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Evolution of cleavage programs in relationship to axial specification and body plan evolution.

We examine egg organization and the role of the early cleavage program in establishing the axial properties of larval and adult body plans. Here we review our own work and that of others on various invertebrate metazoans, including cnidarians, ctenophores, polyclad flat-worms, and some protostome spiralians - nemerteans, molluscs, and polychaete annelids.

The Ctenophores

Most metazoan body plans can be characterized as having, either elements of radial symmetry (such as the Chidaria and Ctenophora) or bilateral symmetry (e.g., protostomes and deuterostomes). Cnidarians are considered to be radially symmetrical around their longitudinal body axis, called the oral-aboral axis, whereas ctenophores display "biradial symmetry" around their oralaboral axis. Although their phylogenetic relationship to other metazoans remains controversial, ctenophores may represent the sister-group to the Bilateria. The transition from radial to bilateral symmetry can be viewed as one of the most important events in body plan evolution, and the study of the extant cnidarians and ctenophores may therefore help us to understand the evolution of the anterior-posterior and dorso-ventral axes of bilaterians.

Virtually all bilaterian metazoan phyla undergo a stereotyped, species-specific cleavage program, but some basal metazoans (i.e., sponges and most cnidarians) do not. This raises the question of how and why stereotypical cleavage programs evolved. One distinct feature of ctenophores, which sets them apart from other radially symmetrical forms, is their phylum-specific, highly stereotyped mode of development (see 1-3 for reviews). Previous work has demonstrated that the cleavage program is causally involved with the establishment of cell fates in the ctenophore (4-6), and that the capacity to replace structures derived from missing blastomeres ("mosaic development") is lacking. For example, previous chalk-particle marking experiments indicated that the eight rows of comb plates in ctenophores are derived from the four [e.sub.1] micromeres of the 16-cell embryo (7), and deletion of these four micromeres results in the absence of ctene rows and their associated endodermal canal system (8-10).

Using intracellular cell lineage techniques on embryos of the lobate ctenophore Mnemiopsis leidyi, however, we showed that the [m.sub.1] micromeres [ILLUSTRATION FOR FIGURE 1A OMITTED] also contribute to comb plate formation during normal development. Thus, if comb plates do not form after [e.sub.1] micromere removal, then some blastomere fates in the early embryo must not be precociously specified at the time of their birth, as previously argued. Rather, inductive interactions by the descendants of the [e.sub.1] micromeres organize [ILLUSTRATION FOR FIGURE 1B OMITTED] development in adjacent ectodermal and endodermal lineages (11, 12). We suggest that stereotypic cleavage programs arose during metazoan evolution as a reliable means of segregating factors to distinct embryonic lineages, some of which serve as inductively active "signaling centers." These signaling centers organize subsequent development in adjacent lineages. Stereotypic cleavage patterns are a means of reliably positioning these organizing centers and the cells that respond to their signals. Other cells may be determined by autonomous mechanisms. These strategies for early patterning are prevalent in many metazoan embryos (13, 14). Although the molecular nature of inductive signals in ctenophores is unknown, several known pathways, such as those involving wg/[Beta]-catenin, are reasonable places to start looking.

Most authorities believe that bilaterally symmetrical organisms evolved from a radially symmetrical ancestor. Little is known about how this transition occurred. For example, no agreement about the relationship between the oral-aboral axes of cnidarians and ctenophores and the anterior-posterior axis of bilaterians has been reached. The apparent conservation in the molecular mechanisms leading to the establishment of the dorsoventral axis in the common ancestor of protostomes and deuterostomes (the dpp/sog orthologs) adds to speculation that an existing axis was co-opted for the dorso-ventral axis. On the other hand, this axis may have arisen de novo (15). We have shown in ctenophores that some mesodermal and endodermal lineages are organized in a pattern that is diagonally opposed to the first and second cleavage planes [ILLUSTRATION FOR FIGURE 1C OMITTED]. Because these lineages give rise to the oral-anal plane, this organization could reflect a transition from a radial to a bilaterally symmetrical body plan (16). We propose different scenarios for generating these changes in body plan organization based on the expression of highly conserved developmental regulatory genes.

The Spiralians

The highly stereotypic cleavage pattern referred to as "spiral cleavage" occurs in most of the extant invertebrate phyla, including the molluscs, annelids, vestimentiferans, pogonophorans, echiurans, sipunculids, nemerteans, gnathostomulids, mesozoans, and polyclad turbellarians. Cell lineage analyses, mainly conducted on annelidan and molluscan embryos, suggested that the ultimate fates of blastomeres are tremendously conserved.

More recently, we have been examining the development of representatives from a number of different spiralian phyla to determine the extent of homologies in the spiralian developmental program. For instance, our work in collaboration with Barbara Boyer has confirmed earlier reports that the polyclad flatworms display a cell lineage fate map similar to that of the annelids and molluscs (17, 18, 19). Early investigators suggested that the acoelomate platyhelminthes (flatworms) are basal to the bilaterian metazoans, but more recent phylogenetic analyses place them as basal members of the protostome spiralians (20, 21). In either case, the developmental pattern exhibited by the polyclads should be more closely representative of the basal condition within the Spiralia.

We have also demonstrated that the Nemertea, a coelomate invertebrate phylum, also exhibits strong homologies to the basic spiralian cleavage program. In addition to possessing cell quadrant identities similar to those found in other spiralians (i.e., A, B, C, and D quadrants), the embryos also give rise to both ecto- and endomesoderm (22, 23). Although the general spiralian developmental program is highly conserved in this group, it does exhibit some modifications in the form of what Lillie referred to as "adaptations in cleavage" (23). These include the formation of a first quartet of micromeres of greatly increased size that generates the majority of the larval ectoderm. Other changes have occurred in the sub-lineages that give rise to certain structures, such as the ciliated band (derived from first, second, and third quartet derivatives) and the ectomesoderm (derived entirely from 3a and 3b).

The most significant modifications in Nemertea of the spiralian developmental program seem to have affected the mechanisms involved in cell fate and axis determination. Those employed by the nemerteans appear to be distinct from those utilized by equal-cleaving molluscs (24, 25), and differences are encountered between different nemertean species. Our research indicates that larval nemertean axial properties are actually specified before cleavage begins, a condition that does not appear to take place in the embryos of equal-cleaving molluscs (24). Furthermore, the embryos of the indirect-developing nemertean Cerebratulus lacteus appear to exhibit a great deal of regulation, while those of a direct-developing species, Nemertopsis bivittata, do not (25). We believe that nemerteans exhibit a derived developmental condition, and agree with previous reports that the ancestral spiralian developmental condition was one in which equal, quartet spiral cleavage occurred, and quadrant fates and axial properties were established epigenetically via inductive interactions (26).


The authors thank the organizers of this meeting and NASA for inviting us to this workshop. M.Q.M. was supported by an American Cancer Society Illinois Division Grant #92-43, NSF grant #9315653, and MBL Spiegel, Davis and NASA Fellowships. J.Q.H. (J.J.H.) was supported by an MBL Associates' Fellowship, a Lemann Fellowship, a Spiegel Fellowship, and a NASA Fellowship.

This paper was originally presented at a workshop titled Genetic Regulatory Networks in Embryogenesis and Evolution. The workshop, which was held at the Marine Biological Laboratory. Woods Hole, Massachusetts, from 11 to 14 June 1997, was sponsored by the Center for Advanced Studies in the Space Life Sciences at MBL and funded by the National Aeronautics and Space Administration under Cooperative Agreement NCC 2-896.

Literature Cited

1. Reverberi, G. 1971. Ctenophores. Pp. 85-103 in Experimental Embryology of Marine and Fresh-water Invertebrates, G. Reverberi, ed. North-Holland, Amsterdam.

2. Ortolani, G. 1989. The ctenophores: a review. Acta Embryol. Morphol. Exp. 10: 13-31.

3. Martindale, M. Q., and J. Q. Henry. 1997. The Ctenophora. Pp. 87-111 in Embryology. The Construction of Life, S. Gilbert and A. Raunio, eds. Sinauer, Sunderland, MA.

4. Freeman, G. 1976. The role of cleavage in the localization of developmental potential in the ctenophore Mnemiopsis leidyi. Dev. Biol. 49: 143-177.

5. Freeman, G. 1976. The effects of altering the position of cleavage planes on the process of localization of developmental potential in ctenophores. Dev. Biol. 51: 332-337.

6. Freeman, G. 1977. The establishment of the oral-aboral axis in the ctenophore embryo. J. Embryol. exp. Morphol. 42: 237-260.

7. Reverberi, G., and G. Ortolani. 1963. On the origin of the ciliated plates and mesoderm in the Ctenophore. Acta Embryol. Morphol. Exp. 6: 175-199.

8. Driesch, H., and T. H. Morgan 1895. Zur Analysis der ersten Entwickelungsstadien des tenophoreneies. Arch. Entwicklungsmech. Organ. 2: 204-224.

9. Farfaglio, G. 1963. Experiments on the formation of the ciliated plates in Ctenophores. Acta Embryol. Morphol. Exp. 6: 191 203.

10. Martindale, M. Q. 1986. The expression and maintenance of adult symmetry properties in the ctenophore, Mnemiopsis mccradyi. Der. Biol. 118: 556-576.

11. Martindale, M. Q, and J. Q. Henry. 1996. Development and regeneration of comb plates in the ctenophore Mnemiopsis leidyi. Biol. Bull. 191: 290-292.

12. Martindale, M.Q., and J.Q. Henry. 1997. Reassessing embryogenesis in the Ctenophora: The inductive role of [e.sub.1] micromeres in organizing ctene row formation in the "mosaic" embryo, Mnemiopsis leidvi. Development 124: 1999-2006.

13. Davidson, E. H. 1991. Spatial mechanisms of gene regulation in metazoan embryos. Development 113: 1-26.

14. Schnabel, R. 1997. Why does a nemotode have an invarient cell lineage? Semin. Cell Der. Biol. 8: 341-349.

15. Lacalli, T. 1996. Dorsoventral axis inversion: a phylogenetic perspective. BioEssays 18: 251-254.

16. Martindale, M. Q., and J. Q. Henry. 1995. Diagonal development: establishment of the anal axis in the ctenophore Mnemiopsis leidvi. Biol. Bull. 189: 190-192.

17. Henry, J.Q., M.Q. Martindale, and B.C. Boyer. 1995. Axial specification in a basal member of the spiralian clade: lineage relationships of the first four cells to the larval body plan in the polyclad turbellarian Hoploplana inquilina. Biol. Bull. 189: 194-195.

18. Boyer, B.C., J. Q. Henry, and M. Q. Martindale. 1996. Dual origins of mesoderm in a basal member of the spiralian clade: cell lineage studies in the polyclad turbellarian Hoploplana inquilina. Dev. Biol. 179: 329-338.

19. Boyer, B.C., J.Q. Henry, and M.Q. Martindale. 1998. The cell lineage of a polyclad turbellarian embryo reveals close similarity to coelomate spiralians. Dev. Biol. (in press).

20. Aguinaldo, A. M. A., J. M. Turbeville, L. S. Linford, M. C. Rivera, J. R. Garey, R. A. Raff, and J. A. Lake. 1997. Evidence for a clade of nematodes. arthropods and other moulting animals. Nature 387: 489-493.

21. Balavoine, G. 1997. The early emergence of platyhelminths is contradicted by the agreement between 18S r RNA and Hox genes data. C. R. Acad. Sci. Paris 320: 83-94.

22. Henry, J. Q., and M. Q. Martindale. 1996. The origins of mesoderm in the equal-cleaving nemertean worm Cerebratulus lacteus. Biol. Bull. 191: 286-288.

23. Henry, J. Q., and M. Q. Martindale. 1997. Conservation of the spiralian developmental program: cell lineage of the nemertean Cerebratulus lacteus. Dev. Biol. 200 (in press).

24. Henry, J. Q., and M. Q. Martindale. 1996. The establishment of embryonic axial properties in the nemertean, Cerebratulus lacteus. Dev. Biol. 180: 713-721.

25. Martindale, M. Q., and J. Q. Henry. 1995. Modifications of cell fate specification in equal-cleaving nemertean embryos: alternate patterns of spiralian development. Development 121: 3175-3185.

26. Freeman, G., and J. W. Lundelius. 1992. Evolutionary implications of the mode of D quadrant specification in coelomates with spiral cleavage. J. Evol. Biol. 5: 205-247.
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Title Annotation:Genetic Regulatory Networks in Embryogenesis and Evolution
Author:Henry, Jonathan Q.; Martindale, Mark Q.
Publication:The Biological Bulletin
Date:Dec 1, 1998
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