Preservation of duplicate genes by complementary, degenerative mutations

Allan Force, Michael Lynch, F. Bryan Pickett, Angel Amores, Yi Lin Yan, John Postlethwait

Research output: Contribution to journalArticle

2415 Citations (Scopus)

Abstract

The origin of organismal complexity is generally thought to be tightly coupled to the evolution of new gene functions arising subsequent to gene duplication. Under the classical model for the evolution of duplicate genes, one member of the duplicated pair usually degenerates within a few million years by accumulating deleterious mutations, while the other duplicate retains the original function. This model further predicts that on rare occasions, one duplicate may acquire a new adaptive function, resulting in the preservation of both members of the pair, one with the new function and the other retaining the old. However, empirical data suggest that a much greater proportion of gene duplicates is preserved than predicted by the classical model. Here we present a new conceptual framework for understanding the evolution of duplicate genes that may help explain this conundrum. Focusing on the regulatory complexity of eukaryotic genes, we show how complementary degenerative mutations in different regulatory elements of duplicated genes can facilitate the preservation of both duplicates, thereby increasing long-term opportunities for the evolution of new gene functions. The duplication-degeneration-complementation (DDC) model predicts that (1) degenerative mutations in regulatory elements can increase rather than reduce the probability of duplicate gene preservation and (2) the usual mechanism of duplicate gene preservation is the partitioning of ancestral functions rather than the evolution of new functions. We present several examples (including analysis of a new engrailed gene in zebrafish) that appear to be consistent with the DDC model, and we suggest several analytical and experimental approaches for determining whether the complementary loss of gene subfunctions or the acquisition of novel functions are likely to be the primary mechanisms for the preservation of gene duplicates.

Original languageEnglish (US)
Pages (from-to)1531-1545
Number of pages15
JournalGenetics
Volume151
Issue number4
StatePublished - Apr 1 1999
Externally publishedYes

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Duplicate Genes
Mutation
Genes
Gene Duplication
Zebrafish

ASJC Scopus subject areas

  • Genetics

Cite this

Force, A., Lynch, M., Pickett, F. B., Amores, A., Yan, Y. L., & Postlethwait, J. (1999). Preservation of duplicate genes by complementary, degenerative mutations. Genetics, 151(4), 1531-1545.

Preservation of duplicate genes by complementary, degenerative mutations. / Force, Allan; Lynch, Michael; Pickett, F. Bryan; Amores, Angel; Yan, Yi Lin; Postlethwait, John.

In: Genetics, Vol. 151, No. 4, 01.04.1999, p. 1531-1545.

Research output: Contribution to journalArticle

Force, A, Lynch, M, Pickett, FB, Amores, A, Yan, YL & Postlethwait, J 1999, 'Preservation of duplicate genes by complementary, degenerative mutations', Genetics, vol. 151, no. 4, pp. 1531-1545.
Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J. Preservation of duplicate genes by complementary, degenerative mutations. Genetics. 1999 Apr 1;151(4):1531-1545.
Force, Allan ; Lynch, Michael ; Pickett, F. Bryan ; Amores, Angel ; Yan, Yi Lin ; Postlethwait, John. / Preservation of duplicate genes by complementary, degenerative mutations. In: Genetics. 1999 ; Vol. 151, No. 4. pp. 1531-1545.
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