The evolution of pedicellariae in echinoids: an arms race against pests and parasites Simon E. Coppard, 1 Andreas Kroh 2 and Andrew B. Smith 3 1 Smithsonian Tropical Research Institute, Post Box 0843-03092, Balboa, Ancon, Republic of Panama; 2 Natural History Museum Vienna, Department of Geology & Palaeontology, Burgring 7, 1010 Vienna, Austria; 3 Natural History Museum, Palae- ontology Department, Cromwell Road, London SW7 5BD, UK Keywords: Echinoidea, phylogeny, taxonomy, cladistics, evolution, Mesozoic marine revolution, fossil record Accepted for publication: 12 October 2010 Abstract Coppard, S.E., Kroh, A. and Smith, A.B. (2010). The evolution of pedicellariae in echinoids: an arms race against pests and parasites. —Acta Zoologica (Stock- holm) 00:1–24. Sea urchins (Echinoidea) have evolved a diverse array of jawed appendages termed pedicellariae to deter pests and predators. Pedicellarial structure and function are reviewed and their distribution mapped in 75 extant genera. Using a phylogeny of echinoids at family level constructed from 353 skeletal characters scored across 162 extant and fossil taxa, the evolution of pedicellarial form and function is reconstructed. For much of the Palaeozoic echinoids possessed a very restricted pedicellarial armament. By the early Mesozoic a diverse array of pedi- cellarial types had become established, implying that the threat from predators and pests markedly increased at this time. Since the Triassic, echinoids have continued to improve their defensive capability by evolving more effective venom delivery in globiferous pedicellariae, developing spatulate-tips and curved blades for a more efficient grab in tridentate pedicellariae, and stouter, more robust valves with a stronger bite in ophicephalous pedicellariae to disable and remove ectoparasites. However, pedicellarial types are shown to be particularly prone to subsequent secondary loss, especially among infaunal echinoids, and thus have higher homoplasy levels than other phylogenetically useful skeletal structures. Andrew B. Smith, Natural History Museum, Palaeontology Department, Cromwell Road, London SW7 5BD, UK. E-mail: abs@nhm.ac.uk Introduction All echinoids possess a series of mobile appendages for protection. Most obvious are the primary and secondary spines, which cover the surface of the animal (Fig. 1A) and provide a formidable defence against larger predators. In among the spines are a set of small stalked appendages, the pedicellariae (Fig. 1B). These are pincer-like structures used in defence and cleaning (Von Uexku ¨ ll 1899). They are attached by muscles to a freely rotating joint on the surface of the test and consist of a stalk, a neck and valves, which form the jaws (Nichols 1962). These structures are functionally and structurally highly evolved and come in a bewildering array of different shapes (Fig. 2). Because of this variability, they have been widely used in taxonomy, especially at species and genus level (e.g. Mortensen 1928– 1951; Coppard and Campbell 2006; Coppard 2008). Fur- thermore, characteristic pedicellarial types are restricted in their distribution, providing important phylogenetic markers for higher clades. A similar sort of jaw-like appendage can be found in extant starfishes (Lambert et al. 1984; Lawrence 1987; Gale in press), and these are recorded as far back as the Silurian (Sut- ton et al. 2005). These serve the same overall role as echinoid pedicellariae, but are usually bivalved and are attached directly to underlying plates rather than being stalked. Their different structure suggests that they evolved from dermal spines independently from those of echinoids. Surprisingly little is known about the evolutionary history of echinoid pedicellariae, and the fossil record provides rela- tively few clues. While the first pedicellariae are recorded from the late Ordovician (Nestler 1970), shortly after the earliest records of echinoid tests (Smith and Savill 2002), the small size and fragility of pedicellariae has meant that they are rarely preserved and even more rarely described. Furthermore, those few studies that have described pedicel- lariae are usually based on material found in sieved sediment samples that cannot be assigned to particular taxa with any degree of confidence (e.g. Geis 1936; Mostler 1972, 2009; Boczarowski 2001, 2004, 2005). The evolution of Acta Zoologica (Stockholm) doi: 10.1111/j.1463-6395.2010.00487.x Ó 2010 The Authors Acta Zoologica Ó 2010 The Royal Swedish Academy of Sciences 1