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Divergence and Convergence in Early Embryonic Stages of Metazoans

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Divergence and Convergence in Early Embryonic Stages of Metazoans Contributions to Zoology, 71 (1/3) 101-113 (2002) SPB Academic Publishing bv, The Hague and in of Divergence convergence early embryonic stages metazoans Frietson Galis ¹ & Barry Sinervo2 1 Institute ofEvolutionary and Ecological Sciences, Leiden University, P.O. Box 9516, 2300 RA Leiden, 2 Netherlands, [email protected]: Biology’ Department, University of California Santa Cruz, [email protected]. Keywords: evolutionary conservation, pleiotropy, cleavage, gastrulation, organogenesis, multicellularity, phylotypic stage Abstract and in Conservation, convergence divergence patterns of gastrulation 104 and in Conservation, convergence divergence early The early stages oforganogenesis in metazoans differ drastically organogenesis 106 between order such and classes. The higher taxa as phyla seg- What conservation of of causes early stages organo- mented in the of germ band stage insects, nauplius stage crus- to the at genesisrelative divergence seen other taceans, and the neurula/pharyngula stage in vertebrates are stages 109 examples ofthis diversification. In striking contrast with this Modularity and the divergence of form in late is divergence, the similarity of these stages within these taxa, organogenesis 110 i.e., within insects, crustaceans, and vertebrates. The early sta- The relationship between divergence of early and of ges organogenesis, orphylotypic stages, have, thus, remained late ontogenetic stages 111 in very similar most species since the evolutionary origin of the Early diversification foloowed by stasis of early taxa. These phylotypic stages are considerably more similar to stages of organogenesis 111 each otherthan to the earlier stages ofcleavage and gastrulation. Conclusion 111 Cleavage and gastrulation stages display not only great variability, Acknowledgements 112 but of also striking examples apparent convergence among species References 112 in different for in the of phyla, example many cases epiblastic in This leads the situation cleavage yolk-rich eggs. to paradoxical that the overall similarity ofcleavage and gastrulation stages is in than of Introduction general higher among metazoans the early stages of organogenesis, but within phyla and classes the situation is the We discuss reverse. data on cleavage, gastrulation, and early The of early stages cleavage and gastrulation are organogenesis and evaluate possible causes for conservation, often similar remarkably among metazoans (Gil- homoplasy, and diversification in an attempt to throw light on bert and Raunio, 1997; fig. The this situation. 1). succeeding stage, paradoxical In addition, we discuss a hypothesis is far diverse has to the organogenesis, more meta- that been proposed explain diversity of early stages among than and of organogenesis at the level of metazoans and the similarity zoans cleavage gastrulation (Gilbert and and within many phyla classes. Raunio, 1997). Paradoxically, embryologists have for noticed a long time that within most higher order taxa, e.g. phylum or class, early organogenesis is Contents considerably less variable than earlier stages (Seidel, 1960; Anderson, 1973; Sander, 1983; Hall, 1996; Introduction 101 Elinson, 1987). In particular when we judge simi- due to Similarity conservation or homoplasy 102 larity relative to the number of options available and in Conservation, convergence divergence patterns of for the stage under consideration. Towards the end cleavage 102 of diverse Mechanistic causes of cleavage patterns 102 gastrulation relatively ontogenetic pat- terns Understanding of diversity 103 converge to a highly similar stage. Examples Downloaded from Brill.com10/07/2021 03:14:16PM via free access - 102 F. Galis & B. Sinervo Divergence and convergence in early embryonic stages of metazoans of such similar celled limited highly stages during early organo- stage. Only a number of permuta- in genesis are: the extended/segmented germ-band tions are possible embryos with a few undifferent- stage of insects, the nauplius stage of crustaceans, iatedcells. In contrast, the diversity ofmulticellular and the neurula/pharyngula stage of vertebrates clonal propagules, which lack such a reset to a single- (Seidel, 1960, Anderson, 1973; Sander, 1983; Elin- celled stage, is indeed remarkably high. arises because ofeither similar selec- son, 1987; Hall, 1996; Grbic, 2000; Dahms, 2000; Similarity Galis et al., 2002). During cleavage and gastrula- tion pressures and/or stringent constraints. In the conservation of tion the overall case of constraints, similarity among metazoans is, thus, morphological greater than during early organogenesis, but, within patterns arises either because no genetic variation is or because many higher order taxa the reverse is the case and produced, invariably negative pleio- effects are associated with similarity is higher during early organogenesis than tropic changes. Similarity in have four during cleavage and gastrulation. For instance, the a phylogenetic context, thus, can causes; rapid divisions during cleavage of polyembryonic 1) shared ancestral traits insects and mammals resemble each other more than plesiomorphy, (inherited similarity evolved once); the segmented germband stage and the neurula/ 2) synapomorphy, shared derived traits (novel simi- pharyngula stage, respectively, i.e., the early orga- larity evolved once); nogenesis stages (see below). On the other hand, due to common within mammals of different 3) homoplasy adaptational pres- phylotypic stages spe- sures, or cies are more similar than cleavage and gastrula- 4) homoplasy due to developmental constraints tion stages and the same holds for the segmented derived traits band in To (convergent adaptive promoting germ stage insects (see below). under- trait correlation). stand the evolutionary origin of this counterintuitive situation it is necessary to know whether similar- ity is the result of conservation, convergence, or Conservation, convergence and divergence in parallel evolution. patterns of cleavage Mechanistic causes of cleavage patterns Similarity due to conservation or homoplasy During cleavage, the zygote rapidly divides into It is assumed that usually similarity among early smaller cells. many Patterns of cleavage are deter- is the result of embryonic stages evolutionary con- mined of by a small number mechanistic factors, servation (Seidel, 1960; Sander, 1983; Buss, 1987; variation in which allows a high diversity of cleav- Even Baer Raff, 1996; Hall, 1996). though von One mechanistic age patterns. factor is the amount did not believe in evolution (1828) by descent, and distribution of vitelloprotein within the zygotic he was the first to that early changes in ' propose cytoplasm (Gilbert, 2000). Yolk impedes cleavage. ontogeny were more likely to have cascading con- In with little zygotes yolk, cleavage usually sepa- than later when of devel- sequences changes most rates the embryo into distinct cells (holoblastic has taken place. Although this in opment already cleavage, as sponges, sea urchins, lancelets, most constraint is real In evolutionary undoubtedly (Buss amphibians and mammals). zygotes with a large its has recently been 1987), importance challenged yolk component, cleavage only occurs in the part the revelation of considerable variation in of by early the cytoplasm with little or no yolk. Cleavage In embryonic stages. addition, evolutionary con- proceeds only in this part (meroblastic cleavage), servation of early embryonic stages may be less leading in cephalopods, fishes, reptiles and birds strong than previously thought because of similar- to a germinal disc on the surface of a large yolk ity due to convergent or parallel evolution (ho- mass (epiblastic cleavage, Figs, la and b), and in moplasy). Similarity is almost unavoidable in the some crustaceans and some insects to a superficial early ontogenetic stages of metazoans because of layer of embryonal cells with yolk in the center the complete reset that occurs at the initial single- (periblastic cleavage). For example, most amphib- Downloaded from Brill.com10/07/2021 03:14:16PM via free access Contributions to - Zoology, 71 (1/3) 2002 103 I. Fig. Convergence. Meroblastic, epiblastic cleavage in the (A) cephalopod Loligo pelalei (after Claus and Grobben, 1917) and (B) in the longnose gar Lepisosteus osseus (after Balfour, 1881). ians exhibit holoblastic cleavage. However, eleu- Nutrients obtained can be from either yolk, ma- therodactyline frogs with derived yolky also ternal eggs tissues, or the environment. Specializations have secondarily derived epiblastic cleavage (Elin- for nutrition embryonic uptake can arise as Given the son, 1987). adaptive value of high yolk a direct of consequence constraints, e.g. yolk con- volume for progeny survival and the extreme con- straints (see above), or as adaptations to specialized of or vergence epiblastic periblastic cleavage among conditions. For example, evolution of mammalian diverse taxa, cleavage mechanisms thus, to appear, viviparity has led compaction, a conspicuous constrained to evolve as a result of selection for in specialization which loosely arranged blastomeres nutrient rich eggs (cause 4, above). huddle and suddenly together form a compact mass The second mechanism is the and angle timing (Gilbert,, 2000). Compaction and associated intra- of mitotic spindle formation, and thus, the orienta- cellular changes function during embryonic implan- tion of cleaving cells: (various spiral protostomes), tation in the uterus. Compaction is involved in the radial (various deuterostomes),
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