Org Divers Evol (2016) 16:141–166 DOI 10.1007/s13127-015-0231-9 ORIGINAL ARTICLE Comparative morphology and phylogenetic significance of Gregory’s diverticulum in sand dollars (Echinoidea: Clypeasteroida) Alexander Ziegler1 & Jennifer Lenihan2 & Louis G. Zachos 3 & Cornelius Faber4 & Rich Mooi5 Received: 28 April 2015 /Accepted: 28 July 2015 /Published online: 28 August 2015 # Gesellschaft für Biologische Systematik 2015 Abstract Several derived sand dollar (Echinoidea: This extensive dataset permits establishing a concise Clypeasteroida) families are characterized by the pres- terminology that incorporates all of the organ’s sub- ence of Gregory’s diverticulum, an accessory organ of structures. In addition, three-dimensional models of the digestive tract. This soft tissue structure is com- Gregory’s diverticulum are presented that provide an posed of a central tubular cecum that gives off mul- improved spatial understanding of the organ’smor- tiple lobes into the periphery of the test. Most notable phology in situ. The combined data from dissection, are the organ’s capacity to selectively store sand X-ray imaging, microcomputed tomography, and mag- grains that the animal has taken up from the sur- netic resonance imaging reveal a previously unknown rounding sediment as well as the gradual reduction variability of the structure, which also yields several of Gregory’s diverticulum during ontogeny. Several phylogenetically informative morphological characters. aspects of the biology of this structure have remained Among those sand dollar families that possess unexplored, including the organ’s precise morphology Gregory’s diverticulum, the organ is present in two and structural diversity. In order to provide a concise distinct shapes, which can be distinguished by the basis for future histological, physiological, and func- number, shape, and location of substructures. In addi- tional analyses, a comprehensive comparative morpho- tion, the data provide unequivocal evidence that logical and phylogenetic study across numerous taxa Gregory’s diverticulum is absent in the extant taxa was undertaken. Taxon sampling comprised over 100 Rotulidae and Astriclypeidae, but also in the enigmat- clypeasteroid species, including various fossil taxa. ic Marginoproctus. Electronic supplementary material The online version of this article (doi:10.1007/s13127-015-0231-9) contains supplementary material, which is available to authorized users. * Alexander Ziegler 1 Institut für Zoologie, Rheinische Friedrich-Wilhelms-Universität [email protected] Bonn, Meckenheimer Allee 169, 53115 Bonn, Germany Jennifer Lenihan 2 Museum of Comparative Zoology, Department of Organismic and [email protected] Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, USA Louis G. Zachos 3 [email protected] Department of Geology and Geological Engineering, University of Mississippi, 120 Carrier Hall, Oxford, MS 38677, USA Cornelius Faber 4 Institut für Klinische Radiologie, Westfälische Wilhelms-Universität [email protected] Münster, Albert-Schweitzer-Campus 1, 48149 Münster, Germany Rich Mooi 5 California Academy of Sciences, Golden Gate Park, 55 Music [email protected] Concourse Drive, San Francisco, CA 94118, USA 142 A. Ziegler et al. Keywords Echinodermata . Digestive tract . Gregory’s Le zoologiste qui aurait en main assez de matériaux diverticulum . Magnetite . Comparative morphology . Soft pour entreprendre une étude comparative des tissue . Phylogeny caractères anatomiques des différents genres de Scutellidae ferait certainement des observations très intéressantes. R. Koehler (1922,p.123) Abbreviations μCT Microcomputed tomography 2D Two-dimensional Introduction 3D Three-dimensional Amb Ambulacrum A number of derived sand dollar (Echinoidea: Clypeasteroida) BMNH British Museum of Natural History, London, families possess an accessory digestive tract structure known UK as Gregory’s diverticulum (Gregory 1905; Lawrence 2001). In BPBM Bernice P. Bishop Museum, Honolulu, HI, USA juvenile specimens, this soft tissue organ is frequently filled CASG California Academy of Sciences Geology, San with sand grains of high specific gravity selectively taken up Francisco, CA, USA from the surrounding sediment, in particular magnetite CASIZ California Academy of Sciences Invertebrate (Fe2O3), ilmenite (TiFeO3), and zircon (ZrSiO4)(Chia1973; Zoology, San Francisco, CA, USA Chen and Chen 1994; Borzone et al. 1997; Elkin et al. 2012). CT Computed tomography As the animal matures, the sediment accumulated inside the FDNR Florida Department of Natural Resources, St. diverticulum is successively expelled (Chia 1985), leaving be- Petersburg, FL, USA hind an empty vestigial remnant of the organ that eventually IAmb Interambulacrum ceases to exist (Wagner 1963; Mitchell 1972; Borzone et al. MCZ Museum of Comparative Zoology, Cambridge, 1997). However, some sand dollar species were observed to MA, USA retain a sand-filled diverticulum throughout adulthood MMBS Misaki Marine Biological Station, Misaki, (Mitchell 1972;ChenandChen1994), illustrating a certain Japan degree of morphological and developmental variability. MNHN Muséum national d'Histoire naturelle, Paris, The prevailing hypothesis with regard to the function of France Gregory’s diverticulum is that the structure, when distended MRI Magnetic resonance imaging with sediment, serves the juvenile sand dollar as a Mya Million years ago “balancing aid” (Wagner 1963)or“weight belt” (Chia NMNS National Museum of Natural Science, Taipei, 1973), enabling the animal to maintain its natural position Taiwan in habitats with strong hydrodynamic properties (Borzone SIO Scripps Institution of Oceanography, San Diego, et al. 1997). However, this scenario has not yet been sub- CA, USA stantiated by direct experimental evidence (Lawrence 2001). UB Université de Bourgogne, Dijon, France In addition, the mechanisms for selection of heavy minerals UCMP Museum of Paleontology, University of both on the outside and on the inside of the animal remain California, Berkeley, CA, USA poorly understood (Wagner 1963; Mitchell 1972;Chia UNEFM Museo de la Universidad Nacional Experimental 1985). For example, it was proposed that internal sediment FranciscodeMiranda,Falcón,Venezuela selection could be a result of mass-related differences in the USNM United States National Museum, Washington, movement speed of sand grains contained inside the echi- DC, USA noid gut (Lares 1999; Lawrence 2001), but there are again UT University of Texas at Austin, Austin, TX, USA no experimental data to support this assumption. UTO University of Toronto, Ontario, Canada The histological characteristics of Gregory’s diverticulum WAM Western Australian Museum, Perth, Western have so far only briefly been studied. These results show that Australia, Australia the composition of the wall of the organ resembles that of the ZMB Museum für Naturkunde, Berlin, Germany intestine (Chia 1985), to which it is connected through a short ZMH Zoologisches Museum Hamburg, Hamburg, canal (Mitchell 1972). Even less is known about the early Germany development of Gregory’s diverticulum, in particular during ZMK Zoologisk Museum København, Copenhagen, or directly following the organism’s metamorphosis from larva Denmark to juvenile. Unfortunately, the few studies that provide data on ZSM Zoologische Staatssammlung München, Munich, larval and postmetamorphic anatomy of derived sand dollars Germany were performed before Emily R. Gregory’s description of the Evolution of Gregory’s diverticulum in sand dollars 143 organ in the early twentieth century (Fewkes 1886; Grave uncited manuscripts and conference abstracts. In total, data 1902) or are dealing with very specific aspects of larval mor- for over 600, mostly juvenile specimens pertaining to 104 phology (Burke 1982, 1983). clypeasteroid species were incorporated. Table 1 lists all From a systematic point of view, previous reports suggest samples analyzed and provides taxonomic information, spec- that Gregory’s diverticulum is absent in basal clypeasteroid imen data, information on applied techniques, observations families such as the Clypeasteridae, Laganidae, or Fibulariidae on the absence or presence of Gregory’s diverticulum, as (Chia 1985; Mooi and Chen 1996). Consequently, the presence well as the respective data sources. The taxonomic arrange- of the organ was proposed to constitute a synapomorphy of ment of the species follows recent phylogenetic analyses derived sand dollar families such as the Echinarachniidae, (Kroh and Smith 2010;Mooietal.2014) and nomenclature Dendrasteridae, and Mellitidae (Mooi and Chen 1996). from The World Echinoidea Database (Kroh and Mooi However, to date, only little graphic evidence concerning the 2015), except where noted. absence or presence of the organ and even more so regarding its shape was presented for most clypeasteroid clades. Specimen inspection, dissection, and photography In light of numerous open questions regarding the origin, development, function, and structural diversity of Gregory’s Whenever possible, extant specimens were prescreened by diverticulum, the principal aims of this contribution are (i) to placing them in front of a strong light source (Wagner introduce a concise terminology that incorporates all of the 1963). Due to the tenuity of most juvenile sand dollar tests, organ’s substructures, (ii) to provide the first graphic over- this procedure allowed quick identification of specimens view of its shape across taxa, (iii) to present