrine organ. The question of the origin of the organ also remains open. At present, a hypothesis on the homology between the neural gland and vertebrate hypophysis is the most popular (Julin, 1871).

In order to establish a reliable homology between the neural complex of tunicates and the hypophysis of vertebrates, it is necessary to take into account their topographic relations with the brain, their function, and embryogenetic origin. The first two aspects mentioned testify to the homology of these formations. In ascidians, both gland and ganglion are always situated close to each other. Similar relations are retained in forms with a non-compact complex with the long dorsal tube possessing a ciliary epithelium removed far forward. In a series of works performed on Styela plicata (Lesueuer) using the method of indirect immunofluorescence (Pestarino, 1985), a number of substances similar to adenohypophysial hormones of vertebrates were revealed in the neural gland and ganglion of this ascidian; based on these data, Pestarino accepted the homology between the gland and adenohypophysis.

Many investigators assume in the hypophysial nature of the neural complex. Contradictions between supporters of this hypothesis concern mainly the issue of homology between anterior or posterior lobe of the hypophysis and the gland. To a great extent, these contradictions were provoked by erroneous data on finding two neurohypophysial hormones, oxytocin and vasopressin, in ascidians. Probably, this may be an explanation, why some authors accepted the hypothesis for homology between the gland and the hypophysis (Huus, 1937; Goodbody, 1974; and others). At the same time, neither the ciliated organ nor the dorsal tube were taken into account by the opposite sides.

Let us analyze the third aspect, comparative embryology. Ivanova-Kazas (1995) approaches the issue of possible homology of the above mentioned formations with caution, which can be explained by both different interpretation of developmental processes in this organ, and great variability in the mechanisms of their realization in different representatives of the tunicates. As is known, the vertebrate hypophysis (Fig. 1, B) includes 2 parts: adenohypophysis, developing from an invagination of stomodeum, and neurohypophysis, formed as a result of growing out of bottom of the third ventricle. In reality, the neural complex of tunicates possesses a similar double nature. A generalized scheme of development of the neural complex, composed according to data of different authors obtained on various ascidian species, is shown in Fig. 1, A. After closing of the neural tube, its anterior end splits into two parts. The right half of the tube forms a sensitive vesicle of larva; the left - part of the so called hypophysial, or neurohypophysial rudiment, the channel of which continues into the opening of the neural tube. Larval, or cerebral ganglion is formed of the median part of this tube. After separation of the hypophysial rudiment from the nerve tube, a definitive ganglion is formed by local proliferation of its posterior dorsal part. The rest of the rudiment is the neural gland. The apical end of the gland grows toward protrusion of the gullet, later fusing with it and forming a ciliated organ on its anterior end. Thus, the neuronal origin of the gland is doubtless.

Whereas homology of the neurohypophysis and the neural gland seems reliable, the origin of anterior lobes remains obscure. Which part of the gullet (ecto- or entodermal) involves part in formation of the neural complex, is the crucial question. Early authors assumed that gland duct opens into the gullet before its fusing with the stomodeum, situated on the dorsal side of larva (Willey, 1894, and others). In this case, it would be necessary to accept the entodermal nature of the anterior part of the neural complex. However, as early as 1876 Kovalevsky, upon studying the development of Ascidia (=Ciona) intestinalis (Linnaeus), described development of the anterior lobe of the complex in a different way (Kovalevsky, 1951). The anterior, thinner end of the 'brain vesicle', or hypophysial rudiment, approaches the stomodeal invagination; a diverticulum of the stomodeum, in its turn, growing toward this rudiment. After fusing of these invaginations, a connection between the gland and environment is established. "However, directly after that …at nearly the same place…" (Kovalevsky, 1951: 97) anterior part of the gut, a rudiment of the entodermal gullet, also opens into the stomodeal invagination. During the subsequent organogenesis, an aperture of the neural complex is shifting into the gullet cavity, closer to base of the cloacal syphon.

 

 

Fig. 1. Neural complex of tunicates and vertebrate hypophysis. A - development of the neural complex in ascidians (generalized scheme, composed using data of different authors obtained on different species); B - development of mammal hypophysis (after Romer & Parsons, 1992); C - hypophysis of Cyclostomata (after Tsuneki, 1988). ah - adenohypophysis; cg - cerebral ganglion; dg - definitive ganglion; co - ciliated organ; ng - neural gland; nh - neurohypophysis; nc - nasohypophysial canal; nr - neurohypophysial rudiment; ns - nasohypophysial stalk; nt - neural tube; sv - sensitive vesicle; st - stomodeum; t - third ventricle.

 

The same mechanism of development was revealed later in the number of other ascidians (Damas, 1902; Grave, 1944; and others). Furthermore, according to Ivanov (1945), during formation of the neural complex, ciliate cells are found in a hollow of the stomodeal diverticulum even before it is connected with the hypophysial rudiment. Therefore, I think that the anterior lobe of the hypophysis corresponds to the ciliated organ and the dorsal tube combined. The fact, that the dorsal tube is a derivative of the ciliated organ, is confirmed by presence of a ciliary epithelium in long dorsal tubes of non-compact neural complexes (Ruppert, 1992).

So, according to comparative embryological data, it is possible to homologize the neural complex in general with the hypophysis of vertebrates. This conclusion, on the face of it, seems to contradict the presence of a number of hormone-like substances, typical of the vertebrate adenohypophysis, in the neural gland of ascidians. Based on these data, Pestarino (1985) homologizes adenohypophysis with the latter. However, in my opinion, contradiction is not in the fact of presence of these substances in ascidians, but in the fact, that Pestarino pays much attention to the function of the gland and underestimates comparative embryological aspect of this problem.

The main difference between the neural complex and the vertebrate hypophysis (Fig. 1, A, B) is the following: the gland is separated from the ganglion in tunicates, whereas vertebrate hypophysis is a thickened part (in lampreys) or prominence of the bottom of cerebrum intermedia (rest of vertebrates) (Fig. 1, C). In addition, any connection between adenohypophysis and stomodeum is lost in all tetrapods and higher fishes, although in Cyclostomata and some lower fishes (Latimeria, Crossopterygus, some Palaeozoic forms) this connection is retained (Romer & Parsons, 1992). And, finally, hormones typical of adenohypophysis, are revealed not in the ciliated organ, but in the neural gland of ascidians.

What are evolutionary relations between the hypophysis and the neural complex, and what role does the latter play in the life of tunicates? In my opinion, the assumption of Ivanova-Kazas (1995) that ascidians had originated from some protochordates indirectly, via 'protovertebrates', can be very useful in solving of the first problem. It was in this hypothetical group, that a kind of 'prohypophysis' could have been formed, with the following independent evolution in vertebrates and tunicates. This scheme logically includes the Carlisle's (1953) idea on the origin of olfactory organs of vertebrates by dividing the prohypophysis of protovertebrates, but not the 'hypophysis' of ascidians, as it was assumed by the above author; it is hard to imagine a 'returning' of the neural gland, separated long ago from the cerebral vesicle, to the former locality. As is shown by data on embryology of Cyclostomata, the origin of the anterior lobe of hypophysis in lampreys (Larsen & Rothwell, 1972) and myxines (Fernholm, 1965) is associated with the olfactory organ. Separation of the olfactory organ was explained by Carlisle by transition of fishes from benthic to more active nekton mode of life, with a necessity to possess more rapidly acting olfactory organ. This fast transmission of information in the central nervous system occurs already not by chemical, but by nervous way.

The evolution and pathways of the prohypophysis in ascidians seem to be quite different. Separation of the neural gland from the ganglion led the rest of complex to a kind of autonomy from the nervous system. On the other hand, the presence of hormone-like substances in both gland and ganglion testifies to retaining of some endocrine mechanisms in ascidians, as it has been shown by Carlisle (1951) in his physiological experiments on gamete producing. An injection of gametes of the same species into the ciliated organ provokes a release of sex products of the recipient, with the obligatory participation of both ganglion and neural gland, and formation of gonadotropic hormones in the latter. The fact, that the gland and ganglion are always located close to each other can serve as an indirect confirmation of such relations. More than that, they are always surrounded by blood lacunes of a friable connective tissue, which may be an evidence of the humoral character of connections between the gland and the ganglion.

Apparently, the role of the neural complex is not limited by chemoreceptory and endocrine functions. Ruppert (1992), who has conducted physiological and fine structural investigations of the neural complex in Ascidia interrupta (Heller), interprets it as an organ of blood volume regulation, consisting of a pump, and coarse and fine filters. The cellular apparatus, manufacturing a directed stream of water from the gullet towards the gland, plays the role of a pump. Cilia of the dorsal tube and ciliary epithelium, hampering penetration of large alien particles into the gland, serve as a coarse filter. And, finally, the neural gland serves as a fine filter: gland cells capture small particles and large molecules by endocytosis. Filtered water passes through the gland wall, entering the dorsal vessel and providing a constant volume of blood in an open circulatory system.

 

The studies were carried out with financial support of the Russian Foundation for Basic Research (grant 99-04-49783); FAP "World Ocean: Investigation of Antarctic": (project 9.16).

 

References

Carlisle, D.B. 1951. On the gormonal and neural control of the release of gamets in ascidians. J. exp. Biol. 28 (4): 463-472.

Carlisle, D.B. 1953. Origin of pituitary body of chordates. Nature 172: 1098-1099.

Damas, D. 1902. Recherches sur le developpement des Molgules. Archs Biol., Paris 8 (4): 99-664.

Fernholm, B.O. 1969. A third embryo of myxines considerations on hypophysial ontogeny and phylogeny. Acta zool., Stockh. 50 (1/2): 169-171.

Goodbody, J. 1974. The phisiology of ascidians. In: Advances in marine biology. Vol. 12. (F.S. Rassel and M. Yonge. Eds.). pp. 1-142. London, Academic Press.

Grave, C. 1944. The larva of Styela (Cynthia) partita. J. Morph. 75 (2): 173-188.

Hancock, A. 1868. On the anatomy and physiology of the Tunicata. J. Linn. Soc. Lond. (Zoology) 9: 309-346.

Huus, J. 1937. Ascidiacea - Tethyoideae. In: Kukenthal-Krumbach's Handbuch der Zoologie. Bd. 5 (2). S. 545-692. Berlin/Leipzig.

Ivanov, P.P. 1945. Rukovodstvo po obshchei i sravnitel'noi embriologii [Handbook on general and comparative embriology]. Leningrad, Uchpedgiz. 253 pp. (In Russian).

Ivanova-Kazas, O.M. 1995. Essays on the phylogeny of lower chordates. Trudy S.-Peterb. Obshch. Estest. 84 (4): 1-160. (In Russian).

Julin, C. 1881. Recherches sur l'organisation des Ascidies simples. Sur l'hypophise et quelques organes. Archs Biol., Paris 2: 59-126.

Kovalevsky, A.O. 1951. Further investigations on development of simple ascidians. In: Izbrannye raboty [Selected works]. (A.D. Nekrasov and N.M. Frolov. Eds.). pp. 79-123. Moskva/Leningrad, AN SSSR Publ. (In Russian).

Larsen, L.O. & B. Rothwell. 1972. Adenohypophysis. In: The biology of lampreys. Vol.2. (M.V. Hardisty and J.C. Potter. Eds.). pp. 1-67. London/New York, Academic Press.

Pestarino, M. 1985. A pituitary-like role of the neural gland of an Ascidian. Gen. comp. Endocrinol. 60: 293-297.

Romer, A.Sh. & T. Parsons. 1992. Anatomiya pozvonochnykh [Anatomy of vertebrates]. Vol. 2. Moskva, Mir. 406 pp. (Russian translation.)

Ruppert, E.E. 1990. Structure, ultrastructure and function of the neural gland complex of Ascidia interrupta ( Chordata, Ascidiacea ): clarification of hypotheses regarding the evolution of the vertebrate anterior pituitary. Acta zool., Stockh. 71 (3): 271-297.

Tsuneki, K. 1988. The neurohypophysis of cyclostomus as a primitive hypothalamic center of vertebrates. Zool. Sci. 5 (1): 21-32.

Willey, A. 1894. Studien on the Protochordata. II: The development of neurohypophysial system in Ciona intestinalis and Clavelina lepardiformis. Q. Jl microsc. Sci. 35: 295-316.