Wonderful Ediacarans, wonderful cnidarians?

Abstract

In Wonderful Life, Stephen Jay Gould (1989) argued that the morphological range of arthropods recovered from the Middle Cambrian Burgess Shale fauna in British Columbia demonstrated that morphologic diversity increased more rapidly than taxonomic diversity. As was so often the case with Steve, he was directly challenging what he viewed as the unjustified assumptions of traditional evolutionary theory. Gould’s claim initially generated considerable controversy (Briggs et al. 1992), but Wonderful Life triggered the development of rigorous empirical approaches to quantifying what subsequently became known as morphological disparity. The past 18 years of disparity studies have confirmed that Gould was substantially correct: most clades, particularly from the Paleozoic, display patterns of maximal early disparity relative to taxonomic diversity (Foote 1997; Erwin 2007). Until recently, no one had examined disparity before the onset of the Cambrian diversification some 530Ma. In particular, no one had tried to quantify the morphological disparity of the enigmatic organisms of the Ediacaran Fauna (575–542Ma). However, thanks to a recent paper by Shen et al. (2008) we now know that this earliest assemblage of animals followed the same pattern of an early increase in morphologic disparity uncoupled from taxonomic diversity. Several years ago Waggoner (2003) recognized three discrete Ediacaran assemblages, being, in temporal sequence: a low-diversity Avalonian assemblage, a geographically widespread and high-diversity White Sea assemblage, and a lower diversity Nama assemblage. These three assemblages were originally thought to represent early, middle and late evolutionary phases of the Ediacaran interval. However, it now appears that although the three assemblages do indeed differ in mean age, the earliest, Avalonian elements may have persisted through much of the interval. Shen and his colleagues examined both the taxonomic diversity and morphologic disparity of these three assemblages. They assessed 50 different morphologic characters from some 270 species occurrences at about 30 different localities around the world. They used rarefaction analysis to standardize for differences in sampling, and constructed a morphospace with nonparametric multidimensional scaling. Despite considerable turnover in the genera present between the three assemblages, each assemblage occupied substantially the same region of morphospace. In other words, as with Cambrian arthropods and many other groups, the earliest, Avalonian Ediacaran assemblage established a morphospace that persisted for over 30 million years despite a more than 4-fold increase in taxonomic diversity. The disparity analysis of Shen and colleagues carefully avoids the controversial issue of the phylogenetic affinities of the Ediacaran organisms. Are they a single clade? Do they represent early elements of otherwise familiar groups such as arthropods (Parvancorina, Yorgia), annelids (Dickinsonia), mollusks (Kimberella), echinoderms (Tribrachidium), and cnidarians (the various frond-like forms)? Or are they multicellular forms unrelated to metazoa? Are they, perhaps, even related to lichens or to protozoa? All of these suggestions (and more!) have been made in the past two decades. The variety of perspectives reflects both the wide range of morphologies, including bilateral forms reminiscent of true Bilateria, and the lack of appendages, eyes, mouthparts, and many other useful phylogenetic characters. Perhaps the most intriguing new perspective on the Ediacara fauna comes not from the fossils themselves but from new studies of the development of living cnidarians. The recently sequenced Nematostella genome (Putnam et al. 2007) has confirmed earlier work suggesting that the cnidarian genome is more complex than expected, with gene numbers, structure and organization quite similar to vertebrates but unlike the protostome bilaterians (flies and nematodes). Whether cnidarians were primitively radially or bilaterally symmetrical has been the subject of debate for decades, but evidence that Hox, Dpp, Wnt, and Hh are involved in patterning the primary oral–aboral and secondary axes adds weight to the hypothesis of bilateral symmetry (Ryan and Baxevanis 2007; Matus et al. 2008). Indeed, cnidarians possess a host of genes whose bilaterial toolkit function is axial patterning or mesoderm formation (Harding et al. 2005). EVOLUTION & DEVELOPMENT 10:3, 263 –264 (2008)