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doi: 10.1186/s12915-016-0271-4.

Cambrian suspension-feeding tubicolous hemichordates

Affiliations

Cambrian suspension-feeding tubicolous hemichordates

Karma Nanglu et al. BMC Biol..

Abstract

Background: 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.

Results: 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.

Conclusions: 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.

Keywords: Burgess Shale; Cambrian; Enteropneusta; Hemichordata.

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Figures

Fig. 1
Fig. 1
Schematic anatomy ofOesia disjuncta. Co: collar, Cr: circum-collar ridge, Dg: digestive groove, Pr: proboscis, Hks: heart-kidney-stomochord complex, Gb: gill bars, Gp: gill pores, Mo: mouth, Po: pores, Ps: posterior structure, Tr: trunk, Tu: tube.Dashed lines indicate transverse cross sections
Fig. 2
Fig. 2
General morphology ofOesia disjuncta from the Burgess Shale. (Specimens ind,e andj come from the Walcott Quarry; all other specimens come from Marble Canyon).a Note bilobed posterior structure and extended pharyngeal area (ROM 63737, part and counterpart are superimposed at thedashed line).b,c Tripartite body plan and internal organs in the proboscis (ROM 63711).d,e Large proboscis and possible nuchal skeleton (USNM 509815), see also Additional file 5A–C.f Well-developed bilobed posterior structure (ROM 63713).g–i Details of the pharyngeal area (h, partial counterpart ofg, highlighted byvertical dashed line;i is close-up of framed area ing, ROM 63710).j Left and right pairs of gill bars preserved in lateral view (USNM 277844). Direct light images:a, b,h; polarized light images:c–g,j; SEM image:i. Co: collar, Cr: circum-collar ridge, Dg: digestive groove, Dm: dorsal midline, Gb: gill bars, Hks: heart-kidney-stomochord complex, Ll: lateral side left, Lr: lateral side right, Ns: nuchal skeleton, Pr: proboscis, Ps: posterior structure, Tr: trunk. Scale bars:a = 10 mm,b–e = 1 mm,f–h = 5 mm,i = 500 μm,j = 2 mm
Fig. 3
Fig. 3
Margaretia dorus tubes and associations withOesia disjuncta from the Burgess Shale. Specimens ina andd come from the Raymond Quarry; all other specimens come from Marble Canyon. (a–h) Taphonomic gradient of the worm inside its tube from generally poorly preserved (a) to better preserved (h); the tubes tend to preserve more poorly at Marble Canyon relative to tubes from the Raymond Quarry showing similar amounts of decay of the worm.a Holotype ofM. dorus with worm preserved as a dark/reflective band along the central axis of the tube (USNM 83922).b,c Small fragments of tubes containing worms showing only few recognizable features (b: ROM 63955,c: ROM 63956).d Part of a tube excavated to reveal a poorly preserved worm inside (ROM 63715).e Tripartite body plan recognizable but worm heavily decayed (ROM 63953).f Clear posterior structure but indistinct proboscis and trunk (ROM 63957).g Poorly preserved trunk and faded tube (ROM 63952).h Close-up of framed area ing on counterpart, showing gill bars readily visible.i,j Specimen showing clear tripartite body plan and evidence of gill bars (ROM 63715).k The extant acorn wormSaccoglossus pusillus after 48 hours of decay at 25 °C showing dissociated parts, although the tripartite body plan is still recognizable.l,mO. disjuncta outside of its tube, showing extreme signs of decay comparable withk. Direct light (l) is contrasted with polarized light (m) to reveal different aspects of fossil morphology (ROM 63954). The ectoderm is fraying off, the proboscis is indistinct and the trunk has lost turgidity. Most worms preserved inside their tubes show a similar level of preservation. Direct light images:a,b,d,l; polarized light images:c,e–i,m. Bi: node of bifurcation, Fe: fibrous elements, Wo: worm, other acronyms see Figs. 1 and 2. Scale bars:a–c,e–g,k–m = 10 mm,d,i = 5 mm
Fig. 4
Fig. 4
a,b Spirally arranged pores perforate the tube (ROM 63716; see also Additional file 9A).c Two examples of multiple bifurcation points in a single specimen. Extreme size variation underscores the fragmentary nature of most tubes (left: KUMIP 204373,right: KUMIP 241392).d,e Tube showing three-dimensional preservation.d Large section of the tube has been broken off revealing the other side of the tube.e The broken segment has been placed back in its original configuration to illustrate the three-dimensionality of the tube (KUMIP 147911).f,g Close-up of the pores and fibrous texture of the tube. Individual fibres are micrometre small (ROM 63705). Bi: node of bifurcation, Fe: fibrous elements, Lo: lower surface, Po: pores, Up: upper surface, Wo: worm, other acronyms see Fig. 2. Scale bars:a,b,f,g = 5 mm,c–e = 10 mm
Fig. 5
Fig. 5
a Life reconstruction with hypothetical closed terminal ends of the tubes — part of one tube partially removed to show a worm (drawing by Marianne Collins).b Phylogenetic relationship of Deuterostomia derived from [2]. Mapping of characters based on [1, 2] with our proposed hypothetical position forOesia disjuncta as a basal hemichordate (dashed line with question mark). The position ofSpartobranchus tenuis is based on a taphonomic study of extant and fossil enteropneusts [11]. Character states: 1) pharyngeal gill bars, suspension feeding; 2) notochord; 3) tubicolous; 4) miniaturization, coloniality; 5) fuselli; 6) loss of tubicolous lifestyle, deposit feeding; 7) indirect development via tornaria larva; 8) stereom, water vascular system
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