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

Abstract

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 https://github.com/CristiGuijarro/ComparativeGenomics.

Change history

  • 27 February 2020

    An amendment to this paper has been published and can be accessed via a link at the top of the paper.

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Acknowledgements

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

Contributions

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). https://doi.org/10.1038/s41559-020-1129-2

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