What are lower metazoans and lesser deuterostomes?

Introduction

The Metazoa, today taken as a synonym of Animalia, comprises a large grouping of organisms that may be characterized as being multicellular and heterotrophic, i.e., they do not synthesize their own food, but obtain it from external sources. While there has been some debate in the past, it now seems overwhelmingly likely that the metazoans are monophyletic, and thus that all living examples are descended from an animal that lived some time in the Proterozoic (probably at least 600 million years ago [mya]). Even this statement is controversial, however. Molecular evidence suggests that metazoans had emerged up to one billion years ago or more; but the fossil record is most reasonably read as implying a much later origin, with definitive metazoans not appearing before 600 mya, and perhaps even later. Unfortunately, most "lower" metazoans today lack substantial hard parts such as mineralized shells, so their fossil record is correspondingly very poor. Telling the true time of appearance of such animals just from the fossil record may therefore well be inaccurate.

Animal evolution

Because of their long history and enormous adaptability, animals are organized in a remarkable number of different ways, ranging from simple sponges with only a few cell types through to the vertebrates with their complex nervous and immune systems. Indeed, it is possible to arrange animals in a broad series, from organisms that do not possess true tissues (e.g., sponges), through organisms with tissues but no organs (e.g., cnidarians), into the bilaterally symmetrical animals (the Bilateria) with both. The Bilateria typically also possess a central nervous system and muscles; some of them are segmented; and some possess a body cavity called a coelom.

The evolution of the animals has long been a contentious issue that has generated a huge number of theories. Nevertheless, at the heart of the issue is whether or not the organizational gradient that can be erected tells anything at all about animal evolution, or whether it merely reflects different adaptive needs of each organism. To put it more simply: are all the simple animals more basal than the more complex ones, or is animal evolution less tidy than that? The traditional assumption has been that organization is indeed a reflection of animal relationships and evolution, although the more thoughtful authors have refrained from definitively stating this. In this view, it makes sense to talk about animal evolution being a more or less stately progress from simple to complex; thus, one can label the simple animals, which are at the bottom of the tree, the "lower" metazoans, and the more advanced ones, the "higher" metazoans. To be more precise, animals without coeloms or segments are typically thought of as being "lower." These sorts of organisms show a variety of functional adaptations. Sponges and cnidarians typically have some sort of central fluid-filled cavity, which is critical to many roles including support, nutrition, excretion, and reproduction. Small bilaterians, on the other hand, have typically no need of any such system, as they are small enough to

allow diffusion directly to and from the body tissues. Although lower metazoans by the definition here lack a true coelom, which can be used as a hydrostatic skeleton, such a tack is replaced either by the use of a rather solid array of muscles, or by some other type of body cavity, such as the so-called pseudocoelom. It should be stressed that this "lower" terminology is a remnant of certain types of eighteenth century views of the world that are in many ways entirely inappropriate to the modern evolutionary ways of thinking about animals. Furthermore, modern systematic practice forbids the use of taxonomic units that are defined by exclusion—lower metazoans defined by being everything except the higher metazoans, which are usually taken as deuterostomes, arthropods, mollusks, and perhaps annelids, together with their close allies. Nevertheless, the central issue of the relationship of overall form to evolution remains unsolved, and, indeed, has been in hot contention since the last years of the twentieth century.

The debate has become sharp because of the introduction of entirely new sources of data that have bearing on the problem, i.e., evidence from molecules. Analysis of the nucleic acids allows a view of animal evolution that is completely, or largely, independent from that provided by classical morphological studies, and the results have sometimes been surprising. The sponges, with their relatively poorly organized morphology, remain basal within the tree, followed by the cnidarians (jellyfish, corals, and allies) and the ctenophores (the comb jellies), although the exact relationships between these three is contentious. All other animals fall into the Bilateria, but the relationships within this group remain highly debated. On a strictly "progressionist" view, the most basal bilaterians would be the flatworms, followed by animals that possess a body cavity that is not fully bounded by mesodermally derived epithelium (i.e., the coelom), followed by the coelomates themselves. However, this view, prevalent among scientists in Great Britain and the United States until a few years ago, was always rejected by many zoologists in Germany

and elsewhere. In their view, the basal metazoans already possessed a coelom and segments, and the bilaterians that lack these features have therefore lost them secondarily. Therefore, there are at least two radically differing views of what a "lower metazoan" is, at least as applied to the bilaterians: one, a relatively simple organism with no through-gut, blood vascular system, or coelom, and another with all of these features present.

The advent of molecular systematics has had a dramatic effect on the view of animal relationships, especially within the Bilateria. Two important features stand out. First, the group of lower metazoans referred to collectively as pseudocoelomates, possessing a body cavity that does not fall under the definition of the coelom, is seen to be a highly heteregeneous group. The most surprising aspect of their reassignment has been the proposal that some of them, notably the nematodes and priapulids, are close relatives to the arthropods (forming the Ecdysozoa), displacing the annelids that are traditionally placed in this position. Secondly, at least some of the flatworms have been largely displaced from the base of the tree to form a group loosely related to the annelids and mollusks in a remnant of one of the old branches of the bilaterians, the protostomes. Both these developments lend support to the idea that the ancestral bilaterians were rather complex. Nevertheless, at least some of the flatworms, the acoels, have now been reinstated at the base of the tree. Are their simple features primitive for all of the bilaterians, or have they simply lost their

complex features, as have the other flatworms by implication of their higher position? One further line of evidence has come from the shared developmental mechanisms between the bilaterians. Genes that control the layout of the complex morphology, including segments, eyes, and the development of the heart, are all highly conserved between the "higher" metazoans such as the arthropods and chordates. The implication is that these genes are present in the lower bilaterians (and indeed, this has been shown in some cases), and that they may originally have functioned as they do today—implying the very deep origin of the structures these genes now regulate. Such conclusions are controversial, and have by no means been accepted by all, especially morphologists.

Summary

The lower metazoans comprise animals that are thought to lie relatively close to the evolutionary root of animals as a whole. While they all have their own specializations, it is possible, and to be hoped for, that they retain some features that were characteristic of the very earliest stages of metazoan and bilaterian evolution. Although it is widely accepted that the sponges are basal within the animals, broadly followed by the ctenophores and cnidarians, the relationships of the bilaterians remain highly controversial. Molecular systematics places the bilaterians into three groups: the Deuterostomia (including, among others, echinoderms and chordates); the Ecdysozoa (principally arthropods and nematodes), and the Trochozoa (annelids, mollusks, most flatworms, and several other small groups, including the brachiopods). At least one group of the flatworms may still be basal within the bilaterians, but the implications this position may have for the evolution of the lower metazoans are presently unclear. The fundamental questions about bilaterian evolution, including the origin of the coelom and segmentation, remain unanswered, and, indeed, as vigorously contested as ever.

Resources

Books

Nielson, C. Animal Evolution: Interrelationships of the Living Phyla. Oxford: Oxford University Press, 2001.

Periodicals

Budd, G. E., and S. Jensen. "A Critical Reappraisal of the Fossil Record of the Bilaterian Phyla." Biological Reviews 75 (2000): 253–295.

Graham Budd, PhD