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Widespread patterns of gene loss in the evolution of the animal kingdom

A Publisher Correction to this article was published on 27 February 2020

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The animal kingdom shows an astonishing diversity, the product of over 550 million years of animal evolution. The current wealth of genome sequence data offers an opportunity to better understand the genomic basis of this diversity. Here we analyse a sampling of 102 whole genomes including >2.6 million protein sequences. We infer major genomic patterns associated with the variety of animal forms from the superphylum to phylum level. We show that a remarkable amount of gene loss occurred during the evolution of two major groups of bilaterian animals, Ecdysozoa and Deuterostomia, and further loss in several deuterostome lineages. Deuterostomes and protostomes also show large genome novelties. At the phylum level, flatworms, nematodes and tardigrades show the largest reduction of gene complement, alongside gene novelty. These findings paint a picture of evolution in the animal kingdom in which reductive evolution at the protein-coding level played a major role in shaping genome composition.

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Fig. 1: Reconstruction of ancestral genomic gains and losses in the animal kingdom.
Fig. 2: Levels of gene gains and losses at the phylum level.
Fig. 3: Most abundantly lost and gained molecular functions (GOs).

Data availability

Publicly available genomes are listed in Supplementary Table 1.

Code availability

All the scripts used in this study can be found at

Change history


  1. Egger, B. et al. A transcriptomic-phylogenomic analysis of the evolutionary relationships of flatworms. Curr. Biol. 25, 1347–1353 (2015).

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  3. Marlétaz, F., Peijnenburg, K. T. C. A., Goto, T., Satoh, N. & Rokhsar, D. S. A new spiralian phylogeny places the enigmatic arrow worms among gnathiferans. Curr. Biol. 29, 312–318.e3 (2019).

    Article  Google Scholar 

  4. Giribet, G. New animal phylogeny: future challenges for animal phylogeny in the age of phylogenomics. Org. Divers. Evol. 16, 419–426 (2016).

    Article  Google Scholar 

  5. Halanych, K. M. The new view of animal phylogeny. Annu. Rev. Ecol. Evol. Syst. 35, 229–256 (2004).

    Article  Google Scholar 

  6. Richter, D. J., Fozouni, P., Eisen, M. B. & King, N. Gene family innovation, conservation and loss on the animal stem lineage. eLife 7, e34226 (2018).

    Article  Google Scholar 

  7. Paps, J. What makes an animal? The molecular quest for the origin of the animal kingdom. Integr. Comp. Biol. 58, 654–665 (2018).

    Article  CAS  Google Scholar 

  8. Grau-Bové, X. et al. Dynamics of genomic innovation in the unicellular ancestry of animals. eLife 6, e26036 (2017).

    Article  Google Scholar 

  9. Lankester, E. R. Degeneration. A Chapter in Darwinism (Macmillan and Company, 1880).

  10. Denoeud, F. et al. Plasticity of animal genome architecture unmasked by rapid evolution of a pelagic tunicate. Science 330, 1381–1385 (2010).

    Article  CAS  Google Scholar 

  11. Tsai, I. J. et al. The genomes of four tapeworm species reveal adaptations to parasitism. Nature 496, 57–63 (2013).

    Article  CAS  Google Scholar 

  12. Zmasek, C. M. & Godzik, A. This déjà vu feeling—analysis of multidomain protein evolution in eukaryotic genomes. PLoS Comput. Biol. 8, e1002701 (2012).

    Article  CAS  Google Scholar 

  13. Moore, A. D. & Bornberg-Bauer, E. The dynamics and evolutionary potential of domain loss and emergence. Mol. Biol. Evol. 29, 787–796 (2012).

    Article  CAS  Google Scholar 

  14. Albalat, R. & Cañestro, C. Evolution by gene loss. Nat. Rev. Genet. 17, 379–391 (2016).

    Article  CAS  Google Scholar 

  15. Paps, J. & Holland, P. W. H. Nat. Commun. 9, 1730 (2018).

    Article  Google Scholar 

  16. Dunwell, T. L., Paps, J. & Holland, P. W. H. Novel and divergent genes in the evolution of placental mammals. Proc. R. Soc. B 284, 20171357 (2017).

    Article  Google Scholar 

  17. Simão, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V. & Zdobnov, E. M. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31, 3210–3212 (2015).

    Article  Google Scholar 

  18. Camacho, C. et al. BLAST+: architecture and applications. BMC Bioinform. 10, 421 (2009).

    Article  Google Scholar 

  19. Enright, A. J., Van Dongen, S. & Ouzounis, C. A. An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res. 30, 1575–1584 (2002).

    Article  CAS  Google Scholar 

  20. Pruitt, K. D., Tatusova, T. & Maglott, D. R. NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res. 35, 61–65 (2007).

    Article  Google Scholar 

  21. Arakawa, K. No evidence for extensive horizontal gene transfer from the draft genome of a tardigrade. Proc. Natl Acad. Sci. USA 113, E3057 (2016).

    Article  CAS  Google Scholar 

  22. Yoshida, Y. et al. Comparative genomics of the tardigrades Hypsibius dujardini and Ramazzottius varieornatus. PLoS Biol. 15, e2002266 (2017).

    Article  Google Scholar 

  23. The Gene Ontology Consortium. Expansion of the Gene Ontology knowledgebase and resources. Nucleic Acids Res. 45, D331–D338 (2017).

  24. Simakov, O. et al. Insights into bilaterian evolution from three spiralian genomes. Nature 493, 526–531 (2013).

    Article  CAS  Google Scholar 

  25. Luo, Y.-J. et al. Nemertean and phoronid genomes reveal lophotrochozoan evolution and the origin of bilaterian heads. Nat. Ecol. Evol. 2, 141–151 (2018).

    Article  Google Scholar 

  26. The UniProt Consortium. UniProt: the universal protein knowledgebase. Nucleic Acids Res. 45, D158–D169 (2017).

  27. Jones, P. et al. InterProScan 5: genome-scale protein function classification. Bioinformatics 30, 1236–1240 (2014).

    Article  CAS  Google Scholar 

  28. Laumer, C. E. et al. Spiralian phylogeny informs the evolution of microscopic lineages. Curr. Biol. 25, 2000–2006 (2015).

    Article  CAS  Google Scholar 

  29. Kocot, K. M. On 20 years of Lophotrochozoa. Org. Divers. Evol. 16, 329–343 (2016).

    Article  Google Scholar 

  30. Kocot, K. M. et al. Phylogenomics of Lophotrochozoa with consideration of systematic error. Syst. Biol. 66, 256–282 (2017).

    CAS  PubMed  Google Scholar 

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We thank I. Maeso for comments on the manuscript. C.G.-C. and J.P. received funding from the School of Biological Sciences (University of Essex).

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Authors and Affiliations



C.G.-C., J.P. and P.W.H.H. designed the study and analyses. C.G.-C. performed the analyses. All the authors wrote the manuscript. C.G.-C. drew additional animal outlines (the flatworm and the rotifer, both of which are Public Domain Dedication 1.0 license and No Copyright, see Supplementary Information) in Fig. 1.

Corresponding author

Correspondence to Jordi Paps.

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The authors declare no competing interests.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–15 and Tables 1–3.

Reporting Summary

Supplementary Data 1

HG assignment for each genome, and how many proteins each genome has assigned to each cluster for core novel, core lost, novel and lost HGs for each phylum. Files are named by clade position in the phylogeny followed by the assigned clade name.

Supplementary Data 2

List of protein sequence headers or IDs assigned to each novel and lost HG for each phylum.

Supplementary Data 3

GO and model protein assignment for each of the core HGs analysed in the pipeline. There is a file for each of the core lost and core novel HGs for each clade analysed. GOs were mined from InterProScan.

Supplementary Data 4

GO and model protein assignment for each of the HGs analysed in the pipeline. There is a file for each of the lost and novel HGs for each clade analysed.

Supplementary Data 5

BLAST checks of the novel HGs (all the proteins in each HG) for each phylum with the RefSeq database. Thresholds include 1 × 10−6 e-value and >50% identity matches.

Supplementary Data 6

Available as an xlsx sorted document. The number of protein class Panther hits and other GOs for each node. The numbers between nodes cannot be compared due to the varying model organisms used and protein class annotations; however, each node should be compared internally within the same model organisms. Model organism for protein class used is the same as written in Supplementary Data 3 and 4. Orphan HGs were excluded from the analysis. Urochordate, cephalochordate, hemichordate, platyhelminth and tardigrade novelties were also excluded from these data due to the lack of protein classes in the Panther analysis for specific model organisms. GOs and protein IDs are available in Supplementary Data 3 and 4.

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Guijarro-Clarke, C., Holland, P.W.H. & Paps, J. Widespread patterns of gene loss in the evolution of the animal kingdom. Nat Ecol Evol 4, 519–523 (2020).

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