Meiofaunal deuterostomes from the basal Cambrian of Shaanxi (China)

Journal name:
Nature
Volume:
542,
Pages:
228–231
Date published:
DOI:
doi:10.1038/nature21072
Received
Accepted
Published online

Deuterostomes1 include the group we belong to (vertebrates) as well as an array of disparate forms that include echinoderms2, hemichordates3 and more problematic groups such as vetulicolians4 and vetulocystids5. The Cambrian fossil record is well-populated with representative examples, but possible intermediates6, 7 are controversial and the nature of the original deuterostome remains idealized. Here we report millimetric fossils, Saccorhytus coronarius nov. gen., nov. sp., from an Orsten-like Lagerstätte from the earliest Cambrian period of South China, which stratigraphically are amongst the earliest of deuterostomes. The bag-like body bears a prominent mouth and associated folds, and behind them up to four conical openings on either side of the body as well as possible sensory structures. An anus may have been absent, and correspondingly the lateral openings probably served to expel water and waste material. This new form has similarities to both the vetulicolians4 and vetulocystids5 and collectively these findings suggest that a key step in deuterostome evolution was the development of lateral openings that subsequently were co-opted as pharyngeal gills2, 3, 4, 8. Depending on its exact phylogenetic position, the meiofaunal habit of Saccorhytus may help to explain the major gap between divergence times seen in the fossil record and estimates based on molecular clocks9.

At a glance

Figures

  1. Saccorhytus coronarius gen. et sp. nov. from the Cambrian Kuanchuanpu Formation, South China.
    Figure 1: Saccorhytus coronarius gen. et sp. nov. from the Cambrian Kuanchuanpu Formation, South China.

    ac, Holotype XX45-20. a, Right side. The mouth (M) arched dorsally along the anterior–posterior axis. b, Chevron pattern (Ch) on the inner surface of the integument. c, A spine (Sp) close to the mouth. df, XX45-56. d, Left side. e, Detail of the dorsally arched and folded mouth with radial folds (Rf) and oral protrusions (Op) in d. f, Circular pores (Cp) on the dorsal, right side. gi, XX48-64 with limited compression. g, Ventral view, showing body cones (Bc) bilaterally arranged around the anterior, including the mouth. Two circular pores are adjacent to the first body cones (Bc1) and a small circular pore is on the mid-ventral line of the body. h, Oral protrusions lacking distal ends and appearing as a circle of pores. i, Left view reconstructed by microcomputerized tomography data. Lbc1–Lbc4, left body cones; Nr, nodular rugae; Rbc1–Rbc4, right body cones; Rf, radial folds; Sc, sub-layer of cuticle; arrowed AP, anterior–posterior axis.

  2. Saccorhytus coronarius gen. et sp. nov.
    Figure 2: Saccorhytus coronarius gen. et sp. nov.

    ac XX45-1. a, Left side. b, Detail of mouth with nodular rugae and oral protrusions in a. c, Circular pores on the dorsal side of b. d, e, XX36-22. d, Right view. Nodular rugae visible on ventral posterior part of the body, and body cones with radial ribs (Rr). e, Detail of mouth with radial folds and oral protrusions of which those on the middle line are largest. fh, XX34-298. f, g, Right and left, respectively; four body cones with radial ribs on either side of the specimen with circular pores on the dorsal side. h, Anterior body showing spine and unidentified structure with a sub-rectangular base and pore.

  3. Reconstruction of Saccorhytus coronarius gen. et sp. nov. and the phylogeny of early deuterostomes.
    Figure 3: Reconstruction of Saccorhytus coronarius gen. et sp. nov. and the phylogeny of early deuterostomes.

    a, Lateral, hind and ventral views. b, The most parsimonious tree (tree length, 96; consistency index, 0.6771; retention index, 0.8394; rescaled consistency index, 0.5683) arising from a matrix of 25 taxa and 61 characteristics. The values at nodes indicate bootstrap support greater than 50% (see Supplementary Information for details).

  4. Geographical location of horizon and its petrography.
    Extended Data Fig. 1: Geographical location of horizon and its petrography.

    a, Locality map of the Zhangjiagou section, Xixiang, Shaanxi Province, China. In addition to Saccorhytus, the phosphatic limestone of Bed 2 of the Kuanchuanpu Formation in the Zhangjiagou section (see ref. 16) contains numerous small shelly fossils. b, c, Petrographic sections (plane-polarized light) of Bed 2 showing the phosphatic bioclastic grains, carbonate matrix and cements.

  5. Saccorhytus coronarius gen. et sp. nov.
    Extended Data Fig. 2: Saccorhytus coronarius gen. et sp. nov.

    ac, Holotype XX45-20. a, Left side, showing the body cones and circular pores. b, Two sub-layers of the integument around a body cone (Rbc2),with chevron pattern on the external and inner surfaces in Fig. 1a. c, Close-up of an oral protrusion in Fig. 1a. di, XX45-56. d, e, Close-ups of circular pores on the right, dorsal side. fi, Chevron pattern on integument surface of dorsal side. jl, XX48-64. j, Ventral view. k, Radial ribs of body cones defined as wavy margin, with integument composed of two sub-layers. l, Chevron pattern on integument surface.

  6. Saccorhytus coronarius gen. et sp. nov.
    Extended Data Fig. 3: Saccorhytus coronarius gen. et sp. nov.

    ac, XX45-1. a, Right side. b, Chevron pattern on integument surface. c, Two sub-layers of the integument on the third, left body cone (Lbc3) in Fig. 2a. d, e, XX36-22. d, Left view. A spine close to the second, left body cone (Lbc2); ventral part with nodular rugae. e, Circular pores on the dorsal side of d. fh, XX34-298. f, Close-up of closed mouth with radial folds and oral protrusions in Fig. 2f. g, Two sub-layers of the integument on the second, right body cone (Rbc2) with radial ribs in Fig. 2g. h, Chevron pattern on integument surface.

  7. Saccorhytus coronarius gen. et sp. nov.
    Extended Data Fig. 4: Saccorhytus coronarius gen. et sp. nov.

    ad, XX25-62, highly compressed. a, b, Right and left sides, respectively. c, Close-up of mouth with radial folds and oral protrusions in a; note nodular rugae on ventral anterior of body. d, Third body cone with radial ribs. e–h, XX27-160. e, Right view. f, Ventral view showing ventral mouth with radial folds and anterior nodular rugae. g, Chevron pattern on inner surface of integument. h, Two circular pores to posterior of first body cone.

  8. Saccorhytus coronarius gen. et sp. nov.
    Extended Data Fig. 5: Saccorhytus coronarius gen. et sp. nov.

    af, XX27-168. a, b, Right and left sides, respectively. Two body cones on right in a; two spines close to third left body cone in b. c, Left view of specimen reconstructed by micro-CT showing concealed body cones (Lbc1 and Lbc2). d, Close-up of arched mouth with radial folds and oral protrusions in a. e, Third body cone (Rbc3) with radial ribs and truncated opening. f, Nodular rugae and anterior spine in a. gl XX47-498. g, Ventral view, mouth arched; body cones arranged with bilateral symmetry, delimited by a circular pore at the mid-ventral line. A pair of large and small tubular protrusions (Ltp and Stp, respectively) are visible at the anterior, mid-ventral line of the mouth. h, Dorsal view with body cones arranged bilaterally. i, Close-up of mouth with radial folds and elongate oral protrusions most prominent along the middle line. j, At least 12 circular pores arranged bilaterally in two longitudinal rows. k, Third left body cone with broken scars (Sc) of radial ribs. l, Inconspicuous first and second left body cones.

  9. Saccorhytus coronarius gen. et sp. nov.
    Extended Data Fig. 6: Saccorhytus coronarius gen. et sp. nov.

    a, XX54-354. Dorsal view showing a pair of spines and bilaterally arranged fourth body cones. bd, XX56-192. b, Lateral view of the body. c, d, Integument of body cones consisting of two sublayers. e, XX59-253, showing the ventral anterior location of the mouth. f, g, XX61-27, showing two pairs of tubular projections (Ltp and Stp) at the anterior end of the mouth.

  10. Body dimensions of 44 specimens.
    Extended Data Fig. 7: Body dimensions of 44 specimens.

    a, Rank order of lengths. b, Bivariate plot of height versus length. Despite a positive correlation in b, the low goodness of fit probably reflects the extensive crushing of most of the specimens.

  11. Consensus trees.
    Extended Data Fig. 8: Consensus trees.

    Left, produced by PAUP4.0; right, produced by TNT 1.1. The consensus tree from TNT 1.1 used New Technology Search with default options.

  12. Deuterostomes from the Chengjiang fauna (Stage 3, Series 2), south China.
    Extended Data Fig. 9: Deuterostomes from the Chengjiang fauna (Stage 3, Series 2), south China.

    a, Xidazoon stephanus Shu et al., 1999 (ref. 31) (ELI0000194). b, Didazoon haoae Shu et al., 2001 (ELI0000194). c, Pomatrum ventralis Luo et al., 1999 (ref. 32) (ELIJS010B). d, e, Beidazoon venustum Shu 2005 (ref. 33) (ELIJS454A, B). f, Vetulocystis catenata Shu et al., 2004 (ELISK016A). Double-circlet mouth as seen in Saccorhytus is present in Xidazoon and Pomatrum; gill pouches are visible in Didazoon, Pomatrum and Beidazoon; two body cones similar to those of Saccorhytus can be seen in Vetulocystis; and gill pouches with radial ribs that resemble those of Saccorhytus can also be seen on Beidazoon.

Videos

  1. Reconstructed video of XX25-62.
    Video 1: Reconstructed video of XX25-62.
    Reconstructed video of XX25-62.
  2. Reconstructed video of XX27-168
    Video 2: Reconstructed video of XX27-168
    Reconstructed video of XX27-168.
  3. Reconstructed video of XX34-298
    Video 3: Reconstructed video of XX34-298
    Reconstructed video of XX34-298.
  4. Reconstructed video of XX36-22
    Video 4: Reconstructed video of XX36-22
    Reconstructed video of XX36-22.
  5. Reconstructed video of XX42-83
    Video 5: Reconstructed video of XX42-83
    Reconstructed video of XX42-83.
  6. Reconstructed video of XX48-64
    Video 6: Reconstructed video of XX48-64
    Reconstructed video of XX48-64.

References

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Author information

Affiliations

  1. State Key Laboratory of Continental Dynamics, Department of Geology, Northwest University, Xi’an 710069, China

    • Jian Han &
    • Degan Shu
  2. Department of Earth Sciences, University of Cambridge, Downing Street, Cambridge CB2 3EQ, UK

    • Simon Conway Morris
  3. State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Beijing 100083, China

    • Qiang Ou
  4. Department of Zoology, University of Kassel, Kassel 34132, Germany

    • Qiang Ou
  5. College of Petroleum Engineering, Xi’an Shiyou University, Xi’an 710065, China

    • Hai Huang

Contributions

J.H. and D.S. conceived the project. J.H., S.C.M. and Q.O. wrote early drafts of paper and assessed initial results. J.H. prepared photographs and phylogenetic analysis. H.H. undertook computerized tomography restoration. All authors discussed results, and developed observations and conclusions.

Competing financial interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to:

Reviewer Information Nature thanks A. Hejnol, I. Rahman and J. Vannier for their contribution to the peer review of this work.

Author details

Extended data figures and tables

Extended Data Figures

  1. Extended Data Figure 1: Geographical location of horizon and its petrography. (836 KB)

    a, Locality map of the Zhangjiagou section, Xixiang, Shaanxi Province, China. In addition to Saccorhytus, the phosphatic limestone of Bed 2 of the Kuanchuanpu Formation in the Zhangjiagou section (see ref. 16) contains numerous small shelly fossils. b, c, Petrographic sections (plane-polarized light) of Bed 2 showing the phosphatic bioclastic grains, carbonate matrix and cements.

  2. Extended Data Figure 2: Saccorhytus coronarius gen. et sp. nov. (623 KB)

    ac, Holotype XX45-20. a, Left side, showing the body cones and circular pores. b, Two sub-layers of the integument around a body cone (Rbc2),with chevron pattern on the external and inner surfaces in Fig. 1a. c, Close-up of an oral protrusion in Fig. 1a. di, XX45-56. d, e, Close-ups of circular pores on the right, dorsal side. fi, Chevron pattern on integument surface of dorsal side. jl, XX48-64. j, Ventral view. k, Radial ribs of body cones defined as wavy margin, with integument composed of two sub-layers. l, Chevron pattern on integument surface.

  3. Extended Data Figure 3: Saccorhytus coronarius gen. et sp. nov. (478 KB)

    ac, XX45-1. a, Right side. b, Chevron pattern on integument surface. c, Two sub-layers of the integument on the third, left body cone (Lbc3) in Fig. 2a. d, e, XX36-22. d, Left view. A spine close to the second, left body cone (Lbc2); ventral part with nodular rugae. e, Circular pores on the dorsal side of d. fh, XX34-298. f, Close-up of closed mouth with radial folds and oral protrusions in Fig. 2f. g, Two sub-layers of the integument on the second, right body cone (Rbc2) with radial ribs in Fig. 2g. h, Chevron pattern on integument surface.

  4. Extended Data Figure 4: Saccorhytus coronarius gen. et sp. nov. (798 KB)

    ad, XX25-62, highly compressed. a, b, Right and left sides, respectively. c, Close-up of mouth with radial folds and oral protrusions in a; note nodular rugae on ventral anterior of body. d, Third body cone with radial ribs. e–h, XX27-160. e, Right view. f, Ventral view showing ventral mouth with radial folds and anterior nodular rugae. g, Chevron pattern on inner surface of integument. h, Two circular pores to posterior of first body cone.

  5. Extended Data Figure 5: Saccorhytus coronarius gen. et sp. nov. (674 KB)

    af, XX27-168. a, b, Right and left sides, respectively. Two body cones on right in a; two spines close to third left body cone in b. c, Left view of specimen reconstructed by micro-CT showing concealed body cones (Lbc1 and Lbc2). d, Close-up of arched mouth with radial folds and oral protrusions in a. e, Third body cone (Rbc3) with radial ribs and truncated opening. f, Nodular rugae and anterior spine in a. gl XX47-498. g, Ventral view, mouth arched; body cones arranged with bilateral symmetry, delimited by a circular pore at the mid-ventral line. A pair of large and small tubular protrusions (Ltp and Stp, respectively) are visible at the anterior, mid-ventral line of the mouth. h, Dorsal view with body cones arranged bilaterally. i, Close-up of mouth with radial folds and elongate oral protrusions most prominent along the middle line. j, At least 12 circular pores arranged bilaterally in two longitudinal rows. k, Third left body cone with broken scars (Sc) of radial ribs. l, Inconspicuous first and second left body cones.

  6. Extended Data Figure 6: Saccorhytus coronarius gen. et sp. nov. (423 KB)

    a, XX54-354. Dorsal view showing a pair of spines and bilaterally arranged fourth body cones. bd, XX56-192. b, Lateral view of the body. c, d, Integument of body cones consisting of two sublayers. e, XX59-253, showing the ventral anterior location of the mouth. f, g, XX61-27, showing two pairs of tubular projections (Ltp and Stp) at the anterior end of the mouth.

  7. Extended Data Figure 7: Body dimensions of 44 specimens. (199 KB)

    a, Rank order of lengths. b, Bivariate plot of height versus length. Despite a positive correlation in b, the low goodness of fit probably reflects the extensive crushing of most of the specimens.

  8. Extended Data Figure 8: Consensus trees. (162 KB)

    Left, produced by PAUP4.0; right, produced by TNT 1.1. The consensus tree from TNT 1.1 used New Technology Search with default options.

  9. Extended Data Figure 9: Deuterostomes from the Chengjiang fauna (Stage 3, Series 2), south China. (1,064 KB)

    a, Xidazoon stephanus Shu et al., 1999 (ref. 31) (ELI0000194). b, Didazoon haoae Shu et al., 2001 (ELI0000194). c, Pomatrum ventralis Luo et al., 1999 (ref. 32) (ELIJS010B). d, e, Beidazoon venustum Shu 2005 (ref. 33) (ELIJS454A, B). f, Vetulocystis catenata Shu et al., 2004 (ELISK016A). Double-circlet mouth as seen in Saccorhytus is present in Xidazoon and Pomatrum; gill pouches are visible in Didazoon, Pomatrum and Beidazoon; two body cones similar to those of Saccorhytus can be seen in Vetulocystis; and gill pouches with radial ribs that resemble those of Saccorhytus can also be seen on Beidazoon.

Supplementary information

Video

  1. Video 1: Reconstructed video of XX25-62. (21.66 MB, Download)
    Reconstructed video of XX25-62.
  2. Video 2: Reconstructed video of XX27-168 (21.73 MB, Download)
    Reconstructed video of XX27-168.
  3. Video 3: Reconstructed video of XX34-298 (21.61 MB, Download)
    Reconstructed video of XX34-298.
  4. Video 4: Reconstructed video of XX36-22 (21.65 MB, Download)
    Reconstructed video of XX36-22.
  5. Video 5: Reconstructed video of XX42-83 (21.68 MB, Download)
    Reconstructed video of XX42-83.
  6. Video 6: Reconstructed video of XX48-64 (21.68 MB, Download)
    Reconstructed video of XX48-64.

PDF files

  1. Supplementary Information (1.5 MB)

    This file contains Supplementary Table 1 and Supplementary Data.

Additional data