[Palaeontology, 2013, pp. 1–15]

ONTOGENY, MORPHOLOGY AND OF THE SOFT-BODIED ‘MOLLUSC’ by MARTIN R. SMITH1,2,3 1Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Ontario, M5S 3G5, Canada 2Palaeobiology Section, Department of Natural History, Royal Ontario Museum, Toronto, Ontario, M5S 2C6, Canada 3Current address: Department of Earth Sciences, University of Cambridge, Cambridge, CB2 3EQ, UK; e-mail: [email protected]

Typescript received 26 September 2012; accepted in revised form 25 May 2013

Abstract: The soft-bodied Cambrian organism Wiwaxia . I recognize a digestive tract and creeping foot in poses a taxonomic conundrum. Its imbricated dorsal scleri- Wiwaxia, solidifying its relationship with the contemporary tome suggests a relationship with the . Similarities between the scleritomes of worms, whereas its mouthparts and naked ventral surface Wiwaxia, , Polyplacophora and hint invite comparison with the molluscan and foot. 476 that the taxa are related. A molluscan affinity is robustly new and existing specimens from the 505-Myr-old Burgess established, and Wiwaxia provides a good proxy for Shale cast fresh light on Wiwaxia’s sclerites and scleritome. the ancestral aculiferan – and perhaps molluscan – body My observations illuminate the diversity within the plan. and demonstrate that Wiwaxia did not undergo discrete moult stages; rather, its scleritome developed gradually, with Key words: halwaxiids, scleritomorphs, Aculifera, , piecewise addition and replacement of individually secreted evolution, .

T HE slug-like Cambrian organism Wiwaxia perennially Nevertheless, Butterfield (2006, 2008) identified char- resists classification, in part due to its unusual scleritome acters that could place these taxa deeper within of originally chitinous scales and spines. These sclerites, , and the affinity of Wiwaxia remains preserved in as carbonaceous films, seem to have ambiguous. been secreted by microvilli – placing Wiwaxia among the Wiwaxia has also been connected to Halkieria, another Lophotrochozoa (Butterfield 1990, 2008). The sclerites Cambrian scleritome bearer; organisms of this ilk may were first identified with the elytra (modified bristles belong to a ‘halwaxiid’ or grade (Conway Morris resembling fleshy scales) of annelid worms, although and Caron 2007; Sigwart and Sutton 2007; Vinther et al. annelid paleae (flattened chaetae) more closely match 2008). However, unlike Wiwaxia – whose sclerites are the sclerites’ shape, microstructure and arrangement in a solid and nonmineralized (Butterfield 1990) – Halkieria dorsal, nonmineralized, imbricated scleritome (Butterfield bore hollow sclerites composed of fibrous aragonite. It 1990). However, paleae are invariably paired with neu- has thus been proposed that Halkieria is unrelated to rosetae (chaetae borne on the ventral portion of a bira- Wiwaxia and instead lies with the sponge-like chancellori- mous unit), which are not evident in Wiwaxia. ids and other coeloscleritophorans (Porter 2008). Phylogenetic analyses reflect the limited morphological The species-level taxonomy of Wiwaxia represents a resemblance between Wiwaxia and ; parsimony- further outstanding question. Besides the canonical based reconstructions oppose a position in the annelid Wiwaxia corrugata Matthew 1899, the con- (Eibye-Jacobsen 2004) and instead suggest a tains smaller articulated specimens that lack spines. These molluscan affinity (Sigwart and Sutton 2007; Vinther could represent either juvenile W. corrugata (Conway et al. 2008). The latter affiliation is consistent with Morris 1985) or a separate species. Furthermore, isolated Wiwaxia’s aplacophoran-like body form and radula-like sclerites have been recovered from the Burgess Shale and mouthparts (Conway Morris 1985; Caron et al. 2006, several other early-to-middle Cambrian deposits (Butter- 2007; Smith 2012). Wiwaxia’s close relative Odontogriphus field 1990, 1994; Fatka et al. 2011; Harvey and Butterfield omalus Conway Morris 1976 also has molluscan synapo- 2011; Butterfield and Harvey 2012; Harvey et al. 2012). morphies – notably a radula and a ventral creeping These tend to be an of magnitude smaller than foot surrounded by gills (Caron et al. 2006; Smith 2012). those typical of body fossils and show subtle differences

© The Palaeontological Association doi: 10.1111/pala.12063 1 2 PALAEONTOLOGY in morphology; they may represent multiple species or SCLERITOME ontogenetic stages. Articulated specimens from Kaili, China may belong to W. corrugata (Sun et al. 2013) but Previous research have been proposed as a separate species, Wiwaxia taiji- angensis (Zhao et al. 1994). The dorsal and lateral surfaces of W. corrugata are cov- This study revisits features in Wiwaxia and Odontogri- ered with imbricating leaf-like sclerites. Conway Morris phus that have previously been contentious, and provides (1985) found the sclerites to be consistently arranged in a detailed account of the Wiwaxia scleritome. This abun- seven to nine transverse rows and five distinct regions. dant new material fills a gap in the Wiwaxia size distribu- From the midline out, he recognized zones of (1) tion, resolving the ontogeny of the scleritome and asymmetrical dorsal sclerites; (2) rounded, symmetrical confirming that smaller specimens are more likely to rep- upper-lateral sclerites; (3) more oval-shaped symmetri- resent juveniles than separate taxa. Novel observations cal lower-lateral sclerites; and (4) sickle-shaped ventrolat- substantiate Wiwaxia’s molluscan affinity, but its position eral sclerites. A distinct anterior row forms the fifth within Mollusca remains unsettled. zone; sclerites in this row resemble the upper laterals. Eibye-Jacobsen (2004), however, saw a different number of transverse rows in each scleritome zone, MATERIALS AND METHODS reporting 11–14 rows of upper-lateral sclerites in contrast to seven to eight rows of lower-lateral sclerites. I examined 476 Wiwaxia and 170 Odontogriphus speci- In addition to these ‘body sclerites’, a variable number mens (Table 1 and Table S1), most collected by the Royal of elongate spines (7–11) emerge from the dorsal/lateral Ontario Museum. Backscatter electron micrographs of sclerite zones on each side of larger specimens. Spine uncoated specimens were obtained under environmental length is variable, with spines usually shorter near the pressure SEM (Orr et al. 2002), complementing tradi- front and rear; maximum spine length grows nonlinearly tional light microscopy and digital interference of images with respect to sagittal length (Conway Morris 1985). obtained under plane- and cross-polarized light (Bengtson Each sclerite comprises a hollow tubular root that 2000). Scaling relationships were recovered from log- opens out to form a flattened, one-sided blade (Butter- transformed dimension measurements (obtained from field 1990). The blade is ornamented by a number of lon- digital images) using linear models; sclerite zones were gitudinal ribs, of which more are present in larger treated separately where this improved the Akaike infor- specimens (Conway Morris 1985). These external ribs are mation criterion. restricted to the upper surface of sclerites and are sometimes accompanied by irregularly scattered pustules (Butterfield 1990). In some sclerites from Mount Cap and Kaili, ribs have two thicknesses: prominent ribs alternate TABLE 1. Details of examined material. with fainter ones (Butterfield 1994; Harvey et al. 2012). Taxon Wiwaxia Odontogriphus The full width of each sclerite is striated by finely spaced longitudinal lineations. Parker (1998) argued that Total specimens studied 476 170 these were superficial – although they are not visible on Provenance surfaces imaged under SEM and do not exhibit interfer- 447 167 ence under transmitted light, so might be better inter- Talus below Walcott Quarry 23 1 preted as internal channels indicating microvillar Talus below Raymond Quarry 1 1 (Butterfield 1990). Tulip Beds (locality S7 on 51 Butterfield (1990) suggested that sclerites were moulted Mount Stephen) Status individually, as in Halkieria (Vinther and Nielsen 2005). Articulated specimen 431 160 Conversely, whole-body ecdysis is suggested by a puta- ‘Juvenile’ specimen 52 n/a tively moulting specimen and the absence of specimens in (<25 mm in length) the 15- to 20-mm size range (Conway Morris 1985). Institution Royal Ontario Museum, 443 169 Toronto, Canada (ROM) Sclerite morphology Smithsonian Institution National 31 1 Museum of Natural History, In the examined material, sclerites are uniformly orna- Washington, DC, USA (NMNH) mented with a single order of ribs that are most prominent – Geological Survey of Canada, 2 in the smallest specimens. The ribs’ number generally Ottawa, Canada increases with the fossils’ sagittal length, reaching 9–15 in SMITH: ONTOGENY, MORPHOLOGY AND TAXONOMY OF WIWAXIA 3 adult body sclerites (intercept = 0.88 Æ 0.26, expo- results in a partly open tube (Fig. 1C). The spines are À nent = 0.27 Æ 0.03, R2 = 0.38; p < 10 7) and 5–12 in gently curved in cross section (Fig. 1D). spines (intercept = 0.58 Æ 0.50, exponent = 0.20 Æ 0.06, In six smaller specimens (sclerite length c. 1 mm), scle- R2 = 0.16, p = 0.0037); ventrolateral sclerites are the rites’ fine longitudinal striations (the ‘chambers’ of But- exception, with no statistically significant increase in terfield 1990, around 1 lm in width) contain acicular rib count (p = 0.42, 6.7 Æ 1.3 ribs, n = 11). The ribs’ crystals (Fig. 2A–F). Correspondence between the crystals spacing increases with body sclerites’ length (exponent = and the striations is indicated by their alignment and 0.68 Æ 0.05, R2 = 0.76); ribs are more closely spaced on the identical spacing (Fig. 2B). Some striations are vacant or spines than on the body sclerites (p = 0.048; raw measure- partially filled; in some cases, many short crystals are ments listed in Table S2). Pustules (Fig. 1A–B) are only present throughout a striation (Fig. 2A–B); in others, part present on body sclerites in specimens shorter than 8 mm of the striation is occupied by elongate needles (Fig. 2C– (which lack spines); in four such specimens, they are ubiq- F). Crystals are concentrated within the ribs of each scler- uitous, whereas in two, they are absent on the largest scle- ite and near the sclerites’ tips and bases. Crystals have a rites. Small pustule-bearing sclerites were apparently similar width within each sclerite. replaced by larger sclerites that lacked pustules. The relative abundance of Fe and S in the crystals’ EDS The tubular roots of sclerites appear to represent a spectra is similar to co-occurring pyrite framboids, indi- curled planar surface; in some cases, incomplete curling cating that the crystals are iron sulphides. Because iron sulphides do not freely take an acicular form, the crystals

AC

D

B

FIG. 1. Details of Wiwaxia corrugata sclerites. A–B, NMNH 229901, the smallest known specimen; relative to body length, dorsal sclerites are vast; B, enlargement highlights pustules on sclerites. C, NMNH 199953; tube in sclerite stalk is partially open. D, ROM 62270, kink emphasizes curved cross section of spines. Scale bars represent 1 mm (A, C, D) and 100 lm (B). 4 PALAEONTOLOGY

A C E

D F

B

G H

FIG. 2. Acicular crystals within sclerites of Wiwaxia corrugata and in chaetae of Burgessochaeta.A–F, W. corrugata, NMNH 198674; sagittal length 4 mm. A–B, pyrite crystals are concentrated in ribs (arrowheads) and near tip of sclerite; enlargement shows striations (str) running parallel to incipient needles, and cracks (crack) cutting through carbon film and crystals; C–D, crystals preserved in over- lapping sclerites (topmost sclerite’s margins highlighted with dotted lines in C); needles attain greater lengths within ribs; E, needles most pronounced near the tip of sclerite and in ribs (arrowheads); F, densely packed needles occupying adjacent lineations, interrupted by cracks. G–H, Burgessochaeta setigera (Annelida), NMNH 198634; pyrite framboids (not needles) within chaetae. Scale bars represent 20 lm(A–F) and 200 lm(G–H). must have formed within enclosed spaces – further evi- phase is ever present within the striations, the crystals dence that the striations represent internal chambers cannot represent replacement products of a prior mineral rather than surface features. The crystals formed early in phase. The crystals’ concentration in regions that were diagenesis: they are deflected by later growths of rhombic more resistant to compaction (i.e. ribs and sclerite apices) pyrite and are truncated by cracks in the carbon film. presumably reflects the delayed collapse of chambers in Their tapering ends indicate that they grew into space these areas. (rather than originally occupying the full length of the In contrast, I did not observe acicular crystals in chae- sclerite and later being eroded away). As no other mineral tae of the Burgess Shale annelids or Burgessochae- SMITH: ONTOGENY, MORPHOLOGY AND TAXONOMY OF WIWAXIA 5 ta, despite their comparable internal microstructure (But- considered together. Their width, length and rib count scale terfield 1990). When present, pyrite formed framboids in linearly with total body length (log–log gradient = 1, À longitudinal series (Fig. 2G–H). Apparently the chambers p < 10 6; R2 = 0.88, 0.93 and 0.38, respectively; inter- within annelid chaetae were less robust than Wiwaxia’s and cepts = À1.1 Æ 0.3, À1.6 Æ 0.3 and 0.88 Æ 0.26), and were unable to constrain the growth of pyrite crystals. they are around twice as long as its width at all stages of growth (R2 = 0.92). Ventrolateral sclerites become long and angular in adults, but are relatively rounded at their Sclerite growth inception (Fig. 3A, E–F, I); their length increases faster than body length (exponent = 1.14, intercept = À2.5, Whereas the ventrolateral sclerites and the spines each fol- R2 = 0.97), and although their width increases at the same low their own growth trajectory, there is no statistical dis- rate as the dorsal/lateral sclerites, they are significantly nar- À tinction between the growth of dorsal, upper-lateral and rower (p < 10 4). Spines begin to develop when specimens lower-lateral sclerites, and these latter body sclerites can be are 8–16 mm in length (Fig. 3C–E); they comprise a root

A BC

DEF

GHI

FIG. 3. Ontogeny of Wiwaxia corrugata. Specimen size, and thus ontogenetic stage, increases from A?I. A, dorsal surface of ROM 57195, spines absent. B, ROM 61512, partially enrolled specimen with clear transverse banding; spines absent. Interference imaging. C, ROM 62271, exhibiting short incipient spines. D, ROM 61699, anterolateral view; incipient spines increasing in length. E, NMNH 198675, exhibiting full-length spines. Relatively short ventrolateral sclerites visible at body margin. Interference imaging. F, ROM 62272, spines and ventrolateral spines are progressively longer and narrower as body size increases. G–H, ROM 61511, mature speci- men with a full complement of spines; incipient spines (inc) resemble the distal portion of mature spines (mat). I, ROM 62273, dorsal view, note long and slender ventral sclerites arranged in bunches. Scale bars represent 5 mm. 6 PALAEONTOLOGY akin to other sclerites, an approximately parallel-sided transverse row; each sclerite emerges from an underlying proximal section, and a tapering distal end that culminates fibrous entity. Within each row, sclerites are bunched into in a c.20° point. Incipient spines are triangular and lack bundles, with their roots tightly packed (Figs 3I, 5A–C); the parallel-sided section seen in mature spines (Fig. 3E– these bundles perhaps correspond to Conway Morris’ G); this indicates growth by basal accretion. The length of zones. In complete specimens, the bundles overlap and mature spines increases with body length, but only up to a rotate, often disguising the true number of transverse point; their size is well described by a logistic or asymptotic rows; where the number of rows is unambiguous, there model, tending to a 22-mm asymptote (Fig. 4). In contrast, are always eight. spine width scales linearly with body length, so spines can- The new ROM material contains 13 specimens in the not have grown by isometric inflation (i.e. enlargement 15- to 20-mm size range, bridging the apparent size gap without change in shape). To achieve wider spines with reported by Conway Morris (1985). These specimens are more ribs, spines must have been periodically sloughed and poorly preserved, suggesting that different taphonomic replaced – accounting for the presence of incipient spines processes are active at this scale. in mature specimens (Fig. 3H). Wiwaxia specimens longer than 25 mm have limited morphological disparity. Aside from variations in the number and position of spines, the overall body propor- Scleritome morphology and development tions and sclerite distribution are broadly consistent; there are typically around five ventrolateral sclerites, one lower- Sclerites remain in transverse rows as specimens begin to lateral, c. four upper-lateral and three dorsal sclerites per disintegrate (Fig. 5A), suggesting that rows were under- half-row. ‘Juvenile’ specimens – measuring 2.1–25 mm – lain by robust decay-resistant connective tissue. NMNH have fewer sclerites in each zone (Figs 1, 3): in the 199953 (Fig. 5B) seems to represent a partial, isolated smallest specimens, each zone is represented by a single 20 10 8 6 4 3 2 Spine length (o) and width (+) / mm 1 0.7 0.5

8 9 10 20 30 40 50

Axial length / mm FIG. 4. Spine length (○) and width (+)inWiwaxia; filled circles (●) denote the longest spine in each specimen. Solid line: asymptotic/ logistic model of maximum spine length: 44 residual df, RSS = 1.59 (logistic)/1.61 (asymptotic), AIC = À17.7 (logistic)/À17.2 (asymp- totic), curves cannot be distinguished by eye; dotted line: linear model of spine width, 147 df, R2 = 0.737. All data are log-transformed. SMITH: ONTOGENY, MORPHOLOGY AND TAXONOMY OF WIWAXIA 7

AB

C

FIG. 5. Constitution of the Wiwaxia corrugata scleritome. A, ROM 56965; bunches of sclerites (arrowheads) remain associated in rows as a partially disarticulated scleritome disintegrates. B, NMNH 199953; partial transverse row of sclerites containing spines (sp) and dorsal (d), upper-lateral (ul), lower-lateral (ll) and ventrolateral (vl) body sclerites, arranged in bundles and connected by connective tissue (ct); C, ROM 61510, cracks (arrowheads) indicate that bundles of sclerites occupy several planes of splitting. Scale bars represent 5 mm. large sclerite per half-row, whereas at 7 mm, specimens irregular tubercular ornament that is absent in larger bear around two dorsal sclerites per half-row and five sclerites. The sclerites bore a single order of equally sclerites in their upper-lateral zones. Body sclerite length spaced ribs; these presumably served a structural func- scales linearly with sagittal body length (exponent = tion, as they are more closely spaced on spines than on 1.02 Æ 0.04, R2 = 0.92, n = 65), consistent with the fixed the shorter body sclerites. Although the spines have the number of transverse rows. Although sclerite width scales same ultrastructure as the body sclerites, their growth more slowly than body length (exponent = 0.85 Æ 0.05, proceeds differently, and they were only incorporated R2 = 0.84, n = 65), the addition of sclerites during into the scleritome once body length exceeded 8–16 mm growth means that the cumulative surface area of sclerites (Fig. 6). increases faster than body area (exponent with respect to The sclerites’ lineations represent internal chambers, body length = 2.34 Æ 0.12 > 2). This indicates a greater not superficial grooves. Presuming that the crystals degree of overlap in larger specimens, consistent with occupy the chambers’ original width – as inferred from their deeper scleritome (Fig. 5C). their acicular habit – then the chambers were smooth walled, uniformly sized and occupied a single tier within the sclerite. A planar system of canals is evident in the Reconstruction sclerites of the Cambrian Sinosachites, although – like the aesthete canals found in valves – these The sclerites of W. corrugata were arranged in eight form a higher-order pattern, are perpendicular to the transverse rows, each held together by connective tissue. valve surface and are an order of magnitude wider than The body sclerites grew to a fixed size by basal accretion the micrometre-sized surface-parallel chambers in Wiwaxia and were periodically shed. The smallest sclerites bore an (Vendrasco et al. 2008; Vinther 2009). Rather, the 8 PALAEONTOLOGY

A B C

20° Juvenile 20° Adult Spines absent Infant 2–8 mm 8–16 mm > 25 mm

5–7 ribs

ibs Dorsal 5–7 ribs

Upper lateral 5–12 ribs 9–15 r 5–12 ribs 5–12 ribs

Lower lateral 5–7 ribs 5–12 ribs 9–15 ribs 5–12 ribs 9–15 ribs Ventro-lateral 6–8 ribs 6–8 ribs 6–8 ribs

FIG. 6. Ontogeny of Wiwaxia corrugata. The number of sclerites in each zone changes during ontogeny, as does the shape of the spines and ventrolateral sclerites and the number of ribs on each sclerite. Pustules are only present in the earliest growth stages; spines appear in later growth stages and were shed and replaced throughout the organism’s life. Checkerboard pattern represents 1 mm. chambers seem to denote the longitudinal fabric seen in (Fig. 8A–B). It preserves in a similar fashion to the Odon- lophotrochozoan sclerites that are secreted by microvilli. togriphus foot and occupies most of the ventral surface. Although Butterfield (2006) suggested that transverse lin- eations in the Odontogriphus foot represent segment DIGESTIVE TRACT boundaries, these features bifurcate (Fig. 8C) and do not align exactly with gills. As such, there is no clear evidence The gut of Wiwaxia was originally described based on a for segmentation in either taxon (Eibye-Jacobsen 2004). specimen (ROM 32569: Conway Morris 1985, figs The transverse lineations’ distribution resembles that of – 157 161) that, based on its mouthparts and lack of scle- ’ dorsoventral musculature, which overlies the foot rites, can now be recognized as Odontogriphus. The Wiwax- (Wanninger and Haszprunar 2002). Other specimens pre- – ia gut (Fig. 7A B), like that of Odontogriphus, represents a serve blocks of longitudinal striations running parallel to straight, bilaterally symmetrical tube that runs along the the midline of the foot (Fig. 8D, F), reminiscent of chi- body axis. The identification of the gut allows Conway tons’ more dorsally positioned rectal muscles (Wanninger Morris’s ‘moulting’ specimen (Fig. 7A; Conway Morris and Haszprunar 2002), and radial lineations in the head – 1985, figs 17 19, 27) to be reinterpreted as a single, region (Fig. 8E), reminiscent of chitons’ buccal muscles enrolled, partly decayed individual. It contains just one (Wanninger and Haszprunar 2002). (damaged) set of mouthparts, and a gut can be traced along its length. In Odontogriphus (Fig. 7C–E), the alimentary DIVERSITY tract is ventral to the gills and consists of a narrow tube that continues to the subterminal anus. Ventral to the tube is a broad, originally cylindrical organ that appears to be con- Articulated Wiwaxia specimens are known from the Bur- nected to the tube by a series of lateral ducts to merge into gess Shale and the Kaili biota, with isolated sclerites the tract at its posterior end. This organ is darkly stained obtained from these and other early-to-middle Cambrian and is often associated with pyrite or aluminosilicate min- deposits (Butterfield 1990, 1994; Porter 2004; Fatka et al. erals; it perhaps represents a digestive gland. 2011; Harvey and Butterfield 2011; Butterfield and Harvey 2012; Harvey et al. 2012). Although the Kaili material awaits a detailed description (Steiner et al. 2005), its scle- FOOT rites have been assigned to a separate species, W. taijiang- ensis, based on the details of their shape and the presence The margin of a locomotory foot, usually concealed by of small and large ribs (Zhao et al. 1994). Sclerites from sclerites, is visible on six suitably preserved specimens the Mount Cap Formation (Canada) with transverse rows SMITH: ONTOGENY, MORPHOLOGY AND TAXONOMY OF WIWAXIA 9

A B

CDE

FIG. 7. Digestive tract in Wiwaxia corrugata and Odontogriphus omalus.A–B, Wiwaxia. A, previously interpreted as a newly moulted specimen with exuviae; this specimen of Wiwaxia (NMNH 200101) has one set of mouthparts (mp) and a continuous gut (gut) and bears spines (sp), anterior sclerites (ant) and eight clusters of ventral sclerites (v1–8) on each side; B, ROM 61701, interference image showing mouthparts (mp) and gut trace (gut) on ventral surface of a specimen. C–E, Odontogriphus. C, interference image of ROM 61515, dark-stained gland overlies parallel-sided digestive tract that runs the full length of the body; D, interference image of ROM 57714; in dorsal view, the gland (gland) overlies the digestive tract (tract) and is not entirely distinct; E, partly decayed specimen ROM 57715; sublateral preservation of digestive tract shows that a dark-stained gland (gland) is distinct from the digestive tract (tract), but is connected along its length by ducts (duct) before merging posteriad. Scale bars represent 2 mm. of pustules and a single, diminutive rib size have been a separate species. This is supported by the pustules that proposed as a further species (Butterfield 1994). The sec- adorn the surface and edges of Kaili spines: in W. corrugata, ond order of fainter ribs present in the Kaili and some pustules are not present in specimens that are large Mount Cap body sclerites are not present in any of the enough to have spines. Furthermore, the largest Kaili W. corrugata sclerites recovered from the Burgess Shale spine (Harvey et al. 2012, fig. 3P), which based on its by acid maceration (Butterfield 1990), nor in the bed- profile is almost complete and fully grown, measures just ding-surface fossils examined herein; they seem to denote 0.6 mm long and 80 lm wide – an order of magnitude 10 PALAEONTOLOGY

A B

C DE

F

FIG. 8. Foot region in Wiwaxia corrugata (A–B) and Odontogriphus omalus (C–F). A–B, Wiwaxia (ROM 61519), posterior view, mar- gin of foot (ft) and mouthparts (mp) visible. C, transverse lineations in Odontogriphus (ROM 57723) are unevenly spaced, bifurcate (arrows) and are more closely spaced than gills, hence cannot represent segment boundaries. Additive interference image. D–F, Odon- togriphus (ROM 57725). E, Radial linear features in head region (examples arrowed); F, showing longitudinal lineations in medial region. Scale bars represent 2 mm. smaller than the shortest complete W. corrugata spine RELATIONSHIP TO HALKIERIIDS (3.5 mm 9 600 lm). If, as seems likely, these spines and the co-occurring body sclerites belong to the same organ- In terms of sclerite shape and arrangement, the Wiwaxia ism, W. taijiangensis had a distinct ribbing pattern on its scleritome resembles the halkieriids’ (Jell 1981; Bengtson sclerites and bore spines from an early ontogenetic stage. and Conway Morris 1984; Conway Morris and Peel 1995; The transverse rows of tubercles present in the Mount Conway Morris and Caron 2007). In both Halkieria and Cap sclerite morph – also present on sclerites from the Wiwaxia, sclerites are arranged in regular transverse rows. early Cambrian Mahto formation, the middle Cambrian Distinct sclerite zones are evident in each taxon and arise Monastery Creek Formation and the late middle through the bundling of sclerites into ‘bunches’. Sclerites Cambrian Earlie Formation (Porter 2004; Butterfield are a similar shape in both taxa and can (but do not and Harvey 2012) – are absent in W. taijiangensis and always) bear a range of ornaments including pustules, W. corrugata, supporting Butterfield’s (1994) recognition transverse lineations and longitudinal ribs (Butterfield of these sclerites as a probable third species. 1994; Conway Morris and Chapman 1997). SMITH: ONTOGENY, MORPHOLOGY AND TAXONOMY OF WIWAXIA 11

On the other hand, the sclerites’ homology has been lophotrochozoan crown or stem. Here I explore the questioned based on differences in their mineralogy and implications of some possible phylogenetic placements. topology (Butterfield 2003). Wiwaxia’s sclerites lack the aragonitic component present in Halkieria; and whereas Wiwaxia’s sclerites were flat and solid, halkieriids’ con- Wiwaxia as a sister group to multiple Lophotrochozoan tained a longitudinal cavity – most evident in Sinosachites, phyla which contains secondary lateral chambers attached to the central cavity by small pores (Vinther 2009). Given the uncertain relationships between the Lophotro- I argue that these similarities and differences carry little chozoan phyla, the case for a deep phylogenetic position taxonomic information. Shape and ornament are prone to (Fig. 9A) is difficult to substantiate. Such a placement convergence (Sigwart 2009) and can vary during ontogeny was originally proposed (Butterfield 2006) based on the (Todt and Wanninger 2010). Sclerites commonly have hol- interpretations that have since been overturned: Wiwax- low and filled forms within a species or even within an ia’s mouthparts do not resemble annelid jaws (Smith organism (Okusu 2002; Kingsley et al. 2013). Polychaete 2012); ctenidia can be preserved in the Burgess Shale chaetae can be hollow or filled (Glasby et al. 2000); some, (Smith 2013); and ‘segment boundaries’ in Odontogriphus like those of Wiwaxia, are solid in their distal component are here reinterpreted as internal tissue. Stratigraphically, and have a hollow shaft (Gustus and Cloney 1973); others, a deep position raises few problems: ‘halwaxiid’ sclerites like Sinosachites, feature a complex arrangement of internal appear in the fossil record at the same time as the earliest chambers (Westheide and Watson Russell 1992; Pleijel and Lophotrochozoa (Kouchinsky et al. 2012), and the pau- Gustavsson 2010). And there are several examples of micro- city of carbonaceous preservation in the earliest Cambrian villar ‘sclerites’ that occur in mineralized and nonmineral- (Terreneuvian) leaves scope for earlier wiwaxiids. ized variants (e.g. chiton girdle elements, Fischer et al. The form of pyrite crystals – which are acicular in 1980; Leise and Cloney 1982; molluscan radulae, Kim et al. Wiwaxia but framboidal in annelids – suggests that Wi- 1989; annelid chaetae, Rouse and Pleijel 2001); most strik- waxia sclerites may share less in common with annelid ingly, the Cambrian fossil Orthrozanclus seems to represent chaetae than first anticipated. It is notable that sclerites’ a halkieriid with a nonmineralized scleritome (Conway microvillar fabric is different in annelids and , Morris and Caron 2007). where chambers near the surface of the sclerite are The mode of sclerite secretion is a more fundamental character and may have more taxonomic weight. I suggest that, as in Halkieria (Vinther and Nielsen 2005; Vinther 2009), Wiwaxia’s sclerites grew by basal secretion and were periodically replaced. On this view, the Wiwaxia sclerite would be homologous with the (apparently) organic layer on the surface of halkieriid sclerites (Porter 2008). The construction of scleritome zones from bundles of sclerites also seems to genuinely support the relation- ship between the taxa. On this basis, I tentatively support the parsimony-derived hypothesis of a close relationship between Halkieria, Wiwaxia and (based on its mouth- parts) Odontogriphus (Sigwart and Sutton 2007; Vinther et al. 2008) – whether as a clade or a grade.

AFFINITY

Wiwaxia is not easy to place on the tree of life. Its ventral foot (which was presumably surrounded by gills, as in Odontogriphus) seems to signal a molluscan affinity – but the ciliated sole present in many lophotrochozoan larvae hints that a ‘foot’ of some form might have been present FIG. 9. Phylogenetic positions of Wiwaxia discussed in the in the ancestral lophotrochozoan (Wingstrand 1985). text. A, Wiwaxia as a sister group to multiple Lophotrochozoan Taking microvillus-secreted sclerites to be a lophotrocho- phyla; B, Wiwaxia as an aplacophoran; C, Wiwaxia as an aculif- zoan symplesiomorphy (Butterfield 2008; Giribet et al. eran; D, Wiwaxia as a stem-group mollusc. Highlighted region 2009), Wiwaxia could conceivably sit anywhere in the denotes the phylogenetic position preferred herein. 12 PALAEONTOLOGY generally narrower (Orrhage 1971; Gustus and Cloney At first blush, these shape-based similarities seem to 1972; Hausen 2005), to in chitons, octopus and bryozo- indicate an affinity with the solenogasters. But the ans, where the chambers are of equal size throughout Wiwaxia-like characteristics occur in isolation across the each sclerite (Brocco et al. 1974; Gordon 1975; Fischer solenogaster tree; wherever Wiwaxia is placed, most of et al. 1980; Leise and Cloney 1982). If these patterns are the above comparisons would represent parallel evolution. phylogenetically informative, they would place Wiwaxia What is more, a derived position for Wiwaxia indicates among Mollusca + Bryozoa. an early origin of the Aplacophora. Aplacophora seem to Nevertheless, Wiwaxia’s mouthparts are difficult to rec- have derived from mineralizing chiton-like ancestors, and oncile with a deep phylogenetic position. If a radula-like ‘intermediate forms’ exist from the and Silu- mouthpart was present in the last common ancestor of rian (Sutton and Sigwart 2012; Sutton et al. 2012). If this molluscs and their sister group (bryozoans – or anne- transition pre-dated the earliest (early Cambrian) Wiwax- lids?), then it was lost in this sister group and replaced by ia fossils, then many mineralizing aculiferans have exten- a separate feeding apparatus. If not, then the resemblance sive ghost lineages. to the molluscan radula indicates profound parallel evolu- tion. On this basis, a deep phylogenetic position is not parsimonious. Wiwaxia as an aculiferan

This stratigraphic difficulty disappears if Wiwaxia is inter- Wiwaxia as an aplacophoran preted more basally among the Aculifera (Fig. 9C). Wiwaxia’s mouthparts, sclerites and scleritome could then At the other extreme, one could attempt to shoehorn resemble an ancestral Aculiferan form, which would be Wiwaxia into Aplacophora (Fig. 9B). Aplacophorans consistent with both morphology and the fossil record. exhibit a wide range of radular morphologies, including Because Aculifera (which bear sclerites) are the sister polystichous forms from which the Wiwaxia mouthparts taxon to Conchifera (which do not; Kocot et al. 2011; could easily be derived (Scheltema et al. 2003). There are Smith et al. 2011; Sutton et al. 2012), the presence of also similarities between Wiwaxia’s sclerites and apla- sclerites in the ancestral mollusc can only be inferred by cophoran spicules. The chambers within Wiwaxia sclerites reference to the nearest outgroup. If the earliest represen- seem to lie within a single plane, which suggests a com- tatives of this outgroup had a scleritome (Skovsted et al. parison with the organic pellicle that coats many aculifer- 2008; Zhang et al. 2013), then a scleritome would be an spicules (Fischer et al. 1980; Haas 1981): in other primitive for all Mollusca, and other scleritomous fossils lophotrochozoan sclerites, the full cross section of each (such as the conch-bearing Halkieria) could sit in the sclerite is occupied by a honeycomb-like array of micro- stem lineage of Mollusca, Aculifera or Conchifera. villar chambers. As in modern Aculifera (Haas 1981; Vinther 2009), sclerites of Wiwaxia grow to a fixed size, are secreted by basal microvilli, attach to the integument Wiwaxia as a stem-group mollusc with a chitinous stalk and are periodically replaced on an individual basis. Like in many solenogaster aplacophorans Wiwaxia could equally be accommodated in the mollus- (Todt and Wanninger 2010), sclerites are large relative to can stem-group (Fig. 9D). In this interpretation, its body size in young individuals, becoming relatively smal- mouthparts could represent the ancestral molluscan con- ler during ontogeny. The hollow tubes that constitute the dition or a unique modification to the radular blueprint. basal portion of Wiwaxia sclerites represent a rolled pla- Its scleritome is most simply interpreted as an inheritance nar surface – and the solenogaster Dondersia generates from a sclerite-bearing lophotrochozoan ancestor that was hollow structures in the same fashion (Scheltema et al. retained by Aculifera and lost secondarily by Conchifera 2012). Spinose elements are interspersed with flat sclerites (unless the conchiferan shell represents a fused scleritome; in the solenogaster Meiomenia (Morse and Norenburg cf. Bengtson 1992). The occurrence of sclerite-like 1992), bringing to mind Wiwaxia’s spines; in another elements in derived conchiferans (Brocco et al. 1974; solenogaster, Epimenia, the scleritome comprises discrete Waren et al. 2003) could represent the reactivation of the zones of sclerites with different morphologies (Okusu underlying genetic machinery. 2002), albeit arising in a different fashion to Wiwaxia. Vestigial shell fields sometimes divide the solenogaster scleritome into eight transverse regions, and in other sole- EVALUATION nogasters and caudofoveates, sclerites are arranged in transverse rows (Scheltema and Ivanov 2002; Nielsen Taken together, Wiwaxia’s mouthparts, foot and scleri- et al. 2007). tome indicate a molluscan affinity, whether among the SMITH: ONTOGENY, MORPHOLOGY AND TAXONOMY OF WIWAXIA 13

aculiferans or in the molluscan stem. The deep origin of BUTTERFIELD, N. J. 1990. A reassessment of the enigmatic a scleritome-bearing body plan in Mollusca suggests that Burgess Shale fossil Wiwaxia corrugata (Matthew) and its sclerites emerged at an early stage in lophotrochozoan relationship to the polychaete Canadia spinosa Walcott. 16 – evolution and that conchiferan molluscs bore a scleritome Paleobiology, , 287 303. before they evolved a shell. -1994. Burgess Shale-type fossils from a Lower Cambrian shallow-shelf sequence in northwestern Canada. Nature, 369, 477–479. Acknowledgements. This manuscript benefitted from constructive - 2003. Exceptional fossil preservation and the Cambrian reviews from Bruce Runnegar and anonymous others. I thank Explosion. Integrative and Comparative Biology, 43, 166–177. Nicholas Butterfield for useful discussion and Jean-Bernard -2006. Hooking some stem-group “worms”: fossil lophot- Caron for comments, guidance and access to material. Parks rochozoans in the Burgess Shale. BioEssays, 28, 1161–1166. Canada provided research and collection permits to ROM teams -2008. An Early Cambrian radula. Journal of , led by Des Collins, and Doug Erwin facilitated access to speci- 82, 543–554. mens at the NMNH. Peter Fenton, Rachel Thorpe, Mark Flor- -and HARVEY T. H. P. 2012. Small carbonaceous fossils ence, Kathy Hollis and Gene Hunt provided practical assistance (SCFs): a new measure of early Paleozoic paleobiology. Geology, with collections; Scott Whittaker and Sharon Lackie with scan- 40,71–74. ning electron microscopy. This research forms part of a PhD CARON, J.-B., SCHELTEMA, A. H., SCHANDER, C. and thesis at the Department of Ecology and Evolutionary Biology, RUDKIN, D. 2006. A soft-bodied mollusc with radula University of Toronto, and was funded by a Natural Sciences from the Middle Cambrian Burgess Shale. Nature, 442, 159– and Engineering Research Council of Canada Discovery Grant 163. through Jean-Bernard Caron and a University of Toronto fellow- ---- 2007. Reply to Butterfield on stem-group ship and Geological Society of America research grant to M.R.S. worms: fossil lophotrochozoans in the Burgess Shale. BioEssays This contributes to Royal Ontario Museum Burgess Shale 29, 200–202. Research Project 37. CONWAY MORRIS, S. 1976. A new Cambrian lophophorate from the Burgess Shale of British Columbia. Palaeontology, 19, 199–222. Editor. Phil Lane -1985. The Middle Cambrian metazoan Wiwaxia corrugata (Matthew) from the Burgess Shale and Ogygopsis Shale, British Columbia, Canada. Philosophical Transactions of the Royal SUPPORTING INFORMATION Society of London, Series B: Biological Sciences, 307, 507–582. -and CARON J.-B. 2007. Halwaxiids and the early evolu- Additional Supporting Information may be found in the online tion of the lophotrochozoans. Science, 315, 1255–1258. version of this article: -and CHAPMAN A. J. 1997. Lower Cambrian halkieriids Appendix S1. Details of examined specimens from the Royal and other coeloscleritophorans from Aksu-Wushi, Xinjiang, Ontario Museum (specimens from other institutions are detailed China. Journal of Paleontology, 71,6–22. in Conway Morris, 1985). - and PEEL J. S. 1995. Articulated halkieriids from the Appendix S2. Sclerite dimensions (mm), measured from 90 Lower Cambrian of north Greenland and their role in early Wiwaxia specimens. Protostome evolution. Philosophical Transactions of the Royal Appendix S3. High-resolution colour images of the figured Society of London, Series B: Biological Sciences, 347, 305–358. specimens and images of other fossils studied in this analysis. EIBYE-JACOBSEN, D. 2004. A reevaluation of Wiwaxia and Available from the Data Dryad repository, doi: 10.5061/dryad. the of the Burgess Shale. Lethaia, 37, 317–335. 868sm. FATKA, O., KRAFT, P. and SZABAD, M. 2011. 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