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A Cambrian crown annelid reconciles phylogenomics and the fossil record

Nature volume 583, pages 249–252 (2020)Cite this article

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Abstract

The phylum of annelids is one of the most disparate animal phyla and encompasses ambush predators, suspension feeders and terrestrial earthworms1. The early evolution of annelids remains obscure or controversial2,3, partly owing to discordance between molecular phylogenies and fossils2,4. Annelid fossils from the Cambrian period have morphologies that indicate epibenthic lifestyles, whereas phylogenomics recovers sessile, infaunal and tubicolous taxa as an early diverging grade5. Magelonidae and Oweniidae (Palaeoannelida1) are the sister group of all other annelids but contrast with Cambrian taxa in both lifestyle and gross morphology2,6. Here we describe a new fossil polychaete (bristle worm) from the early Cambrian Canglangpu formation7 that we name Dannychaeta tucolus, which is preserved within delicate, dwelling tubes that were originally organic. The head has a well-defined spade-shaped prostomium with elongated ventrolateral palps. The body has a wide, stout thorax and elongated abdomen with biramous parapodia with parapodial lamellae. This character combination is shared with extant Magelonidae, and phylogenetic analyses recover Dannychaeta within Palaeoannelida. To our knowledge, Dannychaeta is the oldest polychaete that unambiguously belongs to crown annelids, providing a constraint on the tempo of annelid evolution and revealing unrecognized ecological and morphological diversity in ancient annelids.

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Fig. 1: Holotype specimen YKLP 11382 of D. tucolus.
Fig. 2: Anterior region of D. tucolus.
Fig. 3: Morphological details of D. tucolus.
Fig. 4: Reconstruction of Dannychaeta.

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Data availability

All data analysed in this paper are available as part of the Article, Extended Data Figs. 1–8 or Supplementary Information. The nomenclatural acts in this publication have been registered at ZooBank (LSID: urn:lsid:zoobank.org:pub:5BC89E47-2955-4539-94FD-D400E8C947FB).

Code availability

The phylogenetic dataset, and the commands and topological constraints necessary to run the MrBayes analyses, are included as NEXUS formatted files in the Supplementary Information.

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Acknowledgements

This work was supported by NSFC grant 41861134032 and Yunnan Provincial grants 2015HA021, 2019DG050, 2015HC029 and 2018IA073. L.A.P. was supported by a YIBS Donolley Postdoctoral Fellowship. D.Z. is supported by the Key Research Program of the Institute of Geology & Geophysics, Chinese Academy of Sciences (IGGCAS-201905). X.M. is supported by a Natural Environment Research Council Independent Research Fellowship (NE/L011751/1). We thank K. Chen and colleagues from the Yuhua subdistrict office in Chenggong for support in field collection, P. Cong, D. Wu, T. Zhao, Y. Zhao and M. Yin for help with fieldwork, X. Yang and H. Mai for SEM–EDX technical support, R. Zhou for micro-computed tomography scanning, D. Eibye-Jacobsen for providing detailed comments on an earlier version of this manuscript and for his continued support and valuable mentorship, and R. Nicholls for the artistic reconstruction of D. tucolus shown in Fig. 4b.

Author information

Author notes

  1. These authors contributed equally: Hong Chen, Luke A. Parry

Authors and Affiliations

  1. Yunnan Key Laboratory for Palaeobiology, Institute of Palaeontology, Yunnan University, Kunming, China

    Hong Chen, Dayou Zhai, Xianguang Hou & Xiaoya Ma

  2. MEC International Joint Laboratory for Palaeobiology and Palaeoenvironment, Institute of Palaeontology, Yunnan University, Kunming, China

    Hong Chen, Dayou Zhai, Xianguang Hou & Xiaoya Ma

  3. School of Biological Sciences and Technology, Liupanshui Normal University, Liupanshui, China

    Hong Chen

  4. Department of Geology and Geophysics, Yale University, New Haven, CT, USA

    Luke A. Parry

  5. Department of Earth Sciences, University of Oxford, Oxford, UK

    Luke A. Parry

  6. School of Earth Sciences, University of Bristol, Bristol, UK

    Jakob Vinther

  7. School of Biological Sciences, University of Bristol, Bristol, UK

    Jakob Vinther

  8. Centre for Ecology and Conservation, University of Exeter, Penryn, UK

    Xiaoya Ma

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Contributions

L.A.P., H.C., J.V. and X.M. designed the study and interpreted the fossil specimens and their anatomy. H.C., D.Z. and X.H. collected the specimens. H.C. prepared and photographed all specimens and performed the EDAX elemental analysis. L.A.P. made the figures, performed the phylogenetic analyses and composed the first draft of the manuscript with substantial input from all co-authors.

Corresponding authors

Correspondence to Xianguang Hou or Xiaoya Ma.

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The authors declare no competing interests.

Additional information

Peer review information Nature thanks Conrad Helm, Kate Mortimer, Mark D. Sutton and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data figures and tables

Extended Data Fig. 1 Additional details of the holotype specimen.

a, Entire specimen YKLP 11382a, including a possible posterior region. b, Possible posterior region from the region shown in a. c, YKLP 11382a, boxes show regions used for details of the head and interpretative drawing and fluoresence microscopy. d, Interpretative drawing of the specimen shown in c. e, YKLP 11382b. Image shows the regions used in SEM–EDX mapping and fluorescence microscopy. f, Magnification of the anterior region, showing the prostomial lobe and palp attachment. g, Interpretative drawing of the region shown in f, showing major anatomical features. The colour scheme is as in Fig. 1f. The palp attachment was inferred with additional information from the counterpart. h, SEM–EDX elemental maps. Element names for each map are shown in the bottom right corner. i, Fluorescence image showing the anterior region of the body in YKLP 11382b, including the gut, palps and putative blood lacuna. j, Fluorescence image of the putative blood lacuna in YKLP 11382a. k, Magnification of the posterior fragment associated with the holotype with parapodial lamellae. bl, blood lacuna.

Extended Data Fig. 2 Specimen of D. tucolus YKLP 11393 preserved in a dwelling tube.

a, Specimen YKLP 11393b, for which the anterior region, dwelling tube and a partial abdomen are preserved. b, Specimen YKLP 11393a, for which the anterior region, dwelling tubes and a partial abdomen are preserved. c, Specimen YKLP 11393b. Magnification of the anterior region (boxed area shown in a). The white arrowheads indicate the tube margins. d, Interpretative drawing of the region shown in c. e, Magnification of the prostomium and palps shown in c. f, Specimen YKLP 11393a. Magnification of the anterior region (boxed area shown in b). The white arrowheads indicate the tube margins. g, Magnification of the same region as in f, imaged using fluorescence microscopy. h, Interpretative drawing of the region shown in f and g. i, Poorly preserved abdominal region, from the region shown in a, imaged using direct light. j, Same region as in i, imaged using fluorescence microscopy. k, Poorly preserved abdominal region, from the region shown in b, imaged using direct light. l, Same region as in k, imaged using fluorescence microscopy. m, Thoracic chaetiger showing parapodia and chaetae from the region shown in b. n, Thoracic chaetiger showing parapodia and chaetae from the region shown in a.

Extended Data Fig. 3 Additional details of specimen YKLP 11383, preserved inside a dwelling tube parallel to the bedding.

a, YKLP 11383a midbody fragment preserved inside a dwelling tube, part. b, Interpretative drawing of the specimen shown in a, regions demarcated by black and blue brackets represent decayed and well-preserved regions of the body fossil, respectively. c, YKLP 11383b, midbody fragment preserved inside a dwelling tube, counterpart. d, Interpretative drawing of the specimen shown in c. e, Magnification of a well-preserved region of YKLP 11383a as shown in a, showing 11 chaetigers preserved inside the dwelling tube. f, SEM backscatter image of a similar region to EDX maps shown in Fig. 3f, showing bright grains that are associated with the tube and body fossil. The arrowheads indicate the left tube margin and pyritized tube wall. g, Section of the fossil shown in a photographed under low-angle light to indicate the relief of the dwelling tube. h, Section of the fossil shown in c photographed under low-angle light to indicate the relief of the dwelling tube. i, Magnification of three chaetiger regions of the region shown in e. j, Same region as in i, photographed using fluorescence microscopy. k, Magnification of the individual parapodium shown in j, photographed using fluorescence microscopy.

Extended Data Fig. 4 Specimens YKLP 11385a, YKLP 11387 and YKLP 11401, showing effaced specimens preserved in dwelling tubes.

a, YKLP 11385a, anterior fragment comprising the thorax and abdomen preserved inside dwelling tube. b, YKLP 11387a, anterior fragment preserving the thorax and abdomen. c, YKLP 11387b, anterior fragment preserving the thorax and abdomen. d, Magnification of the abdominal chaetigers in YKLP 11387a, from the region shown in b. The white filled arrows indicate the tube margins. e, Same region as in d imaged using fluorescence microscopy. f, YKLP 11401, effaced specimen preserved in a dwelling tube, including the putative blood lacuna. g, Magnification of the region shown in f, showing the gut and possible blood lacuna. Brackets in a–c and f indicate the position of the thoracic region.

Extended Data Fig. 5 Additional details of specimen YKLP 11389, showing details of parapodia, parapodial lamellae and the posterior region.

a, YKLP 11389b, counterpart, posterior fragment preserving parapodia and chaetae. b, YKLP 11389a, part showing preservation of lateral parapodial lamellae. c, Magnification of five chaetigers from the region shown in a. d, Magnification of chaetiger from the region shown in c. e, Magnification of chaetiger in d. f, Magnification of chaetiger, preserving the parapodial lamellae from the region shown in b. g, Chaetigers preserving the parapodial lamellae from the region shown in b. h, Same region as in g, showing the parapodial lamellae, imaged using fluorescence microscopy. i, Posterior region as shown in a, with putative pygidial cirri. j, Magnification of putative pygidial cirri in i. k, same region as in j, imaged using fluorescence microscopy. plm, parapodial lamella; pyc, pygidial cirri.

Extended Data Fig. 6 Specimen YKLP 11384, a decayed specimen preserved in a dwelling tube.

a, YKLP 11384a (the part), a whole specimen in a dwelling tube. The white arrowheads indicate the tube margin. b, YKLP 11384b (the counterpart), a whole specimen in a dwelling tube. The white arrowheads indicate the tube margin. c, Details of YKLP 11384b, showing putative blood lacuna and gut. The white and black arrowheads indicate the tube and body margins, respectively. d, Same view as in c, but imaged using fluorescence microscopy. Note the thick appearance of the tube margin. e, Detail of YKLP 11384a, showing the preservation of the tube wall, indicated by white arrowheads.

Extended Data Fig. 7 Full results of Bayesian phylogenetic analyses.

a, Full results of unconstrained analysis under the mki + gamma model. The topology shows a majority rule consensus tree, the scale bar is in units of expected number of substitutions per site, the numbers at the nodes are posterior probabilities. b, Full results of an analysis with constraints from phylogenomics under the mki + gamma model. The topology shows a majority rule consensus tree, the scale bar is in units of expected number of substitutions per site and the numbers at the nodes are posterior probabilities.

Extended Data Fig. 8 Results of parsimony analyses under equal and implied weighting.

a, Strict consensus tree (length 1,071) of parsimony analysis without topological constraints, numbers at the nodes are support from bootstrapping, jack-knifing and Bremer decay. b, Strict consensus of trees inferred using implied weighting with k = 10 (tree score 46.14190), numbers at the nodes are relative frequencies from symmetric resampling.

Supplementary information

Supplementary Information

This file contains Supplementary Materials – Phylogenetic analyses and data.

Reporting Summary

Supplementary Data

Character taxon matrix in NEXUS format. Morphological dataset for annelids and their close relatives including 143 taxa and 364 characters. This file contains character and state name information that is readable by Mesquite.

Supplementary Data

Morphological dataset including MrBayes commands. Morphological matrix in NEXUS format that is readable by MrBayes. This file contains the necessary commands to run the analyses both with and without topological constraints.

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Chen, H., Parry, L.A., Vinther, J. et al. A Cambrian crown annelid reconciles phylogenomics and the fossil record. Nature 583, 249–252 (2020). https://doi.org/10.1038/s41586-020-2384-8

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