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Data for: Ancient gene linkages support ctenophores as sister to other animals

Cite this dataset

Schultz, Darrin et al. (2023). Data for: Ancient gene linkages support ctenophores as sister to other animals [Dataset]. Dryad. https://doi.org/10.5061/dryad.dncjsxm47

Abstract

A central question in evolutionary biology is whether sponges or ctenophores (comb jellies) are the sister group to all other animals. These alternative phylogenetic hypotheses imply different scenarios for the evolution of complex neural systems and other animal-specific traits1–6. Conventional phylogenetic approaches based on morphological characters and increasingly extensive gene sequence collections have not been able to definitively answer this question7–11. Here we develop chromosome-scale gene linkage, also known as synteny, as a novel phylogenetic character for resolving this question12. We report new chromosome-scale genomes for a ctenophore and two marine sponges, and for three unicellular relatives of animals (a choanoflagellate, a filasterean amoeba, and an ichthyosporean) that serve as outgroups for phylogenetic analysis. Remarkably, we find ancient syntenies that are conserved between animals and their close unicellular relatives. Ctenophores and unicellular eukaryotes share ancestral metazoan patterns while sponges, bilaterians, and cnidarians share derived chromosomal rearrangements. Conserved syntenic characters unite sponges with bilaterians, cnidarians, and placozoans in a monophyletic clade to the exclusion of ctenophores, placing ctenophores as the sister group to all other animals. The patterns of synteny shared by sponges, bilaterians, and cnidarians are the result of rare and irreversible chromosome fusion-and-mixing events that provide robust and unambiguous phylogenetic support for the ctenophore-sister hypothesis. These findings provide a new framework for resolving deep, recalcitrant phylogenetic problems and have implications for our understanding of animal evolution.

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2. Halanych, K. M. The ctenophore lineage is older than sponges? That cannot be right! Or can it? J. Exp. Biol. 218, 592–597 (2015).

3. Jékely, G., Paps, J. & Nielsen, C. The phylogenetic position of ctenophores and the origin(s) of nervous systems. Evodevo 6, 1 (2015).

4. Ryan, J. F. & Chiodin, M. Where is my mind? How sponges and placozoans may have lost neural cell types. Philos. Trans. R. Soc. Lond. B Biol. Sci. 370, 20150059– (2015).

5. Moroz, L. L. et al. The ctenophore genome and the evolutionary origins of neural systems. Nature 510, 109–114 (2014).

6. Burkhardt, P. Ctenophores and the evolutionary origin(s) of neurons. Trends Neurosci. 45, 878–880 (2022).

7. Philippe, H. et al. Phylogenomics revives traditional views on deep animal relationships. Curr. Biol. 19, 706–712 (2009).

8. Simion, P. et al. A Large and Consistent Phylogenomic Dataset Supports Sponges as the Sister Group to All Other Animals. Curr. Biol. 27, 958–967 (2017).

9. Dunn, C. W. et al. Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452, 745–749 (2008).

10. Whelan, N. V. et al. Ctenophore relationships and their placement as the sister group to all other animals. Nat. Ecol. Evol. 1, 1737–1746 (2017).

11. Li, Y., Shen, X.-X., Evans, B., Dunn, C. W. & Rokas, A. Rooting the animal tree of life. Mol. Biol. Evol. 38, 4322–4333 (2021).

12. Simakov, O. et al. Deeply conserved synteny and the evolution of metazoan chromosomes. Sci. Adv. 8, eabi5884 (2022).

Methods

This dataset is a collection of de novo-assembled and already-published genomes, and supplementary analyses/results complementing the main and supplementary figures of this manuscript.

Usage notes

The software necessary to perform these analyses, odp, is included in the linked Zenodo release. No proprietary software is required to open any of these files.

Funding

David and Lucile Packard Foundation

Monterey Bay Aquarium Research Institute

National Science Foundation, Award: NSF GRFP DGE 1339067 to D.T.S.

National Science Foundation, Award: NSF DEB-1542679 to S.H.D.H

European Research Council, Award: 945026 to O.S.

Okinawa Institute of Science and Technology Graduate University

Chan Zuckerberg Initiative (United States)

University of California, Berkeley, Award: Marthella Foskett Brown Chair in Biology