Lineage-specific rediploidization is a mechanism to explain time-lags between genome duplication and evolutionary diversification

Fiona M Robertson, Manu Kumar Gundappa, Fabian Grammes, Torgeir R. Hvidsten, Anthony Redmond, Sigbjorn Lien, Peter W.H. Holland, Samuel A. M. Martin, Simen R. Sandve, Daniel J. MacQueen (Corresponding Author)

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Abstract

Background The functional divergence of duplicate genes (ohnologues) retained from whole genome duplication (WGD) is thought to promote evolutionary diversification. However, species radiation and phenotypic diversification is often temporally separated from WGD. Salmonid fish, whose ancestor underwent WGD by autotetraploidization ~95 Ma fit such a 'time-lag' model of post-WGD radiation, which occurred alongside a major delay in the rediploidization process. Here we propose a model, 'lineage-specific ohnologue resolution' (LORe), to address the consequences of delayed rediploidization. Under LORe, speciation precedes rediploidization, allowing independent ohnologue divergence in sister lineages sharing an ancestral WGD event. Results Using cross-species sequence capture, phylogenomics and genome-wide analyses of ohnologue expression divergence, we demonstrate the major impact of LORe on salmonid evolution. One quarter of each salmonid genome, harbouring at least 4,550 ohnologues, has evolved under LORe, with rediploidization and functional divergence occurring on multiple independent occasions > 50 Myr post-WGD. We demonstrate the existence and regulatory divergence of many LORe ohnologues with functions in lineage-specific physiological adaptations that potentially facilitated salmonid species radiation. We show that LORe ohnologues are enriched for different functions than 'older' ohnologues that began diverging in the salmonid ancestor. Conclusions LORe has unappreciated significance as a nested component of post-WGD divergence that impacts the functional properties of genes, whilst providing ohnologues available solely for lineage-specific adaptation. Under LORe, which is predicted following many WGD events, the functional outcomes of WGD need not appear 'explosively', but can arise gradually over tens of Myr, promoting lineage-specific diversification regimes under prevailing ecological pressures.
Original languageEnglish
Article number111
JournalGenome Biology
Volume18
DOIs
Publication statusPublished - 14 Jun 2017

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Keywords

  • whole genome duplication
  • rediploidization
  • species radiation
  • Lineage-specific Ohnologue Resolution (LORe)
  • duplicate genes
  • functional divergence
  • autotetraploidization
  • salmonid fish

Cite this

Robertson, F. M., Gundappa, M. K., Grammes, F., Hvidsten, T. R., Redmond, A., Lien, S., Holland, P. W. H., Martin, S. A. M., Sandve, S. R., & MacQueen, D. J. (2017). Lineage-specific rediploidization is a mechanism to explain time-lags between genome duplication and evolutionary diversification. Genome Biology, 18, [111]. https://doi.org/10.1186/s13059-017-1241-z