Chapter 10 Origin of the metazoans Key points • Relatively few basic body plans have appeared in the fossil record; most animals have a triploblastic architecture, with three fundamental body layers. • Molecular data show there are three main groupings of animals: the deuterostomes (echinoderm–hemichordate–chordate group), the spiralians (mollusk–annelid– brachiopod–bryozoans–most fl atworms–rotifers (platyzoans) group) and the ecdysozo- ans (arthropod–nematode–priapulid plus other taxa group). Together, the spiralians and ecdysozoans are usually called the protostomes. • Five lines of evidence (body fossils, trace fossils, fossil embryos, the molecular clock and biomarkers) suggest that the metazoans had originated prior to the Ediacaran, 600 Ma. • Snowball Earth by coincidence or design was a pivotal event in metazoan history; bila- terians evolved after the Marinoan glaciation. • The fi rst metazoans were probably similar to the demosponges, occurring fi rst before the Ediacaran. • The Ediacaran biota was a soft-bodied assemblage of organisms largely of uncertain affi nities, reaching its acme during the Late Proterozoic, which may represent the earliest ecosystem dominated by large, multicellular organisms. • The Tommotian or small shelly fauna was the fi rst skeletalized assemblage of metazoans; this association of Early Cambrian microfossils contains a variety of phyla with shells or sclerites mainly composed of phosphatic material. • The Cambrian explosion generated a range of new body plans during a relatively short time interval. • The Ordovician radiation was marked by accelerations in diversifi cation at the family, genus and species levels together with increased complexity in marine communities. Consequently, if my theory be true, it is indisputable that before the lowest Silurian [Cambrian of modern usage] stratum was deposited, long periods elapsed, as long as, or probably far longer than, the whole interval from the Silurian age to the present day; and that during these vast, yet quite unknown, periods of time, the world swarmed with living creatures. Charles Darwin (1859) On the Origin of Species ORIGIN OF THE METAZOANS 235 ORIGINS AND CLASSIFICATION The fi rst metazoans: when and what? When did the fi rst complex animals, the meta- Life on our planet has been evolving for nearly zoans, appear on Earth and what did they 4 billion years. Molecular data suggest meta- look like? How could complex, multicelled zoans have probably been around for at least animals evolve from the undifferentiated 600 myr (Fig. 10.1), during which time, single-celled organisms of most of the Pre- according to some biologists, as many as 35 cambrian? Why did they take almost 4 separate phyla have evolved. Five lines of evi- billion years to appear? These questions have dence have fi gured prominently in the search puzzled scientists, including Charles Darwin, for the earliest metazoans: body fossils, trace for over two centuries. In the last few decades fossils, fossil embryos, the molecular clock a range of multidisciplinary techniques, from and biomarkers. molecular biology to X-ray tomography, has Much controversy still surrounds the timing helped generate new testable hypotheses of their origin. Was there a long cryptic inter- regarding the origins of our early ancestors. val of metazoan evolution prior to the Edia- Apart from the fossil evidence of metazoan caran – a time when we do not fi nd fossils body and trace fossils, the investigation of preserved, either because the animals lacked minute fossil embryos, carefully calibrated preservable bodies, or they were small, or molecular clocks and more recently biomark- perhaps a combination of both? Or, as the ers have placed the investigation of Precam- recalibrated molecular clocks suggest, can brian life at the top of many scientifi c animal origins be tracked back only to the agendas. Ediacaran, when there was also a sudden rise C Crinozoa 535 Eleutherozoa 200 metazoan orders Hemichordata metazoan classes C Pteriomorpha 604 molecular clock estimates C Nuculoida 160 C molecular clock calibration 579 C Vetigastropoda feeding larva 545 non-feeding larva Sorbeochoncha Oman biomarker record 549 493 Phyllodicida 120 Spionidea + Serpulidea 604 561 494 Hoplonemertea Heteronemertea 80 634 546 Arthropoda EcdysozoaPriapulida Spiralia Deuterostomia Number ofNumber classes/orders 543 Anthozoa 40 664 Hydrozoa Cnidaria Calcispongia Demospongia “Porifera” N-D T AB/T MMLateEarly Late Cryogenian Ediacaran Early Cambrian Ordovician 700 635 600 575 555 542 513 501 488 472 461 443 Ma Figure 10.1 Time scale and tempo of early animal evolution: the key metazoan groups are shown with the putative age of their last common ancestor, together with an estimate of the respective numbers of classes and orders indicated against a stratigraphy indicating key biological and chemical events. N–D, Nemakit-Daldynian; T, Tommotian; A, Atdabanian; B/T, Botomian. (Courtesy of Kevin Peterson.) 236 INTRODUCTION TO PALEOBIOLOGY AND THE FOSSIL RECORD in oxygen levels in the deep ocean (Canfi eld et al. 2007). Body fossil evidence Body fossils of basal metazoans in the Edia- caran Period are few and far between. The morphology of an early metazoan fossil must be clearly described and convincingly illus- trated, different organs and tissues identifi ed, and comparisons drawn with other extant and fossil organisms. Many Upper Precam- brian successions have been subjected to intense metamorphism and tectonism (see p. 48) and are now located in some of the Earth’s mountain belts. The chances of fi nding ade- Figure 10.2 Putative trace fossils from the quately preserved fossils are slight. Neverthe- Precambrian of Australia, showing less, the earliest undoubted metazoans occur Myxomitodes, a presumed trail of a mucus- within the widespread Ediacara biota (see p. producing multicellular organism about 1.8–2 242) dated at approximately 600–550 Ma. billion years old from Stirling Range, Western Moreover the fact that a relatively advanced Australia. (Photo is approximately 65 mm wide.) metazoan, the mollusk Kimberella, possibly (Courtesy of Stefan Bengtson.) equipped with a foot and radula (see p. 330), occurs within the Ediacara biota from south- trace fossils are from about 550 Ma (Droser ern Australia and Russia could suggest a et al. 2002) from northwest Russia, whereas history of metazoan evolution prior to the fecal strings have been reported from rocks Ediacaran. But although a strong case can be some 600 Ma (Brasier & McIlroy 1998) sug- made for a signifi cant Proterozoic record for gesting the existence of an ancient digestive the cnidarians and sponges and perhaps some system. In fact no convincing trace fossils are other metazoans, the Cambrian explosion still known from successions older than the Mari- marks the arrival, center stage, of the bilateri- noan glaciation (635 Ma), the second main ans (Budd 2008). icehouse event associated with snowball Earth (see p. 112). Trace fossil evidence Embryo fossil evidence Trace fossils are the behavior of organisms recorded in the sediment (see p. 510). By their Fossil Neoproterozoic embryos are now very nature they occur in place and thus known from a number of localities, although cannot be transported or reworked by cur- claims that they represent sulfur-oxidizing rents. Nevertheless these too must be convinc- bacteria or that they are not embryos at all ingly demonstrated as biogenic and the age of have their advocates. Some of the best studied their enclosing sediments accurately deter- examples are from the Doushantuo Forma- mined. If and when metazoans developed tion, South China. The part of the formation locomotory organs, such as the molluskan yielding the embryos was fi rst dated at approx- foot, and digestive systems, we might expect imately 580 Ma, predating much of the Edia- to fi nd burrows and trails together with fecal caran but postdating the Marinoan glaciation. pellets. Records of trace fossils from rocks Revised dates seem to suggest that the faunas older than 1 Ga in India (Seilacher et al. 1998) are younger and that they overlap with the and over 1.2 Ga in the Stirling biota of Aus- older Ediacaran assemblages. Cell division tralia (Rasmussen et al. 2002) generated and cleavage patterns are obvious although it considerable excitement (Fig. 10.2). Both is diffi cult to assign the material to distinct suggested metazoan life older than 1 Ga but metazoan groups in the absence of juvenile both are now considered questionable (Jensen and adult forms. There are, however, a lack 2003). The oldest undoubted locomotory of epithelia even in clusters of over 1000 cells ORIGIN OF THE METAZOANS 237 suggesting that the embryos examined are sial. For example, the last common ancestor those, at best, of stem-group metazoans of the bilaterians, the metazoan clade exclud- (Hagadorn et al. 2006); they could equally ing the sponges and cnidarians, has been vari- well be fungi or rangeomorphs (enigmatic ously placed at anywhere between 900 and frond-like fossils). Nonetheless the Doushan- 570 Ma. Why is there such a spread of ages tuo embryos, although unplaced taxonomi- in a seemingly exact science? The rates of cally, provide our earliest body fossil evidence molecular evolution in various groups are for probable metazoan life, albeit very basal, unfortunately not constant. The vertebrates and a fascinating insight into embryologic appear to have reduced their rates of molecu- processes in deep time (Donoghue 2007) lar change through time. So, using the slow (Box 10.1). vertebrate rates of molecular evolution to calibrate the date of origin of Bilateria gives dates that are too ancient (900 Ma). On the Molecular evidence other hand, using mean bilaterian rates of molecular evolution gives a date (570 Ma) Not only have the morphologies of organisms that is more in keeping with evidence from evolved with time, but so too have their mol- the fossil record (e.g. Budd & Jensen 2000) ecules. This forms the basis of the concept of and thus makes the Cambrian explosion much the molecular clock (see p. 133).