Metamorphosis in Craniiformea Revisited Novocrania Anomala Shows Delayed Development of the Ventral Valve Altenburger, Andreas; Wanninger, Andreas; Holmer, Lars E
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Metamorphosis in Craniiformea revisited Novocrania anomala shows delayed development of the ventral valve Altenburger, Andreas; Wanninger, Andreas; Holmer, Lars E. Published in: Zoomorphology DOI: 10.1007/s00435-013-0194-3 Publication date: 2013 Document version Early version, also known as pre-print Citation for published version (APA): Altenburger, A., Wanninger, A., & Holmer, L. E. (2013). Metamorphosis in Craniiformea revisited: Novocrania anomala shows delayed development of the ventral valve. Zoomorphology, 132(4), 379-387. https://doi.org/10.1007/s00435-013-0194-3 Download date: 02. Oct. 2021 *Manuscript Click here to download Manuscript: 130422 Metamorphosis in Novocrania.docx Click here to view linked References 1 Metamorphosis in Craniiformea revisited – Novocrania anomala shows delayed 1 2 development of the ventral valve 3 4 5 6 7 Running title: Metamorphosis in Novocrania 8 9 10 11 12 Andreas Altenburger, Andreas Wanninger, Lars E. Holmer 13 14 15 16 Authors’ names and addresses 17 18 19 Andreas Altenburger, University of Copenhagen, Natural History Museum of 20 21 Denmark – Zoological Museum, Universitetsparken 15, DK-2100 Copenhagen, 22 23 24 Denmark, [email protected], phone: +45 35321114 25 26 Andreas Wanninger, University of Vienna, Dept. of Integrative Zoology, Althanstr. 27 28 29 14, AUT-1090 Vienna, Austria 30 31 Lars E. Holmer, Uppsala University, Department of Earth Sciences, Palaeobiology, 32 33 SE-752 36 Uppsala, Sweden 34 35 36 37 38 Abstract 39 40 41 We revisited the brachiopod fold hypothesis and investigated metamorphosis in the 42 43 craniiform brachiopod Novocrania anomala. Larval development is lecithotrophic 44 45 46 and the dorsal (brachial) valve is secreted by dorsal epithelia. We found that the 47 48 juvenile ventral valve, which consists only of a thin layer that was previously 49 50 described as periostracal, is not a valve, and is not secreted by the same epithelia as 51 52 53 the dorsal valve. It is secreted by the attachment area of the larva at the posterior-most 54 55 tip of the posterior larval lobe. The same attachment area is used by larvae of 56 57 58 rhynchonelliform brachiopods during metamorphosis to cement their pedicle to the 59 60 substrate. N. anomala is therefore not initially attached by a valve but by material 61 62 63 64 65 2 corresponding to pedicle cuticle. This is different to previous descriptions, which had 1 2 led to speculations about a folding event in the evolution of Brachiopoda. We show 3 4 5 that the “brachiopod fold hypothesis”, which argues that brachiopods are transversely 6 7 “folded” across the ontogenetic anterior-posterior axis, should be rejected at least with 8 9 10 respect to the craniiforms. The data now suggest that the Craniiformea may be a 11 12 derived group within the Rhynchonelliformea. This interpretation suggests that the 13 14 15 last common ancestor of the Craniiformea has lost the pedicle and the ventral valve in 16 17 early juvenile development. Characters that have previously been considered to be 18 19 shared between the Craniiformea and the Linguliformea (clade Inarticulata), such as a 20 21 22 through-gut and missing hinge articulation, may thus be secondarily derived 23 24 characters of the Craniiformea within the Rhynchonelliformea. 25 26 27 28 29 Keywords 30 31 32 ontogeny, development, Craniiformea, phylogeny, morphology, body plan, evolution 33 34 35 36 Introduction 37 38 39 Brachiopoda is a marine animal phylum with a rich fossil record and approximately 40 41 370 recent species divided into the three clades, Craniiformea, Rhynchonelliformea, 42 43 44 and Linguliformea (Williams et al. 1996; Zezina 2008). The evolution of the 45 46 brachiopod body plan with two valves that enclose the soft tissue and a pedicle that 47 48 49 attaches the animal to the substrate has puzzled researchers since the naming of the 50 51 phylum by Duméril (1806). Brachiopods have since been deemed related to various 52 53 phyla such as molluscs, bryozoans, annelids and recently, based on molecular data, to 54 55 56 nemerteans (Grey 1848; Huxley 1853; Morse 1870; Dunn et al. 2008). 57 58 59 60 61 62 63 64 65 3 Brachiopod internal relationships between the three clades, and the relation of 1 2 brachiopods to phoronids, have not been completely resolved to date by molecular 3 4 5 methods (Cohen et al. 1998; Cohen 2000; Cohen and Weydmann 2005; Sperling et al. 6 7 2011; Cohen 2013). Also, the comparative morphological analyses found an equal 8 9 10 amount of characters shared among the Craniiformea and the Linguliformea (formerly 11 12 the clade Inarticulata) and the Craniiformea and the Rhynchonelliformea (Carlson 13 14 15 1995). This has led to different outcomes in analyses concerning brachiopod internal 16 17 phylogeny, depending on the chosen character polarities (Carlson 1995; Holmer et al. 18 19 1995; Williams et al. 1996). Characters shared among the craniiforms and the 20 21 22 linguliforms include a through-gut, a circumferential mantle cavity, a muscular 23 24 system consisting of oblique and two pairs of adductor muscles, as well as a transient 25 26 27 median tentacle (Williams et al. 1996). Characters shared among the Craniiformea 28 29 and the Rhynchonelliformea include a proteinaceaous calcitic shell, a single row of 30 31 32 tentacles on trocholophous lophophores, gonads suspended in mantle sinuses, and 33 34 lecithotrophic larvae (Holmer et al. 1995; Williams et al. 1996). 35 36 There are various hypotheses about the evolution of the brachiopod body plan. During 37 38 39 the years, four hypotheses have been put forward. 1. The ancestor of brachiopods was 40 41 a tube-dwelling polychaete-like metameric worm with a hydraulic body construction 42 43 44 (Gutmann et al. 1978). 2. The ancestor of brachiopods was an oligomerous worm with 45 46 setae, protocoel, mesocoel, and three segments in the metacoel (Temereva and 47 48 49 Malakhov 2011). 3. The ancestor of brachiopods was a halkieriid-like organism, 50 51 comprising a worm-like body with sclerites and shells at the anterior and posterior 52 53 end (Conway Morris and Peel 1995; Cohen et al. 2003). 4. Brachiopods evolved from 54 55 56 sclerite-bearing, tube-dewelling, worm-like organisms such as the tommotiids 57 58 59 60 61 62 63 64 65 4 Micrina, Eccentrotheca, and Paterimitra (Williams and Holmer 2002; Holmer et al. 1 2 2008; Skovsted et al. 2009a; 2009b; Holmer et al. 2011; Murdock et al. 2012). 3 4 5 In living brachiopods, members of each clade have a distinct mode of development. 6 7 The larvae of Craniiformea are lecithotrophic, bilobed, with three pairs of dorsal setal 8 9 10 bundles on the posterior lobe. The larvae of Rhynchonelliformea are lecithotrophic, 11 12 have three lobes and four setal bundles at the mantle lobe, while the Linguliformea 13 14 15 have planktotrophic, swimming juveniles (Nielsen 2005). Larvae of Craniiformea and 16 17 Rhynchonelliformea metamorphose upon settlement. Swimming juveniles of 18 19 Linguliformea do not undergo metamorphosis upon settlement because 20 21 22 metamorphosis is mainly completed at the end of the embryonic stage in lingulids or 23 24 shortly after hatching in the discinids (Lüter 2001, 2007; Popov et al. 2012). 25 26 27 Hypotheses concerning the putative body plan of the ancestor of Brachiopoda often 28 29 focus on the development of Novocrania anomala (Müller 1776) (previously assigned 30 31 32 to several genera and therefore also referred to as Crania anomala or Neocrania 33 34 anomala) (Lee and Brunton 1986, 2001), a member of the Craniiformea (Nielsen 35 36 1991; Popov et al. 1993; Conway Morris 1998; Cohen et al. 2003). It has been 37 38 39 claimed that both valves in juveniles of N. anomala are secreted by mantle epithelia 40 41 that originate at the dorsal side of the posterior lobe (Nielsen 1991). This notion has 42 43 44 led to the conclusion that a “folding-event” happened during brachiopod evolution 45 46 (Cohen et al. 2003; Malakhov and Kuzmina 2006). The concept was subsequently 47 48 49 termed “brachiopod fold hypothesis”, according to which brachiopods are assumed to 50 51 transversely “fold” across the larval anterior-posterior axis. According to this theory, 52 53 the brachiopod body plan needs to be conceptually “unfolded” in order to make useful 54 55 56 comparisons with the body plans of other animal phyla (Cohen et al. 2003). The body 57 58 plan of Halkieria evangelista as a possible stem group brachiopod was used to 59 60 61 62 63 64 65 5 support this view (Conway Morris and Peel 1995; Cohen et al. 2003). However, the 1 2 hypothesis that H. evangelista represents a brachiopod stem species has since been 3 4 5 questioned (Vinther and Nielsen 2005). 6 7 The metamorphosis of N. anomala was described in detail with the claim that prior to 8 9 10 metamorphosis ‘most larvae become inactive and lie curled together on the bottom 11 12 with the pair of ventral muscles maximally contracted’ (Nielsen 1991). We tested 13 14 15 whether these curled, inactive larvae are able to metamorphose by live observation, 16 17 the use of F-actin labelling, confocal laser scanning microscopy, and scanning 18 19 electron microscopy. 20 21 22 23 24 Materials and Methods 25 26 27 Collection of developmental stages 28 29 Adults of Novocrania anomala where obtained by dredging in the vicinity of the Sven 30 31 32 Lovén Centre for Marine Sciences, Gullmarsfjord, Sweden (58°15’921”N, 33 34 11°25’103”E), in September 2008. The rocks with attached N. anomala were kept in 35 36 running seawater at 14°C. Adults were removed from the rocks and dissected.