Regulative development in a spiralian embryo as shown by cell deletion experiments on the Acoel, Childia.

Spiral cleavage and mosaicism are closely associated in the Annelida, Mollusca, and probably the polyclad Turbellaria, but the evolutionary history of these phenomena remains uncertain. The Acoela, the most primitive order of turbellarians, exhibit spiral cleavage but with the formation of duets of micromeres rather than the more typical quartets. The regulative versus mosaic capacities of the acoel, Childia groenlandica, were investigated by deleting various combinations of blastomeres from the two-cell stage through the third duet. The acoel embryo showed extensive regulative ability since all experiments yielded normal animals except those in which both macromeres were deleted. These abnormal animals were ciliated spheres with a central cavity and indicated that the macromeres are necessary for form and organ differentiation. An inductive interaction between the micromeres and macromeres is suggested. Since mosaicism is probably specialized and a derivative of the indeterminate type of development, the regulative capacity of the acoel embryo suggests that this order lies near the ancestral line of the spiralia and represents an evolutionary stage where the very defined pattern of spiral cleavage is not yet associated with early programming of the cell's fate. Since the turn of the century radial or unorganized cleavage has suggested regulation while spiral cleavage has been linked with mosaicism. Regulative development is characterized by the occurrence of cell interactions during early cleavage stages and partial embryos may develop into whole animals. In the classic cases of mosaic development, on the other hand, each blastomere as it forms has only the self-differentiative capacity to give rise to a particular larval structure and partial embryos therefore will develop into deficient animals. (It should be noted that recent investigations by Clement ('52, '62) and Cather ('67) have shown that the concept of strict mosaicism is, at least in some cases, an oversimplification.) Spiral cleavage occurs in the turbellarian flatworms, nemertines, annelids, molluscs, some crustaceans, and a few small phyla, though in its most characteristic form is found only in polyclad turbellarians, nemertines, annelids and molluscs. The evolutionary relationships among the various spiralian groups and the association between spiral cleavage and J. EXP. ZOOL., 176; 97-106. mosaicism have been established and verified many times within the past century. The studies of Wilson (1892) on the polychaete Nereis and Conklin (1897) on the gastropod Crepidula showed that these spiralian embryos, representing two different phyla, cleaved in essentially the same manner and that their cell lineages were almost identical, establishing beyond question a close phylogenetic relationship between annelids and molluscs. Experiments soon followed which proved the mosaic nature of the spiralian embryo. In separating the blastomeres of the annelids Lanice (Wilson, '04a) and Chaetopterus (Tyler, '30) at the two-cell stage, Wilson and Tyler found that neither half was able to form a complete trochophore larva. Similar experiments on Subellaria (Hatt, '32; Novikoff, '38a,b) and Tubifex (Penners, '26) indicated a high degree of mosaicism in the annelid embryo. In the most com1 This paper was par t of a dissertation presented for the degree of Doctor of Philosophy i n The University of Michigan. 2 Present address: Department of Biology, Whitman Laboratory, The University of Chicago, Chicago, Illinois.