Modern Phyla Research Articles

The advent of animals: The view from the Ediacaran

Patterns of origination and evolution of early complex life on this planet are largely interpreted from the fossils of the Precambrian soft-bodied Ediacara Biota. These fossils occur globally and represent a diverse suite of organisms living in marine environments. Although these exceptionally preserved fossil assemblages are typically difficult to reconcile with modern phyla, examination of the morphology, ecology, and taphonomy of these taxa provides keys to their relationships with modern taxa. Within the more than 30 million y range of the Ediacara Biota, fossils of these multicellular organisms demonstrate the advent of mobility, heterotrophy by multicellular animals, skeletonization, sexual reproduction, and the assembly of complex ecosystems, all of which are attributes of modern animals. This approach to these fossils, without the constraint of attempting phylogenetic reconstructions, provides a mechanism for comparing these taxa with both living and extinct animals.

Expression of Distal-less, dachshund, and optomotor blind in Neanthes arenaceodentata (Annelida, Nereididae) does not support homology of appendage-forming mechanisms across the Bilateria.

The similarity in the genetic regulation of arthropod and vertebrate appendage formation has been interpreted as the product of a plesiomorphic gene network that was primitively involved in bilaterian appendage development and co-opted to build appendages (in modern phyla) that are not historically related as structures. Data from lophotrochozoans are needed to clarify the pervasiveness of plesiomorphic appendage-forming mechanisms. We assayed the expression of three arthropod and vertebrate limb gene orthologs, Distal-less (Dll), dachshund (dac), and optomotor blind (omb), in direct-developing juveniles of the polychaete Neanthes arenaceodentata. Parapodial Dll expression marks pre-morphogenetic notopodia and neuropodia, becoming restricted to the bases of notopodial cirri and to ventral portions of neuropodia. In outgrowing cephalic appendages, Dll activity is primarily restricted to proximal domains. Dll expression is also prominent in the brain. dac expression occurs in the brain, nerve cord ganglia, a pair of pharyngeal ganglia, presumed interneurons linking a pair of segmental nerves, and in newly differentiating mesoderm. Domains of omb expression include the brain, nerve cord ganglia, one pair of anterior cirri, presumed precursors of dorsal musculature, and the same pharyngeal ganglia and presumed interneurons that express dac. Contrary to their roles in outgrowing arthropod and vertebrate appendages, Dll, dac, and omb lack comparable expression in Neanthes appendages, implying independent evolution of annelid appendage development. We infer that parapodia and arthropodia are not structurally or mechanistically homologous (but their primordia might be), that Dll’s ancestral bilaterian function was in sensory and central nervous system differentiation, and that locomotory appendages possibly evolved from sensory outgrowths.

Trace fossils and the Cambrian explosion

In two recent contributions to TREE[1xThomas, A.R.L. Trends Ecol. Evol. 1998; 13: 129Abstract | Full Text | Full Text PDF | PubMedSee all References, 2xThomas, A.R.L. Trends Ecol. Evol. 1998; 13: 322Abstract | Full Text | Full Text PDF | PubMedSee all References], Thomas has argued that trace fossils (trails, burrows, etc.) support deep Precambrian divergence of metazoans, and concludes that the Cambrian explosion is a taphonomic event of the appearance of hard parts. Speaking from experience, he calls upon `Ediacaran' sites in Sweden said to have beautifully preserved the Precambrian sea floor with an `astonishing abundance of trace fossils'. This would be indeed compelling evidence—except that there are no Ediacaran sites in Sweden. Reference to the occurrence of Psammocorallia, however, shows that Thomas is thinking of the Mickwitzia sandstone[3xJensen, S. Fossils & Strata. 1997; 42: 1–110See all References[3]. This unit is actually late Early Cambrian. In fact, there are no convincing trace fossils anywhere in the world older than 600 Ma (Ref. [4xSee all References[4]) and all moderately diverse terminal Proterozoic trace fossil assemblages may be younger than 550 Ma (Ref. [5xGrotzinger, J.P. et al. Science. 1995; 270: 598–604CrossrefSee all References[5]).Trace fossils do not suffer from the same taphonomic peculiarities that complicate arguments about the nature of the soft-bodied Ediacara-type fossils. Unless contrived ad hoc hypotheses are to be invoked, it may thus be safely assumed that their appearance marks the appearance of macroscopic bilaterians.Additionally we would like to comment on the frequently-aired hypothesis of cryptic evolution of miniature Precambrian metazoans[6xFortey, R.A., Briggs, D.E.K., and Wills, M.A. BioEssays. 1997; 19: 429–434CrossrefSee all References, 7xCooper, A. and Fortey, R. Trends Ecol. Evol. 1998; 13: 151–156Abstract | Full Text | Full Text PDF | PubMed | Scopus (119)See all References]. In this scheme the Cambrian explosion is seen as little more than an increase in size and, in some groups, the acquisition of hard parts, in already well-separated lineages. However, such miniature stem-group animals would have faced extremely different ecological conditions to macroscopic animals, and it is difficult to see how many of the shared morphological features of the modern phyla—such as blood vascular systems[8xRuppert, E.E. and Carle, K.J. Zoomorphology. 1983; 103: 193–208Crossref | Scopus (54)See all References[8]and body cavities—could have been functionally useful in such a setting. Either these features were acquired in an avalanche of convergence in the separate lineages, or—much more likely—characters that are used to define eumetazoan phyla appeared in the latest Vendian–Cambrian and in most cases even later. This in turn would imply that the cladogenesis leading to the modern phyla is indeed accurately reflected by the increase in diversity of trace and body fossils from the latest Vendian to the Cambrian, a gradual process taking at least 20 million years. We conclude that `accurate' analysis of the fossil evidence strongly suggests the Cambrian explosion is a reality representing the origins of first stem-group and then crown-group members of the Bilateria.

Reply from R. Fortey and A. Cooper

Budd and Jensen have pointed out once again the importance of negative evidence in the interpretation of the so-called Cambrian evolutionary `explosion'. They regard lack of Precambrian body and trace fossils as indicating the evolution of metazoan body plans within 20 million years of post-Vendian time. They criticize hypotheses of Precambrian origins of metozoan phyla as `ad hoc', and reject the idea that Precambrian ancestors were small and lacked hard parts (hence rare as fossils): `it is difficult to see how the shared morphological features of the modern phyla could have been functionally useful' in a Precambrian setting.What Budd and Jensen fail to acknowledge is evidence from the living fauna relevant to early history of animal phyla. The most primitive living members of phyla are very small animals that lack preservable hard parts[1xSee all References][1]. The aplacophoran molluscs are small; so are the tardigrades, a group that is increasingly understood as a likely sister group to the higher arthropods[2xSee all References][2]; the ctenostome bryozoans occupy a similar position in lophophorates; Cephalodiscus may be comparable among hemichordates. We can identify no reason why any of these animals should not have been functionally viable in the late Precambrian. Since early Cambrian phyla are already differentiated into several body designs (`Classes'), an earlier history of differentiation at small size is plausible, and supported by the living fauna.Independent evidence on Precambrian history of major metazoan groups is derived from phyletic divergence times obtained from molecular sequence studies of proteins and DNA[3xWray, G.A., Levinton, J.S., and Shapiro, L.H. Science. 1996; 274: 568–573Crossref | Scopus (351)See all References][3]. These studies are seldom uncontroversial, and all are vulnerable to criticisms concerning the reliability of molecular `clocks'. But as more and more evidence from different parts of the genome converges on deep divergence times the possibility of biases due to methodology or insufficient data becomes less plausible. Recent studies by Bromham et al.[4xSee all References][4]and others have sought to counter earlier criticisms levelled at such analyses through more critical methods of detecting rate variation and calculating realistic confidence intervals around divergence dates[5xRambaut, A. and Bromham, L.D. Mol. Biol. Evol. 1998; 15: 442–448Crossref | PubMedSee all References][5]. Regardless of method, all studies show divergence between major groups (e.g. protostomes and deuterostomes) as before about 700 million years ago, thus adding 150 million years to the potential time for differentiation of phyla.If these figures are even broadly correct it suggests that field palaeontologists should concentrate their search for hints of early metazoan life in rocks of these particular ages. The recent discovery of late Precambrian metazoan embryos[6xXiao, S., Zhang, Y., and Knoll, A. Nature. 1998; 391: 553–554Crossref | Scopus (455)See all References][6]indicates that this search may not be fruitless, difficult though it will undoubtedly be. By contrast, Budd and Jensen's hypothesis is discouraging of such a creative field approach. It is worth remembering that it is not many decades since a search in the Precambrian for any fossils was regarded as a foolish pastime. In the face of suggestive evidence, let's not make that mistake again.