SKELETAL MICROSTRUCTURE INDICATES CHANCELLORIIDS and HALKIERIIDS ARE CLOSELY RELATED by SUSANNAH M

Home , Canadia (annelid), Halkieriid, Hyolitha, Kimberella, Sclerite, Wheeler Shale

[Palaeontology, Vol. 51, Part 4, 2008, pp. 865–879]

SKELETAL MICROSTRUCTURE INDICATES CHANCELLORIIDS AND HALKIERIIDS ARE CLOSELY RELATED by SUSANNAH M. PORTER Department of Earth Science, University of California at Santa Barbara, Santa Barbara, CA 93106, USA; e-mail: [email protected]

Typescript received 7 November 2005; accepted in revised form 7 September 2007

Abstract: Chancelloriids are problematic, sac-like animals and siphogonuchitid sclerites are homologous. The difference whose sclerites are common in Cambrian fossil assemblages. in chancelloriid and halkieriid body plans can be resolved in They look like sponges, but were united with the slug-like two ways. Chancelloriids either represent a derived condition halkieriids in the group Coeloscleritophora Bengtson and exhibiting complete loss of bilaterian characters or they repre- Missarzhevsky, 1981 based on a unique mode of sclerite con- sent the ancestral condition from which the bilaterally sym- struction. Because their body plans are so different, this pro- metric halkieriids, and the Bilateria as a whole, derived. The posal has never been well accepted, but detailed study of their latter interpretation, proposed by Bengtson (2005), implies sclerite microstructure presented here provides additional that coeloscleritophoran sclerites (‘coelosclerites’) are a plesi- support for this grouping. Both taxa possess walls composed omorphy of the Bilateria, lost or transformed in descendent of a thin, probably organic, sheet overlying a single layer of lineages. Given that mineralized coelosclerites appear in the aragonite fibres orientated parallel to the long axis of the fossil record no earlier than c. 542 Ma, this in turn implies sclerite. In all halkieriids and in the chancelloriid genus Archi- either that the Ediacaran record of bilaterians has been misin- asterella Sdzuy, 1969, bundles of these fibres form inclined terpreted or that coelosclerite preservability increased at the projections on the upper surface of the sclerite giving it a beginning of the Cambrian Period. The former is difficult to scaly appearance. On the lower surface of the sclerite, the pro- reconcile with Ediacaran trace and body fossil evidence, but jections are absent. This microstructure appears to be unique the latter may be possible, reflecting either independent min- to chancelloriids, halkieriids, and their relatives, siphogonu- eralization of organic-walled sclerites in chancelloriids and chitids and sachitids. (The sclerites of another putative hal- halkieriids or the opening of a taphonomic window that kieriid relative, Wiwaxia Walcott, 1911, are unmineralized, favours coelosclerite preservation. making direct comparisons impossible.) Thus, similarity both at the level of sclerite construction and the level of sclerite Key words: chancelloriids, halkieriids, biomineralization, microstructure suggests that chancelloriid, halkieriid, sachitid, microstructure, sclerites, Coeloscleritophora.

Chancelloriids were Cambrian animals that pos- Butterfield and Nicholas (1996) rejected a coeloscleritoph- sessed a radially symmetrical, sac-like body covered with oran affinity and instead supported the original interpre- an array of star-shaped sclerites. Their phylogenetic affini- tation of chancelloriids as sponges. Mehl (1996) also ties are controversial; first interpreted as sponges (Walcott rejected a coelosceritophoran affinity, and speculated that 1920; Sdzuy 1969), they were later united with the halki- chancelloriids may be related to ascidians. Conway Morris eriids, wiwaxiids, sachitids, and siphogonuchitids into the and Chapman (1996) suggested that the chancelloriid and Coeloscleritophora Bengtson and Missarzhevsky, 1981, a halkieriid body plans are so different that it is likely their group characterized by a multisclerite exoskeleton and sclerites are convergent. In a later paper, they recognized mineralized sclerites displaying a prominent internal only halkieriids, siphogonuchitids, and wiwaxiids as a cavity, a restricted basal foramen, and no evidence of natural group (Conway Morris and Chapman 1997). accretionary growth (Bengtson and Missarzhevsky 1981). Most recent systematic treatments are agnostic about the Later, Bengtson et al. (1990) and Bengtson (2005) added higher-level relationships of chancelloriids (e.g. Mehl some microstructural observations in support of the 1998; Fernańdez Remolar 2001; Janussen et al. 2002; hypothesis. Randell et al. 2005); only Bengtson and Hou (2001) The affinities between chancelloriids and other coelo- and Bengtson (2005) have argued recently in favour scleritophorans have never been well accepted, however. of a coeloscleritophoran affinity. Criticism of a

ª The Palaeontological Association doi: 10.1111/j.1475-4983.2008.00792.x 865 866 PALAEONTOLOGY, VOLUME 51 chancelloriid-coeloscleritophoran relationship has been Swedish Museum of Natural History, Stockholm; SM, Sedgwick based primarily on the dissimilarity between chancelloriid Museum, University of Cambridge; GPIN, Nanjing Institute of and wiwaxiid sclerites (a criticism that is undermined by Geology and Paleontology, Nanjing; and GSC, Geological Survey the questionable status of the wiwaxiids themselves; see of Canada, Ottawa. Butterfield 1990), but rejection of the concept reflects a more general unease about the fundamental difference in chancelloriid and halkieriid body plans (e.g. Dzik 1994; MICROSTRUCTURE OF Conway Morris and Chapman 1996). Halkieriids clearly COELOSCLERITOPHORAN SCLERITES possessed bilateral symmetry and exhibited additional characters, including accretionary shells and a slug-like Halkieriid sclerites foot, that suggest a relationship with members of crown- group Bilateria, in particular, members of the Lophotro- Porter (2004b) studied well-preserved sclerites belonging chozoa (Conway Morris and Peel 1995). They thus to halkieriids from the Middle Cambrian Georgina presumably possessed other bilaterian or eumetazoan char- Basin, Australia, and provided a reconstruction of scler- acters such as a gut, internal organs, and a coelom. Chan- ite microstructure. Comparison with other halkieriid celloriids, in contrast, lack bilateral symmetry, as well as a species described in the literature indicates that there is gut, internal organs, and a coelom (Bengtson 2005). a microstructural theme that characterizes the entire Given such distinct differences in body plans, it is pos- group. It consists of the following four characters (see sible that the similarity in halkieriid and chancelloriid Text-fig. 1): sclerite construction noted by Bengtson and Missarzhev- 1. A thin outer layer, possibly organic in original compo- sky (1981) is the result of convergent evolution. But even sition. Almost all halkieriid casts exhibit this outer layer, when skeletal elements are similar at one level, conver- preserved through secondary phosphatization. It can be gence can often be detected by examining other structural identified by its smooth or granular, wrinkled appearance. levels (Hickman 2004). Here, I build on the observations It is often partly degraded, particularly where it covers of Bengtson et al. (1990), Porter (2004b), and Bengtson tubercles or plates (Pl. 1, figs 4, 6, 15, 17, 20); fibrous ele- (2005) as well as new observations of the chancelloriid, ments of the inner layer are occasionally visible beneath Archiasterella hirundo Bengtson, in Bengtson et al. 1990, (Pl. 1, fig. 4). The outer layer is distinct from any second- presented here, to show that the sclerites of chancelloriids, ary diagenetic coating, which is usually thicker, consists halkieriids, sachitids, and siphogonuchitids not only have of radially orientated crystals, and obscures detail on the a unique mode of sclerite construction but also share a sclerite surface (e.g. Pl. 1, figs 7–8). A primary origin is unique sclerite microstructure. also suggested by its contact with internal moulds (Porter 2004b). An originally organic composition, now replaced by calcium phosphate, is suggested by two observations. MATERIAL AND METHODS First, it sometimes appears wrinkled, indicating a degree of pliability (Pl. 1, figs 11–12). Second, its texture, con- Sclerites of Archiasterella hirundo were picked from acid sisting of spheroidal, randomly orientated calcium phos- maceration residues obtained during an earlier study of phate crystals, appears similar to that observed in Early Cambrian fossils from South Australia (Bengtson secondarily phosphatized fossils known to have been et al. 1990). The fossils come from samples UNEL1763a originally organic (Porter 2004b). Whether or not the and UNEL1848 from the Parara Limestone, Curramulka, layer may have been lightly mineralized is unclear. For a Yorke Peninsula (localities described in Bengtson et al. more detailed discussion of primary versus secondary 1990). Sclerites are preserved as phosphatic casts and diagenetic coating and evidence for original composition, moulds. Specimens were coated with gold and palladium see Porter (2004b). and viewed using a JEOL JSM-6300V scanning electron 2. An inner layer composed of aragonite fibres orientated microscope at 15 kV. Specimens of Australohalkieria parallel to the long axis of the sclerite and either parallel superstes Porter, 2004b and Wiwaxia Walcott, 1911 were to the sclerite surface or inclined toward its distal tip. processed in an earlier study of Middle Cambrian phos- Phosphatic casts of longitudinally orientated fibres may phatized assemblages from the Georgina Basin, Australia be observed where the outer organic layer is degraded (Porter 2004b). (e.g. Pl. 1, fig. 4) or entirely gone (Pl. 1, figs 10, 22). Fibres may also be preserved as external moulds, giving Repositories. The specimens illustrated here are housed in the steinkerns a ‘subdued fibrosity’ (Bengtson et al. 1990, p. following repositories, which are abbreviated as follows: CPC, 81, fig. 62F). Fibres may be either more or less parallel to Commonwealth Palaeontological Collections, Geoscience Austra- the sclerite surface (Porter 2004b, fig. 6.5) or imbricated lia, Canberra; SAM, South Australia Museum, Adelaide; SMNH, toward the distal tip of the sclerite (Pl. 1, figs 9–10, 14– PORTER: RELATIONSHIP OF CHANCELLORIIDS AND HALKIERIIDS 867

A 3 1

? ? ?? ? ? ???

4 2

organic layer

100 µm aragonite fibres

TEXT-FIG. 1. A model of halkieriid sclerite microstructure. Sclerite is shown in longitudinal section. Scale bar is a rough approximation of size; sclerites of different species can vary in size by a factor of two or more. A, close-up of the upper sclerite surface, illustrating microstructural characters 1, 2, and 3. Note also the pits in the inner surface, represented by bumps in internal moulds. Relationship between the projections and the main wall is uncertain, as indicated by question marks. Note that the larger view of the sclerite shows a continuous relationship between the projections and the main wall; see Bengtson (2005) for a dissenting view. B, close-up of the lower sclerite surface. Microstructural character 4 is indicated in the large model.

15, 22). An originally aragonitic composition of the inner 2005, fig. 4) or they may be continuous with it (cf. layer is suggested by its fibrous structure and ubiquitous Porter 2004b, fig. 7). Projections are commonly inclined remineralization (Bengtson and Conway Morris 1984; from the vertical toward the tip of the sclerite (Pl. 1, Runnegar 1985; Bengtson et al. 1990; Porter 2004b). figs 3–4, 14–15, 18, 21; Bengtson et al. 1990, figs 46F, Bumps on the surfaces of internal moulds suggest that 48F–G). this inner layer was either pitted or permeated by pores 4. A lower surface where the projections are absent. No (Pl. 1, fig. 13; cf. Wrona 2004). tubercles, spines, plates or lamellae are observed on the 3. Aragonite fibres bundled into discrete ‘projections’ underside of halkieriid sclerites. Instead, there are thin, that are commonly inclined from the vertical toward imbricated layers of fibres (Pl. 1, fig. 22), which impart the distal tip of the sclerite. Sclerites may exhibit just an undulating appearance to the overlying organic layer one kind of projection (e.g. lamellae, Pl. 1, fig. 14; the (Pl. 1, figs 1–2). Other authors have noted that the lower ‘rows’ of Porter 2004b), or a combination: plates in the surface appears to be covered in fine transverse lineations central region of the sclerite flanked by tubercles on its (Jell 1981; Bengtson and Conway Morris 1984; Bengtson outer rims and central ribs (Pl. 1, figs 16–18); plates et al. 1990; Conway Morris and Chapman 1997); these that trend distally into tubercles (Pl. 1, figs 19–20), or are interpreted here to reflect the imbricated layers of tubercles interspersed with spines (Pl. 1, fig. 21). In fibres (Text-fig. 1B). some cases, these projections are missing, probably incompletely phosphatized and thus dissolved during acid maceration, leaving holes in the outer organic Sachitid and siphogonuchitid sclerites layer indicating where they once were (e.g. Pl. 1, figs 6, 12; Bengtson et al. 1990, fig. 48A–E). The projections A survey of published photographs and descriptions sug- appear to be formed by bundles of fibres, seen beneath gests that sachitids and siphogonuchitids exhibit the same the degraded outer layer (e.g. Pl. 1, figs 4, 15; Bengtson microstructure as halkieriids. Most sclerites of the sachitid et al. 1990, fig. 51I), and are not simply thickened out- Hippopharangites dailyi Bengtson, in Bengtson et al. 1990, growths of the organic layer. It is not clear how these for example, exhibit a thin outer layer comparable to the bundled fibres interact with the other fibres that make organic layer seen in halkieriids (Text-fig. 2A–B, H–J). up the wall; they may form a separate entity embedded Longitudinally orientated fibres visible in some partially within the larger wall (cf. the ‘platelets’ of Bengtson eroded specimens of H. dailyi (Text-fig. 2C–D) and in a 2005, fig. 6, and the ‘oblong structures’ of the chancel- specimen of Sachites proboscideus Meshkova, 1969; (Text- loriid Archiasterella Sdzuy, 1969; noted by Randell et al. fig. 2E–G) are consistent with an inner layer composed of 868 PALAEONTOLOGY, VOLUME 51

fibrous aragonite (also see Bengtson et al. 1990, p. 63, Chancelloriid sclerites who inferred that the sclerites were originally calcareous and that their inner surfaces had ‘fine longitudinal stria- The chancelloriid Archiasterella hirundo, from the Early tions’). Sclerites of H. dailyi display prominent, flattened Cambrian of South Australia, exhibits all four microstruc- tubercles on their upper surfaces that imbricate toward tural characters found in other Coeloscleritophora: the distal tip of the sclerite (Text-fig. 2A–B, H–I; S. probo- 1. A thin outer layer, possibly organic in original compo- scideus lacks projections). As with halkieriid sclerites, the sition. A thin outer layer is observable in casts of most A. tips of these tubercles are often eroded, leaving holes hirundo sclerites (Pl. 2, figs 1–10, 13). This layer is closely beneath where aragonite fibres presumably had been comparable to the outer layer found in halkieriids: it is (Text-fig. 2B, H). The lower surface of the sclerite is <1 lm thick, has a smooth or granular texture, and may smooth (Text-fig. 2I–J). be partly degraded (e.g. Pl. 2, fig. 3) or absent (Pl. 2, figs Siphogonuchitid sclerites also possess a thin, smooth 5–6, 13) where it covers tubercles. Interestingly, the outer covering comparable to the outer layer observed in organic coating covers the entire sclerite rosette in a sin- halkieriids (Text-fig. 3A–F, H). One species, Siphogonuch- gle continuous layer, rather than wrapping each individ- ites cf. triangularis Qian, 1977, possesses prominent, ual ray. This is also true for the inner fibrous layer (Pl. 2, inclined tubercles on the upper surface of their sclerites fig. 11), suggesting that the rosette was mineralized as a (Text-fig. 3A–C), although in most species, these are sub- whole, rather than fused together after ray mineralization dued (e.g. Text-fig. 3D–E) or absent (Text-fig. 3G–I). An (Mehl 1996). Its consistent thickness and lack of radially inner fibrous microstructure is evident in some specimens orientated crystals (Pl. 2, fig. 10 vs. Pl. 1, fig. 8) suggests (Text-fig. 3F, H–I; also see Qian and Bengtson 1989, fig. that, as inferred for halkieriids, it is a primary component

16A5–A6, and Conway Morris and Chapman 1996, ﬁg. of the sclerite wall, now secondarily phosphatized, rather 9H–I). than a product of diagenetic overgrowth by phosphate

EXPLANATION OF PLATE 1 Scanning electron microscopy (SEM) images of diagenetically phosphatized halkieriid sclerites. Figs 1–2, 7–8, 13–15, 22. Australohalkieria superstes Porter, 2004b. 1–2, CPC 37219. 7–8, CPC 37205. 13, CPC 37214. 14, CPC 37216. 15, CPC37180. 22, CPC 37174. Specimens in 1–2 from sample PK98-42, all others from PK98-41. All specimens from the Middle Cambrian Monastery Creek Formation, Rogers Ridge, Duchess Embayment, Georgina Basin, Australia. Images originally published in Porter (2004b) as figs 9.5, 6.11, 10.12, 10.14, 6.4, 7, 6.8, and 6.1, respectively, and reprinted here by permission of the Paleontological Society. Figs 3–4, 19–20. Thambetolepis delicata Jell, 1981. 3–4, SAM P30452. 19–20, SAM P30417. All specimens from sample UNEL 1763a, Abadiella huoi Zone, Lower Cambrian Parara Limestone, Curramulka Quarry Section, Curramulka, Yorke Peninsula, South Australia. Images originally published in Bengtson et al. (1990) as figs 56I–J and 50J–K, and reprinted here by permission of the Association of Australasian Palaeontologists. Figs 5–6. Halkieriid sclerite. SAM P41615, sample UNEL 1848, Abadiella huoi Zone, Lower Cambrian Parara Limestone, Curramulka Quarry Section, Curramulka, Yorke Peninsula, South Australia. Figs 9–10. Halkieria sp. SMNH X2095, sample Sib73-15-SB, Aldanocyathus sunnaginicus Zone, Lower Cambrian Pestrotsvet ‘Formation’, ‘Dvortsy’, River Aldan, Yakutia. Images reprinted from fig. 3B and D in ‘A comparative study of Lower Cambrian Halkieria and Middle Cambrian Wiwaxia’, Lethaia, 17, 307–329, by permission of Taylor and Francis AS. Figs 11–12. Possible halkieriid spine. SAM P42162, sample UNEL 1763a, Abadiella huoi Zone, Lower Cambrian Parara Limestone, Curramulka Quarry Section, Curramulka, Yorke Peninsula, South Australia. Figs 16–17. Australohalkieria parva (Conway Morris, in Bengtson et al. 1990). SAM P30355, sample UNEL 1846, Abadiella huoi Zone, Lower Cambrian Parara Limestone, Curramulka Quarry Section, Curramulka, Yorke Peninsula, South Australia. Images originally published in Bengtson et al. (1990) as fig. 41C–D, and reprinted here by permission of the Association of Australasian Palaeontologists. Fig. 18. Halkieria mira (Qian and Xiao, 1984). SM X26087, sample X1 ⁄ 91 ⁄ 44, Xiaoerbulak phosphorite mine. Lower Cambrian Yurtus Formation, Xinjiang, China. Image originally published in Conway Morris and Chapman (1997) as fig. 6.10, and reprinted here by permission of the Paleontological Society. Fig. 21. Halkieriid sclerite. SM X26111, sample X1 ⁄ 91 ⁄ 17, Aksu phosphorite mine, Lower Cambrian Yurtus Formation, Xinjiang, China. Image originally published in Conway Morris and Chapman (1997) as fig. 8.2, and reprinted here by permission of the Paleontological Society. PLATE 1

1 2 50 µm 3 4 5 6 20 µm 100 µm

60 µm

2 µm 25 µm

7 8 9 10

200 µm Fig. 10

in Fig.15 50 µm 1 µm 14 25 µm

11 in 12 13 15 Fig. 12

200 µm

20 µm

16 17 18 20 19

200 µm

50 µm 200 µm 50 µm

21 10 µm 100 22 µm

100 µm

PORTER, halkieriid sclerites 870 PALAEONTOLOGY, VOLUME 51

(Porter 2004b). Its original composition is unknown, but pattern is interpreted to be impressions of the fibrous ara- is assumed to have been organic because of its similarity gonite layer (no longer present) that lay just beneath. Note to the presumed organic layer of halkieriids. that the Mount Cap specimens comprise more than simply Butterfield and Nicholas (1996) isolated organically pre- the outer organic layer; some specimens preserve remnants served chancelloriid sclerites from the Mount Cap Forma- of soft tissue that filled the interior of the sclerite (Butter- tion, north-west Canada, that exhibit what they referred to field and Nicholas 1996). as a ‘cellular’ pattern on their outer surface (Text-fig. 4; see Many authors have noted the presence of a tough, also Butterfield and Nicholas 1996, fig. 5.2). This surface is organic integument covering intersclerite areas of the interpreted here to be the outer organic layer; the ‘cellular’ chancelloriid body (Walcott 1920; Butterfield and Nicho- las 1996; Bengtson and Hou 2001; Janussen et al. 2002; Randell et al. 2005). It is possible that this is continuous A B with the outer organic layer of the sclerite discussed here (Mehl 1996; Bengtson and Hou 2001; Janussen et al. B 2002; Bengtson 2005), as it also exhibits imbricated projections similar in size to those on the surface of Archias- terella sclerites (see below). 2. An inner layer composed of aragonite fibres orientated parallel to the long axis of the sclerite and either parallel to the sclerite surface or inclined toward its distal tip. In A. 250 µm hirundo sclerites with an outer layer that is missing or 50 µm partly degraded, an inner layer consisting of c.1-lm-thick fibres may be visible (Pl. 2, figs 3, 11–12). The fibres are C D orientated parallel to the long axis of each ray in the compound sclerite. Similar fibres have been observed in other chancelloriid species; in addition to their longitudinal ori- entation, these fibres are inclined toward the tip of each ray, similar to those observed in halkieriids (Bengtson et al. 1990; Mehl 1996, 1998; Kouchinsky 2000a; Janussen et al. D 50 µm 2002; Wrona 2004). There is a general consensus that these 100 µm fibres were originally aragonitic, as suggested by their acic- ular morphology (Bengtson et al. 1990; Mehl 1996; Kouchinsky 2000a; Janussen et al. 2002; Wrona 2004). F G E Primary aragonite mineralogy is also indicated by chancelloriid specimens from the Early Cambrian Forteau Forma- tion in Canada, which are preserved as calcite spar-filled G moulds and co-occur with primary calcite skeletons exhibiting fabric retention (James and Klappa 1983). 3. Aragonite fibres bundled into discrete ‘projections’ that are commonly inclined from the vertical toward the distal 800 µm tip of the sclerite. The upper surface of A. hirundo scle- 50 µm rites is covered with c. 20-lm-long tubercles, which, like

TEXT-FIG. 2. SEM images of diagenetically phosphatized H I J sachitid sclerites. A–D, H–J, Hippopharangites dailyi Bengtson, in Bengtson et al. 1990. E–G, Sachites proboscideus Meshkova, 1969. A–B, SAMP 30340. C–D, SAMP 30336. E–G, SMNH 3251. H, SAMP 30347. I–J, SAMP 30346. A–D, H–J, from sample UNEL 1852, Pararaia tatei Zone, Lower Cambrian Parara Limestone, Horse Gully Section, Ardrossan, Yorke Peninsula, South Australia. E–G, sample 241, coll. N. P. Meshkova, Tommotian Stage, River Rassokha, Siberian Platform. Images courtesy of S. Bengtson and originally published in Bengtson 150 µm 150 µm 150 µm et al. (1990) as figs 38C–D, 40D–E, 22B, A, C, and 39M, K, L, respectively. Reprinted here by permission of the Association of Australasian Palaeontologists. PORTER: RELATIONSHIP OF CHANCELLORIIDS AND HALKIERIIDS 871 the tubercles, plates, and lamellae of halkieriid sclerites, in the same direction, toward the tip of the larger median appear to be composed of bundled fibres and covered by ray and away from the strongly recurved ray (Pl. 2, figs 1, an organic layer (Pl. 2, fig. 3; see also Pl. 2, figs 1–2, 7–9). 7; see also Bengtson et al. 1990, figs 29–30). This is con- The tubercles are often arranged in a roughly regular pat- sistent with the observation, noted above, that the sclerite tern of transverse rows (Pl. 2, figs 2, 6, 13), and may be rosette was mineralized as a single unit. Tubercles are more concentrated in the centre part of the compound often missing, represented only by holes in the outer layer sclerite, particularly where the rays join (Pl. 2, figs 8, 13). (Pl. 2, figs 5–6, 9, 13). As with halkieriids, most tubercles are inclined, although Randell et al. (2005) described regularly spaced, 40– rather than inclining in four different directions toward 50 lm ‘oblong structures’ on the surfaces of both the in- the distal tip of each ray, the tubercles tend to be inclined tersclerite areas and the sclerites of Archiasterella fletcherg- ryllus Randell et al., 2005. Their size and distribution suggest that they may be homologous to the tubercles A B C observed in Archiasterella hirundo (Bengtson and Hou 2001; Bengtson 2005). Similar structures have been noted in the intersclerite areas of the chancelloriid Allonnia Dore´ and Reid, 1965 (Bengtson and Hou 2001; Janussen et al. 2002). Note that the tubercles observed in A. hirundo are different from, and not necessarily related to, the prominent bumps commonly found on chancelloriid steinkerns (e.g. 25 µm Pl. 2, fig. 15; see also Wrona 2004, fig. 6M–O, Q, and 200 µm 50 µm Bengtson et al. 1990; fig. 35). These are likely to be moulds of pores in the inner wall (Wrona 2004). Steink- D E erns of halkieriid sclerites may exhibit similar bumps on their surface (Pl. 1, fig. 13); these were interpreted by Porter (2004b) to represent moulding of a pitted surface on the inner wall, and were speculated to mirror the projections above (Text-fig. 1). 4. A lower surface where the projections are absent. The sides of Archiasterella hirundo sclerites may be covered in tubercles, but with the exception of the ray tips, the lower 300 µm surface of the sclerite is devoid of them (Pl. 2, figs 4–5). 25 µm F

F G Wiwaxiid sclerites

The relationship between wiwaxiids and other coeloscleritophorans is in dispute (Butterﬁeld 1990, 2006; Bengtson internal outer mold layer TEXT-FIG. 3. SEM images of diagenetically phosphatized siphogonuchitid sclerites. A–C, GPIN 106810. D–F, GPIN inner 106824. G–I, SMNH X2237. A–F, sample 159a, Meishucunian 200 µm H 10 µm layer Stage, Zhongyicun Member, Dengying Formation, Xianfeng, Yunnan, China. G–I, sample B-9 ⁄ 85, Lower Cambrian Bayan- Gol ‘Formation’, Salany Gol section, Khasagt-Khairkhan Range, H I Altai Mountains, western Mongolia. Images A–F reprinted from

ﬁgs 11A2, 11A5, 11A8, 13E3, 13E8, and 13E7, respectively, in ‘Palaeontology and biostratigraphy of the Early Cambrian Meishucunian Stage in Yunnan Province, South China’, from outer inner Fossils and Strata, 1989, 24, 1–156, by permission of Blackwell layer layer Publishing. Images G–I reprinted from ﬁg. 8H–J in ‘The cap- shaped Cambrian fossil Maikhanella and the relationship between coeloscleritophorans and mollusks’ from Lethaia, 1992, 25 µm 25 µm 25, 401–420, by permission of Blackwell Publishing. All images courtesy of S. Bengtson. 872 PALAEONTOLOGY, VOLUME 51

1994); these are reminiscent of the transverse rows of tubercles exhibited by the sclerites of sachitids and halkieriids. A third wiwaxiid species, represented by a single, secondarily phosphatized specimen, has a very different microstructure, however: no longitudinal lineations and transverse rows of pits instead of tubercles (Text-ﬁg. 5G– H). In addition, this species has longitudinally orientated channels instead of longitudinally orientated ribs observed distal in other wiwaxiid species and other Coeloscleritophora. direction Assuming this fossil is indeed a cast of a wiwaxiid sclerite (and not an external mould), its microstructure bears little resemblance to that of the halkieriids and other Coelo- scleritophora.

Summary

100 µm Table 1 summarizes microstructural data for halkieriids, sachitids, siphogonuchitids, and chancelloriids; wiwaxiids are not included as their unmineralized sclerites are not TEXT-FIG. 4. Light microscopy view of organically preserved directly comparable. Each family includes at least some chancelloriid sclerite from the Middle Cambrian Little Bear biota, Mackenzie Mountains, north-west Canada. Arrows species that exhibit all four microstructural characters. Sa- indicate ‘undulating’ texture of outer wall. Slide C LB-C21, coll. chitids, siphogonuchitids, and chancelloriids also include N. J. Butterfield. species with simpler microstructures: they lack the projections (character 3) that are so prominent in other species 2005; Caron et al. 2006; Conway Morris and Caron and which give them their ‘scaly’ appearance. (Interest- 2007). Because wiwaxiid sclerites are unmineralized (Con- ingly, not only do all halkieriids exhibit this character but way Morris 1985), their microstructures cannot be also the family as a whole displays a much wider diversity directly compared with those of other Coeloscleritophora. of projection ‘types’.) Whether the simpler microstructure However, it is noteworthy that the sclerites of some wi- is derived or whether it represents the primitive condition waxiid species do exhibit micro-scale patterns that are for the Coeloscleritophora is not known. broadly similar to the microstructural theme described above (see also Bengtson 2005). The phosphatized and organically preserved sclerites of Wiwaxia corrugata COELOSCLERITOPHORAN (Matthew, 1899), for example, exhibit sub-lm-scale, MICROSTRUCTURE IS UNIQUE longitudinally orientated lineations (Text-fig. 5B; also see Butterfield 1990, fig. 3B) that could be homologous to Similar microstructure in the chancelloriids, halkieriids, the longitudinally orientated aragonite fibres found in and other Coeloscleritophora would not be remarkable if other Coeloscleritophora. Similarly, some wiwaxiid scle- such microstructure were widespread. But even among rites exhibit tubercles on their surface (Text-fig. 5C–F; Cambrian animals, which might be expected to have simi- Butterfield 1990, fig. 3B), in some cases arranged in lar microstructures given their relatively recent common prominent transverse rows (Text-fig. 5E–F; Butterfield ancestor, coelosclerite microstructure is unique. Although

EXPLANATION OF PLATE 2 Figs 1–15. SEM images of diagenetically phosphatized sclerites from the chancelloriid Archiasterella hirundo Bengtson, in Bengtson et al. 1990. 1–3, SAM P41616, upper surface of sclerite. 4–5, SAM P41617, lower surface of sclerite. 6, SAM P41618, close-up of individual sclerite ray, showing holes in outer organic layer where tubercles once were. 7–10, SAM P41619, upper surface of sclerite. 11–12, SAM P41620, surface of sclerite showing ﬁbrous inner layer. 13, SAM P41621, upper surface of sclerite with holes where tubercles are missing. 14–15, SAMP 41622, upper surface of steinkern. 1–13, sample UNEL 1763a; 14–15, sample UNEL 1848. All specimens from the Abadiella huoi Zone, Lower Cambrian Parara Limestone, Curramulka Quarry Section, Curramulka, Yorke Peninsula, South Australia. See Bengtson et al. (1990) for more information. PLATE 2

1 2 3 Fig. 2

Fig. 3

100 µm 100 µm 10 µm

4 5 6 100 µm Fig. 5

100 µm 10 µm

7 8 Fig. 9 9

Fig. 10

100 µm 100 µm 10 µm

12 10 11

1 µm 100 µm 10 µm

15 13 14

Fig. 15

100 µm 100 µm 50 µm

PORTER, Archiasterella 874 PALAEONTOLOGY, VOLUME 51

A B C D

50 µm 2 µm 10 µm 2 µm

E F 50 µm G H

100 µm 25 µm 20 µm

TEXT-FIG. 5. Wiwaxiid sclerites. A–D, G–H, SEM images of diagenetically phosphatized specimens from the Middle Cambrian Monastery Creek Formation, Rogers Ridge, Duchess Embayment, Georgina Basin, Australia, sample PK98-48. A–D, no accession number; unfortunately specimen was destroyed during manipulation. Remains are located on SEM stub PK98-41-HP2, housed at the Commonwealth Palaeontological Collections (CPC), Geoscience Australia, Canberra, Australia. G–H, CPC 37228. A–C, G–H originally published in Porter (2004b) as figs 11.7, 11.10, 11.9, 11.8, and 11.11, and reprinted here by permission of the Paleontological Society. E–F, light microscopy images of organically preserved specimens, GSC 108958, GSC locality C-24836, North Colville L-21 drill-core at 1124 m, Lower Cambrian Mount Cap Formation, District of Mackenzie, Northwest Territories, Canada. Image E originally published as fig. 2b in Butterfield (1994) and reprinted by permission from Macmillan Publishers Ltd: Nature, copyright (1994). Image F courtesy of N. Butterfield. many Cambrian skeletal elements appear to have been Bengtson 1989; Bengtson 1992). The spicules of Maikha- composed of fibres, reflecting the common crystal habit nella are thought to be homologous with entire coeloscle- of aragonite (e.g. hyoliths, anabaritids, cambroclaves, and rites, however; the spine-like projections seen in several mollusc and mollusc-like taxa), the arrangement phosphatic specimens have been interpreted to be internal of these fibres in most taxa differs substantially from that moulds of a siphogonuchitid-like spine (Bengtson 1992). of coelosclerites (Runnegar 1985; Conway Morris and The microstructure of Ramenta appears to be much more Chen 1989; Bengtson et al. 1990; Kouchinsky 1999, complex, with a crossed lamello-fibrillar inner layer cov- 2000a, b; Feng et al. 2001; Kouchinsky and Bengtson ered by an outer layer of vertical fibres (Feng et al. 2002). 2002; Feng and Sun 2003). Two exceptions are some cambroclaves and ‘cap-shaped fossils’. Like coelosclerites, cambroclave sclerites appear to COELOSCLERITOPHORAN SCLERITES be composed of a single layer of fibrous aragonite, orien- ARE HOMOLOGOUS tated parallel to the long axis of the sclerite and covered by a smooth outer layer reminiscent of the outer organic If it is true that chancelloriids and halkieriids are unre- layer of coeloscleritophoran sclerites (Bengtson et al. 1990; lated, then sclerite similarities reflect convergent evolu- Conway Morris and Chen 1991). They lack, however, the tion. The idea of convergent sclerites by itself is not distally inclined projections (i.e. tubercles, lamellae, plates, surprising; biomineralization evolved independently many or spines) that characterize most Coeloscleritophora. times in animals (Bengtson and Conway Morris 1992) Similarity between cap-shaped fossil and coelosclerite and multi-element skeletons in particular seem to be microstructure would not be surprising given that repre- widespread (Kingsley 1984; Bengtson and Conway Morris sentatives of the former have been hypothesized to be 1992). But chancelloriid and halkieriid sclerites appear to part of a coeloscleritophoran scleritome (Bengtson 1992; share both macrostructural similarities (i.e. those noted Conway Morris and Chapman 1996). Some cap-shaped by Bengtson and Missarzhevsky 1981) and microstruc- fossils possess a fibrous texture (e.g. Maikhanella Zhe- tural similarities, and it seems unlikely that both arose by gallo, in Voronin et al. 1982 and Ramenta Jiang, in Luo convergent evolution. Convergence arises either because et al. 1982; see Bengtson 1992; Feng et al. 2002) and are similar characters experienced similar selective regimes or covered in granules, scales, or spicules reminiscent of the because of a limited number of ways a character can be inclined projections on most coelosclerites (e.g. Ernogia made (cf. Hickman 2004). The latter explanation is unli- Jiang, in Luo et al. 1982; Maikhanella; see Qian and kely to be true for coelosclerites; the variety of sclerite PORTER: RELATIONSHIP OF CHANCELLORIIDS AND HALKIERIIDS 875

TABLE 1. Distribution of microstructural characters 1–4 in mineralized coeloscleritophorans (the wiwaxiids are excluded because of their questionable status and because their sclerites are unmineralized).

Character # 1 2 3 4

Thin outer Single inner layer of longitudinally Projections Lower surface organic layer orientated aragonitic ﬁbres smooth

Halkieriidae Yes Yes Lamellae Yes Platelets Tubercles Spines Sachitidae Yes Yes Tubercles Yes None Siphogonuchitidae Yes Yes Tubercles Yes None Chancelloriidae Yes Yes Tubercles Yes None

‘Yes’ indicates there is evidence for this character in at least one species in the family. For character 3, the type of projection is listed for each family. Note that some species of sachitids, siphogonuchitids, and chancelloriids do not exhibit this character, as indicated by ‘none’. macro- and microstructures encountered in metazoans represent a derived body plan relative to halkieriids suggests there are many ways to make a sclerite (e.g. (Text-fig. 6A; Bengtson and Conway Morris 1984). In this Lowenstam 1989; Lowenstam and Weiner 1989). This is case, halkieriid-like ancestors of chancelloriids lost bilat- true even for the earliest animals, whose skeletons exhibit eral symmetry and, presumably, changed their mode of a wide range of constructional types (Thomas et al. 2000) feeding as they switched from a vagrant to a sessile life- and microstructures (Runnegar 1985; Kouchinsky 1999, style. Loss of overt bilateral symmetry is common in ani- 2000a, b; Feng et al. 2001; Kouchinsky and Bengtson mals (e.g. echinoderms, priapulids, and kinorhynchs), but 2002; Feng and Sun 2003). Furthermore, skeletal macro- even so, these taxa retain vestiges of their former symme- and microstructures often behave as independent charac- try as well as other key features that indicate membership ters; congruence, therefore, cannot simply be explained by in the Bilateria, such as a gut and internal organs. Chan- constraints imposed by one structural level dictating the celloriids, in contrast, betray no evidence of a bilaterian design of the other. For example, the trabecular bone of ancestry, despite their exceptional preservation (Bengtson vertebrates, the ossicles of echinoderms, and the skeletons 2005). Thus, if chancelloriids are secondarily derived, of acroporid scleractinians are all similar in their open their transformation from an ancestral bilaterian body framework architectures, although their mineralogy and plan is unparalleled. length scale of the supporting elements are quite different The second possibility, recently suggested by Bengtson and, indeed, taxon-specific (Lowenstam and Weiner 1989; (2005), is that chancelloriids represent the ancestral body J. Weaver, pers. comm. 2007). Likewise, similar micro- plan from which halkieriids were derived (Text-fig. 6B–C). structures do not necessarily induce similar macrostruc- If halkieriids are at least stem-group bilaterians, the tures, as evident by, for example, the variety of skeletal hypothesis implies that the transformation between chan- architectures built from spherulites (Lowenstam and Wei- celloriids and halkieriids captured the evolution of bilateral ner 1989). Thus, if chancelloriid and halkieriid sclerites symmetry, a gut, and internal organs that we know must are convergent, their sclerites must have been subject to have occurred at some point in bilaterian ancestry (Bengt- remarkably similar selection regimes operating at both the son 2005). Furthermore, it implies that coelosclerites are a macrostructural and microstructural level. This seems symplesiomorphy of crown group Bilateria, secondarily lost unlikely given their rather different life habits. or transformed in descendent lineages (Bengtson 2005). Significantly, the evolution of coelosclerites would predate that of other bilaterian characters, including those assumed DISCUSSION to be lacking in chancelloriids: bilateral symmetry, a gut, and internal organs (Text-fig. 6B–C). If chancelloriids and halkieriids are closely related, then This poses a conundrum. Mineralized coelosclerites the difference in chancelloriid and halkieriid body plans appear no earlier than c. 542 Ma, yet Ediacaran trace can be resolved in one of two ways, both with challenging fossils and body fossils suggest that bilaterally symmetric implications. The first possibility is that chancelloriids animals had evolved by c. 555 Ma (Narbonne 2005), 876 PALAEONTOLOGY, VOLUME 51

chancelloriids halkieriids loss of gut, halkieriids internal organs, bilateral symmetry mineralized coelosclerites Coeloscleritophora (<542 Ma) mineralized chancelloriids coelosclerites multiple losses (<542 Ma) of coelosclerites mineralized among bilaterian coelosclerites clades (<542 Ma) Crown-group Bilateria Crown-group Bilateria bilateral symmetry (>555 Ma), bilateral symmetry (>555 Ma), gut, internal organs gut, internal organs Coeloscleritophora

organic-walled coelosclerites AB

Phosphatization halkieriids window coelosclerites preserved chancelloriids

multiple losses of coelosclerites among bilaterian clades Crown-group Bilateria bilateral symmetry (>555 Ma), gut, internal organs coelosclerites not preserved Coeloscleritophora

mineralized coelosclerites C

TEXT-FIG. 6. Possible reconstructions of coeloscleritophoran and bilaterian relationships and character evolution. Of the Coeloscleritophora, only halkieriids and chancelloriids are shown because these are the only taxa whose body plans are known. A, halkieriids and chancelloriids are both crown-group bilaterians; chancelloriid morphology reflects loss of several bilaterian synapomorphies. B–C, bilaterians are nested within the Coeloscleritophora (Bengtson 2005); chancelloriids are outside crown-group Bilateria and halkieriids may be within the stem- or crown-group. Coelosclerites are a plesiomorphy of crown-group Bilateria, lost or transformed in multiple clades. B, mineralized coelosclerites evolve independently in halkieriids and chancelloriids from an organic- walled precursor. C, mineralized coelosclerites are homologous in chancelloriids and halkieriids but do not appear in the fossil record until secondary phosphatization of fossils is widespread. and molecular clock analyses suggest an even earlier Cambrian rocks suggests that unless these animals were date, >570 Ma (Peterson et al. 2004). This means that extremely rare, their sclerites should have been preserved, either the Ediacaran fossil record has been misinter- unless sclerite preservability itself changed at the begin- preted and bilaterally symmetric (stem- or crown- ning of the Cambrian Period. Bengtson (2005) proposed group) Bilateria did not appear until Early Cambrian that chancelloriids and halkieriids may have indepen- time or there is a hidden Precambrian record of coelo- dently evolved mineralized sclerites from organic-walled sclerites (and chancelloriids) (Bengtson 2005). While the precursors. In other words, while the macro- and micro- evidence for crown group Bilateria during Ediacaran structure of chancelloriid and halkieriid sclerites would be time has been challenged (see Budd and Jensen 2000, and homologous (dictated by their homologous organic Benton and Donoghue 2007 for reviews), evidence for framework), the impregnation of biominerals would not bilaterally symmetric stem-group bilaterians is difficult to (Text-fig. 6B). Their appearance in the Early Cambrian dismiss (e.g. Fedonkin and Waggoner 1997; Jensen 2003; would thus reflect the convergent evolution of biominer- Droser et al. 2005). On the other hand, the abundance alization in the two groups, not the initial evolution of and widespread occurrence of coelosclerites in Lower coelosclerites. PORTER: RELATIONSHIP OF CHANCELLORIIDS AND HALKIERIIDS 877

Alternatively, sclerite preservability may have changed Astrobiology Institute, and the University of California at at the beginning of the Cambrian owing to the opening Santa Barbara. of a ‘phosphatization window’ (Text-fig. 6C; Porter 2004a). Preservation and sampling of many small shelly fossils, including coeloscleritophoran sclerites, is largely REFERENCES dependent on their secondary phosphatization; the appar- ent decline of small shelly fossil diversity at the end of the BENGTSON, S. 1992. The cap-shaped Cambrian fossil Mai- Early Cambrian may have been exaggerated by the closure khanella and the relationship between coeloscleritophorans of this phosphatization window (Porter 2004a). It is like- and molluscs. Lethaia, 25, 401–420. —— 2005. Mineralized skeletons and early animal evolution. wise possible that the appearance of small shelly fossils at 101–124. In BRIGGS, D. E. G. (ed.). 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