Chin. Sci. Bull. (2014) 59(7):639–644 DOI 10.1007/s11434-013-0099-z
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Article
Geology
Tetraradial symmetry in early poriferans Joseph P. Botting • Xunlai Yuan • Jih Pai Lin
Received: 13 July 2013 / Accepted: 27 November 2013 / Published online: 15 January 2014 Ó Science China Press and Springer-Verlag Berlin Heidelberg 2014
Abstract Here is currently little consensus on the branching order and phyletic status of the oldest metazoan groups, but sponges are widely believed to be the earliestbranching living metazoans. Porifera are thought to have diverged before the emergence of developmental characters typical of Eumetazoa, such as well-defined symmetry; extant sponges show radial symmetry of indeterminate high order, or none, combined with polarisation along the axis. In contrast, other early-branching phyla include bilateral and tetraradial (Cnidaria) and biradial (Ctenophora) symmetry, or none (Placozoa). A variety of prismatic early fossil sponges had shown here where the shared symmetry has been overlooked, and also describe structural tetraradial symmetry in Cambrian sponges from South China. Based on this study, this symmetry is likely to have been a primitive feature of sponges, and that the earliest-known fossil sponges were highly organised, cellularly integrated individuals whose body form was under strict genetic control. Keywords Porifera Guizhou Hetang Biota Skeletal architecture Spicules
1 Introduction Sponges are almost universally regarded as the earliestbranching living animals [1, 2]. Their apparently primitive cellular characteristics and organisational simplicity are
J. P. Botting X. Yuan J. P. Lin (&) State Key Laboratory of Paleobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing 210008, China e-mail:
[email protected]
confirmed by many molecular phylogenies [3, 4], with only a few recent papers, suggesting either ctenophores [5] or placozoans [6] to have branched earlier, and both results being convincingly rejected by others due to artefacts [7]. However, the relationship of Porifera to the other earlybranching phyla (Ctenophora, Cnidaria, Placozoa) remains disputed. Relationships within the sponges are also unclear [8], but critical to understanding early animals [9]. The exact topology will determine whether higher animals arose directly from sponges, or whether they share a common ancestor. Among the most fundamental features separating the earliest-branching animal groups is body symmetry. Bilateria show bilateral symmetry with dorsoventral polarisation, whereas Ctenophora are biradial with eight radially arranged comb rows [1]. Cnidaria are in part tetraradial (specifically Medusozoa), and partly bilateral; the latter usually regarded as either primitive [10] or secondarily derived from cylindrical symmetry [11]. Recent discoveries of very early Cambrian fossils with scyphozoan affinities [12] show both tetraradial and pentaradial symmetry, but there is no direct fossil evidence as to which was primitive. There are also cnidarian fossils with hexagonal symmetry from the same age [13], implying early diversification of body forms within the group. Porifera are normally asymmetric or radially symmetric, and Placozoa have no definite symmetry, perhaps due to secondary simplification. The enigmatic Ediacaran organisms of the Precambrian show a wide range of symmetries [14], but their affinities remain highly debatable. Symmetry of a particular polyradial order is virtually unknown in living sponges. In living species, such symmetry is difficult to detect because of their complex skeleton, the trend towards compound, plastic body form, and hexactinellid syncytiality, all of which potentially obscure fundamental
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symmetry that may be present in their organisation but not visibly expressed. Many hexactinellids and Calcarea show repeating skeletal or organisational structures in cross section [11], but no examples with consistent polyradial order are known. The only expression of poriferan polyradial symmetry described [15] is the tetraradial ‘‘cellules en croix’’ in the larva of Sycon (Calcarea) [16]. This may be visible because the early growth stage allows the fundamental distribution of primary cell types to be recognisable, before being obscured by cell multiplication in later ontogeny. Among fossil sponges, derived members of most lineages are thick-walled, complex, and sometimes irregularly lobate; for example, the Ordovician Brachiospongia [17] and Aulocopella [18] usually show eight to ten lobes. In contrast, early sponges such as reticulosan hexactinellids, protomonaxonids, and eiffeliid heteractinids (Fig. 1) were much more constrained in body form, with a clear vertical axis [19]. Symmetry is visible when the body wall is distinctly prismatic, or when expressed in distinctive spicule distribution around the circumference.
2 Materials and methods This study is based on a survey of palaeontological literature that reveals a previously unrecognised pattern examination, combined with new specimens of fossil sponges from the Hetang Biota of Anhui, China [20, 21]. The new material is from the Xidi brick pit in southern Anhui, China
Chin. Sci. Bull. (2014) 59(7):639–644
(29°520 N; 118°030 E). The rocks are largely homogeneous, pyritic black mudstones of imprecisely constrained, early Cambrian age (Meishucunian–Qiongzhusian, equivalent to Tommotian–Atdabanian) [20], including an organic-rich ‘‘Stone Coal’’ in the lower part. Sponges are abundant and preserved largely as spicule replacement by pyrite and/or clay minerals [21]. Specimens were photographed using a Nikon D80 with extension tubes and Sigma 105-mm macro lens and whitened with magnesium oxide smoke. All specimens (NIGP154642-154662) are housed in the Nanjing Institute of Geology and Palaeontology, China.
3 Prismatic sponges Examples of prismatic and other sponges with polyradial symmetry are illustrated in the Fig. 1. Known examples of prismatic sponges include several of the mostly Devonianage prismodictyine dictyosponges [17, 22]. Prismatic taxa are generally octagonal, but this common symmetry has been overlooked and no significance has previously been attached to their body form. Hydnoceras shows a regular array of nodes, arranged in four pairs around the axis to give pseudo-octagonal, tetragonal symmetry. The Carboniferous Ursaspongia [17] is tetrastellate, and the Burgess Shale (Middle Cambrian) dictyospongioid Protoprisma annulata [23] is octastellate. We have not found any examples of prismatic sponges with polyradial symmetry of different order.
Fig. 1 Illustrations of representative Palaeozoic sponges with polyradial symmetry, redrawn from the published sources indicated: a Cyathophycus loydelli [24]; b Petaloptyon danei [23]; c Prismodictya telum [17, 22]; d Ursaspongia tulipa [17]; e Protoprisma annulata [23]; f Takkakawia lineate [18]
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In the circular Carboniferous dictyospongioid Uphantaenia, the skeleton consists of orthogonal bundles of monaxon spicules, with 32 bundles around the perimeter [17]. A similar numerical symmetry is seen in Cyathophycus loydelli, where the youngest known juveniles of C. loydelli possessed a grid with eight spicules around the circumference [24]. These taxa include both tetraradial and octaradial symmetry, but the clustering of nodes in Hydnoceras [22] and the body form of Ursaspongia [17] imply that tetraradiality is primary.
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than only body outline. A tetraradial protospongiid has also recently been described [26], with four columns of projecting monaxons. Such structural differences in the skeleton indicate genetic control over placement of particular spicule types. Polyradial symmetry is also present in the problematic heteractinid calcarean Petaloptyon danei (Burgess Shale, Middle Cambrian), which was divided into longitudinal panels with and without gaps [23]. In this case, the panels and symmetry were irregularly developed, such that Petaloptyon’s symmetry appears to have been variable (although in some cases approximately hexagonal).
4 Structural symmetry The Burgess Shale sponge Takakkawia possessed an elongate body with eight longitudinal spiculate strands [23], which results from division of primary tetraradial symmetry [25]. In this case, structural differences in the skeleton define the symmetry, rather
5 Metaxyspongia Metaxyspongia is a reticulosan (hexactinellid-like) sponge with discrete longitudinal columns of larger, diagonally
Fig. 2 Metaxyspongia sp. from the Hetang Biota, South China, showing tetraradial symmetry of spicule columns (numbered and stippled in camera lucida drawings). a NIGP154642 entire specimen showing variation along length of vertical spicule columns, with columns 1 and 3, and impression of column (2) on opposite surface visible; another specimen partly overlies the base, and the centre is cut by a tool mark. b, d Photograph and camera lucida drawing of specimen NIGP154643, flattened along a plane between spicule columns. c, e Light photograph and camera lucida drawing of specimen NIGP154644 flattened approximately along the plane aligned with spicule columns. Numbers in brackets refer to columns on opposite surface, and therefore largely obscured by skeletal wall. Scale bars 5 mm
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Fig. 3 Additional new taxa with similar skeletal architecture to Metaxyspongia, all from the Hetang Biota, South China. a, b New species 2: a NIGP154648, partial specimen with semi-overlying columns (numbered) of asymmetric, pyritised spicules and weakly preserved inter-column spiculation; b detail of modified spicules in single column of specimen NIGP154649. c, e, f New species 3: c NIGP154650, poorly preserved but showing rapidly expanding outline and traces of spicule columns; e, f NIGP154651, faintly preserved specimen with boxed area (shown in detail, f) of column showing very small, diagonally oriented spicules (clearest examples arrowed). d NIGP154652, Metaxyspongia? sp., damaged specimen, with wall torn and partly uncurled so that all four columns are visible. Scale bars: a, c–e 10 mm; b, f 5 mm
oriented spicules. The only described species is from the early Cambrian Huangbeiling fauna of Anhui, China [27]; it shows four evenly separated longitudinal columns of modified hexactine spicules. Although the description [27] states three columns, this is presumably due to the fourth being on the opposite side of the specimen, as shown by the equal spacing of the three visible columns across its flattened diameter. New collections from the Hetang Biota [20, 28] of Anhui, China, confirm tetraradial symmetry in a new species of Metaxyspongia (Fig. 2) and several related new sponges (Fig. 3).
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Metaxyspongia was thin-walled, and the sponges preserved flattened; the two surfaces are superimposed with one wall partially obscuring the other (Fig. 2a). Specimens were compressed in various orientations (Fig. 2a–c), implying a circular rather than polygonal cross section. There are four columns of prominent, diagonally oriented spicules, often with non-orthogonal rays, such that the lower pair of rays form an acute angle, and the upper pair an obtuse angle. The inter-column wall of Metaxyspongia consists of mostly diagonally oriented spicules (Fig. 2), usually simple hexactines or stauractines in an irregular
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Fig. 4 Phylogenetic relationship of some early sponges, including Metaxyspongia. a Reconstruction of Metaxyspongia showing skeletal architecture and tetraradial symmetry. b Distribution of tetraradial (including secondary octaradial) symmetry in the stem and crown groups of Hexactinellida (Hex), Demospongiae (Dem.), and Calcarea (Cal.). For discussion of phylogeny, see Botting et al. [21]; Protomonaxonida may be stem-group sponges rather than stem-group Silicea. Homoscleromorpha are not shown, although most phylogenetic reconstructions show them as sister-group to Calcarea
array. The vertical spicule columns are distinct and clear, but sometimes obscured for part of their length by the superimposed body wall, or by a thin layer of sediment that entered the central cavity. Where partly concealed, the columns are visible as ridges with some spicule rays visible. In all cases, the spicule columns are clearly visible at least at the apex of the sponge, and in each specimen, there were four columns. In some specimens, the sponge is compressed such that one column is positioned centrally, and two at the edges of the flattened sponge; the fourth is therefore almost superimposed on the central column (Fig. 2c). When compressed in other orientations, the sponges show either all four columns clearly separated (Fig. 2a) or the sponge is preserved at 45° to the columns, such that there are two pairs of columns nearly overlying each other. In all cases, the spacing between circumferentially adjacent columns is half the flattened diameter, which rules out any possibility of additional, concealed columns. A reconstruction is provided (Fig. 4a).
6 Discussion The Hetang fauna is among the earliest definite sponge faunas yet known [20]. Isolated spicules are known from basal Cambrian and Ediacaran deposits [29], but many are ambiguous and uninformative. Metaxyspongia and its relatives possessed a simple body form, loose spiculation, and no anchoring spicules, features considered primitive among hexactinellid-like sponges [17, 19, 24]. The group therefore
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appears to represent an early-branching lineage within spiculate sponges, although its exact relationships are unclear; it may fall into the stem-group of Silicea, or of a more inclusive group. The presence of polyradial symmetry in reticulosans (presumed stem-group Hexactinellida or Silicea), protomonaxonids (stem-group Silicea or Porifera), and heteractinids (uncertain affinity) implies a broad distribution among early sponges (Fig. 4b), supported by similar symmetry in larval Calcarea [16]. Although the exact relationships of some taxa are ambiguous, the symmetry is present in several highly distinct lineages. The relationships of protomonaxonids were discussed by Botting et al. [21], and may be more basal than shown here, further implying a broad distribution. It is unclear whether Cyathophycus and Protoprisma represent the stem-group of Silicea or Hexactinellida, and here, they are left in an unresolved polychotomy (Fig. 4b). Dictyosponges possessed hexactinellid-diagnostic microscleres, and represent a more derived lineage [30]. This distribution of taxa implies that tetraradial symmetry was present at the base of Silicea and the base of Porifera. It might be argued that this distribution reflects convergence, with tetraradial symmetry conferring an advantage to erect sea floor organisms. However, every early sponge group with consistent symmetry shows tetraradiality. This contrasts dramatically with the diverse symmetry shown by members of the Ediacaran Biota [14]. This strongly suggests shared ancestry of tetraradiality in sponges, as multiple convergence should have resulted in a range of symmetry types. The distribution of this symmetry among all major lineages implies that it was primitive for Silicea, and probably also Porifera (Fig. 4b). Loss of expressed symmetry in all lineages is an inevitable result of increasing morphological complexity obscuring the primitive organisation. The repeated appearance of tetraradiality in later Palaeozoic groups suggests that the genetic basis was retained but not visibly unexpressed through a range of lineages.
7 Conclusions It remains unclear whether tetraradial symmetry in sponges is shared with, for example, that in medusozoan Cnidaria. Although octaradial symmetry appeared early in cnidarians [31], most current hypotheses regarding cnidarian ancestral symmetry [10, 11] do not allow primitive tetraradiality or octoradiality. No genes coding for such symmetry have been found in extant sponges, and it is likely that if they still exist they are now highly modified. Nonetheless, significant implications arise from the existence of regular symmetry in early poriferans, irrespective of whether this
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symmetry is homologous with that in other groups. Sponges are traditionally thought to have evolved directly from amorphous, semi-integrated choanoflagellate colonies, but our observations imply that the earliest-known sponges were highly regular, genetically constrained individuals. This supports the emerging view from molecular biology that implies that basal sponges possessed sufficiently complex genetics to construct differentiated tissues in an organised body [32]. The apparent simplicity and disorganisation of modern sponges is therefore likely to be secondary.
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Acknowledgments We thank Lucy Muir for helpful discussions and several anonymous reviewers for comments on previous versions. Photographs of Petaloptyon and access to specimens were kindly provided by Jean-Bernard Caron and Peter Fenton (Royal Ontario Museum). This study was supported by the Chinese Academy of Sciences (KZZD-EW-02), the Project-Oriented Hundred Talents Program of the Chinese Academy of Sciences (KZCX2-YW-BR-23), and the National Science Foundation of China Research Fellowship for International Young Scientists (41150110152).
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References
21.
1. Brusca RC, Brusca GJ (2003) The invertebrates, 2nd edn. Sinauer, Sunderland, Massachusetts 2. Giribet G, Dunn CE, Edgecomb GD et al (2007) A modern look at the animal tree of life. Zootaxa 1668:61–79 3. Philippe H, Derelle R, Lopez P et al (2009) Phylogenomics revives traditional views on deep animal relationships. Curr Biol 19:1–7. doi:10.1016/j.cub.2009.02.052 4. Sperling EA, Peterson KJ, Pisani D (2009) Phylogenetic-signal dissection of nuclear housekeeping genes supports the paraphyly of sponges and the monophyly of Eumetazoa. Mol Biol Evol 26:2261–2274. doi:10.1093/molbev/msp148 5. Dunn CW, Hejnol A, Matus DQ et al (2008) Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452:745–749. doi:10.1038/nature06614 6. Schierwater B, Eitel M, Jakob W et al (2009) Concatenated analysis sheds light on early metazoan evolution and fuels a modern ‘‘urmetazoon’’ hypothesis. PLoS Biol 7:e1000020. doi:10.1371/journal.pbio.1000020 7. Philippe H, Brinkman H, Lavrov DV et al (2011) Resolving difficult phylogenetic questions: why more sequences are not enough. PLoS Biol 9:e1000602. doi:10.1371/journal.pbio. 1000602 8. Erpenbeck D, Wo¨rheide G (2007) On the molecular phylogeny of sponges (Porifera). Zootaxa 1668:107–126 9. Sperling EA, Pisani D, Peterson KJ (2007) Poriferan paraphyly and its implications for Precambrian palaeobiology. Geol Soc Spec Publ 286:355–368. doi:10.1144/SP286.25 10. Finnerty JR (2003) The origins of axial patterning in the metazoa: how old is bilateral symmetry? Int J Dev Biol 47:523–529 11. Manuel M (2009) Early evolution of symmetry and polarity in metazoan body plans. C R Biol 332:184–209. doi:10.1016/j.crvi. 2008.07.009 12. Dong X, Cunningham JA, Bengtson S et al (2013) Embryos, polyps and medusae of the Early Cambrian scyphozoan Olivooides. Proc R Soc B. doi:10.1098/rspb.2013.0071 13. Van Iten H, Zhu M, Li G (2010) Redescription of Hexaconularia He and Yang, 1986 (Lower Cambrian, South China): implications
123
19.
20.
22.
23.
24.
25.
26.
27.
28.
29. 30.
31.
32.
for the affinities of conulariid-like small shelly fossils. Palaeontology 53:191–199. doi:10.1111/j.1475-4983.2009.00925.x Xiao S, Laflamme M (2009) On the eve of the animal radiation: phylogeny, evolution and ecology of the Ediacaran Biota. Trends Ecol Evol 24:31–40. doi:10.1016/j.tree.2008.07.015 Bergquist PR (1978) Sponges. University of California Press, Berkeley Tuzet O (1941) Sur les cellules en croix des Sycon (Sycon ciliatum F., Sycon coronatum Ellis et Sol., Sycon elegans Bower.) et leur signification. Arch Zool Exp Gen 4:151–163 Finks RM, Rigby JK (2004) Palaeozoic hexactinellid sponges. In: Finks RM, Reid REH, Rigby JK (eds) Treatise on invertebrate paleontology, part E (revised), vol 3. Geological Society of America and the University of Kansas Press, Lawrence, pp 320–448 Finks RM, Rigby JK (2004) Palaeozoic demosponges. In: Finks RM, Reid REH, Rigby JK (eds) Treatise on invertebrate paleontology, part E (revised), vol 3. Geological Society of America and the University of Kansas Press, Lawrence, pp 9–171 Botting JP, Butterfield NJ (2005) Reconstructing basal sponge relationships using the Burgess Shale fossil Eiffelia. Proc Natl Acad Sci USA 102:1554–1559 Xiao S, Hu J, Yuan X et al (2005) Articulated sponges from the Lower Cambrian Hetang Formation in southern Anhui, South China: their age and implications for the early evolution of sponges. Palaeogeogr Palaeoclimatol Palaeoecol 220:89–117 Botting JP, Muir LA, Xiao S et al (2012) Evidence for spicule homology in calcareous and siliceous sponges: biminerallic spicules in Lenica sp. (Porifera; ?Protomonaxonida) of early Cambrian age (535–520 Ma) from South China. Lethaia 45:463–475. doi:10.1111/j.1502-3931.2012.00308.x Hall J, Clarke JM (1899) A memoir of the Palaeozoic reticulate sponges constituting the family Dictyospongidae. N Y State Mus Mem 2:1–350 Rigby JK, Collins D (2004) Sponges of the Middle Cambrian Burgess and Stephen Shale Formations, British Columbia. R Ontario Mus Contrib Sci 1:1–164 Botting JP (2004) An exceptional Caradoc sponge fauna from the Llanfawr Quarries, Central Wales, and phylogenetic implications. J Syst Palaeontol 2:31–63 Botting JP (2012) Reassessment of the problematic Burgess Shale sponge Takakkkawia lineata Walcott, 1920. Can J Earth Sci 49:1087–1095 Jell PA, Cook AG (2011) Musaspongia amnicola, a new sponge from the Lower Devonian of Victoria. Proc R Soc Vic 123:136–140 Wu W, Yang A, Janussen D et al (2005) Hexactinellid sponges from the Early Cambrian black shale of South Anhui, China. J Paleontol 79:1043–1051 Yuan X, Xiao S, Parsely RL et al (2002) Towering sponges in an early Cambrian Lagerstatte: disparity between nonbilaterian and bilaterian epifaunal tiers at the Neoproterozoic-Cambrian transition. Geology 30:363–366 Pisera A (2006) Palaeontology of sponges—a review. Can J Zool 84:242–261 Kling SA, Reif W-E (1969) The Paleozoic history of amphidisc and hemidisc sponges: new evidence from the Carboniferous of Uruguay. J Paleontol 43:1429–1434 Park T, Woo J, Lee D-J et al (2011) A stem-group cnidarian described from the mid-Cambrian of China and its significance for cnidarian evolution. Nat Commun 2(442). doi:10.1038/ ncomms1457 Degnan BM, Leys SP, Larroux C (2005) Sponge development and antiquity of animal pattern formation. Integr Comp Biol 45:335–341