Cambrian suspension-feeding tubicolous hemichordates
© Nanglu et al. 2016
Received: 4 April 2016
Accepted: 8 June 2016
Published: 7 July 2016
The combination of a meager fossil record of vermiform enteropneusts and their disparity with the tubicolous pterobranchs renders early hemichordate evolution conjectural. The middle Cambrian Oesia disjuncta from the Burgess Shale has been compared to annelids, tunicates and chaetognaths, but on the basis of abundant new material is now identified as a primitive hemichordate.
Notable features include a facultative tubicolous habit, a posterior grasping structure and an extensive pharynx. These characters, along with the spirally arranged openings in the associated organic tube (previously assigned to the green alga Margaretia), confirm Oesia as a tiered suspension feeder.
Increasing predation pressure was probably one of the main causes of a transition to the infauna. In crown group enteropneusts this was accompanied by a loss of the tube and reduction in gill bars, with a corresponding shift to deposit feeding. The posterior grasping structure may represent an ancestral precursor to the pterobranch stolon, so facilitating their colonial lifestyle. The focus on suspension feeding as a primary mode of life amongst the basal hemichordates adds further evidence to the hypothesis that suspension feeding is the ancestral state for the major clade Deuterostomia.
KeywordsEnteropneusta Hemichordata Cambrian Burgess Shale
Hemichordates are central to our understanding of deuterostome evolution. The two classes (tubicolous Pterobranchia and vermiform Enteropneusta) are monophyletic [1–3], but are morphologically disparate (however, see [4, 5] for an alternate viewpoint of Pterobranchia as sister to the family Harrimaniidae within a paraphyletic Enteropneusta). Accordingly they give only generalized clues as to both the anatomy and mode of life of the last common ancestor as well as its connections to the sister phylum Echinodermata (collectively Ambulacraria). The resistant tubaria of pterobranchs (notably the Paleozoic graptolites ) provide an adequate fossil record, but in contrast that of the enteropneusts is almost non-existent [7–9]. One exception is a tubicolous taxon (Spartobranchus tenuis) from the middle Cambrian Burgess Shale . This enteropneust is closely comparable to extant harrimaniids, although its organic tube finds no modern counterpart . The coeval Oesia disjuncta Walcott  has been compared to groups as diverse as annelids , appendicularian tunicates  and chaetognaths [14, 15], thus remaining in phylogenetic limbo. The proposed chaetognath affinity was refuted by Conway Morris  and a hemichordate affinity briefly suggested instead, albeit without detailed re-observation of original specimens or consideration of new material. On the basis of hundreds of specimens from the newly discovered Marble Canyon fossil locality (Kootenay National Park, British Columbia) , we not only identify Oesia as a primitive enteropneust but also demonstrate that it constructed the perforated tube-like fossils previously assigned to Margaretia dorus and interpreted as thalli of a green alga similar to Caulerpa .
Tubes with irregular undulations and lacking the spiral pattern were previously interpreted as prostrate subterranean rhizomes (Fig. 4.2-3 ). While the reassignment from alga to organically produced tube invalidates this identification, it remains plausible that subterranean, lateral extensions of the tube could serve as an anchor. In any individual the width of the tube is usually consistent along the length, but otherwise it varies considerably (4–20 mm). Occasionally a tube shows one (Fig. 3i; Additional files 7A, C, 8A–C, 9D–F) or, more rarely, two bifurcations (Fig. 4c). Each bifurcates at approximately the same angle and has the same width as the primary tube. The tube wall is perforated by spirally arranged pores (about 10 openings per revolution; Fig. 4a, b). In a single tube pore size varies. Some may be almost closed, but others have diameters equivalent to about a third of the tube width (Fig. 4a, b, d, e; Additional file 9A). Pore shape varies from circular to oblong ellipse and rhombic. That these might simply be taphonomic variations is less likely given that the specimens are preserved parallel to the bedding plane (Fig. 4a, b, g–e; Additional file 9A). The margins of the pores tend to be raised, imparting a semi-corrugated texture to the external surface of the tube (Fig. 4a, b; Additional file 9A). The tube is composed of narrow fibres (about 7 μm) that are braided and/or overlain in bundles (Fig. 4f, g).
Margaretia dorus is unlike any known species of Paleozoic algae. In particular, the combination of a fibrous composition and elaborate pore architecture are inconsistent with an algal grade of organization, as are its biotic associations and size in relation to well-established Cambrian macroalgae . This in turn argues against Oesia being an example of inquilinism. While the dozens of co-occurrences of O. disjuncta and its tube strongly suggest an original association, the preservation of large numbers of isolated Oesia specimens on single bedding surfaces (Additional files 3, 4) at Marble Canyon also needs an explanation. One possibility is that the association was facultative and Oesia could alternate between a tubicolous and non-tubicolous existence. Alternatively the worm may have been forced to vacate the tube as an en masse evacuation prior to final burial. This may be related to both the high-energy burial events  and the resultant dysoxic conditions that such events create , although this hypothesis is weakened by the lack of obvious exit structures (i.e. there is no evidence the worms could enter or leave the tubes at either end).
In this context, fragmentation of the tubes and dispersal during transport is perhaps a more plausible explanation as to how the worms became isolated. This appears to be reasonable given the observation that although tubes with a length of up to 544 mm are known (Fig. 4c), tubes of comparable width can be not only significantly shorter (e.g. Figs. 3b, 4c), but sometimes are even smaller than the worms themselves. A related observation is that along the tube margins showing evidence for breakage, the bundles of fibres may exhibit a pattern of ’unbraiding.’ This suggests that originally the tubes were vulnerable to damage (Fig. 3b).
The second factor is that in at least some cases the tube evidently serves to conceal the worm. For a worm to be readily visible, the tube either needs to be prepared mechanically, split more or less along the axis or be sufficiently degraded so as to allow a view of the interior. Accordingly, tubes showing such evidence of degradation also contain worms in an evident state of decay (Fig. 3b–h). In such cases worms are poorly preserved and are effectively reduced to a narrow band of reflective carbon (Fig. 3k–m). Worms in such late stages of decay also show a tendency to bend at sharp angles into semi-discrete sections (Figs. 2g, 3e, f, l, m). This appearance may represent adjacent sets of gill bars maintaining their articulation through attachment to the collagenous basal lamina, but at points where this basal lamina has degraded, the more acutely angled bending occurs .
Establishing Oesia as an enteropneust that inhabited the tube previously identified as the alga Margaretia has significant implications for the Cambrian paleogeography and paleoecology of this group. Until now, Oesia was one of the rarest of Burgess Shale taxa and was restricted to the Walcott Quarry . At the coeval Marble Canyon locality, however, it is amongst the five most abundant taxa  and occupied a key trophic position. In marked contrast, Margaretia is recorded from various Burgess Shale sites in Laurentia (including the Stephen Formation of British Columbia and the Spence and Wheeler Shales of Utah  — Additional file 11: Table S1), eastern Yunnan, China  and further afield in Siberia (originally referred to as Aldanophyton ) . This expanded distribution suggests that enteropneusts were a significant component of many Cambrian communities (Additional file 6, Additional file 11: Table S1).
The strikingly extended pharynx and numerous gill bars that were employed in suspension feeding are functionally convergent with the hyperpharyngotremy seen in the tunicates , cephalochordates  and some Paleozoic jawless fish  (Fig. 5a). More generally, however, the pharyngeal arrangement seen in Oesia suggests that within the hemichordates as a whole suspension feeding was primitive. Whilst a few members of the basal harrimaniids facultatively filter interstitial pore water [27, 28], in extant enteropneusts the primary mode is deposit feeding, consistent with their mostly infaunal existence. Such a migration from an epifaunal existence may have been in response to increased predation pressure and as a consequence entailed significant anatomical changes. Notably in Oesia the post-pharyngeal trunk appears to lack the esophageal organ, which in extant forms serves to remove excess water from the food cord (and presumably performed the same function in Spartobranchus tenuis where it is also present; a summary of the main differences between S. tenuis and O. disjuncta can be found in Additional file 10). So too in the more derived taxa the hepatic caeca increase the absorptive area, presumably reflecting the increased demands of deposit feeding.
Oesia shares with the co-eval tubicolous S. tenuis  a bulbous posterior structure which may have acted as an anchor. In Oesia, however, the claw-like arrangement points to a more active role in attachment and release, perhaps as a consequence of its inhabiting a commodious tube. This interpretation draws potential comparisons to the juvenile post-anal tail of harrimaniid enteropneusts. This tail serves in ciliary locomotion and as an attachment device and may also be the homologue of the pterobranch stalk . In this context, the specialized posterior structures seen in S. tenuis and O. disjuncta may actually be ancestral features. If so, these were ultimately lost in the crown group Enteropneusta, but in the Pterobranchia they helped to pave the way towards coloniality.
While too few morphological characters are available to permit a meaningful cladistic analysis, the unique combination of characters found in O. disjuncta encourages us to present a preliminary re-interpretation of early hemichordate evolution. First, a tubicolous, epifaunal and solitary habit are evidently primitive. The fibrous filaments of the Oesia tube have some resemblance to the fusellar fibres seen in graptolites such as the Cambrian Mastigograptus , as well as the comparable periderm of rhabdopleurid  and cephalodiscid pterobranchs . An important inference is that Oesia (and Spartobranchus) possessed secretory glandular cells, presumably homologous with those located on the cephalic shield of the pterobranchs. The apparent absence of fibres in the tubes of Spartobranchus suggests that their loss may have preceded the loss of the tube itself. Concurrent with a shift to a burrowing and deposit feeding existence, the crown group enteropneusts abandoned the construction of such tubes. In contrast, the tubes of pterobranchs (and correspondingly the posterior stalk) were elaborated in parallel with their miniaturization and sessile coloniality (Fig. 5b). Crucially, the unique mix of pterobranch and acorn worm characteristics seen in Oesia suggests that an extensive pharynx and undifferentiated trunk are basal to the hemichordates, whereas Spartobranchus is more derived and is basal to the acorn worms . Future discoveries of new Cambrian hemichordates will help elucidate the hypothesized transformation of the posterior structures into the pterobranch stolon and critically unveil the order of both trait acquisition and loss during the early diversification of this phylum.
Finally, the evidence that primitive enteropneusts were suspension feeders is congruent with the hypothesis that suspension feeding represents the primitive mode of life in deuterostomes  as a whole. In particular, it is notable that this lifestyle is seen in early stem-group echinoderms  and stem-group ambulacrarians , and is inferred in the ur-ambulacrarians  as well as the more problematic vetulicolians  and yunnanozoans .
Sediment overlaying sections of some specimens was removed using a micro-engraving tool with a carbide bit. Specimens were observed using a stereomicroscope and photographed using different illuminations, using direct or cross-polarized light on dry or wet specimens. Backscatter scanning electron images were obtained to visualize fine anatomical features. Measurements of morphology were made using the program ImageJ. A list of specimens used in the analysis can be found in Additional file 11: Table S1 [38–47].
We thank P. Fenton, D.H. Erwin and M. Florence and B. Lieberman for collections assistance at the Royal Ontario Museum, Smithsonian Institution and the University of Kansas Natural History Museum respectively. We also thank S. Loduca for helpful comments on the manuscript regarding algal affinities and locality information as well as two anonymous reviewers for their constructive comments. Material for this study was collected under several Parks Canada Research and Collections permits. The 2014 field expedition at Marble Canyon was partially funded by a National Geographic Society research grant to J.-B. Caron. K. Nanglu’s doctoral research is supported by fellowships from the University of Toronto (Department of Ecology and Evolutionary Biology) and J.-B. Caron’s NSERC Discovery Grant (number 341944). This is Royal Ontario Museum Burgess Shale project number 63.
KN and JBC took photos of specimens. KN took measurements of all specimens. All authors made observations and wrote the manuscript. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
- Cameron CB. A phylogeny of the hemichordates based on morphological characters. Can J Zool. 2005;83:196–215.View ArticleGoogle Scholar
- Peterson KJ, Su YH, Arnone MI, Swalla B, King BL. MicroRNAs support the monophyly of enteropneust hemichordates. J Exp Zool Part B Mol Dev Evol. 2013;320:368–74.View ArticleGoogle Scholar
- Cannon JT, Kocot KM, Waits DS, Weese DA, Swalla BJ, Santos SR, et al. Phylogenomic resolution of the hemichordate and echinoderm clade. Curr Biol. 2014;1–6. Available from: http://dx.doi.org/10.1016/j.cub.2014.10.016.
- Halanych KM, Cannon JT, Mahon AR, Swalla BJ, Smith CR. Modern Antarctic acorn worms form tubes. Nat Commun. 2013;4:2738.View ArticlePubMedGoogle Scholar
- Stach T. Larval anatomy of the pterobranch Cephalodiscus gracilis supports secondarily derived sessility concordant with molecular phylogenies. Naturwissenschaften. 2013;100:1187–91.View ArticlePubMedGoogle Scholar
- Mitchell CE, Melchin MJ, Cameron CB, Maletz J. Phylogenetic analysis reveals that Rhabdopleura is an extant graptolite. Lethaia. 2013;46:34–56.View ArticleGoogle Scholar
- Arduini P, Pinna G, Terruzzi G. Megaderaion sinemuriense n.g. n.sp. a new fossil enteropneust of the Sinemurian of Osteno in Lombardy. Atti Soc Ital Sci Nat Mus Civ Sotria Nat Milano. 1981;122:104.Google Scholar
- Maletz J. Hemichordata (Pterobranchia, Enteropneusta) and the fossil record. Palaeogeogr Palaeoclimatol Palaeoecol. 2014;398:16–27. Available from: http://dx.doi.org/10.1016/j.palaeo.2013.06.010.View ArticleGoogle Scholar
- Alessandrello A, Bracchi G, Riou B. Polychaete, sipunculan and enteropneust worms from the lower Callovian (Middle Jurassic) of La Voulte-sur-Rhône (Ardèche, France). Atti Soc Ital Sci Nat Mus Civ Sotria Nat Milano. 2004;32:3–14.
- Caron J-B, Morris SC, Cameron CB. Tubicolous enteropneusts from the Cambrian period. Nature. 2013;495:503–6.View ArticlePubMedGoogle Scholar
- Nanglu K, Caron J-B, Cameron CB. Using experimental decay of modern forms to reconstruct the early evolution and morphology of fossil enteropneusts. Paleobiology. 2015;41:460–78.View ArticleGoogle Scholar
- Walcott CD. Cambrian geology and paleontology. Middle Cambrian annelids. Smithson Misc Collect. 1911;57:107–44.Google Scholar
- Lohmann H. Oesia disjuncta Walcott, eine Appendicularie aus dem Kambrium. Mitteilungen aus dem Zool Staatsinstitut Zool Museum Hamburg. 1920;38:69–75.Google Scholar
- Szaniawski H. Cambrian chaetognaths recognized in Burgess Shale fossils. Acta Palaeontol Pol. 2005;50:1–8.Google Scholar
- Szaniawski H. Fossil chaetognaths from the Burgess Shale: a reply to Conway Morris (2009). Acta Palaeontol Pol. 2009;54:361–4.View ArticleGoogle Scholar
- Conway Morris S. The Burgess Shale animal Oesia is not a chaetognath: a reply to Szaniawski (2005). Acta Palaeontol Pol. 2009;54:175–9.View ArticleGoogle Scholar
- Caron J-B, Gaines RR, Aria C, Mángano MG, Streng M. A new phyllopod bed-like assemblage from the Burgess Shale of the Canadian Rockies. Nat Commun. 2014;5:3210. Available from: http://www.nature.com/ncomms/2014/140211/ncomms4210/full/ncomms4210.html.View ArticlePubMedGoogle Scholar
- Conway Morris S, Robison RA. More soft-bodied animals and algae from the Middle Cambrian of Utah and British Columbia. Univ Kansas Paleontol Contrib. 1988;122:1–48.Google Scholar
- Loduca ST, Wu M, Zhao Y, Schiffbauer JD, Leroy M, O'Neil E. Seaweed through time: the early Paleozoic. The Geological Society of America. 2015. Available from: https://gsa.confex.com/gsa/2015AM/webprogram/Paper268008.html.
- Gaines RR, Droser ML. The paleoredox setting of Burgess Shale-type deposits. Palaeogeogr Palaeoclimatol Palaeoecol. 2010;297:649–61.View ArticleGoogle Scholar
- Caron JB, Jackson DA. Paleoecology of the Greater Phyllopod Bed community, Burgess Shale. Palaeogeogr Palaeoclimatol Palaeoecol. 2008;258:222–56.View ArticleGoogle Scholar
- Hu SX, Zhu MY, Luo HL, Steiner M, Zhao FC, Li GX, Liu Q, Zhang ZF. The Guanshan biota. Kunming, China: Yunnan Science and Technology Press; 2013.Google Scholar
- Ivantsov AY, Zhuravlev AY, Leguta AV, Krassilov VA, Melnikova LM, Ushatinskaya GT. Palaeoecology of the early Cambrian Sinsk biota from the Siberian platform. Palaeogeogr Palaeoclimatol Palaeoecol. 2005;220:69–88.View ArticleGoogle Scholar
- Chang P, Bone Q, Carre C. Tunicate feeding filters. J Mar Biol Assoc United Kingdom. 2003;83:907–19.View ArticleGoogle Scholar
- Ulrik H, Svane I. Filter feeding in lancelets (amphioxus), Branchiostoma lanceolatum. Invertebr Biol. 2015;118:423–32.Google Scholar
- Janvier P, Lund R. Hardistiella montanensis n. gen. et sp. (Petromyzontida) from the Lower Carboniferous of Montana, with remarks on the affinities of the lampreys. J Vertebr Paleontol. 1983;2:407–13.View ArticleGoogle Scholar
- Cameron CB. The anatomy, life habits, and later development of a new species of enteropneust, Harrimania planktophilus (Hemichordata: Harrimaniidae) from Barkley Sound. Biol Bull. 2002;202:182–91.View ArticlePubMedGoogle Scholar
- Gonzalez P, Cameron CB. The gill slits and pre-oral ciliary organ of Protoglossus (Hemichordata: Enteropneusta) are filter-feeding structures. Biol J Linn Soc. 2009;98:898–906.View ArticleGoogle Scholar
- Bates D, Kozlowska A, Loydell D, Urbanek A, Wade S. Ultrastructural observations on some dendroid and graptoloid graptolites and on Mastigograptus. Bull Geosciences. 2009;84:21–6.View ArticleGoogle Scholar
- Mierzejewski P, Kulicki C. Cortical fibrils and secondary deposits in periderm of the hemichordate Rhabdopleura (Graptolithoidea). Acta Palaeont Pol. 2003;48:99–111.Google Scholar
- Gonzalez P, Cameron CB. Ultrastructure of the coenecium of Cephalodiscus (Hemichordata : Pterobranchia). Can J Zool. 2012;1269:1261–9.View ArticleGoogle Scholar
- Simakov O, Kawashima T, Marlétaz F, Jenkins J, Koyanagi R, Mitros T, et al. Hemichordate genomes and deuterostome origins. Nature. 2015;527:459–65.View ArticlePubMedPubMed CentralGoogle Scholar
- Zamora S, Rahman IA. Deciphering the early evolution of echinoderms with Cambrian fossils. Palaeontology. 2014;57:1105–19.View ArticleGoogle Scholar
- Caron J-B, Conway Morris S, Shu D. Tentaculate fossils from the Cambrian of Canada (British Columbia) and China (Yunnan) interpreted as primitive deuterostomes. PLoS One. 2010;5:e9586. Available from: http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0009586.View ArticlePubMedPubMed CentralGoogle Scholar
- Smith AB. Deuterostomes in a twist: The origins of a radical new body plan. Evol Dev. 2008;10:493–503.View ArticlePubMedGoogle Scholar
- Ou Q, Conway Morris S, Han J, Zhang Z, Liu J, Chen A, et al. Evidence for gill slits and a pharynx in Cambrian vetulicolians: implications for the early evolution of deuterostomes. BMC Biol. 2012;10:81. Available from: http://dx.doi.org/10.1186/1741-7007-10-81.View ArticlePubMedPubMed CentralGoogle Scholar
- Chen A, Huang D. Gill rays of primitive vertebrate Yunnanozoon from Early Cambrian: A first record. Front Biol China. 2008;3:241–4.View ArticleGoogle Scholar
- O’Brien LJ, Caron J-B. Paleocommunity analysis of the Burgess Shale Tulip Beds, Mount Stephen, British Columbia: comparison with the Walcott Quarry and implications for community variation in the Burgess Shale. Paleobiology. 2016;42:27–53.View ArticleGoogle Scholar
- Johnston PA, Johnston KJ, Collom CJ, Powell WG, Pollock RJ. Palaeontology and depositional environments of ancient brine seeps in the Middle Cambrian Burgess Shale at The Monarch, British Columbia, Canada. Palaeogeogr Palaeoclimatol Palaeoecol. 2009;277:86–105.View ArticleGoogle Scholar
- Caron J-B, Gaines RR, Mángano MG, Streng M, Daley A. A new Burgess Shale-type assemblage from the “thin” Stephen Formation of the southern Canadian Rockies. Geology. 2010;9:811–4.View ArticleGoogle Scholar
- Walcott CD. Addenda to descriptions of Burgess Shale fossils. Smithson Misc Collect. 1931;85:1–46.Google Scholar
- Resser CE, Howell BF. Lower Cambrian Olenellus zone of the Appalachians. Geol Soc Am Bull. 1938;49:195–248.View ArticleGoogle Scholar
- Resser CE. Middle Cambrian fossils from Pend Oreille Lake, Idaho. Smithson Misc Collect. 1938;97:1–12.Google Scholar
- Waggoner B, Hagadorn JW. An unmineralized alga from the Lower Cambrian of California, USA. Neues Jahrb Geol Paläontol. 2004;231:67–83.Google Scholar
- Kimmig J, Pratt BR. Soft-bodied biota from the middle Cambrian (Drumian) Rockslide Formation, Mackenzie Mountains, Northwestern Canada. J Paleo. 2015;89:51–71.View ArticleGoogle Scholar
- Krishtofovich AN. Discovery of Lycopodiaceae in the Cambrian deposits of eastern Siberia. Dokl Akad Nauk SSSR. 1953;91:1377. 1379.Google Scholar
- Hu SX, Zhu MY, Steiner M, Luo HL, Zhao FC, Liu Q. Biodiversity and taphonomy of the early Cambrian Guanshan biota, eastern Yunnan. Sci China Earth Sci. 2010;53:1765–73.View ArticleGoogle Scholar