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Hyoliths are Palaeozoic lophophorates

Abstract

Hyoliths are abundant and globally distributed ‘shelly’ fossils that appear early in the Cambrian period and can be found throughout the 280 million year span of Palaeozoic strata1,2. The ecological and evolutionary importance of this group has remained unresolved, largely because of their poorly constrained soft anatomy and idiosyncratic scleritome, which comprises an operculum, a conical shell and, in some taxa, a pair of lateral spines (helens)3,4,5. Since their first description over 175 years ago, hyoliths have most often been regarded as incertae sedis4,6, related to molluscs7,8 or assigned to their own phylum1,2. Here we examine over 1,500 specimens of the mid-Cambrian hyolith Haplophrentis from the Burgess Shale and Spence Shale Lagerstätten. We reconstruct Haplophrentis as a semi-sessile, epibenthic suspension feeder that could use its helens to elevate its tubular body above the sea floor3,9,10,11,12. Exceptionally preserved soft tissues include an extendable, gullwing-shaped, tentacle-bearing organ surrounding a central mouth, which we interpret as a lophophore, and a U-shaped digestive tract ending in a dorsolateral anus. Together with opposing bilateral sclerites and a deep ventral visceral cavity, these features indicate an affinity with the lophophorates (brachiopods, phoronids and tommotiids), substantially increasing the morphological disparity of this prominent group.

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Figure 1: Haplophrentis carinatus from the Burgess Shale.
Figure 2: Soft tissues associated with the Haplophrentis operculum.
Figure 3: Anatomical reconstruction of Haplophrentis.
Figure 4: Possible position of hyoliths within Lophophorata.

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Acknowledgements

J.M. wrote an initial draft of this paper as part of an unpublished independent undergraduate research report (Research Opportunity Program EEB299Y) under J.B.C.’s supervision at the University of Toronto. We thank B. Lieberman for access to the University of Kansas Natural History Museum collections, S. Lackie for elemental maps, R. Strathmann for images of larval brachiopods (Extended Data Figs 1d and 2e), D. Dufault for drawings and P. Fenton and M. Akrami for collections assistance. Stanley Glacier and Marble Canyon specimens were collected under Parks Canada Research and Collections permits to J.B.C. Funding for this research comes principally from the Royal Ontario Museum and NSERC (Discovery Grant number 341944 to J.B.C.). M.R.S. acknowledges funding from Clare College, Cambridge and the Malacological Society of London. This is Royal Ontario Museum Burgess Shale project number 70.

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All authors contributed to the examination and interpretation of fossils and the writing of the paper.

Corresponding authors

Correspondence to Joseph Moysiuk or Jean-Bernard Caron.

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The authors declare no competing financial interests.

Additional information

Reviewer Information Nature thanks U. Balthasar, M. Martí Mus and M. Sutton for their contribution to the peer review of this work.

Extended data figures and tables

Extended Data Figure 1 Retracted lophophore of Haplophrentis.

a, b, H. carinatus, dorsal view of specimen ROM63983.1 from Stanley Glacier. a, The entire specimen photographed dry with polarized light. b, Detail of tissue associated with the operculum. c, Dorsal view of specimen KUMIP366447 from the Spence Shale, photographed wet with polarized light. d, Larva of the extant brachiopod Glottidia, with retracted lophophore. This image was from figure 1b of ref. 31. Scale bars, 2 mm (ac) and 0.2 mm (d). Abbreviations: bw, body wall; c, conical shell; cl, clavicle; cp, cardinal process; ct, connective tissue; es, embryonic shell; g, gut; lh, left helen; ls, larval shell; ms, muscle scar; mt, medial tentacle; o, operculum; pd, pedicle; rh, right helen; t, tentacle.

Extended Data Figure 2 H. carinatus from Stanley Glacier.

ad, Specimen ROM63981.1. a, The operculum, showing an extended pharynx and lophophore, photographed dry with polarized light. b, An interpretive drawing of image a. c, d, Part and counterpart of the specimen, photographed wet with polarized light. e, Larva of the extant brachiopod Glottidia, with extended lophophore. This image was reprinted from figure 1a of ref. 31. Scale bars, 2 mm (ad) and 0.2 mm (e). Abbreviations: ag, anal branch of the gut; bw, body wall; cl, clavicle; cp, cardinal processes, embryonic shell; g, gut; ls, larval shell; m, mouth; og, oral branch of gut; p, pharynx; pl, pharynx lumen; t, tentacle.

Extended Data Figure 3 H. carinatus from Stanley Glacier (specimen ROM 59943.1).

a, b, Photographs of part and counterpart of the specimen. a, Part, photographed dry with polarized light. b, Counterpart, photographed wet with polarized light. c, Operculum (composite image of part and counterpart) showing extended tentacles, photographed dry with polarized light. Scale bars, 2 mm. Abbreviations: cl, clavicle; cp, cardinal process; ct, connective tissue; g, gut; ms, muscle scar; pl, pharynx lumen; t, tentacle; vo, visceral organ.

Extended Data Figure 4 H. reesei from the Spence Shale (specimen KUMIP204340).

a, b, Operculum, showing extended pharynx and lophophore. a, Specimen photographed dry with polarized light. b, Specimen photographed wet with polarized light. ce, Whole specimen photographed dry with unpolarized light (c), dry with polarized light (d) and wet with polarized light (e). Scale bars, 2 mm (a, b) and 5 mm (ce). Abbreviations: c, conical shell; ct, connective tissue; g, gut; lh, left helen; m, mouth; o, operculum; p, pharynx; pl, pharynx lumen; rh, right helen; t, tentacle.

Extended Data Figure 5 U-shaped digestive tract of H. carinatus.

a, b, Specimen ROM63982.1 from Stanley Glacier. a, Ventral view of the specimen, photographed wet with polarized light. b, Magnified image of the boxed area in a. c, Specimen ROM63984.1. Dorsal view of the specimen, photographed dry with polarized light. Scale bars, 1 mm (ac). Abbreviations: a, anus; ag, anal branch of the gut; og, oral branch of the gut; p, pharynx; t, tentacle; vo, visceral organ.

Extended Data Figure 6 Musculature and visceral area of H. carinatus.

a, Specimen ROM63985.1 from Marble Canyon. The specimen is laterally oriented, showing the position of visceral organs and gut within the conical shell. Photographed wet with polarized light. b, Specimen ROM62928.5 from Marble Canyon in dorsal view, showing paired visceral organs flanking the gut. Photographed wet with polarized light. c, Specimen ROM63986.1 from Marble Canyon in dorsal view with paired visceral organs adjacent to the gut. Photographed dry with polarized light. d, e, Specimen ROM63987.1 from Mount Odaray, photographed wet with polarized light. d, Ventral view of the operculum, showing connective tissue dorsal to the pharynx. e, Detail of the area boxed in d. f, Specimen ROM63988.1 from Stanley Glacier in dorsal view of the operculum with preserved muscle scars and connective tissue, dorsal to the pharynx. Photographed dry with polarized light. Scale bars, 1 mm (af). Abbreviations: ag, anal branch of the gut; bw, body wall; ct, connective tissue; g, gut; m, mouth; ms, muscle scar; og, oral branch of gut; p, pharynx; t, tentacle; vo, visceral organ.

Extended Data Figure 7 Haplophrentis scleritome.

a, Specimen ROM62968.4 from Marble Canyon, in lateral view. Note the downward disposition of the right helen, which emerges from the commissure just above the ligula of the conical shell. Photographed dry with polarized light. b, Specimen ROM62968.2, obliquely preserved specimen with anteriorly directed helens, showing the shape of the aperture of the conical shell. Photographed dry with polarized light. c, Backscatter scanning electron microscopy image showing the bulb-shaped larval shell at the apex of the conical shell of specimen ROM63989.1 from Marble Canyon. d, Specimen ROM63991.1 from Marble Canyon, with a slightly displaced operculum and the helens directed anteriorly and curving below the body. Photographed dry with polarized light. e, Specimen ROM63993.1 from Marble Canyon, operculum closing the conical shell aperture, both helens directed posteriorly with the left one preserved in the same plane as the body and the right one curving below. Photographed dry with polarized light. f, g, Specimen ROM64005.1 (f) and ROM63989.1 (g) from Marble Canyon in ventral view showing variation in the curvature and twist of the helens (the visible portion is in the same plane as the conical shell in both). Photographed wet with polarized light. h, A dorsal view of the right helen of specimen ROM63992.1 from the Raymond Quarry, curving posteriorly (inserting into the body on the upper right side) with the direction of the twist indicated by the arrow. Photographed using unpolarized light. i, Specimen ROM63994.1 from the Walcott Quarry, backscatter scanning electron microscopy image of a helen showing an ornament of transverse ribs. j, k, Specimen ROM63995.4 from the Walcott Quarry, photographed wet with polarized light. Whole specimen (j) and detail (k) of the boxed area in j, showing an ornament of transverse ribs on the conical shell. Scale bars, 2 mm (a, b, d, e, h, j), 0.5 mm (c) and 1 mm (f, g, i, k). Abbreviations: c, conical shell; cp, cardinal process; g, gut; lh, left helen; o, operculum; p, pharynx; rh, right helen; vo, visceral organ.

Extended Data Figure 8 Brachiopod epibionts on Haplophrentis.

Arrows indicate brachiopods. a, Specimen ROM63996.1, H. carinatus with Nisusia? burgessensis, photographed using ammonium chloride sublimates. b, c, Specimen ROM63997.1, H. carinatus with an acrotretid brachiopod, note the soft tissue preserved below the operculum. Photographed dry with polarized (b) and unpolarized light (c). df, Specimen KUMIP314211, H. reesei (d) with Micromitra sp. (magnified in e, f). Photographed using unpolarized light. g, h, Specimen KUMIP304352, H. reesei (g) with Nisusia sp. (magnified in h). Photographed using unpolarized light. Scale bars, 2 mm (a, b), 1 mm (c, e, f, h) and 5 mm (d, g).

Extended Data Figure 9 Elemental distribution in H. carinatus from Marble Canyon (specimen ROM63998.1).

Brighter colours represent higher concentrations of elements. Scale bars, 2 mm. Abbreviations: PL, polarized light (photographed wet); SE, secondary electron micrograph; C, carbon; S, sulfur; Mg, magnesium; Fe, iron; K, potassium; P, phosphorous; Ca, calcium; Al, aluminium; Na, sodium; O, oxygen; Si, silicon; Ti, titanium.

Extended Data Figure 10 Detail of elemental composition of H. carinatus from Marble Canyon.

ad, Specimen ROM63998.1. a, b, Carbon maps of part (a) and counterpart (b); note the concentration of carbon in the transverse shell ornament, clavicles and cardinal processes—evidence of an organic component of the skeleton. c, Sulfur map (composite image of part and counterpart) showing soft tissues, including tentacles, partially replaced by pyrite. d, Phosphorous map (composite image of part and counterpart) showing phosphatized gut. e, f, Specimen ROM63999.1. Carbon maps of part (e) and counterpart (f); carbon surrounding the clavicles and cardinal processes may be related to the attachment of muscles and connective tissue in these regions. Scale bars, 1 mm. Abbreviations: cl, clavicle; cp, cardinal process; g, gut; lh, left helen; p, pharynx; t, tentacle; vo, visceral organ.

Supplementary information

Supplementary Information

This file contains a Supplementary Discussion and Supplementary References. (PDF 162 kb)

Supplementary Table 1

This table contains a list of specimens with preserved soft tissues. (XLSX 97 kb)

Supplementary Table 2

This table contains measured data for Haplophrentis, organised by locality. (XLSX 131 kb)

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Moysiuk, J., Smith, M. & Caron, JB. Hyoliths are Palaeozoic lophophorates. Nature 541, 394–397 (2017). https://doi.org/10.1038/nature20804

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