The Pronephric Duct in Elasmobranchs

THE PRONEPHRIC DUCT IN ELASMOBRANCHS GEORGE A. BATES From the Tufts College Medical School SIXTY-ONE FIQURES (FIVE PLATES) HISTORICAL RESUME The development of the pronephric duct in elasmobranchs has been studied by a number of observers, with verydifferent conclusions as to its origin. These differences have arisen, in part, from the difficulty of demonstrating cell boundaries and limiting membranes in embryos preserved by the usual methods and, in part, from the difficulty of interpreting oblique sections. The theory that the vertebrates stand in phylogenetic relations with the annelids and the consequent attempt to homologize the nephridial system of the two is, in a measure, responsible for the discussion and the resulting conflict of opinions. The question in controversy is: Whether the duct takes its origin in whole or in part from the mesoderm, or whether it arises from or is contributed to by the ectoderm. At first there seems to have been no hesitancy in pronouncing the origin to be entirely mesodermic, and all the early papers (Semper, et al) so described it. In 1888 Johannes Riickert (’88) stated that “the duct is developed (in the group) from the ectoderm.” Van Wijhe (’89) claimed to have found evidence for the same conclusion. Several papers followed in rapid succession describing similar conditions in other groups; one author comparing the growth of the duct to that of the lateral line nerve which, he claimed, is developed from the ectoderm in the same way as the pronephric duct. The question raised by such comparison has been answered by Harrison (’03, ’10). Within more recent years the statements have been very conflicting, some stating that it is, at least in part, ectodermal 315 346 GEORGE A. BATES in origin, while others claim that the cells concerned in its development arise wholly from the mesoderm. It has been generally assumed that in the phylogenetic history of vertebrates the pronephric duct once opened directly to the exterior through the ectoderm, which assumption had its origin in the theory of the phylogenetic relationship of annelid and vertebrate. This is presented very clearly by Haddon (’87) and also in his “Introducjion to the study of embryology” (’87, p. 239). In these publications he recapitulates the discussion from the time (’75), when Hensen determined for the rabbit that the pronephric duct is of ectodermal origin, to Perhyi (’87) who claimed the same thing for the frog. He quotes Spee ( ’84)for the guinea-pig and Flemming (’86) as confirming Hensen for the rabbit; also Van Wijhe ( ’86) as saying that the duct arises from the ectoderm in the thornback ray (Raja clavata). He says: “The origin of the segmental duct from the epiblast being now known to occur in Elasmobranchs, Anura, Lacertilia and Rodents we are justified in assuming that this is the general fact. ” Upon this assumption he proceeds to present an hypothesis by which he homologizes the pronephric duct of vertebrates with the nephridia of the chaetopod worms. He says: “There can be little doubt that the segmental duct arises from the epiblast. This discovery will necessarily lead to a modification in our views concerning the morphology of the vertebrate excretory organs. ” He quotes Hatschek as having deseribed a single nephridium in Amphioxus which is in all re- spects comparable with a vermian nephridiuin and then makes the following statement : We have, then, only to assume that a pair of similar vermian nephridia occurred in each body segment of the ancestral vertebrate, and that the nephridia of each side of the body opened externally into a lateral groove [which he has previously described as developed in the epiblast much as the neural tube is developed]. It would further only be neces- sary for the groove to deepen and next to form a canal (just as does the neural groove) to bring about the vertebrate arrangement. Thus, in vertebrates, as in invertebrates, the nephridia open by epiblastic pores, but in the former the area into which they open is precociously converted into a canal which subsequently acquires a secondary opening to the ex- PRONEPHRIC DUCT IN ELASMOBRANCHS 347 terior through the cloaca. On this hypothesis the nephridia of vertebrates always open by their original epiblastic pores, primitively directly to the exterior, secondarily into a canal separated from the epiblast. Hertwig (’92, pp. 358-9) states the case very clearly and brings the discussion down to the date of his own publications. He speaks of the view entertained by almost all investigators that “the duct arises from the mesoderm and grows by proliferation of its own cells as far as the hind gut (proctodaeum) and thus was constricted off from neither the outer nor the middle germ-layers nor yet derived from them cell-material for its increase.” He claims, however, that this interpretation has become untenable, quoting various authors to substantiate the fact that, in several classes of vertebrates, the duct in process of growth is in close union with the outer germ-layer and that it is prolonged backward by means of cell-proliferation in that layer, while in front it is being constricted off from that layer or, as he terms it, the par- ent-tissue. He further states that “the pronephric duct grows at the expense of the outer germ-layer and moves, as it were, along the latter, with its terminal opening behind, as far as the hind gut. ” This interpretation led, later, to the assumption by various authors of the view that not only the pronephric duct but the entire urinary system was derived from the ectoderm (Hertwig ’92, p. 358). Hertwig, later, shows that such views cannot be made to har- monize entirely with conditions found in the lower vertebrates and, making allowance for all observations, he summarizes the subject thus: “The pronephros is developed from the middle germ plate, and that then its posterior end comes into union with the outer germ-layer and in conjunction with the latter grows farther backward as the pronephric duct.” He quotes Van Wijhe and Riickert in support of this explanation and then inter- prets the pronephric duct “ at its first appearance as a short canal- like perforation of the wall of the body, which begins in the body- cavity with one or several ostia and opens out upon the skin by a single orifice. Originally the outer and inner openings lay near together, later they moved so far apart that the outer opening of the canal united with the hind gut.” 348 GEORGE A. BATES It will be seen that these statements present the two phases of the problem, i.e., the origin of the duct from the mesoderm and the contribution of the ectoderm to its development. The phylogenetic theoretical consideration is also suggested. Among the many observers who have discussed the development of the pronephric duct may be mentioned Semper ( ’74, ’75), Balfo-m ( ’78), Spee (’84), Beard (’87), Haddon (’87), Ruckert ( ’88), Van Wijhe ( ’86, ’88, ’89), Mitsukuri ( ’88), Rabl ( ’96), Gregory ( ’98, ’00). Of these Ruckert, Van Wijhe and Rabl have entered actively into the controversy, the two former being advo- cates of the theory of ectodermic origin or contribution to the duct, and the latter directly and radically opposed and an ardent supporter of the theory of its exclusive mesodermic origin. Riickert (’88) seems to have taken the initiative in his very radical position, stating “that the duct is developed wholly from the ectoderm. ” In his figure 36, plate 16, he shows three mitotic figures at the point of union of the ectoderm and anlage of the duct. He states that two layers, ectoderm and anlagal, are fused together at the point of contact, making the thickness of the wall much greater, and this, in conjunction with the presence of the numerous mitotic figures in this region, gives much reason forhis contention. He says: “Die auffallend zahlreichen Mitosen, welche sich stets in diezer Region des Ectoblast finden, geben einen weiteren Beleg fiir diese Adassung. Ein in dieser Hin- sicht ziemlich pragnanter Schnitt (Horizontal-schnitt) durch das hintere Ende des Vornierenganges ist in Fig. 36 dargestellt.” Van Wijhe claims that the ectoderm contributes to the struc- ture of the duct, and compares its growth to that of the nerve of the lateral line organ which, according to his interpretation, is developed in part at least from cells contributed by the ectoderm. He admits the possibility of the duct growing by the division of its own cells, but considers it improbable, his general conclusion being that the ectoderm is in considerable measure responsible for its growth. He says: Was nun seine Abstammung betrifft, so betheiligt sich das Ektoderm sicher an seiner Bildung, indem er in ahnlicher Weise wie die Nerven der Seitenorgane weiterwachst. Ebensowenig wie bei diesen Nerven mochte ich eine ausschliessliche Abstammung von der Haut behaupten, PRONEPHRIC DUCT IN ELASMOBRANCHS 349 da die Moglichkeit nicht ausgeschlossen ist, dm Zellen des Pro- nephros unter fortgesetzten Theilungen den Gang in seiner genzen Lange mitbilden helfen. Doch kommt mir Letzteres nicht wAhracheinlich vor. He quotes Balfour (’87, p. 127). Here Balfour describes the pronephros as . arising as a solid knob from the somstic layer of the mesoblast and growing outward toward the epiblast. The knob consists of from 20 to 30 cells agreeing in character with the neighboring cells of the intermediate cell-mass and are, at this period, rounded. It is mainly, if not entirely, derived from the somatic layer of the mesoblast. From this knob there grows backward a solid rod of cells which keeps in very close contact with the epiblast, and rapidly diminishes in size toward its posterior extremity.

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