Asymmetry in an Ordovician conulariid cnidarian CONSUELO SENDINO, KAMIL ZA´GORSˇEK AND PAUL D. TAYLOR
Sendino, C., Za´gorsˇek, K. & Taylor, P.D. 2012: Asymmetry in an Ordovician conulariid cnidarian. Lethaia, DOI: 10.1111/j.1502-3931.2011.00302.x Conulariids are fossils of the presumed polyps of an extinct scyphozoan cnidarian group. Their cone-shaped skeletons normally show perfect tetraradial symmetry. However, in the Ordovician species Metaconularia anomala (Barrande 1867) from Drabov (Czech Republic), tetraradial symmetry is compromised in three ways: (1) the skeleton often shows torsion; (2) the four sides may vary in width at the same level within one individual; and (3) one side may be deleted to give a triradial skeleton. Almost 2000 specimens were studied in museum collections. About 56% of analysed specimens are twisted in an anticlockwise direction (sinistral) when viewed from the apex towards the aperture, 28% show no torsion, 1% exhibit clockwise torsion (dextral) and the remaining 15% cannot be classified. Maximum measured torsion rate was 1.5 ⁄ mm. A significant negative correlation between torsion rate and length suggests that more highly torted individuals may have survived less well. Almost 5% of individuals show loss of one side for at least part of their lengths. Although many individuals have four sides of equal width, in a significant proportion the sides are of unequal width, up to a maximum ⁄ minimum side width ratio of 2 (i.e. widest face twice the width of the narrowest). In the absence of a satisfactory taphonomic model to explain the asymmetries, they are regarded as mirroring asymmetries in the living conulariids, with the strong preference for sinistral torsion interpreted as an example of a fixed asymmetry that was genetically controlled and heritable. It is speculated that the signalling protein Nodal as well as Hox-like genes were involved in controlling the asymmetries described in M. anomala. Consuelo Sendino [
[email protected]], Department of Palaeontology, Natural History Museum, Cromwell Road, London SW7 5BD, UK; Kamil Za´gorsˇek [
[email protected]], Paleontologicke´ oddeˇlenı´, Na´rodnı´ muzeum, Va´clavske´ na´m. 68, CZ – 115 79 Praha 1, Czech Republic; Paul D. Taylor [
[email protected]], Department of Palaeontology, Natural History Museum, Cromwell Road, London SW7 5BD, UK; manuscript received on 22 ⁄ 8 ⁄ 2011; manuscript accepted on 15 ⁄ 12 ⁄ 2011.
The great majority of invertebrates living today and represented in the fossil record show a high degree of morphological symmetry, which is typically either bilateral or radial. However, there are some notable exceptions showing asymmetry. The discovery of asymmetrical species prompts several questions, notably: (1) what is the cause of the asymmetry; (2) how did the asymmetry evolve; and (3) does it have any adaptive value? For example, Fu¨rsich & Palmer (1984) studied commissural asymmetry in brachiopods, noting that it had arisen independently on several occasions, but may have been of no overall selective advantage or disadvantage to the brachiopods. Other examples of invertebrate asymmetry include the enlargement of claws on one side of the body in species of crabs, and the spiral coiling of gastropods, which is dextral in the great majority of species, but sinistral in some individuals and also in particular species (see Palmer 1996; Levin 2005). Research on modern invertebrates shows that such asymmetries: (1) may originate at different stages during development; (2) can affect the entire body plan or be restricted to certain structures; (3) are inherited or triggered by environmental factors; and
(4) may be either random or fixed in their directionality (Grande 2010). In his review of asymmetry in fossils, Babcock (2005) distinguished between conspicuous and subtle asymmetries, and between directional (or fixed) asymmetries and random or fluctuating asymmetries. An example of conspicuous asymmetry concerns the Ordovician conulariid Metaconularia anomala (Barrande, 1867), originally described from Mt Drabov, near Beroun in the Czech Republic by Barrande (1867). Locally abundant in marine fossil communities, conulariids range from Ediacaran to Upper Triassic. Most evidence points to conulariids being benthic animals that lived with the narrower end either attached to a substrate or partly buried in sediment (see Leme et al. 2008). A strong case has been made for the cnidarian affinities of conulariids (Van Iten et al. 2006), and it is generally believed that they represent biomineralized scyphozoan polyps, closely related to living coronates or stauromedusae. Conulariids are characterized by phosphatic exoskeletons in the form of acute four-sided cones, each individual having four sides separated by four corners. In addition, a midline structure is usually developed along the median line of
DOI 10.1111/j.1502-3931.2011.00302.x 2012 The Authors, Lethaia 2012 The Lethaia Foundation
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each side. Exceptionally preserved conulariids reveal the presence of four bifurcating internal septa (e.g. Jerre 1994). Some instances of hexaradial symmetry in conulariids have been described in a few individuals of otherwise tetraradial species (Babcock et al. 1987). A Vendian conulariid-like fossil is also hexaradial (Ivantsov & Fedonkin 2002; Van Iten et al. 2005). Except for the hexaradial examples noted above, conulariids generally show perfect or near-perfect tetraradial symmetry. The Ordovician species M. anomala is a rare exception that deviates from tetraradial symmetry in several ways: skeletons frequently exhibit conspicuous degrees of torsion, the four faces may be of unequal width, and occasionally one of the faces is missing, resulting in a fossil of triangular cross-section. These deviations from tetraradial symmetry have long been known (Barrande 1867; Babcock et al. 1987), but never previously studied in detail. Herein, we use collections from several museums, totalling almost 2000 specimens, to describe and quantify the asymmetry of M. anomala, and explore the cause, consequences and implications of this unusual feature.
Material and methods Conulariid steinkerns were studied from the collections of the Faculte´ des Sciences de la Terre, Universite´ Claude Bernard Lyon 1 (21 specimens), Na´rodni Museum, Prague (NMP) (1689 specimens), Natural History Museum, London (NHMUK) (35 specimens) and Naturhistorisches Museum, Vienna (38 specimens). All of these fossils come from the Libenˇ and Letna´ formations, Upper Ordovician of the same site, Mt Drabov, near Beroun in the Czech Republic (Fig. 1). Most were collected for Joachim Barrande in the middle of the 19th century. The exposure at Mt Drabov (= Mt Deˇd) was badly degraded when we visited the site in September 2010, and no further specimens were found. After carefully inspecting all of the specimens, we selected 391 from the NMP collections for detailed analysis, which represents 22% of the total of 1772 M. anomala specimens available. Note that this species is assignable to the genus Metaconularia Foerste (see
Prague Prague
Beroun
Beroun
Drabov Brno
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Vienna
50 km
Ordovician
A
60-800 m
Shales
50-300 m
Basaltic volcanics
Letna
Sandstone, greywacke, siltstone alternations
Berounian
Quartzose sandstones
Sandbian
B
Liben
C
Siluro-devonian
Fig. 1. Locality and stratigraphy. A, B, maps of the Czech Republic showing Mt Drabov, the source locality for museum collections of the asymmetrical conulariid Metaconularia anomala. C, stratigraphical column showing the two formations in which M. anomala has been found (after Chlupa´cˇ et al. 1992).
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E
F
B
C D
A
J
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K
Fig. 2. Metaconularia anomala (Barrande, 1867). A, slightly torted specimen with a schott, NMP L40890. B,C NHMUK PI CL 487; B, profile of specimen; C, view looking from the schott along the length showing slight sinistral torsion of the corners. D, E, three-sided specimen, NMP L40891; D, profile showing torsion. E, three-sided cross-section. F, specimen starting with three and a half faces and ending in four faces (arrow shows the origin of a midline from a corner), NMP L40892. G, specimen with very slight dextral torsion and broken apex, NMP L40893. H–J, specimen beginning with four sides and ending with three, NMP L40894; H, profile; I, view from the schott showing four sides; J, distal cross-section showing three sides. K, extremely torted specimen. NHMUK PI CL 506. L, view looking from the schott along the length showing strong sinistral torsion, NHMUK PI CL 508. Scale bars = 10 mm.
John et al. 2010) because of the occurrence of accessory lines and subtle wrinkling of the periderm (see Sendino et al. 2011, fig. 1); given the preservation of the specimens as steinkerns in a coarse sandstone, it is not surprising that these structures are visible in only a minority of examples. Figures 2 and 3 show
representative examples of M. anomala with varying amounts of asymmetry. The following measurements were made on each specimen using calipers: preserved length and maximum and minimum side width close to the aperture. The number of sides present in each specimen and
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Fig. 3. Metaconularia anomala (Barrande, 1867). A, B, small specimen with apex and slight sinistral torsion, NMP L40949; A, lateral view. B, distal cross-section showing sides of varying width. C, D, specimen showing sinistral torsion that is particularly clear in the view from the apex (D), NHMUK PI CL 511. E, F two different views of the same broken specimen with sinistral torsion, NMP L40950. Scale bars: A, B = 5 mm; C–F = 10 mm.
whether that number changed along the length of the specimen were also recorded. The following states were found: four sides along the entire length; three sides along the entire length; three sides transitioning to four sides towards the aperture; four sides transitioning to three sides towards the aperture; 3.5 sides (i.e. three sides with midlines plus one ‘half-side’ lacking a midline); and four sides transitioning to 2 plus 2 ‘half-sides’ towards the aperture. The direction of torsion (twisting) was assessed by viewing each specimen from the apex looking towards the aperture. In some cases, the corners at boundaries between faces were almost straight, but in others they were curved in either a clockwise (dextral) or an anticlockwise (sinistral) direction. Photographs of 26 specimens taken from the apex were used to quantify degree of torsion: the angular change in the position of the corners from the apex to the apertural end of the specimen was measured on each photograph using a protractor, this angle being divided by the length of the specimen to
give the angle of torsion per millimetre. Finally, in specimens with unbroken ends, the presence of a pointed apex or, alternatively, of a rounded ‘schott’, was recorded. The schott in conulariids apparently formed through sealing of the narrow end of the skeleton following breakage of the apex (see Van Iten 1991). Full data can be found in the Supporting Information, details of which are given below.
Results Torsion could be evaluated in about 75% of the specimens studied. Of these, 110 (28%) showed no discernible torsion, 4 (1%) showed clockwise torsion, and 220 (56%) showed anticlockwise torsion (Fig. 4). Therefore, more than half of the individuals were twisted in a sinistral direction when viewed from the apex towards the aperture (Figs 2A, C, L, K, 3A–F),
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375
? (57) 370
Frequency
Sinistral (220)
No torsion (110)
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Dextral (4) Fig. 4. Frequency of different torsion directions in Metaconularia anomala. Numbers of specimens are given in brackets. The ? indicates specimens in which the occurrence of torsion or its direction could not be determined unambiguously.
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3
?3 to 4 4 to 3
3.5
Number of sides
4 to 2 + 2 halves
Fig. 6. Frequencies of specimens of Metaconularia anomala with different numbers of sides. Grey-filled polygons are diagrammatic cross-sections with ticks indicating face midlines if present. Arrows show proximal to distal transitions in side numbers or midline occurrences.
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Torsion rate (degrees/mm)
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0.0
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Length (mm)
Fig. 5. Relationship between torsion rate and length in 26 specimens of Metaconularia anomala. There is a significant negative correlation between torsion rate and size (R2 0.2759).
0
0–1.99
2–3.99
4–5.99
6–7.99 8–9.99 10–11.9912–13.99 14–15.99 Length (cm)
Fig. 7. Frequency distributions of lengths of Metaconularia anomala specimens preserving an apex or a schott.
whereas dextral twisting was extremely rare (Fig. 2G). It should be noted that the degree of torsion often varies according to which corner was being observed – some corners show a greater curvature than do others in the same specimen. In the sample of 26 individuals in which torsion was quantified, almost half (12) had a torsion rate of 0.2–0.3 per mm (Fig. 5). Maximum torsion rate was found to be 1.5 ⁄ mm, but only six specimens had rates exceeding 0.5 ⁄ mm. Torsion rate was found to be negatively correlated with length (i.e. short specimens had higher torsion rates than long specimens), the correlation (R2 = 0.2759, P = 0.005) being statistically significant. The majority (95%) of specimens were four-sided (Fig. 6), as in most species of conulariids. Slightly over 1% were three-sided throughout (Fig. 2D, E), an
equal proportion had 3.5 sides, whereas slightly fewer than 1% possessed four sides transitioning to three sides towards the aperture (Fig. 2H–J). A very small proportion (0.25%) of specimens were found to have four sides transitioning to two sides plus two ‘halfsides’, or three sides transitioning to four sides (Fig. 2F). Preserved length ranged from 9 to 155 mm (Fig. 7). Partitioning lengths into 20 mm bins, the highest proportion of specimens occupied the 20–39 mm bin, with a long-tailed distribution of individuals in larger size bins. Both minimum and maximum width of sides range from 3 to 38 mm. In some specimens, the sides are of equal width (i.e. minimum width = maximum
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likely to be twisted as were individuals that had three sides or showed other deviations from perfect tetraradial symmetry.
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Frequency
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Discussion
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>2.00
1.90-1.99
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Maximum/minimum width
Fig. 8. Frequency distribution of the ratio between maximum and minimum side width in specimens of Metaconularia anomala.
width) but in others the widest faces are significantly broader than the narrowest, up to twice the width (Fig. 8). Specimens with unequal sides deviate appreciably from the square cross-section typical of conulariids, and instead usually have two narrow sides alternating with two broader sides (Fig. 3B). As might be expected, length correlates significantly with both minimum width (R2 = 0.6322, P < 0.001) and maximum width (R2 = 0.6983, P < 0.001), and minimum width correlates very strongly with maximum width (R2 = 0.9053, P < 0.001). It was impossible to determine the form of the apical end in about 43% of specimens, while 30% had a pointed apex and 27% a rounded schott (Fig. 2A, B, H), which is distinct from an irregularly fractured end (e.g. Fig. 3F). The relative size (length) distributions of specimens with an apex (Fig. 3A) when compared with those with a schott clearly shows that the specimens having an apex are shorter than those with a schott (Fig. 7). This is consistent with an increasing probability during life of the apex being broken-off and a schott developing at the point of breakage: relatively few individuals of M. anomala evidently survived to attain a large size with the pointed apex still present, the majority losing their apex and secreting a schott. It was possible to observe torsion in specimens of M. anomala of all sizes, from the smallest and presumed youngest specimens, to the largest and presumed oldest specimens. There was no relationship between torsion and the possession of a pointed apex or rounded schott, torsion occurring in an equal frequency in specimens with an apex or a schott. The number of sides had no bearing on torsion or its direction: normal, four-sided individuals were just as
Most individuals of M. anomala from the Ordovician of the Czech Republic deviate from the usual condition for conulariids of having a perfectly straight pyramidal exoskeleton with tetraradial symmetry and four sides of equal or almost equal width. The majority (57%) show torsion, almost always sinistral, many have sides of unequal width, and a few have only three sides or possess ‘half-sides’ lacking midlines. There are far too many specimens showing these asymmetries for their occurrence to be dismissed as pathological. Furthermore, the incidence of asymmetry cannot be explained simply by the large population (almost 2000 specimens) available for study as other large populations of conulariid species lack asymmetrical individuals, e.g. the 344 conulariid specimens from the Upper Ordovician Starfish Bed (Upper Drummuck Group) of Thraive Glen, Girvan, Scotland in the NHMUK collections. Before discussing possible biological explanations for asymmetry, however, it is necessary to consider whether the observed asymmetries can be explained by taphonomic processes. All specimens of M. anomala are found as steinkerns in sandstone without preservation of the exoskeleton. Is it conceivable that taphonomic processes are responsible for the asymmetry of these fossils? Compression, partial collapse and distortion of fossils after burial could in theory convert a symmetrical conulariid exoskeleton into an asymmetrical fossil. There are, however, objections to a taphonomic cause for each of the three kinds of asymmetry seen in M. anomala, i.e. complete or partial loss of side, torsion and sides of varying width. Apparent loss of sides could potentially be caused by collapse of the exoskeleton during burial such that one side is folded inwards and becomes invisible. However, the existence of individuals showing a gradual ontogenetic change in side number along the length of the fossil is inconsistent with this taphonomic explanation. Torsion is also difficult to explain as a taphonomic artefact, given the overwhelming dominance of sinistral twisting; torsion after burial would be expected to be random in direction, unless all of the conulariids were buried upright and subjected to the same shearing force that twisted the fossils in a single direction, which is considered to be a very unlikely scenario. Compression after burial could in theory account for individuals having two broad and two narrow sides, the narrow sides being those oriented at right angles to bedding and subjected
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to the greatest compressive forces. Indeed, the diamond-shaped cross-sections of many specimens, with two corners of less than 90 and two of more than 90, is probably the result of such compaction. However, this explanation cannot apply when, as in the majority of specimens, torsion is also present, in which case, particular sides have different orientations along the length of the conulariid with respect to bedding and the presumed direction of maximum compression. Other conulariid species described from Mt Drabov by Joachim Barrande (1867), and revised by Boucˇek (1939; see also John et al. 2010), are Metaconularia bohemica (Barrande 1867), M. consobrina (Barrande 1867), M. munita (Barrande 1867) and Conularia rugulosa Barrande 1867 (personal observations of CS on collections in the NHMUK and NMP). All are preserved in three dimensions and all lack the torsion seen in M. anomala. Furthermore, the typical features resulting from taphonomic compression of conulariids, as discussed by Babcock et al. (1987) and John et al. (2010), are not seen in the specimens of M. anomala studied here. Therefore, asymmetry of M. anomala characterized the living conulariid animal and is not a taphonomic artefact. According to Palmer (2009), asymmetries induced by environmental factors show no preference for one direction over the other, whereas fixed asymmetries (either dextral or sinistral) are inherited features controlled genetically. The very high proportion of sinistral compared with dextral individuals of M. anomala is good evidence that the asymmetry of this species has a genetic, heritable basis; reversed individuals are known to occur occasionally in species with fixed asymmetry (Palmer 2009), which is consistent with the occurrence of a small number of dextral specimens of M. anomala. Deviations from tetrameral symmetry are quite common in the living scyphozoan relatives of conulariids. While it is generally assumed that scyphomedusae are tetramerous (Eggers & Jarms 2007), variation in symmetry is observed in most populations at a rate of approximately 2%, but sometimes as high as 10% (Gershwin 1999). For example, in a population of Aurelia labiata, Gershwin (1999) found individuals with bimerous, trimerous, pentamerous, hexamerous and heptamerous symmetry. The lack of a difference in the proportion of non-tetramerous medusae produced by strobilation by stressed and unstressed polyps suggested to Gershwin that environmental factors did not play an important role in symmetry determination, but that asymmetry was instead genetically controlled. Although these living scyphomedusae show deviations in the number of sides in the medusae, there is no indication in the literature of torsion in the polyp stage (ephyrae) from which the medusae
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are strobilated; M. anomala is perhaps the only example of a scyphozoan polyp stage, living or fossil, routinely showing torsion. It is informative to place the asymmetry of M. anomala into the broad context of metazoan evolution and developmental biology. Cnidarians represent the sister group of the Bilateria and have been invoked as proxies for the pre-bilaterian ancestral condition (Finnerty 2003). Genomic sequencing has shown that the vast majority of genes involved in axial organization and the generation of bilaterian mesoderm were already present in the common ancestor of cnidarians and bilaterians (Martindale 2005). Studies examining the spatial deployment of these genes during cnidarian development indicate that cnidarians are much more complex at the molecular level than they appear at the morphological level, challenging conventional wisdom about the rate and direction of evolutionary change. Current data favours the interpretation that bilateral symmetry evolved once in the common ancestor of cnidarians and bilaterians (Finnerty 2003). Advances in molecular developmental biology have revealed several factors that can influence the symmetry of organisms, notably: (1) Hox genes which are switches that allow for regionalization, determining the structure and orientation of the organism; and (2) the signalling molecules Nodal (encoded by the nodal gene) regulating left-right asymmetry and MAPK (Mitogen-activated protein kinase) specifying the dorsal–ventral (DV) axis. These are discussed below. The Hox genes of Bilateria and the Hox-like genes found in diploblastic animals are closely related to the primary body axes (oral-aboral (OA) axis and anterior–posterior (AP) axis) (Schierwater & Kamm 2010). The adult plan of cnidarians reveals regionalization along the primary body axis (head, column and foot in polyps), which is the OA axis. Embryological evidence implies homology between the OA axis of cnidarians and the AP axis of bilaterians (Finnerty 2003). It seems likely that Hox and other genes were involved in patterning the main longitudinal axis of cnidarians and bilaterians before these two groups split about 600 Ma (Martindale 2005). The anterior-Hox-like genes cnox1-Pc and cnox2-Pc and the posterior-Hox-like gene cnox4-Pc have been found along the OA axis of the planula larva of cnidarians (Finnerty 2003). Three Hox-like genes (hox7, hox8 and hox1a) and two transforming growth factor-b (TGF-b) family members are expressed asymmetrically along the axis that runs perpendicular to the OA axis (Martindale 2005). Although cnidarians appear to possess fewer Hox genes than bilaterians, they are expressed in a similar developmental context. Therefore, Hox-like genes
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might be responsible for patterning the axis and, if so, the axial patterning mechanisms responsible for regionalization of the primary body axis may have had its origin in the common ancestor of cnidarians and bilaterians. Nodal is a protein regulating left-right asymmetry in deuterostomes (Duboc et al. 2005), a member of the TGF-b family. This protein has also been identified in molluscs and annelids. In gastropods, Nodal is asymmetrically expressed along the left–right axis and functions in left–right asymmetry: dextral species show Nodal expression on the right side of the embryo, sinistral species show it on the left (Grande & Patel 2009). Patterning of left–right asymmetry depends upon a cascade of inductive and repressive interactions between asymmetrically expressed genes such as those coding for Nodal and also for MAPK. Grande & Patel’s (2009) experiments on gastropods suggest that a role in left–right asymmetry determination may be the earliest function of Nodal in the embryo. The MAPK network regulates cell division, gene transcription and cell differentiation in metazoans (Iakovleva et al. 2006). Inactivation of the pathway can lead to abnormalities. MAPK has been investigated in groups of molluscs and annelids where it is critical for the normal cleavage (division of cells in the early embryo) cycles of the D-quadrant, normal induction of the D-quadrant to the micromeres and subsequent organizer activity and proper differentiation (Grande 2010) that have direct consequences on the DV axis. Its applicability to cnidarians remains unclear. In summary, there are two potential developmental controls that may have been fundamental in determining the asymmetry observed in the conulariid Metaconularia anomala: Hox-like genes and the Nodal protein. The likely existence of one or both of these factors in an Ordovician putative scyphozoan provides a deep time perspective on evolutionary development in cnidarians. Functional advantages conferred by the three kinds of asymmetry seen in M. anomala (i.e. torsion, loss of sides and unequal side widths) are difficult to conceive, especially in view of the varying degrees to which these asymmetries are expressed between different individuals. More likely, selection pressures were sufficiently lax that individuals with asymmetries were not disadvantaged seriously enough to prevent them from surviving and reproducing. Nevertheless, the significant negative correlation between rate of torsion and length does suggest that individuals with minor degrees of torsion were able to survive for longer and hence grow larger than individuals with high degrees of torsion.
LETHAIA 10.1111/j.1502-3931.2011.00302.x Acknowledgements. – This study was partly funded by the Czech government Project of the Ministry of Culture: DE06P04OMG009: Veˇdecka´ a muzeologicka´ revize a dokumentace vybrany´ch cˇa´stı´ typove´ho materia´lu ve sbı´rka´ch paleontologicke´ho oddeˇlenı´ NM. Comments of the two reviewers, Nigel Hughes and Mark Wilson, helped to improve this paper. Piotr Kuklinski is thanked for providing statistical advice.
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Asymmetry in a conulariid cnidarian
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Supporting Information Additional Supporting Information may be found in the online version of this article: Table S1. Data collected from 391 specimens of Metaconularia anomala. Please note: Wiley-Blackwell are not responsible for the content or functionality of any supporting materials supplied by authors. Any queries (other than missing material) should be directed to the corresponding author for the article.
