Contributions to Zoology, 71 (1/3) (2002)Frederick R. Schram: Editorial

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The papers herein

The paper on “Cleavage, gastrulation, and germ disc formation of the amphipod Orchestia cavimanna (Crustacea, Malacostraca, Peracarida)” by Gerhard Scholtz and Carsten Wolff demonstrates that not all types of determinate cleavage within protostomes are necessarily spiral. While spiral determinate cleavage is the classic, oft-stated, great autapomorphy of the protostome metazoans, it is often overlooked that other forms of cleavage exist among these animals. For example, spiral duet cleavage is a hallmark of acoel flatworms, and this process is indeed sometimes cited as evidence for the separate status of the acoels from the regular Platyhelminthes. And a determinate quartet cleavage that ranges from holoblastic to quite superficial is seen in a variety of arthropods and molluscs. The case documented here seems to be unique to amphipods. The pattern of cleavage shifts from one of initially totally dividing cells to one where the expulsion of yolk into a central position in the embryo occurs along with formation of a superficial germ band of cytoplasm. Nevertheless, the use of florescent dyes reveals that clear cell lineages exist in amphipods. Though this has been informally known for some time, Scholtz and Wolff document this here for the first time. It also suggests that it would be profitable to re-examine the purported spiral cleavages that have been noted among the cirripedes and pycnogonids.

An interesting review, “The improbability of dorsal-ventral axis inversion during animal evolution, as presumed by Geoffroy Saint Hilaire,” by Jo van den Biggelaar, Eric Edsinger-Gonzales, and myself is an example that illustrates the importance of looking in detail at the study of real animals. The issue of axis inversion between protostomes and deuterostomes originated in the early 1800’s with the writings of Etienne Geoffroy Saint Hilaire, and has been resurrected in recent years by some researchers based on apparently anomalous dorso-ventral patterns of expression in developmental genes. However, it is our contention that if Geoffroy Saint Hilaire had known more about comparative embryology, he would never have come up with the idea of axis inversion. In the same vein, if modern molecular geneticists knew more about comparative embryology, their discovery of the conservation of pattern forming genes in vertebrates as well as invertebrates would not have lead to a revival of dorso-ventral axis inversion. It is not that we have the direct exchange of dorsal and ventral surfaces between protostomes and deuterostomes. Rather, there is a complex series of cell migrations that occur during the embryogenesis of protostomes that accounts for the shift of originally dorsal cells to a postero-ventral position, and concomitant migration of the posteriorly oriented blastopore to an antero-ventral location. The evolution of protostomes is a lot more complicated than text-book knowledge would lead us to believe.

Peter Damen and Wim Dictus present part of their results on cell lineage studies, “Newly-discovered muscle in the larva of Patella (Mollusca, Gastropoda) suggests the presence of a larval extensor.” This paper emphasizes again that careful embryological and anatomical work is still capable of discovering entirely new things. All one has to be is observant. In this case, the extension and retraction of larval bodies out of their shells are processes that everyone implicitly understood had to be under control of antagonistic muscles. However, until Damen and Dictus’ work, we had no proof of this, nor any clear understanding of how these movements occurred. The paper is an object lesson to students who often wonder if there is anything new to be discovered in science.

Stefan Koenemann and I with the paper, “The limitations of ontogenetic data in phylogenetic analyses,” take inspiration from the work of the research group at Leiden University under the direction of Prof. dr. Michael Richardson. It has long been a dictum of comparative biology that developmental data is important towards understanding the evolution of organisms. Indeed, Haeckel’s Biogenic Law, ‘ontogeny recapitulates phylogeny,’ appeared soon after Darwin’s The Origin of Species. More recently, Gould’s most effective book, Ontogeny and Phylogeny, reintroduced considerations of heterochronic processes in evolutionary studies. Yet, while direct application of data on heterochrony, especially for vertebrates, often gives phylogenetic trees not unlike those drawn from either molecular or adult anatomical features, data from other groups seems to be less effective. We conclude that this is due to the lack of an effective analytical algorithm to handle such data. Ordinary cladistic programs, such as PAUP, are essentially interpretations of data derived from 3-dimensional forms, but these programs are not particularly effective in handling 4-dimensional constructs, i.e., data that includes a time element derived from consideration of sequences of ontogenetic stages. Thus, the change noted in anatomy through ontogenetic time is ill handled by such methods.

Ronald Jenner again takes a look at methodological and epistemological issues in cladistic analysis of animal phylogeny, “Boolean logic and character state identity: pitfalls of character coding in metazoan cladistics.” The most common scoring of characters involves simple absence/presence determinations. However, this procedure has several problems. Chief of these is that the so-called “plesiomorphic absence” often entails several undefined alternative states. For example, the issue of spiral determinate cleavage [absent or present] is an excellent example. The traditional opposition to this state is posed to be radial indeterminate cleavage. However, as already noted, other possibilities exist. The scoring of an undefined absence thus masks a tremendous amount of truly significant information in sorting out the phylogeny of animals, and it suggests unique homology of unrelated and dissimilar morphologies. Indeed, this and other papers by Jenner have given us insight as to why we have such a forest of cladograms for the Metazoa and little consensus as to the phylogeny of the animal kingdom.

We might conclude with all the above that only molecules afford us the best opportunity to discern the lines of metazoan evolution. However, least we become too complacent, Maximilian Telford, provides a lesson on the limits of even those kinds of data, “Cladistic analysis of molecular characters: the good, the bad, the ugly.” Essentially, all the often recognized difficulties of morphological data placed in a cladistic matrix have their correspondences on the molecular side. This is not to state that nothing is sacred. It merely means that we need to abandon the obsession we have with finding absolute truth when we undertake analyses of metazoan, indeed any, phylogeny. We have to always keep in mind that all data is relative and is imbued with varying levels of subjectivity. In other words, we need to treat all data equally with more respect.

Frietson Galis and Barry Sinervo take up “Divergence and convergence in early embryonic stages of metazoans.” This subject is really a critical issue when trying to combine systematic analyses with the results of developmental gene research. So often we read in the literature about conserved genes or functions. Galis and Sinervo ask when are these phenomena due to true conservation, i.e., ho-mologies, and when are they merely homoplasies? Even then, it is sometimes difficult to sort out functional considerations from true genealogical matters. Care must be taken in pushing scenarios of evolution derived from developmental studies without framing discussions in a properly cast phylogenetic understanding.

Prof. van den Biggelaar and I had originally thought in the mid-1990s that we had an easy set of goals to achieve: sorting out the early ontogeny and evolution of protostomes, and set a master tree for metazoan phylogenetic relationships. Now we find that as our particular cooperative research program comes to an end, our goals are even more elusive than when we originally started out. Nevertheless, the work goes on.