Published April 3, 2023 | Version v1

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

  • 1. University of Vienna
  • 2. Monterey Bay Aquarium Research Institute
  • 3. University of California, Berkeley
  • 4. University of California, Santa Cruz

Description

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.

1. Ryan, J. F. et al. The genome of the ctenophore Mnemiopsis leidyi and its implications for cell type evolution. Science 342, 1242592 (2013).

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).

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 provided by: David and Lucile Packard Foundation
Crossref Funder Registry ID: http://dx.doi.org/10.13039/100000008
Award Number:

Funding provided by: Monterey Bay Aquarium Research Institute
Crossref Funder Registry ID: http://dx.doi.org/10.13039/100019189
Award Number:

Funding provided by: National Science Foundation
Crossref Funder Registry ID: http://dx.doi.org/10.13039/100000001
Award Number: NSF GRFP DGE 1339067 to D.T.S.

Funding provided by: National Science Foundation
Crossref Funder Registry ID: http://dx.doi.org/10.13039/100000001
Award Number: NSF DEB-1542679 to S.H.D.H

Funding provided by: H2020 European Research Council
Crossref Funder Registry ID: http://dx.doi.org/10.13039/100010663
Award Number: 945026 to O.S.

Funding provided by: Okinawa Institute of Science and Technology
Crossref Funder Registry ID: http://dx.doi.org/10.13039/501100004199
Award Number:

Funding provided by: Chan Zuckerberg Initiative
Crossref Funder Registry ID: http://dx.doi.org/10.13039/100014989
Award Number:

Funding provided by: University of California Berkeley
Crossref Funder Registry ID: http://dx.doi.org/10.13039/100006978
Award Number: Marthella Foskett Brown Chair in Biology

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