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Escape from adaptive conflict after duplication in an anthocyanin pathway gene

Nature volume 454, pages 762–765 (2008)Cite this article

Abstract

Gene duplications have been recognized as an important source of evolutionary innovation and adaptation since at least Haldane1, and their varying fates may partly explain the vast disparity in observed genome sizes2. The expected fates of most gene duplications involve primarily non-adaptive substitutions leading to either non-functionalization of one duplicate copy or subfunctionalization3, neither of which yields novel function. A significant evolutionary problem is thus elucidating the mechanisms of adaptive evolutionary change leading to evolutionary novelty. Currently, the most widely recognized adaptive process involving gene duplication is neo-functionalization (NEO-F), in which one copy undergoes directional selection to perform a novel function after duplication4. An alternative, but understudied, adaptive fate that has been proposed is escape from adaptive conflict (EAC), in which a single-copy gene is selected to perform a novel function while maintaining its ancestral function5,6. This gene is constrained from improving either novel or ancestral function because of detrimental pleiotropic effects on the other function. After duplication, one copy is free to improve novel function, whereas the other is selected to improve ancestral function. Here we first present two criteria that can be used to distinguish NEO-F from EAC. Using both tests for positive selection and assays of enzyme function, we then demonstrate that adaptive evolutionary change in a duplicated gene of the anthocyanin biosynthetic pathway in morning glories (Ipomoea) is best interpreted as EAC. Finally, we argue that this phenomenon likely occurs more often than has been previously believed and may thus represent an important mechanism in generating evolutionary novelty.

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Figure 1: Gene tree of sampled DFR copies from Convolvulaceae and outgroup taxa.
Figure 2: Results of enzyme activity assays.

Accession codes

Primary accessions

GenBank/EMBL/DDBJ

Data deposits

The new DNA sequences reported here are deposited in GenBank under accession numbers EU189072, EU189073, EU189074, EU189075, EU189076, EU189077, EU189078, EU189079, EU189080, EU189081 and EU189082.

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Acknowledgements

We thank E. Grotewold and B. Winkel for technical advice, and R. Hopkins for implementation of statistical models. This work was supported by National Science Foundation funding. D.L.D. was supported in part by a National Institutes of Health training grant to Duke University’s University Program in Genetics and Genomics.

Author Contributions D.L.D. and M.D.R. designed the research; D.L.D. performed the research and the analyses; D.L.D. and M.D.R. wrote the paper.

Author information

Authors and Affiliations

  1. Department of Biology and University Program in Genetics and Genomics, Box 90338, Duke University, Durham, North Carolina 27708-0338, USA,

    David L. Des Marais & Mark D. Rausher

Authors
  1. David L. Des Marais
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  2. Mark D. Rausher
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Corresponding authors

Correspondence to David L. Des Marais or Mark D. Rausher.

Supplementary information

Supplementary Information

This file contains Supplementary Methods, Supplementary Tables 1-3 showing model parameters from selection analyses and of enzyme assay results and Supplementary Figures 1-2 with Legends showing ancestral reconstruction of enzyme structure and function. (PDF 773 kb)

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Des Marais, D., Rausher, M. Escape from adaptive conflict after duplication in an anthocyanin pathway gene. Nature 454, 762–765 (2008). https://doi.org/10.1038/nature07092

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