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Cellular Interactions in the Development of the Shell Gland of the Gastropod, Ilyc~Nc~Ssa

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Cellular Interactions in the Development of the Shell Gland of the Gastropod, Ilyc~Nc~Ssa Cellular Interactions in the Development of the Shell Gland of the Gastropod, Ilyc~nc~ssa JAMES N. CATHER Associate Professor of Zoology, The University of Michigan, Ann Arbor, Michigan ABSTRACT To determine the cell lineage of the shell gland in Ilyunassa, the 2d and 2c micromeres were marked with carbon granules. The 2d micromere derivatives form the shell gland, but 2c derivatives are later incorporated into the mantle. Dr?- letion of 2d causes shell abnormalities but, in about 10% of the cases, the shell ap- pears normal although somewhat small. Deletion of 2c also causes characteristic shell abnormalities. After deletion of both 2d and 2c, no shell forms. When 2c is marked and 2d deleted, the shell gland is marked. Any one-quarter embryo can form internal shell masses. In 1013 isolated ectoblasts (-3A, -3B, -3C, -3D), no shell material formed. Ectoblast with any single macromere formed shell with good morphogenesis, as did ectoblast plus 4d. Posterior ectoblast plus 4d, equivalent in size to isolated whole ectoblast, formed external shell. Properly oriented ectoblast, grown in contact with a polar lobe, formed shell in up to 70% of the cases; in one-half of these, the shell was external. Deletion of the macromere from an ectoblast plus 3C series of embryos at intervals through the first day resulted in embryos which did not form shell. Ectoblast in contact with polar lobe for six days, then separated, developed shell on the seventh or eighth day. (1) Neither ectoderm nor endoderm in isolation will form shell but any ectoderm-endoderm combination has the histogenetic ability to form shell na- terial; (2) the endoderm exerts its influence between the second and sixth days of development; (3) only those combinations including or in contact with polar lobe cytoplasm through the third quartet stage undergo normal morphogenesis; (4) trans- planted polar lobes can induce ectoderm to form shell; (5) the histogenetic ability to form shell is suppressed or unactivated when polar lobe cytoplasm is present, except in the D quadrant; (6) specialization of the D quadrant is one of the major evo- lutionary trends in spiralians. Evidence for correlative differentiation self-differentiate, so that each cell will - the developmental modifications due form the same structure in isolation as it to the interaction between cells and tis- would in the intact embryo. Therefore the sues -in embryos from spirally cleaving prospective potency of the isolated or trans- mosaic eggs has generally eluded investi- planted blastomere is said to be the same gators since the origin of the theory of as the fate of the blastomere in the em- mosaic development three-quarters of a bryo. The potency may or may not equal century ago. Classical studies of embryos the fate but will not surpass it, according from eggs from which the polar lobe was to the theory. Other evidence indicates removed (lobeless embryos) by Crampton that the differentiative capacities of the (1896) and Wilson ('04a) and of isolated blastomeres are fixed through a precocious blastomeres by Wilson ('04b) and Costello segregation of qualitatively different cyto- ('45) indicate a progressive segregation of plasmic areas, especially the cortex, by capacities during development, so that at a highly determined cleavage pattern to each cleavage there is a part of the em- form a mosaic of self-differentiating cells bryo formed with the potentiality to form (Raven, '58). a particular structure and a remainder Although self-differentiation is dominant which does not have such a potential. This, during the early development of spiralians, in itself, does not necessarily imply that great correlative capacities are shown in the whole embryo had such a capacity the regenerative ability of these forms after prior to the segregative cleavage, as is metamorphosis. At present, little is known often stated; and the evidence for such an of the transition of the embryo from a idea is, at best, equivocal. Isolated blasto- group of independent blastomeres, pre- meres or groups of blastomeres tend to cisely arranged and tightly bound to one J. EXP. ZOOL., 166: 205-224. 205 206 JAMES N. CATHER another, into a highly integrated organism the polar lobe or D quadrant cytoplasm can capable of delicate responses to the devel- be considered the primary morphogenetic opmental environment. Whether the capac- organizer of molluscan development. ity for correlation develops gradually or Other evidence for regulative ability instantaneously is unknown, as is the tem- comes from the studies of Penners ('37), poral assumption of correlative abilities in who showed that the mesentoblast cell the different structures or systems in the (4d) of Tubifex, under suitable conditions, individual. can form ectodermal structures normally Although early development was demon- formed from the primary somatoblast (2d), strated to be primarily due to self-differen- which derives pole plasm from the same tiatlon, a large number of studies have area of the egg as the mesentoblast. Un- indicated a special developmental signifi- fortunately, this work has never been cance for the D quadrant, in addition to confirmed or extended to other species. the origin of the mesoderm. Clement's in- Novikoff ('38a) showed that twins could vestigations ('52, '56, '62) are the most develop from a Sabellaria egg when the complete in this regard. He has shown that formation of the polar lobe was suppressed D quadrant material, in this case derived so that the first cleavage was equal. Rather from the polar lobe, is necessary for the than a true correlative interaction between establishment of normal symmetry, as a cells, this can be interpreted as an equal regulator of the rate and pattern of cleav- distribution of lobe substance providing age in the D quadrant, and for the normal each of the two cells with its organizer. morphogenesis of the foot, shell, eyes, oto- Carefully designed experiments (Novikoff, cysts, and heart. The potency of the foot '38b) failed to demonstrate cellular or lobe and shell does not exceed the fate but interaction in Subellaria. Costello ('45) D quarter embryos can produce eyes which showed that gastrulation would occur in are normally derived from la and lc Nereis only in those blastomere combina- (Clement, personal communication) so tions which include both endoderm and that the D quadrant retains a significant ectoderm. Using combined animal and veg- ability to regulate. Thus its potency can etal tiers or vertical half-combinations, exceed its fate. Furthermore, Clement has Horstadius ('37) failed to demonstrate cel- clearly demonstrated that the morpho- lular interactions in embryos of the nemer- genetic influence of the polar lobe region tine, Cerebratulus. No comparable experi- is exerted during the formation of the four ments have been done with mollusks. quartets of micromeres but that not all Raven's series of studies of lithium- lobe-dependent larval features are deter- treated Limnaea embryos provide two val- mined at the same time. External shell uable cases in the analysis of regulative appears only after the formation of the ability in mollusks (Raven, '58). The first second quartet; however, normal morpho- involves the differentjation of head struc- genesis of the shell, as well as the foot, tures, particularly the eyes and tentacles. velum and eyes, occurs only after the for- A gradient-field concept was developed in mation of the third quartet. The heart and which there is a peak of activity at the ani- intestine are determined with the forma- mal pole, the region which later becomes tion of 4d. The 4D macromere is evidently the apical plate. The lateral cephalic plates, nutritive and of no morphogenetic value. where the eyes and tentacles form, are Although cytoplasmic segregation appears areas of intermediate dominance. Raven adequate to account for the determination explained the abnormalities produced by of the intestine and heart, it is necessary lithium - synopthalmia, cyclopia, aceph- to look to a mechanism of inductive nature aly - on the basis of gradient suppression. to explain the relation of the polar lobe to Although this concept has provoked valu- the morphogenesis of shell, foot, velum, able experimental analysis the work of and eyes. Clement's ('62) experiments in- Verdonk ('65) carried out in Raven's lab- dicate that the fate of all the cells in mo- oratory makes the concept questionable. saic eggs is not irrevocably determined at Verdonk showed that lithium treatment some early stage but is progressively de- modifies the direction of cleavage in spe- termined through development. Certainly cific cells. These cells, which cease division ILYANASSA SHELL GLAND DEVELOPMENT 207 in the normal embryo, then continue to gastrulates by epibole. This is true of a divide to form a cluster of small cells. The large part of molluscan species where the treatment', in this case, appears to release shell gland forms prior to the formation of certain cells from a division inhibitor. the endodenn in the proximity of the shell However, other cells which normally con- gland. tinue division are blocked by such treat- The present investigation was initiated ment so that their progeny are not formed. to determine the role of induction in the The end result is that the anlagen of the formation of the shell gland in mollusks. eyes and tentacles are displaced so that they give rise to the structure equal to their METHODS fate but in the wrong position. Modifica- tion of cleavage pattern alone can account The experiments were performed on the for the abnormalities and regulation is not prosobranch gastropod Nassarius obsoletus demonstrated. Although the cortex may Say, commody known to embryologists by represent a prepatterned series of anlagen its subgeneric name Ilyanassa, which will sites, no gradient hypothesis need be in- be used hereafter. Animals were obtained voked. from the Marine Biological Laboratory, Raven's ('52) analysis of the develop- Woods Hole or were collected on the coast ment of the molluscan shell gland showed of the Olympic Peninsula in Washington.
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