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Phylogenomic analyses unravel annelid evolution

Abstract

Annelida, the ringed worms, is a highly diverse animal phylum that includes more than 15,000 described species and constitutes the dominant benthic macrofauna from the intertidal zone down to the deep sea. A robust annelid phylogeny would shape our understanding of animal body-plan evolution and shed light on the bilaterian ground pattern. Traditionally, Annelida has been split into two major groups: Clitellata (earthworms and leeches) and polychaetes (bristle worms), but recent evidence suggests that other taxa that were once considered to be separate phyla (Sipuncula, Echiura and Siboglinidae (also known as Pogonophora)) should be included in Annelida1,2,3,4. However, the deep-level evolutionary relationships of Annelida are still poorly understood, and a robust reconstruction of annelid evolutionary history is needed. Here we show that phylogenomic analyses of 34 annelid taxa, using 47,953 amino acid positions, recovered a well-supported phylogeny with strong support for major splits. Our results recover chaetopterids, myzostomids and sipunculids in the basal part of the tree, although the position of Myzostomida remains uncertain owing to its long branch. The remaining taxa are split into two clades: Errantia (which includes the model annelid Platynereis), and Sedentaria (which includes Clitellata). Ancestral character trait reconstructions indicate that these clades show adaptation to either an errant or a sedentary lifestyle, with alteration of accompanying morphological traits such as peristaltic movement, parapodia and sensory perception. Finally, life history characters in Annelida seem to be phylogenetically informative.

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Figure 1: Reconstruction of the Annelida phylogenetic tree.
Figure 2: Ancestral reconstructions of body and parapodial characters.

Accession codes

Data deposits

Sequence data have been deposited in the NCBI Expressed Sequence Tag database (dbEST) under accession numbers FN424437–FN428571, FR754554–FR771822, HQ729923–HQ729975. The largest aligned data set has been deposited at http://www.treebase.org.

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Acknowledgements

We are grateful to I. Ebersberger, S. Strauss and A. von Haeseler for the processing of our raw EST libraries. We also thank M. Aguado for species identification of Typosyllis pigmentata, as well as K. M. Halanych and P. A. Ramey-Balci for suggestions. T.H.S. and C.B. acknowledge support from the marine biological stations in Bamfield, Helgoland, List and Roscoff for collection of annelids. This work was funded by the priority programme ‘Deep Metazoan Phylogeny’ of the Deutsche Forschungsgemeinschaft by grants DFG-STR 683/5-2 (T.H.S.), DFG-Pu-84/5-1 (G.P. and T.H.S.), DFG-TI-349/4-1 (R.T.), DFG Li 998/3-1 (B.L.), DFG-HA 5744/1-1 (S.H.) and DFG-BL-787/2-1 (C.B.).

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Contributions

T.H.S., G.P., R.T. and C.B. conceived this study. T.H.S. took the lead on data collection of sedentary polychaetes, and writing. T.H.S. and S.H. performed phylogenomic analyses. C.H. aided in the data collection of Sedentaria. C.B. and C.P. took the lead on data collection of errant polychaetes, and C.B., S.H. and N.H. on compilation of the data sets from the EST libraries. A.M. and B.L. generated the EST library of Sipunculus nudus, and M.K. was responsible for the sequencing of the EST libraries. T.H.S., G.P., R.T. and C.B. were the main contributors to the writing of the manuscript.

Corresponding authors

Correspondence to Torsten H. Struck or Christoph Bleidorn.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

The file contains Supplementary Results, additional references, Supplementary Figures 1-8 with legends and Supplementary Tables 1-6. (PDF 1926 kb)

Supplementary Data Set

This file contains the morphological data matrix used in the ancestral reconstructions. Modifications in the character matrix in comparison to Zrzavy et al (2009) are in bold. Converting it to a plain text file allows opening it with Mesquite to show the results of our ancestral reconstructions. (RTF 33 kb)

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Struck, T., Paul, C., Hill, N. et al. Phylogenomic analyses unravel annelid evolution. Nature 471, 95–98 (2011). https://doi.org/10.1038/nature09864

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