PLoS Biology | www.plosbiology.orgPLoS Biology | www.plosbiology.org0029January 2009 | Volume 7 | Issue 1 | e1000007PrimerA New Look at Some Old AnimalsNeil W. BlackstoneWhen teaching an introductory zoology course, it is always entertaining to show students some specimens of the only described species of placozoans—Trichoplax adhaerens, a tiny, simple, nearly worldwide marine organism (Figure 1) [1,2]. The inevitable disbelief—those are animals?—leads naturally to enumerating the shared derived features of all animals (Box 1) and in turn to discussing the relationships among the various groups at the base of the animal or “metazoan” tree of life. These early diverging or “basal” groups include bilaterians, the bilaterally symmetric forms that most students recognize as animals—worms, flies, mice, and many more. Most students are also familiar with cnidarians—corals, anemones, jellyfish, hydroids—and perhaps even with sponges, known for their soft and porous skeletons. Less familiar are the ctenophores—comb jellyfish—and the enigmatic placozoans. How these five groups fit together at the root of the metazoan tree is a matter of intense debate and considerable study. Indeed, the ordering of the divergence of these basal groups affects our inferences of the features of the common ancestor of all animals. This in turn influences our understanding of the evolution of all animal characteristics, whether molecular, physiological, or morphological.Placozoans and the Root of the Metazoan TreeOf the five groups, the position of the placozoans has perhaps been the most contentious. They are clearly animals by virtue of having four somatic (i.e., non-reproductive) cell types—cover, cylinder, gland, and fiber cells [1,2]. All other animals, however, have many more somatic cell types. Further, the cell-level dynamics of Trichoplax are unusual. While cylinder cells may give rise to gland cells, otherwise the three major cell types (cover, cylinder, and fiber) give rise to their own cell type and none other during growth and reproduction. In contrast to other early diverging animals, placozoans do not seem to have a stem cell lineage that gives rise to more than one cell type (but see [2] for further discussion). Although the process is incompletely studied, placozoans do form germ cells, apparently from the somatic cells of the lower epithelium [1]. Cells are organized into two surface layers—a functional lower and upper side. Both cell layers lack underlying “basal lamina”—an extracellular matrix on which the cells sit—or other traces of such a matrix. These microscopic structures are found in all other animals [1–3]. Both sides of a placozoan are covered with flagella, with a higher density on the lower side. Morphologically, a living Trichoplax resembles a small, often highly irregular “plate” of cells, 2–3 mm in diameter, moving by means of flagella and constantly changing in outline (Video S1). Individuals are free-living and heterotrophic, but their natural history remains poorly known [4].When considering such a creature, biologists must try to determine whether the observed simplicity is primary or secondary. In other words, was the evolutionary lineage leading to Trichoplax always highly simplified, or is Trichoplaxthe simplified descendent of a more complex ancestor? The latter situation is commonly found in many parasitic species but is considerably less common in free-living ones. In the late 19th century, the first descriptions of Trichoplaxsuggested that it exhibited primary simplicity [2]. This view was enthusiastically incorporated into “scenario-based” views of animal evolution, in which biological observations are synthesized into plausible historical narratives. In particular Otto Bütschli developed the “placula hypothesis,” which featured a Trichoplax-like organism as the ancestor of all animals [2]. As with other animals, of course, modern placozoans are separated from such an ancestor by perhaps a billion years of evolution. Many features of modern Trichoplaxmay thus differ from such a putative ancestor.By the early 20th century, however, the view of Trichoplaxas secondarily simplified became widely accepted. For some time, placozoans were classified as degenerate cnidarian larvae (see [5] for discussion). While careful study of the morphology in fact provides little support for this notion [3,5], in the case of such divergent opinions it is often helpful to look at other sources of information. Indeed, by the late 20th century DNA sequence data became widely available. Such data are particularly helpful with simple organisms such as Trichoplax, which exhibit relatively few morphological characters. Also by this time, considerably more rigorous methods had been developed for evaluating phylogenetic Citation: Blackstone NW (2009) A new look at some old animals. PLoS Biol 7(1): e1000007. doi:10.1371/journal.pbio.1000007Copyright: © 2009 Neil W. Blackstone. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.Neil W. Blackstone is with the Department of Biological Sciences, Northern Illinois University, DeKalb, Illinois, United States of America. E-mail: [email protected] 1. Characteristics of AnimalsAnimals or “metazoans” are typically heterotrophic, multicellular organisms with diploid, eukaryotic cells. They are defined by a number of features, including several related to gamete formation and structure [3]. Since the life cycle of Trichoplax is incompletely known, these characteristics are of little use in this context. Presence of a collagenous extracellular matrix is often used to define animals; in the case of Trichoplax,the absence of such a matrix would then have to be interpreted as a secondary loss [3]. Animals, however, are also defined by the presence of different somatic (i.e., non-reproductive) cell types and by impermeable cell–cell connections. By these criteria, Trichoplax are animals, while related multicellular protists (e.g., choanoflagellates) are not.Primers provide a concise introduction into an important aspect of biology highlighted by a current PLoS Biology research article.PLoS Biology | www.plosbiology.orgPLoS Biology | www.plosbiology.org0030January 2009 | Volume 7 | Issue 1 |
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