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Kk233.Pdf (1.935Mb) Reference: Biol. Bull. 222: 233–269. (June 2012) © 2012 Marine Biological Laboratory Hard and Soft Anatomy in Two Genera of Dondersiidae (Mollusca, Aplacophora, Solenogastres) AME´ LIE H. SCHELTEMA1,*, CHRISTOFFER SCHANDER2†, AND KEVIN M. KOCOT3 1Woods Hole Oceanographic Institution, Biology Dept., Woods Hole, Massachusetts 02543; 2University Museum of Bergen, P.O. Box 7800, Bergen N-5020, Norway; Uni Environment, Uni Research AS, Bergen N-5020, Norway; and 3Department of Biological Sciences, Auburn University, 101 Rouse Life Sciences, Auburn, Alabama 36849 Abstract. Phylogenetic relationships and identifications Introduction in the aplacophoran taxon Solenogastres (Neomeniomor- pha) are in flux largely because descriptions of hard parts–– The cylindrical, vermiform, sclerite-covered Aplaco- sclerites, radulae, copulatory spicules––and body shape phora has been a perplexing taxon of molluscs ever since have often not been adequately illustrated or utilized. With the first two species, representatives of the only two clades, easily recognizable and accessible hard parts, descriptions were discovered: Chaetoderma nitidulum Love´n, 1844, ϭ of Solenogastres are of greater use, not just to solenogaster Caudofoveata ( Chaetodermomorpha Pelseneer) and Neo- ϭ taxonomists, but also to ecologists, paleontologists, and menia carinata Tullberg, 1875, Solenogastres ( Neomen- evolutionary biologists. Phylogenetic studies of Aplaco- iomorpha Pelseneer). The puzzle was first of all whether N. carinata phora, Mollusca, and the Lophotrochozoa as a whole, they were molluscs at all, because lacks a radula, and the radula of C. nitidulum is a strange, 2-den- whether morphological or molecular, would be enhanced. ticled affair attached to a long cuticular cone. Indeed, the As an example, morphologic characters, both isolated hard great malacologist Johannes Thiele, with far less informa- parts and internal anatomy, are provided for two genera in tion than is now available, and who published over 20 the Dondersiidae. Five species are described or redescribed aplacophoran species descriptions, concluded that aplaco- and earlier descriptions corrected and enhanced. Three be- phorans were not molluscs as such, but phylogenetically long to Dondersia: D. festiva Hubrecht, D. incali (Schel- between annelids and molluscs and ancestral to the latter tema), and D. namibiensis n. sp., the latter differentiated (Thiele, 1913c; Glaubrecht et al., 2005). More usually, unambiguously from D. incali only by sclerites and copu- Aplacophora was placed with the Polyplacophora as Acu- latory spicules. Two species belong to Lyratoherpia: L. lifera or Amphineura (see especially Hoffman, 1949). No carinata Salvini-Plawen and L. californica (Heath). Notes one now disputes their molluscan nature. are given for other species in Dondersiidae: L. bracteata The next puzzles were two questions: Are the aplaco- Salvini-Plawen, Ichthyomenia ichthyodes (Pruvot), and phoran Solenogastres and Caudofoveata monophyletic or Heathia porosa (Heath). D. indica Stork is synonymized diphyletic? Are they plesiomorphic, positioned at the base with D. annulata. A cladistic morphological analysis was of the mollusc tree, or are they derived? These two ques- conducted to examine the utility of hard parts for recon- tions remained unresolved for many years, whether using structing solenogaster phylogeny. Results indicate mono- comparative descriptive morphologies (e.g., Scheltema, phyly of Dondersia and Lyratoherpia as described here. 1993), descriptive embryology (Okusu 2002; Nielsen et al., 2007; Todt and Wanninger 2010), cladistics (e.g., Haszpru- nar, 2000), or molecular phylogenetics (e.g., Passamaneck, 2003; Giribet et al., 2006; Wilson et al., 2010). However, Received 20 March 2011; accepted 15 May 2012. * To whom correspondence should be addressed. E-mail: ascheltema@ Sigwart and Sutton (2007) conducted a cladistic morpho- whoi.edu logical analysis including polyplacophoran fossils and, for † Deceased. the first time, resolved a monophyletic Aculifera as Apla- 233 This content downloaded from 131.204.174.034 on February 14, 2020 12:07:31 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). 234 A. H. SCHELTEMA ET AL. cophora plus Polyplacophora. Additionally, the weight of emended. A reexamination of the type histologic slides of evidence from recent molecular studies (Kocot et al., 2011; D. californica (Heath, 1911) indicates that it is a second Vinther et al., 2011; and Smith et al., 2011) is also in favor Lyratoherpia species. Notes are given for other species of a monophyletic Aplacophora that is recovered with putatively belonging to the two genera under discussion or Polyplacophora as a clade we call Aculifera. Earlier hypoth- to the Dondersiidae: D. annulata Nierstrasz, 1902; D. indica eses are reviewed in their papers, as well as in Ponder and Stork, 1941; L. bracteata Salvini-Plawen, 1978; Ichthyome- Lindberg (2008, Chapters 2 and 4). nia ichthyodes (Pruvot, 1890); and Heathia porosa (Heath, Within Aplacophora, the separation of Caudofoveata 1911). from Solenogastres (which was the original name for both Additionally, using detailed morphological data collected groups, e.g., Thiele, 1913c) and the membership of species from these two genera of Dondersiidae (summarized in in one or the other remains stable and unquestioned. How- Table 2) plus two outgroup taxa, we conducted a cladistic ever, relationships particularly within Solenogastres remain morphological analysis to examine the utility of characters unresolved. An early study of the Antarctic and Subantarctic related to hard parts and body shape and proportions in Solenogastres (Salvini-Plawen, 1978) was the first to ar- reconstructing Solenogastres phylogeny. range families into orders, but without cladistic analysis and with internal hard parts––radulae and copulatory spicules–– described from histologic material, not from isolated, entire Materials and Methods hard parts. A later morphologic cladistic analysis by Sal- vini-Plawen (2003b) failed to recover two recognized orders The numbers of individuals of each species range from and several families as monophyletic, suggesting either the 147 entire specimens of Dondersia namibiensis sp. nov. failure of the existing taxonomy to reflect the evolutionary to two D. festiva (sectioned) and one Lyratoherpia cali- history of the group or a lack of appropriate signal in the fornica (sectioned). Descriptions of internal anatomy are analyzed data. Notably, Salvini-Plawen himself states “the based on older, rather thick histologic sections of D. available characters are extremely homoplastic and that festiva and L. californica and on newly prepared histo- homology decisions are far too uncertain to accept the logic sections at 2 ␮m (Epon-embedded, Richardson- resulting trees as reflections of the phylogeny of the Sole- stained) or 7 ␮m (wax-embedded, hematoxylin and eo- nogastres.” Therefore, studies of entire internal hard parts sin-stained) for specimens of D. namibiensis, D. incali, are desirable to provide additional characters to evaluate and L. carinata. Photographic images were made with solenogaster evolution. MD-290 Kodak, Nikon 5400, or Canon A650 IS digital Here we present new codable morphological characters cameras with a Zeiss microscope attachment and en- of two genera in the Solenogastres family Dondersiidae (see hanced in Photoshop. Except for D. festiva and L. cali- Table 2), both for body shape and isolated hard parts— fornica, radulae and copulatory spicules were isolated sclerites, radulae, and copulatory spicules—and for internal anatomic characters, particularly those broadly applicable to with warm potassium hydroxide or with sodium hypo- Solenogastres. The importance of hard parts for taxonomy chlorite (standard household bleach) and thoroughly has been stressed earlier (Scheltema and Schander, 2000, washed after dissecting anterior and posterior ends. Scan- 2006). The intention here is to provide informative charac- ning electron microscope (SEM) and light microscope ters for cladistic analyses, eventually leading to a better (LM) images and drawings were made of entire speci- understanding of relationships among Solenogastres, be- mens, sclerites, and radulae (D. incali, D. namibiensis, tween Solenogastres and Caudofoveata, among clades LM, SEM; L. carinata, LM) and SEM or LM images of within Mollusca and Lophotrochozoa, and with the fossil copulatory spicules (D. namibiensis, L. carinata, SEM; record. D. incali, LM). The radula and copulatory spicules of D. We describe or redescribe five species of Dondersiidae. festiva were interpreted from histologic sections of two Three species belong to Dondersia. One expands the de- individuals. scription of the nominate species, D. festiva Hubrecht, 1888, All material examined is on deposit at Muse´um National including radula morphology, ventrolateral foregut glands, d’Histoire Naturelle (MNHN, Paris); National Museum of and descriptions and illustrations of the reproductive sys- Natural History–Naturalis (NNM, Leiden); Smithsonian In- tem. The second emends and expands the original illustra- stitution, National Museum of Natural History (USNM, tive material and description of D. incali (Scheltema, 1999), Washington, DC); and California Academy of Sciences correcting the earlier interpretation of the upper reproduc- (CAS, San Francisco). tive system. The third describes D. namibiensis n. sp. Two The cladistic morphological analysis was conducted us- species
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