Downloaded from rspb.royalsocietypublishing.org on February 24, 2012 A molecular palaeobiological hypothesis for the origin of aplacophoran molluscs and their derivation from chiton-like ancestors Jakob Vinther, Erik A. Sperling, Derek E. G. Briggs and Kevin J. Peterson Proc. R. Soc. B 2012 279, 1259-1268 first published online 5 October 2011 doi: 10.1098/rspb.2011.1773 Supplementary data "Data Supplement" http://rspb.royalsocietypublishing.org/content/suppl/2011/10/04/rspb.2011.1773.DC1.h tml References This article cites 66 articles, 27 of which can be accessed free http://rspb.royalsocietypublishing.org/content/279/1732/1259.full.html#ref-list-1 Subject collections Articles on similar topics can be found in the following collections evolution (1141 articles) palaeontology (94 articles) taxonomy and systematics (144 articles) Receive free email alerts when new articles cite this article - sign up in the box at the top Email alerting service right-hand corner of the article or click here To subscribe to Proc. R. Soc. B go to: http://rspb.royalsocietypublishing.org/subscriptions Downloaded from rspb.royalsocietypublishing.org on February 24, 2012 Proc. R. Soc. B (2012) 279, 1259–1268 doi:10.1098/rspb.2011.1773 Published online 5 October 2011 A molecular palaeobiological hypothesis for the origin of aplacophoran molluscs and their derivation from chiton-like ancestors Jakob Vinther1,*, Erik A. Sperling1,†, Derek E. G. Briggs1,2 and Kevin J. Peterson3 1Department of Geology and Geophysics, and 2Yale Peabody Museum of Natural History, Yale University, PO Box 208109, New Haven, CT 06520-8109, USA 3Department of Biological Sciences, Dartmouth College, Hanover, NH 03755, USA Aplacophorans have long been argued to be basal molluscs. We present a molecular phylogeny, including the aplacophorans Neomeniomorpha (Solenogastres) and Chaetodermomorpha (Caudofoveata), which recovered instead the clade Aculifera (Aplacophora þ Polyplacophora). Our relaxed Bayesian molecular clock estimates an Early Ordovician appearance of the aculiferan crown group consistent with the presence of chiton-like molluscs with seven or eight dorsal shell plates by the Late Cambrian (approx. 501–490 Ma). Molecular, embryological and palaeontological data indicate that aplacophorans, as well as chitons, evolved from a paraphyletic assemblage of chiton-like ancestors. The recovery of cepha- lopods as a sister group to aculiferans suggests that the plesiomorphic condition in molluscs might be a morphology similar to that found in monoplacophorans. Keywords: Polyplacophora; Aculifera; Mollusca; palaeoloricates 1. INTRODUCTION outgroup(s) to all other molluscs (Polyplacophora þ Molluscs are among the most familiar invertebrates. The Conchifera ¼ Testaria) [5–7]. The testarian molluscs well-known shelled taxa, clams, snails and squids, share a number of characters absent in aplacophorans, together with some rarer forms, are collectively referred such as a broad ciliary creeping sole, distinctly compart- to as conchiferans (Bivalvia, Gastropoda, Cephalopoda, mentalized alimentary tract, radula morphology, as well as Monoplacophora and Scaphopoda). Our tetraneurous nervous system, and aorta. This hypothesis focus here, however, is on a small group of worm-like would imply that total-group Aplacophora appeared no molluscs known as aplacophorans, which are character- later than the Early Cambrian because crown-group ized by a vestigial or completely reduced foot. The Conchifera such as stem bivalves (Pojetaia runnegari)[8] mantle (girdle) of aplacophorans is covered by a dense and stem gastropods (Aldanella and Pelagiella) were pre- coat of sclerites (often referred to as spicules) [1,2]. sent by this time [9]. There are two distinct groups: the chaetodermomorphs The second, the Aculifera hypothesis, posits that the (also called caudofoveates) and neomeniomorphs (sole- vermiform morphology of aplacophorans is secondarily nogastres; figure 1a,b). The chaetodermomorphs are modified from a more typical molluscan ancestor, such infaunal selective detrital feeders, whereas most neo- as a chiton-like form with serial rows of shell plates and a meniomorphs feed on cnidarian colonies [1,2]. mantle with sclerites [4,10–12]. Embryological evidence Aplacophorans share a number of characters such as the for the monophyletic Aculifera hypothesis includes the vermiform shape, dorsoterminal sense organ, distichous presence of seven repeated regions devoid of sclerites in a radula, specialized reproductive system and small pos- neomeniomorph post-larva [13](figure 1f ), and seven terior mantle cavity that indicate their monophyly [4]. dorsal rows of calcium carbonate-secreting cells in a Aplacophorans also share many similarities with chitons chaetodermomorph larva [3](figure 1e; but see also (Polyplacophora; figure 1c,d), such as the presence of [14]). These larval forms express a potentially primitive aragonitic sclerites and papillae in the mantle, and a morphology akin to chitons. suprarectal commissure [4]. This embryological evidence is echoed in fossil There are two main hypotheses for the systematic pos- forms. The Silurian (Wenlock) aplacophoran-like mollusc ition of aplacophorans. The first, the Testaria hypothesis, Acaenoplax hayae [15](figure 2c) from the Herefordshire posits that aplacophorans are the most proximal Lagersta¨tte possessed seven dorsal shell plates, the last (together with its terminal ventral shell plate) enclosing a possible posterior mantle cavity with gills [15,17] (see * Author and address for correspondence: Jackson School of alternative interpretation in [18]). Chiton-like fossils Geoscience, University of Texas–Austin, TX 78703, USA with eight plates from the Cambrian and Ordovician, ([email protected]). †Present address: Department of Earth and Planetary Sciences, collectively referred to as palaeoloricates [19], typically Harvard University, Cambridge, MA 02138, USA. have extensive tunnels or lacunae inside their shell Electronic supplementary material is available at http://dx.doi.org/ plates (figure 2d–f ). The presence of these lacunae, 10.1098/rspb.2011.1773 or via http://rspb.royalsocietypublishing.org. which have been homologized to the subapical cavities Received 23 August 2011 Accepted 14 September 2011 1259 This journal is q 2011 The Royal Society Downloaded from rspb.royalsocietypublishing.org on February 24, 2012 1260 J. Vinther et al. Aplacophoran origins (a) (b) (c) (d) (e) ( f) (ii) (i) Figure 1. Modern aculiferan diversity. (a) An unknown species of aplacophoran neomeniomorph, Antarctica. Yale Peabody Museum of Natural History no. 51789. (b) The aplacophoran chaetodermomorph Chaetoderma intermedium, Greenland. Zoo- logical Museum of Copenhagen, Denmark, ZMUC-APL-10. (c) The chiton Chiton tuberculatus, photographed in the intertidal zone, Barbados. (d) The chiton Leptochiton asellus, underwater photograph, Norway (www.uwphoto.no; copyright q Erling Svensen). (e) Late trochophore larva of Chaetoderma nitidulum showing seven conspicuous dorsal ridges (i) with calcium carbonate-secreting cells and (ii) the secondarily reduced ventral foot region, from Nielsen et al.[3]. Scale bars, 20 mm. ( f ) Neomeniomorph postlarva with seven naked dorsal regions and sclerites arranged in transverse rows and in lateral zones [4]. Scale bar, 0.1 mm. in the shell plates of forms related to Acaenoplax [20,21], group, given this scenario, is provided by Late Cambrian is suggestive of a relationship between palaeoloricates (501–490 Ma) forms with serial shell plates, such as and aplacophorans, thus supporting the hypothesis Matthevia (figure 2f )[24,25]. Thus, the fossil record (based on a cladistic analysis [19,22]) that palaeoloricates suggests that aplacophorans could have evolved from a are a paraphyletic suite of stem-aculiferans as well as chiton-like ancestor. This result, paraphyly of polyplaco- stem chitons and aplacophorans [19,22]. According to phorans with respect to aplacophorans, has been this interpretation, the possession of a foot and dorsal obtained in some cladistic analyses [19,22], while others shell plates, which were subsequently reduced, is have found all fossil and recent polyplacophorans to be primitive for Aplacophora. An Upper Ordovician form monophyletic [26]. (Helminthochiton thraivensis) with eight overlapping Molecular phylogenetics provides an independent plates [23] and a mantle that extends ventrally (figure 2a), test of morphological and palaeontological hypotheses, leaving little room for an elaborate foot, pushes the mini- but studies to date have not resolved the relation- mum age for an aculiferan divergence back to the Late ships at the base of the molluscan tree. Most early Ordovician (earlier than 443 Ma) [19]. Helminthochiton studies provided support for neither the Testaria nor thraivensis occurs at the same locality as Septemchiton Aculifera hypothesis, but instead found aplacophorans grayiae (figure 2b), another possible stem-group aplaco- and chitons to be unrelated and nested within different phoran [19], which has a similar laterally compressed conchiferan sub-groups [27–29]. Later studies, however, morphology that may indicate a reduced foot. Since the found a relationship between aplacophorans, chitons and ancestral aculiferan would have been a chiton-like form, cephalopods, but until recently this has been largely a possible age for the origin of the aculiferan crown unresolved [30–32]. Proc. R. Soc. B (2012) Downloaded from rspb.royalsocietypublishing.org on February 24, 2012 Aplacophoran origins J.