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95 the Evolutionary Significance Of 95 THE EVOLUTIONARY SIGNIFICANCE OF THE EMBRYO- LOGY OF THE AMPHIBIAN NEPHRIC SYSTEM BY R. J. O'CONNOR Department of Anatomy, University College, London THE ONTOGENY OF THE AMPHIBIAN NEPHRIC SYSTEM IN RELATION TO PHYLOGENY MANY theories have been advanced to explain the arrangement of the verte- brate nephric system, and the most generally accepted is set forth by Goodrich (1930). He states that Craniata were provided originally with a paired series of segmental excretory tubules which coalesced to give rise to a longitudinal duct opening into the cloaca. This primitive archinephros then became specialized into pronephric and mesonephric regions. The pronephros showed a tendency to earlier differentiation; and the portion of the primitive archi- nephric duct formed in association with it tended to grow back independently to the cloaca so that species arose where it was completed before the formation of the mesonephric tubules, and the latter communicated with the already formed duct without contributing to its formation. Thus, for ontogeny to be in accordance with this phylogenetic view, it would be necessary for the pronephros to develop before the mesonephros and for the pronephric duct to grow caudally from the pronephric rudiment to the cloaca and be joined by the mesonephric tubules when they later developed. Such a plan of development has been described both in birds and in mammals, and in the chick this description has been confirmed by the experimental findings of Boyden (1924), Waddington (1937) and Grunwald (1937). However, in Amphibia the position has not been so clear. Early observations on the embryology of the nephric system in Triton alpestris by Mollier (1890) led him to the conclusion that the evidence at his disposal favoured the formation of the pronephric duct in situ and not as a caudal outgrowth of the pronephric rudiment. Field (1891), working on Amblystoma punctatum, was more definite in his opinion and concluded that the pronephric duct was derived from a proliferation of the somatopleure in each segment, his evidence being the similarity of the yolk granules in the two structures. Brauer (1902), however, investigated the rare Gymnophiona and here came to the conclusion that the pronephric duct was formed by an independent caudal growth of the pronephric rudiment. The position was thus established that with the exception of the Gymnophiona the pronephric duct in Amphibia was derived from a pro- liferation of the somatopleure in situ, a view expressed by the synonym "segmental duct". This position has been accepted by later writers and is repeated by Felix (1906) and Goodrich (1930). Burlend (1931) also accepts 96 R. J. O'Connor this opinion on the mode of formation of the pronephric duct in Amphibia, and uses it as an argument against the current views on the phylogeny of the vertebrate nephric system. Subsequent experimental work, however, is pertinent to the manner of formation of the pronephric duct. In Amphibia, several workers (Burns, 1934, 1936; Waddington, 1937; O'Connor, 1938) found that the formation of the pronephric duct could be prevented either by removing the pronephric rudiment or by placing a transplant at its caudal extremity and thus preventing any extension in a caudal direction. These results strongly suggest a formation of the pronephric duct from the pronephric rudiment but are not absolutely conclusive. There still remains the possibility that the pronephric duct is formed in situ in response to some stimulating force passed from the pronephric rudiment in a caudal direction. That is to say, the formation of the pronephric duct from the somatopleure in one segment may stimulate its formation in the segment immediately caudal and this stimulus may be removed by the above procedures. The formation of the entire pronephric duct from the pronephric rudiment is, however, established by vital staining experiments (O'Connor, 1938) where the pronephric rudiment was stained with Nile blue sulphate in'the living embryo. When subsequent development was followed the dye could be traced into the pronephric duct in its whole length from pronephros to cloaca. These experiments were performed on Amblystoma tigrinum and Triton taeniatus, and in these species they establish the formation of the pronephric duct from the pronephric rudiment and not from the somatopleure of each individual segment, and they justify the generalization that this is the mode of formation of the pronephric duct in all amphibian species. To this extent, therefore, the embryology of the pronephric duct can be reconciled with accepted views on its phylogeny. THE PURPOSE OF A VESTIGIAL PRONEPHROS In higher vertebrates the pronephros appears first in the development of the nephric system, but soon degenerates and is never a functioning urinary organ. In Amphibia, however, it functions as an organ of urinary secretion for some time and in Amblystoma punctatum its bilateral removal results in the death of the embryo (Howland, 1921). Waddington (1937) investigated the importance of this vestigial organ in the chick and came to conclusions similar to those of Grunwald (1937). The results obtained by these two workers showed that the formation of the pronephric duct could be prevented in the caudal region of the embryo by making an incision in the path of the caudal extension of the duct. In such cases the mesonephros developed in the absence of the pronephric duct, and was much retarded in its development, tubule formation not taking place. Waddington therefore propounded the theory that the pronephros in the chick, although non-functional from the physiological point of view, gave rise to the pronephric duct which induced the formation 'of-the mesonephros, and: therefore the pronephros could ''be The amphibian nephric system 97 regarded as having a morphogenetic function. Boyden (1924) has shown that the pronephric duct is of importance in the development of the avian cloaca. When the formation of the pronephric ducts is prevented, the middle chamber of the cloaca (urodaeal sinus) undergoes a deficient development. It would therefore appear that in the chick the pronephros, by giving rise to the pro- nephric duct, exerts an important influence on the development of both the mesonephros and the cloaca. It is now proposed to use existing evidence to test the applicability of this hypothesis to Amphibia where several species are available for consideration. In order to establish the hypothesis in Amphibia it would be necessary to show: (a) That the pronephros gives rise to the pronephric duct. (b) That the pronephric duct stimulates the formation of the mesonephros. (c) That the pronephric duct affects the development of the cloaca. The origin of the amphibian pronephric duct. In Amblystoma tigrinum and Triton taeniatus the pronephric rudiment appears soon after the closure of the neural folds and consists of a thickening of the somatopleure at the ventrolateral border of the somites. It lies immediately beneath the ectoderm and so is visible as an external swelling and can be seen to lie in the third to seventh trunk segments. Experimentally it has been possible to place Nile blue sulphate in this pronephric rudiment so that localized portions of it were stained (O'Connor, 1938). The stain was applied to the embryos before the appearance of the rudiment by staining the cells that later would give rise to it. In one group of experiments the stain was placed in the third and fourth trunk segments. In this case it was found that the stain was confined to the portion of the rudiment found in these segments, and in no other portion of it. Subsequent observation as development proceeded showed that the dye remained confined to the pronephros, and at no stage was there any found in the pronephric duct. In a second series of experiments the dye was placed in the fifth to seventh body segments, and when the pronephric rudiment appeared the dye was confined to its caudal portion that formed in segments 5-7. Subsequently the dye in these cases extended caudally throughout the duct while at all stages the pronephros remained free from the dye. Therefore the pronephric rudiment can be divided into two portions: (a) A portion derived from segments three and four, the cells of which can be traced into the pronephros but not into the pronephric duct. (b) A portion derived from segments 5-7, the cells of which can be traced into the pronephric duct but not into the pronephros. Thus it is seen that the pronephros and the pronephric duct arise from different portions of the pronephric rudiment and these portions arise from different body segments. Hence, although the pronephric duct is derived from the pronephric rudiment it cannot be said to arise from the pronephros. Anatomy 75 7 98 R. J. O'Connor Moreover, it is possible to show that the formation of the pronephric duct is independent of any influence on the part of the pronephros. Experiments were performed where the portion of the pronephric rudiment giving rise to the pronephros was removed. The operation was performed before the pronephric rudiment had begun to extend caudally to form the duct and the tissue removed is indicated in Fig. 1. A flap of ectoderm was dissected back to expose the pronephric rudiment. The anterior portion of the rudiment was then removed, and the flap of ectoderm allowed to fall back into position. Embryos were sectioned at various periods after the operation with the results given below. The time periods are only approximate but the results apply to all three species employed, namely Pleurodeles walthii, Triton taeniatus and a species of Amblystoma. Fig. 1. Removal of the anterior portion of the pronephric rudiment. (a) One to ten days after operation. On the operated side there was a normal formation of the pronephric duct.
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