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Subfunctionalization versus neofunctionalization after whole-genome duplication

Nature Genetics volume 50, pages 908–909 (2018)Cite this article

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To the Editor: The question of what the predominant evolutionary fate is of genes after duplication events has been intensely debated for decades1,2. Two articles in Nature (Lien et al.3) and Nature Genetics (Braasch et al.4) investigated the regulatory fate of gene duplicates after the salmonid-specific (Ss4R) and teleost-specific (Ts3R) whole-genome duplication (WGD) events, respectively. Both studies relied on tissue expression atlases to estimate regulatory divergence and used closely related unduplicated sister taxa (Northern pike and spotted gar, respectively) as proxies for the ancestral expression state. Surprisingly, the two studies reach very different conclusions about the evolutionary mechanisms impacting gene expression after WGD. Braasch et al.4 concluded that expression divergence was consistent with partitioning of tissue regulation between duplicates (subfunctionalization), whereas Lien et al.3 concluded that most divergences in tissue regulation were consistent with one copy maintaining ancestral tissue regulation while the other diverged (in line with neofunctionalization). Here we show that this discrepancy in the conclusions of the two studies is a consequence of the analytical approach and is not related to underlying differences in the data.

To evaluate the underlying cause of the discrepancies between the two studies, we reanalyzed the data from Braasch et al.4 using the approach of Lien et al.3, and vice versa. Both studies computed expression correlation to the unduplicated sister taxon as a measure of divergence—for the two duplicates individually (duplicate 1 and duplicate 2) and for the summed expression of the duplicates (sum duplicates). The only aspect of the analyses that differed was how the individual genes within the duplicate pairs were ranked. In Braasch et al.4, the duplicate pairs were ordered randomly (i.e., the two genes were assigned labels ‘duplicate 1’ and ‘duplicate 2’ at random; see Chapter 13.1 (p. 36) of the supplementary material of Braasch et al.4). In contrast, Lien et al.3 ranked the two genes in each duplicate pair as ‘most diverged’ (i.e., the gene with the lowest expression correlation with the ortholog in the unduplicated sister taxon; duplicate 1) and ‘most conserved’ (i.e., the gene with the highest expression correlation with the ortholog; duplicate 2).

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Fig. 1: Tissue expression divergence in real and simulated data.

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Acknowledgements

S.R.S. was supported by Norwegian Research Council projects 221734 and 244164.

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Authors and Affiliations

  1. Center for Integrative Genetics (CIGENE), Faculty of Biosciences, Department of Animal and Aquacultural Sciences, Norwegian University of Life Sciences, Ås, Norway

    Simen R. Sandve

  2. Department of Biology, San Francisco State University, San Francisco, CA, USA

    Rori V. Rohlfs

  3. Faculty of Chemistry, Biotechnology and Food Science, Norwegian University of Life Sciences, Ås, Norway

    Torgeir R. Hvidsten

  4. Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, Umeå, Sweden

    Torgeir R. Hvidsten

Authors
  1. Simen R. Sandve
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  2. Rori V. Rohlfs
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  3. Torgeir R. Hvidsten
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Contributions

S.R.S. and T.R.H. conceived the study. T.R.H. analyzed the expression data, and R.V.R. performed the simulations. All authors interpreted the results and wrote and approved the manuscript for publication.

Corresponding authors

Correspondence to Simen R. Sandve or Torgeir R. Hvidsten.

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The authors declare no competing interests.

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Sandve, S.R., Rohlfs, R.V. & Hvidsten, T.R. Subfunctionalization versus neofunctionalization after whole-genome duplication. Nat Genet 50, 908–909 (2018). https://doi.org/10.1038/s41588-018-0162-4

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