Metazoan Complexity Research Articles

New Perspectives on the Origin of Metazoan Complexity: An Introduction to the Symposium

New Perspectives on the Origin of Metazoan Complexity: An Introduction to the Symposium

The Origin of Metazoan Complexity: Porifera as Integrated Animals

Sponges [Porifera] are the phylogenetically oldest metazoan phylum still extant today; they share the closest relationship with the hypothetical common metazoan ancestor, the Urmetazoa. During the past 8 years cDNAs coding for proteins involved in cell-cell- and cell-tissue interaction have been cloned from sponges, primarily from Suberites domuncula and Geodia cydonium and their functions have been studied in vivo as well as in vitro. Also, characteristic elements of the extracellular matrix have been identified and cloned. Those data confirmed that all metazoan phyla originate from one ancestor, the Urmetazoa. The existence of cell adhesion molecules allowed the emergence of a colonial organism. However, for the next higher stage in evolution, individuation, two further innovations had to be formed: the immune- and the apoptotic system. Major defense pathways/molecules to prevent adverse effects against microbes/parasites have been identified in sponges. Furthermore, key molecules of the apoptotic pathway(s), e.g., the pro-apoptotic molecule comprising two death domains, the executing enzyme caspases, as well as the anti-apoptotic/cell survival proteins belonging to the Bcl-2 family have been identified and cloned from sponges. Based on these results-primarily obtained through a molecular biological approach-it is concluded that cell-cell- and cell-matrix adhesion systems were required for the transition to a colonial stage of organization, while the development of an immune system as well as of apoptotic processes were prerequisites for reaching the integrated stage. As the latter stage already exists in sponges, it is therefore likely that the hypothetical ancestor, the Urmetazoa, was also an "integrated colony."

Bridging Morphological Transitions to the Metazoa

Our inability to answer many questions regarding the development of metazoan complexity may be due in part to the prevailing idea that most eukaryote "phyla" originated within a short period of geologic time from simple unicellular ancestors. This view, however, is contradicted by evidence that larger groups of eukaryotes share characters, suggesting that these assemblages inherited characters from a common ancestor. Because molecular analyses have had limited success in resolving the relationships of higher eukaryote taxa, we have undertaken a phylogenetic analysis based primarily on morphological characters. The analysis emphasizes characters considered to have a high probability of having evolved only once. Transitions between taxa are evaluated for the likelihood of character-state transformations. The analysis indicates that the evolutionary history of the clade containing the Metazoa has been complex, encompassing the gain and loss of a secondary and perhaps a primary photosynthetic endosymbiont with accompanying changes in trophic level. The history also appears to have included a hetero-autotrophic ancestor that possessed a "conoid" feeding apparatus and may have involved a transformation from a flagellate to an amoeboid body form, a trend toward increased intracellular compartmentation, and the development of complex social behavior. Such changes could have been critical for establishing the underlying complexity required for a rapid diversification of cell and tissue types in the early stages of metazoan evolution.

Epithelium--The Primary Building Block for Metazoan Complexity

In simplest terms, the complexity of the metazoan body arises through various combinations of but two tissue types: epithelium and mesenchyme. Through mutual inductions and interactions, these tissues produce all of the organs of the body. Of the two, epithelium must be considered the default type in the Eumetazoa because it arises first in embryonic development and because mesenchyme arises from it by a switching off of the mechanisms that underly differentiation and maintenance of epithelial cells. In the few model metazoans whose epithelia have been studied by molecular techniques (largely Drosophila, Caenorhabditis, mouse), the molecular mechanisms underlying differentiation of epithelia show remarkable similarity. Extrapolating from these studies and from comparisons of the morphology of epithelia in lower metazoans, I propose how epithelia arose in the stem metazoan. Steps in epithelial differentiation include 1) establishment of cell polarity by molecular markers confined to either apical or basolateral domains in the plasma membrane; 2) aggregation of cells into sheets by localization of cell-adhesion molecules like cadherin to the lateral membrane; 3) formation of a zonula adherens junction from the cadherins by their localization to a discrete belt; 4) cell-to-cell linking of certain transmembrane proteins (primitively in the septate junction) to produce gates that physiologically isolate compartments delimited by the cells; and 5) synthesis of a basal lamina and adaptation of receptors (integrins) to its components. Despite morphological differences in the variety of cell junctions evident in various epithelia, the underlying molecular markers of these junctions are probably universally present in all eumetazoan epithelia.

Two genomic paths to the evolution of complexity in bodyplans

Morphologically complex metazoans appear abruptly during the Cambrian explosion. Suggested measures of metazoan complexity include number of cell morphotypes and aspects of the genome such as the amount of DNA, the number of genes, and the information content of the genome or egg. Estimates of gene numbers are now available for metazoan species belonging to five different phyla or subphyla. There is little correlation between gene number and morphological complexity in the invertebrates: relatively complex forms can have fewer genes than relatively simple forms. Presumably, the more complex forms use more gene-expression events during development, implying that, on average,cis-regulatory elements of more complex invertebrates are richer in binding sites than are those of simpler forms. Vertebrates have many more genes than invertebrates and therefore have more total gene-expression events during development, although they may have, on average, fewer expression events per gene than the invertebrates. There are thus two genomic pathways in the evolution of metazoan complexity: one involves increasing the number of genes, the other involves increasing the number ofcis-regulatory binding sites. Both modes were associated with the origin of bodyplans that first appear as fossils during the Cambrian explosion.

The Taxonomy of Developmental Control in Caenorhabditis elegans

The Caenorhabditis elegans genome sequence was surveyed for transcription factor and signaling gene families that have been shown to regulate development in a variety of species. About 10 to 25 percent of the genes in most of the gene families already have been genetically analyzed in C. elegans, about half of the genes detect probable orthologs in other species, and about 10 to 25 percent of the genes are, at present, unique to C. elegans. Caenorhabditis elegans is also missing genes that are found in vertebrates and other invertebrates. Thus the genome sequence reveals universals in developmental control that are the legacy of metazoan complexity before the Cambrian explosion, as well as genes that have been more recently invented or lost in particular phylogenetic lineages.

Perspective: Metazoan Complexity and Evolution: Is There a Trend?

Perspective: Metazoan Complexity and Evolution: Is There a Trend?