Lethaia Focus

Nectocaris and early cephalopod evolution: reply to Mazurek & Zaton´

MARTIN R. SMITH AND JEAN-BERNARD CARON

We recently redescribed the Middle Cambrian organism Nectocaris mineralized shell de novo in later cephalopods. We recognize the pteryx, known from 92 specimens from the Burgess Shale (Smith & likelihood that the ancestral conchiferan bore a shell-field, perhaps Caron 2010). In contrast to the single, ill-preserved specimen that akin to the stiffened integument of Kimberella (Fedonkin et al. formed the basis to earlier studies, this new material allowed us to 2007) or Odontogriphus (Caron et al. 2006). (In the case of Nectoc- identify new features consistent with a cephalopod affinity. But Nec- aris, this would have encompassed both the dorsal and ventral sur- tocaris clearly lies outside the cephalopod crown-group, not least faces.) But is it unthinkable that conchiferan lineages mineralized because it lacks a mineralized shell – a plesiomorphy of the crown- this structure independently? Calcification is not, in fact, a major group Cephalopoda. Mazurek & Zaton´ (2011) object to our classifi- evolutionary leap. Perhaps triggered by minor changes in shell cation of Nectocaris in the cephalopod stem lineage because of matrix pH (Dauphin 1996), cephalopods mineralized at least twice: perceived differences between Nectocaris and crown-group once in the coleoids’ common ancestor, and again in Spirula and cephalopods. As the authors themselves state, such differences are the sepiids, which descended from non-mineralized neocoleoids tangential to Nectocaris’s affinity. Rather, synapomorphies hold the (Young et al. 1998; Strugnell & Nishiguchi 2007). Shell microstruc- key to classifying Cambrian oddballs: but Nectocaris shares no tures, genes, proteins, and nucleation patterns demonstrate great homologous characters with the anomalocaridids (stem-group homoplasy (Marin et al. 2007; de Paula & Silveira 2009; Jackson Arthropoda), where the authors propose it belongs. Mazurek and et al. 2010), not ‘unity’. Whether taken to imply independent Zaton´ present no meaningful challenge or alternative to Nectocaris’s mineralization or secondary loss, non-mineralization does not interpretation as a ‘primitive’ – that is, stem-group – cephalopod. compromise our hypothesis.

How are Cambrian fossils classified? Absence of radula The absence of a radula is intriguing. The authors correctly indicate Mazurek & Zaton´ open their paper by asking what Nectocaris needs that the Miocene–Recent cephalopod Spirula lacks a radula; per- if it is to be called a cephalopod. Their survey of cephalopod char- haps Nectocaris lost its too. Or could preservation be to blame? acters missing in Nectocaris does indeed place the organism outside Cephalopod radulae are scarce in the fossil record. Among the the cephalopod crown-group, which Mazurek & Zaton´ define by ammonites, they are known from just 9 of 43 genera; even where the presence of a siphuncle. But to suggest that this contradicts our they are preserved, their identification requires the fortuitous proposed affinity is to misunderstand the process of phylogenetic splitting and orientation of the host fossil (Kruta et al. 2011). With classification (Jenner & Littlewood 2008). an infilled funnel to cover it and dense carbonaceous tissue to Since many Cambrian fossils fall outside the boundaries of obfuscate it, the radula may simply be obscured in the few (eleven) extant taxa, they are often placed in such phylogenetic limbos as Burgess Shale specimens that bear a visible, unweathered, head. ‘Problematica’ or ‘phyla nova’ (e.g. Chen et al. 2005). A more Perhaps new material will reveal a radula; meanwhile, any taxo- informative, if more difficult, approach recovers relationships with nomic diagnosis resting on its absence has a shaky foundation. extant clades based on shared homologous characters (Budd & Jen- sen 2000). Once a stem-group taxon is understood, its formerly fuddling combination of primitive and derived characters may Absence of beak become an important, even pivotal, contribution to phylogenetic analysis (Gauthier et al. 1988). Beaks, although common in ammonoids, have only tentatively Nectocaris, if a stem-group cephalopod, will bear some – but not been identified in more basal cephalopods (Gabbott 1999). Since all – features of the crown-group. In particular, it should lack fea- the beak is an apomorphy of the cephalopod crown-group – in tures (such as a beak or ink sac) that are present only in a subset of fact, it is not even clear that a beak was present in the last common the crown-group (Budd & Jensen 2000). Parsimony would indicate ancestor of ‘true cephalopods’ – its absence in Nectocaris is imma- that features absent in Nectocaris but present in extant coleoids terial. evolved after the two lineages diverged in (probably) the Early Cambrian. With this in mind, we proceed to consider each of the features that trouble our critics. Axial cavity and funnel We are unconvinced by our critics’ interpretation of the Nectocaris nozzle as a ‘feeding apparatus’ with a terminal mouth, making the Stumbling blocks for a cephalopod axial cavity an alimentary canal: we know of no organism whose gills lie within its gut. Such an interpretation raises taphonomic affinity – and their resolution questions: why is this cavity filled with aluminosilicate minerals, which are consistently concentrated towards its anterior? Why do these interdigitate between gill blades (Smith & Caron 2010; fig. Lack of mineralized shell 1E, suppl. fig. 9B)? The gills cannot represent infoldings of the digestive tract, as they run the entire length of the axial cavity and Mazurek & Zaton´ present a false dichotomy between the secondary are regularly spaced, symmetrical, and connected by a rod on their loss of the Nectocaris shell, and the evolution of a shell field and outermost side. The pattern of relief in the aluminosilicate infill

DOI 10.1111/j.1502-3931.2011.00295.x 2011 The Authors, Lethaia 2011 The Lethaia Foundation 2 Lethaia Focus LETHAIA 10.1111/j.1502-3931.2011.00295.x

A fluids within this cavity rapidly mineralized and were later replaced by aluminosilicates. We interpret the rarely preserved dark axial stain (Smith & Caron 2010; fig. 1c) to represent part of the gut – perhaps analogous to the cephalopod crop (cf. Westermann et al. 2002). Because it is offset from the main plane of splitting (which usually transects the axial cavity), the full length of the gut is never preserved; whether or not it was U-shaped (Kro¨ger et al. 2011) remains undetermined. There is no a priori reason that the funnel could not have served a propulsive function. Its inner channel may flare, be parallel-sided, or narrow distally (as in Fig. 1), accommodating a variable aper- ture width. The flaring is not enough to produce disruptive flow detachment in the low Reynolds number environment (Re  101) that characterizes this small organism (Leneweit & Auerbach B 1999). Appropriately resizing the aperture during a jet pulse will improve efficiency, and further gains occur (in small cephalopods) at larger aperture sizes (Bartol et al. 2008). In the context of its par- ticular fluid dynamics, the Nectocaris funnel is appropriately shaped.

Convergence The authors dismiss the cephalopod-like body outline, eyes, gills and fins on the grounds of convergence. We acknowledge the twin difficulties of discriminating convergent characters from homolo- gies, and of identifying convergence in the absence of strong phylo- genetic constraint (Wiens et al. 2003). But potential convergence does not discount a character; if this were so, the shell (convergently produced by, for example, foraminifera), jaws (annelids), distinct mouth (chordates), frontal appendages (arthropods) and even the locomotory funnel (aplysiomorphs) would at once be removed from consideration. Convergent characters still represent data, and the inclusion of more characters in an analysis reduces the impact of convergence. Further, character combinations can form compel- ling synapomorphies even when the constituent characters are indi- Fig. 1. Funnel morphology in Nectocaris pteryx: in ROM 60104, vidually uninformative (Butterfield 2005). Stalked, camera-type the funnel’s central canal (cc) narrows distally, and takes a different eyes, cephalic tentacles, a neck-borne funnel, paired gills within an shape from the fleshy portion (f). A, low angle lighting, emphasiz- axial cavity, and lateral fins with crisscrossing connective tissues ing relief. B, enlargement of boxed area; direct lighting emphasizes only occur together in cephalopods. the carbonaceous boundary of the infilled central canal. Scale It is important to recognize that each organ in Nectocaris is con- bars = 2 mm. stituted in a similar fashion to its cephalopod analogue. The same cannot be said for anomalocaridids (or other arthropods): none of their apparent similarities with Nectocaris represent true homolo- does not match that of other Burgess Shale guts (e.g. Briggs 1977; gies (Table 1). Their two ‘lateral flap-like appendages … in front Conway Morris 1979), nor that produced by gut gland phosphati- of the head’ bear spines, are clearly segmented, flex in a single zation (Butterfield 2002). Rather, it suggests that mud was plane, and – rather than being lateral – attach to the ventral surface squeezed or inhaled (prior to diagenesis) into an open cavity con- of the head (Daley & Budd 2010); the tentacles of nectocaridids are taining rigid, partly decayed gill-supporting structures – or that fundamentally dissimilar in position (anterolateral), segmentation

Table 1. Detailed comparison of potential homologies between Nectocaris, cephalopods and anomalocaridids.

Character Anomalocaridids Nectocaris Ancestral crown-group cephalopod

Frontal appendages Segmented Non-segmented Non-segmented (tentacles and arms ⁄ Ventral Anterolateral Anterior great appendages) Flexible in single plane Flexible in any plane Flexible in any plane Spine-bearing Unornamented Unornamented Gills External Internal Internal One per segment Paired, in axial cavity Paired, in axial cavity Lamellae Comb-like (ctenidia) Comb-like (ctenidia) Eyes Compound Camera-type Camera-type Funnel Absent Open tube on ventral surface of Open tube on ventral surface of head connected to axial cavity head connected to axial cavity Fins ⁄ lateral flaps Segmented Non-segmented (Non-segmented)* Non-continuous margin Continuous margin (Continuous margin)* No connective tissue preserved Connective tissue preserved (Connective tissue preserved)*

Characters absent in Nectocaris cannot be meaningfully compared and are thus not listed. Nautilus is used as a model for the ancestral cepha- lopod in most instances. *In extant coleoids; absent in Nautilus and unconstrained in ancestral cephalopod due to a lack of soft-tissue preservation. LETHAIA 10.1111/j.1502-3931.2011.00295.x Lethaia Focus 3

(absent), ornamentation (none) and flexibility (possible in any Butterfield, N.J. 2002: Leanchoilia guts and the interpretation of plane). The compound anomalocaridid eye is multifaceted (Whit- three-dimensional structures in Burgess Shale-type fossils. Paleo- tington & Briggs 1985); the nectocaridid eye simple. The lateral biology 28, 155–171. lobes that propel anomalocaridids are segmented and bear gill Butterfield, N.J. 2005: Probable Proterozoic fungi. Paleobiology 31, lamellae; the Nectocaris fin is non-segmented, has a continuous 165–182. margin, and lacks gill lamellae; indeed, whereas anomalocaridid Caron, J.-B., Scheltema, A.H., Schander, C. & Rudkin, D. 2006: A gills are external, nectocaridid gills are internal. Certainly, none of soft-bodied mollusc with radula from the Middle Cambrian these characters links Nectocaris with the anomalocaridids. Burgess Shale. Nature 442, 159–163. Chen, J.-Y., Huang, D.-Y. & Bottjer, D.J. 2005: An Early Cambrian problematic fossil: Vetustovermis and its possible affinities. Implications for cephalopod ancestry Proceedings of the Royal Society B: Biological Sciences 272, 2003– 2007. Mazurek & Zaton´ reduce cephalopod origins to a ‘known and logi- Conway Morris, S. 1979: Middle Cambrian polychaetes from the cal sequence of events’, but the reality is somewhat more compli- Burgess Shale of British Columbia. Philosophical Transactions of cated. There are at least four possible ancestries for Plectronoceras, the Royal Society of London B 285, 227–274. the earliest siphunculate cephalopod (Yochelson et al. 1973; Dzik Daley, A.C. & Budd, G.E. 2010: New anomalocaridid appendages 1981, 2010; Kobayashi 1987; Peel 1991), notwithstanding disputed from the Burgess Shale, Canada. Palaeontology 53, 721–738. alternatives (Jell 1976; Teichert 1988). The characters that tie mis- Dauphin, Y. 1996: The organic matrix of coleoid cephalopod shells: cellaneous Cambrian shelly taxa to the cephalopod lineage are few molecular weights and isoelectric properties of the soluble in number, and are prone to both convergence and controversy; matrix in relation to biomineralization processes. Marine Biology their interpretations should be regarded with suspicion. The scar- 125, 525–529. city of soft-tissue characters leaves early molluscan evolution Dzik, J. 1981: Origin of the Cephalopoda. Acta Palaeontologica ill-constrained; future fossil discoveries, especially from Burgess Polonica 26, 161–191. Shale-type deposits, will undoubtedly refine the nectocaridids’ phy- Dzik, J. 2010: Brachiopod identity of the alleged monoplacophoran logenetic position. Until then, a cephalopod affinity is (on balance) ancestors of cephalopods. Malacologia 52, 97–113. the most parsimonious hypothesis. Fedonkin, M.A., Simonetta, A. & Ivantsov, A.Y. 2007: New data on Kimberella, the Vendian mollusc-like organism (White Sea region, Russia): palaeoecological and evolutionary implications. In Vickers-Rich, P., Komarower, P. (eds): The Rise and Fall of Conclusion the Ediacaran Biota, Special Publication of the Geological Society, 286, 157–179 pp. Geological Society of London, London. Missing characters rarely constitute strong phylogenetic evidence: Gabbott, S.E. 1999: Orthoconic cephalopods and associated fauna their absence may reflect taphonomy (Sansom et al. 2010); taxon- from the late Ordovician Soom Shale Lagersta¨tte, South Africa. omy (due to a stem-group position, cf. Smith 1984) or even sec- Palaeontology 42, 123–148. ondary loss. Rather than differences, classification is informed by Gauthier, J., Kluge, A.G. & Rowe, T. 1988: Aminote phylogeny and shared derived characters. Although it is easy to spot superficial the importance of fossils. Cladistics 4, 105–209. similarities between Nectocaris and anomalocaridids, genuinely Jackson, D.J., McDougall, C., Woodcroft, B., Moase, P., Rose, R.A., homologous structures share a common construction: for example, Kube, M., Reinhardt, R., Rokhsar, D.S., Montagnani, C., Jou- camera-type or compound eyes. Once one recognizes that (by defi- bert, C., Piquemal, D. & Degnan, B.M. 2010: Parallel evolution nition) stem-groups such as Nectocaris lack some of the characters of nacre building gene sets in molluscs. Molecular Biology and that define the crown group, the objections of Mazurek and Zaton´ Evolution 27, 591–608. evaporate. Jell, P.A. 1976: Mollusca. In: Lapedes, D.N. (ed.) McGraw-Hill Yearbook of Science and Technology 1976, 269–271pp. McGraw- Hill, New York. Jenner, R.A. & Littlewood, D.T.J. 2008: Problematica old and new. Acknowledgements. – This manuscript benefited from the reviews Philosophical Transactions of the Royal Society B: Biological of Bruce Runnegar and two anonymous referees. MS’s research is Sciences 363, 1503–1512. supported by fellowships from the University of Toronto and JBC’s Kobayashi, T. 1987: The ancestory of the Cephalopoda: from Hel- Natural Sciences and Engineering Research Council Discovery cionella to Plectronoceras. Proceedings of the Japan Academy Series Grant (#341944). B: Physical and Biological Sciences 63, 135–138. Martin Smith [[email protected]], Department of Ecology Kro¨ger, B., Vinther, J. & Fuchs, D. 2011: Cephalopod origin and and Evolutionary Biology, University of Toronto, 25 Willcocks Street, evolution: a congruent picture emerging from fossils, develop- Ontario, M5S 3B2, Canada; Palaeobiology, Royal Ontario Museum, ment and molecules. Bioessays 33, 602–613. 100 Queen’s Park, Toronto, Ontario, M5S 2C6, Canada; Jean- Kruta, I., Landman, N., Rouget, I., Cecca, F. & Tafforeau, P. 2011: Bernard Caron [[email protected]], Palaeobiology, Royal Ontario The role of ammonites in the Mesozoic marine food web Museum, 100 Queen’s Park, Toronto, Ontario, M5S 2C6, Canada; revealed by jaw preservation. Science 331, 70–72. Department of Ecology and Evolutionary Biology, University of Tor- Leneweit, G. & Auerbach, D. 1999: Detachment phenomena in low onto, 25 Willcocks Street, Ontario, M5S 3B2, Canada; manuscript Reynolds number flows through sinusoidally constricted tubes. received on 01/03 ⁄ 2011; manuscript accepted on 08 ⁄ 09 ⁄ 2011. Journal of Fluid Mechanics 387, 129–150. Marin, F., Luquet, G., Marie, B. & Medakovic, D. 2007: Molluscan shell proteins: primary structure, origin, and evolution. Current Topics in Developmental Biology 80, 209–276. References Mazurek, D. & Zaton´, M. 2011: Is Nectocaris pteryx a cephalopod? Lethaia 44, 2–4. Bartol, I.K., Krueger, P.S., Thompson, J.T. & Stewart, W.J. 2008: de Paula, S.M. & Silveira, M. 2009: Studies on molluscan shells: Swimming dynamics and propulsive efficiency of squids contributions from microscopic and analytical methods. Micron throughout ontogeny. Integrative and Comparative Biology 48, 40, 669–690. 720–733. Peel, J.S. 1991: The classes Tergomya and Helcionelloida, and early Briggs, D.E.G. 1977: Bivalved arthropods from the Cambrian molluscan evolution. Grønlands Geologiske Undersøgelse Bulletin Burgess Shale of British Columbia. Palaeontology 20, 595–621. 161,11–65. Budd, G.E. & Jensen, S. 2000: A critical reappraisal of the fossil Sansom, R.S., Gabbott, S.E. & Purnell, M.A. 2010: Non-random record of the bilaterian phyla. Biological Reviews of the decay of chordate characters causes bias in fossil interpretation. Cambridge Philosophical Society 75, 253–295. Nature 463, 797–800. 4 Lethaia Focus LETHAIA 10.1111/j.1502-3931.2011.00295.x

Smith,A.B.1984:ClassificationoftheEchinodermata.Palaeontology X-ray analytical and computational tomography study on the 27,431–459. living animal. Journal of Experimental Biology 205, 1617–1624. Smith, M.R. & Caron, J.-B. 2010: Primitive soft-bodied cephalo- Whittington, H.B. & Briggs, D.E.G. 1985: The largest Cambrian pods from the Cambrian. Nature 465, 469–472. animal, Anomalocaris, Burgess Shale, British Columbia. Philo- Strugnell, J. & Nishiguchi, M.K. 2007: Molecular phylogeny of sophical Transactions of the Royal Society of London B 309, 569– coleoid cephalopods (Mollusca: Cephalopoda) inferred from 609. three mitochondrial and six nuclear loci: a comparison of Wiens, J.J., Chippindale, P.T. & Hillis, D.M. 2003: When are phy- alignment, implied alignment and analysis methods. Journal of logenetic analyses misled by convergence? A case study in Texas Molluscan Studies 73, 399–410. cave salamanders Systematic Biology 52, 501–514. Teichert, C. 1988: Main features of cephalopod evolution. In Yochelson, E., Flower, R.H. & Webers, G.F. 1973: The bearing of Clarke, M.R., Trueman, E.R. (eds): Palaeontology and Neontol- new Late Cambrian monoplacophoran genus Knightoconus ogy of Cephalopods, Vol. 12, 11–79pp. Academic Press, New upon the origin of Cephalopoda. Lethaia 6, 275–309. York. Young, R.E., Vecchione, M. & Donovan, D.T. 1998: The evolution Westermann, B., Ruth, P., Litzlbauer, H.D., Beck, I., Beuerlein, K., of coleoid cephalopods and their present biodiversity and ecol- Schmidtberg, H., Kaleta, E.F. & Schipp, R. 2002: The digestive ogy. South African Journal of Marine Science 20, 393–420. tract of Nautilus pompilius (Cephalopoda, Tetrabranchiata): an