Conservation, convergence and divergence in patterns of cleavage
Mechanistic causes of cleavage patternsnext section
During cleavage, the zygote rapidly divides into many smaller cells. Patterns of cleavage are determined by a small number of mechanistic factors, variation in which allows a high diversity of cleavage patterns. One mechanistic factor is the amount and distribution of vitelloprotein within the zygotic cytoplasm (Gilbert, 2000). Yolk impedes cleavage. In zygotes with little yolk, cleavage usually separates the embryo into distinct cells (holoblastic cleavage, as in sponges, sea urchins, lancelets, most amphibians and mammals). In zygotes with a large yolk component, cleavage only occurs in the part of the cytoplasm with little or no yolk. Cleavage proceeds only in this part (meroblastic cleavage), leading in cephalopods, fishes, reptiles and birds to a germinal disc on the surface of a large yolk mass (epiblastic cleavage, Figs. 1a and b), and in some crustaceans and some insects to a superficial layer of embryonal cells with yolk in the center (periblastic cleavage). For example, most amphibians exhibit holoblastic cleavage. However, eleutherodactyline frogs with derived yolky eggs also have secondarily derived epiblastic cleavage (Elinson, 1987). Given the adaptive value of high yolk volume for progeny survival and the extreme convergence of epiblastic or periblastic cleavage among diverse taxa, cleavage mechanisms appear, thus, constrained to evolve as a result of selection for nutrient rich eggs (cause 4, above).
The second mechanism is the angle and timing of mitotic spindle formation, and thus, the orientation of cleaving cells: spiral (various protostomes), radial (various deuterostomes), and rotational (mammals) cleavage.
The third mechanism is differential cell adhesion. Differential adhesion can cause important shape differences, for instance in compaction in mammals and polyembryonic wasps, in which blastomeres are not loosely packed but very closely joined together; or in coeloblastulas, in which the blastula is a hollow ball of cells instead of a solid ball as in stereoblastulae.
Understanding of diversity and similarity
Diversity in cleavage patterns can be understood in terms of adaptations for embryonic life such as nutrient uptake, locomotion, and maternal determination.
Nutrients can be obtained from either yolk, maternal tissues, or the environment. Specializations for embryonic nutrition uptake can arise as a direct consequence of constraints, e.g. yolk constraints (see above), or as adaptations to specialized conditions. For example, evolution of mammalian viviparity has led to compaction, a conspicuous specialization in which loosely arranged blastomeres suddenly huddle together and form a compact mass (Gilbert, 2000). Compaction and associated intracellular changes function during embryonic implantation in the uterus. Compaction is involved in the separation of the inner cell mass (from which the embryo will develop) from the trophoblast (which provides fetal contributions to the placenta). Interestingly, polyembryonic insects have independently evolved compaction, together with early separation of embryonic and extraembryonic cell lineages (Grbič et al., 1998), presumably because endoparasitism imposes similar spatial constraints as viviparity (an example of cause 3 above).
Locomotor demands also influence cleavage (Buss, 1987). Free-living dispersal stages have external ciliated cells and internal dividing cells. This configuration appears to be largely the result of locomotor demands combined with a universal metazoan constraint (an example of cause 1) – cells cannot divide when ciliated (Buss 1987). Metazoan cells have only one microtubule center, which can be used either for a mitotic spindle or for cilia, axons, dendrites and other microtubular specializations. Thus, cilia are concentrated on the surface and dividing cells without cilia are inside propagules to prevent interference with locomotion.
Maternal determination. Buss (1987) argued that selection for maternal determination has shaped the evolution of cleavage. Determination of early development via maternal cytoplasmic factors provides a powerful means for the mother to prevent proliferation of one cell line at the expense of others, thus helping establish selection at the level of the individual. The amount of development under maternal control is necessarily limited; only a finite number of maternal cytoplasmic factors can be provided to the zygote. Unequal cleavage potentially increases effectiveness of maternal control. In unequal cleavage, some cells differentiate and begin zygotic transcription (end of maternal control) and thus lose the capacity to become germ cells, whereas others continue as undifferentiated and divide under maternal control. Differentiated cells usually lose the capacity to divide, which is why they can no longer become germ cells. Unequal cleavage typically occurs in taxa with spiral cleavage such as turbellarians, annelids and molluscs (Buss, 1987).
Polyembryony. Cleavage is radically different in polyembryonic parasitic wasps relative to other insects (Grbič et al., 1998). Cleavage is holoblastic, and the zygote produces not one, but many small embryos. Cellularization occurs immediately, whereas in most other insects (including drosophilids) nuclei first divide into a syncytium and cellularization occurs later. Further specializations of compaction and early separation of embryonic and extraembryonic tissues (see above) are probably caused by the endoparasitic lifestyle, which is to a certain extent convergent with viviparity in mammals, i.e., living in another organism.
In conclusion, cleavage patterns are diverse, but important similarities occur because of evolutionary convergence due to similar embryonic adaptations and constraints. The most striking examples of convergent embryonic adaptations are compaction in mammals and polyembryonic insects and epiblastic cleavage in yolk-rich embryos.