Sea urchins (Echinoidea) Andrew B. Smith (Euechinoidea), and this division is reP ected at the Department of Palaeontology, The Natural History Museum, subclass level (1, 2). Cidaroids and euechinoids diB er Cromwell Road, London SW7 5BD, UK ([email protected]) in their style of ambulacral plating, and have diB erent jaw apparatus morphologies and musculature. Whereas cidaroids remained rather conservative in their morph- Abstract ology, the euechinoids have given rise to a wide diver- The Echinoidea (sea urchins) is one of the fi ve classes of the sity of forms (3), currently classiA ed into 13 orders. 7 ere Phylum Echinodermata and includes ~900 living species are a number of small, early branching groups but about in 50 families. Their traditional taxonomy, based on skel- 80% of the modern diversity lies in two major clades, the etal characters, has been largely corroborated by recent Irregularia and the Echinacea. Irregular echinoids are so molecular phylogenetic analyses with one marked excep- named because their pentameral symmetry is disrupted tion: clypeasteroids are not found to be monophyletic. The by migration of the anus from an apical to a poster- echinoid timetree deduced from molecular data is largely ior position during ontogeny, and most live infaunally. concordant with the fossil record, placing the basal diver- Echinacea are regular echinoids with a derived lantern gence in the late Paleozoic (265 million years ago, Ma). morphology and keeled teeth and all are epifaunal. Echinoids diversifi ed during the Mesozoic (251–66 Ma) and 7 e classiA c at ion of t he E ch i nacea ha s been pa r t ic ula rly there is a good match between paleontological and molecu- di1 cult and relies on small diB erences rarely preserved lar estimates of divergence times, with clypeasteroids again in fossils (4). 7 e taxonomy of irregular echinoids, on proving to be an exception. the other hand, has been much less problematic with the long-standing major groups (spatangoids, holasteroids, 7 e Phylum Echinodermata is a clade of marine inverte- clypeasteroids, and cassiduloids) readily diB erentiated brate deuterostomes that includes such well-known ani- mals as the starA shes and sea urchins. All echinoderms possess a calcitic endoskeleton with a distinctive and unique three-dimensional structure, a stereom, and they all undergo an unusual asymmetrical development in which right larval coelomic components are suppressed and lost. 7 ere are A ve living classes of echinoderm, of which the Echinoidea or sea urchins (Fig. 1) is probably the best known and certainly the one that has leJ the most complete fossil record. Living echinoids have a mesoder- mal skeleton constructed of 10 columns of plates, all of which bear tubercles and spines. 7 e modern taxonomy of echinoids was established by Mortensen (1), based primarily on the detailed arrangement of plates making up the skeleton. 7 is has the great advantage of allow- ing fossils to be placed with conA dence into any taxo- nomic scheme constructed for the living species. About 900 living species of echinoids have been described and placed in ~50 families (1, 2), not all of which are consid- ered monophyletic. Here, I review the relationships and divergence times of the major echinoid groups. It has long been recognized that the cidaroids dif- Fig. 1 An echinoid (Arbacia punctulata) from Carrie Bow Cay, fer in several fundamental ways from other echinoids Belize, viewed from above. Credit: A. B. Smith. A. B. Smith. Sea urchins (Echinoidea). Pp. 302–305 in e Timetree of Life, S. B. Hedges and S. Kumar, Eds. (Oxford University Press, 2009). HHedges.indbedges.indb 330202 11/28/2009/28/2009 11:27:52:27:52 PPMM Eukaryota; Metazoa; Echinodermata; Echinoidea 303 Temnopleuridae 15 Genocidaridae 26 Toxopneustidae 12 Strongylocentrotidae 20 Echinidae Camarodonta 7 19 Echinacea Echinometridae Stomopneustidae 11 Arbaciidae Spatangidae 24 Loveniidae 21 Archaeopneustes 25 16 Brissidae 5 Paleopneustidae Spatangoida 9 18 Schizasteridae Acroechinoidea Acroechinoidea Plexechinidae Astriclypeidae 17 Irregularia 8 Mellitidae 14 Laganidae 22 2 13 Echinocyamidae Clypeasteroida 6 Echinolampadidae 10 23 Cassidulidae Arachnoididae Cassiduloida 1 Echinoneidae Diadematidae 3 Aspidodiadematidae 4 Pedinidae Echinothuriidae Triassic Jurassic Cretaceous Pg Ng MESOZOIC CENOZOIC 250 200 150 100 50 0 Million years ago Fig. 2 A timetree of sea urchins (Echinoidea). Divergence times are from Table 1. Abbreviations: Ng (Neogene) and Pg (Paleogene). on morphological grounds (1, 2). 7 e monophyly of the from nuclear and mitochondrial ribosomal RNA genes clypeasteroids, a group characterized by the unique syn- (18S, 28S, and 16S rRNA), sometimes with the addition apomorphy of multiple tube feet (and pores) on each of sequence data from three subunits of mitochondrial ambulacral plate, has never been disputed from morpho- cytochrome oxidase genes (COI, COII, and COIII). 7 e logical grounds (5), though the cassiduloids, from which A rst studies achieved only a very sparse taxonomic cover- they emerged, are now recognized to be a paraphyletic age and failed to A nd convincing evidence for the cidar- grade (6). oid–euechinoid basal dichotomy (6). By 1995, however, Molecular phylogenies for the Echinoidea that encom- the A rst analysis that could claim reasonable taxonomic passed a number of diB erent families started to appear coverage appeared (7) and showed good correspondence from 1992 onward (6–10). 7 ese have all been constructed with morphology-based phylogenetic trees. In the latest HHedges.indbedges.indb 330303 11/28/2009/28/2009 11:27:55:27:55 PPMM 304 THE TIMETREE OF LIFE Table 1. Divergence times (Ma) and their confi dence/ genus level (e.g., temnopleuroids (11), spatangoids (12), credibility intervals (CI) among sea urchins strongylocentrotids (13)] and species level [e.g. Eucidaris (Echinoidea), based on ref. (10). (14), Diadema (15)). Timetree From the beginning, phylogenetic studies have oJ en Node Time analyzed morphological and molecular data in parallel and in combination, and have used the rich fossil record 1245for dating divergences. 7 e basic taxonomic framework 2232for echinoids established from skeletal morphology has 3221stood up well to this molecular scrutiny (1). Cidaroids 4210consistently turn out to represent the deepest branch in 5193the echinoid tree and echinothurioids the deepest branch 6181on the euechinoid side, exactly as predicted by morph- 7171ology. 7 e next few branches are very closely spaced and branching order of pedinoids and diadematoids is not 8164 clear. 7 ere is a monophyletic Irregularia, within which 9160the echinoneid Echinoneus represents the basal branch, 10 138 and holasteroids and spatangoids are closest relatives. 11 137 7 ere is one major surprise—molecular data suggest that 12 111 clypeasteroids are not monophyletic. 7 e two suborders 13 109 (Clypeasterina and Scutellina) are recognized, but they 14 98 are not identiA ed as closest relatives. Instead, representa- 15 97 tives from two families of cassiduloid are the closest rela- tives of the Scutellina. 7 e very short branches leading to 16 95 the cassiduloid taxa suggest that this is not a long-branch 17 86 attraction problem, and the inferred relationships are 18 72 robust to addition or removal of taxa. However, it is hard 19 65 to reconcile this observation with the strong morpho- 20 61 logical evidence for clypeasteroid monophyly. 21 54 Only one study has estimated divergence times among 22 41 echinoid families from molecular data (10). 7 is study 23 37 examined 26 internal nodes and compared molecular estimates based on ribosomal gene divergence with pale- 24 36 ontological estimates (Fig. 2). In order to generate a sem- 25 33 ilinearized tree one taxon was selected from each family, 26 28 avoiding extremely long or short terminal and branches. Note: Molecular dates are the means of estimates obtained Bayesian and nonparametric rate smoothing semipara- from the analysis of concatenated 18S rRNA, 28S rRNA, and metric penalized likelihood methods were all used for COII partial gene sequences using different methodologies: estimating divergence times along with the Langley– LF (Langley–Fitch), NPRS (nonparametric rate smoothing), PL-A (penalized likelihood with additive penalty function, PL-L Fitch strict clock method, and error bars calculated. (penalized likelihood with logarithmic penalty function), and A selection of taxa from the other echinoderm classes Bayesian. formed the outgroup, with a prior depth of the root node set at 480 My based on the fossil record. Four internal calibrations were set as minimal divergence times from across the tree topology to provide constraints on local analysis (10), the molecular phylogeny is now based on rate variation. gene sequence data from almost 50 taxa, with representa- Molecular estimates of divergence times derived from tives from 13 of the 14 extant orders. In addition to these applying both molecular clock and relaxed molecular studies addressing the higher-level relationships of echi- clock models are concordant with estimates based on noids, detailed molecular phylogenies have appeared out- the fossil record for 70% of the nodes. Mismatch is con- lining the phylogenetic relationships of speciA c groups at A ned to three areas of the tree, the most serious of which HHedges.indbedges.indb 330404 11/28/2009/28/2009 11:27:56:27:56 PPMM Eukaryota; Metazoa; Echinodermata; Echinoidea 305 concerns the clypeasteroids, where a late Jurassic diver- 2. A. B. Smith, e Echinoid Directory, http://www.nhm. gence (156 ± 24 Ma) for Clypeasterina from Scutellina ac.uk/research-curation/projects/echinoid-directory was predicted from molecular data. In contrast, the fossil (7 e Natural History Museum, London, 2006). record provides no evidence for any clypeasteroid before 3. A. B. Smith, in Evolving Form and Function—Fossils and 60 Ma (Middle Paleocene) (2, 16). Development, D. E. G. Briggs, Ed. (Yale University Press, New Haven, 2005), pp. 181–194. 7 e fact that so much of the molecular phylogeny 4.