Preservation of Duplicate Genes by Complementary, Degenerative Mutations

Corresponding author: Allan Force, Department of Biology, University of Oregon, Eugene, OR 97403., force{at}oregon.uoregon.edu (E-mail)

Communicating editor: A. G. CLARK

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. For a newly duplicated paralog, survival depends on the outcome of the race between entropic decay and chance acquisition of an advantageous regulatory mutation.

SIDOW 1996 (p. 717) On one hand, it may fix an advantageous allele giving it a slightly different, and selectable, function from its original copy. This initial fixation provides substantial protection against future fixation of null mutations, allowing additional mutations to accumulate that refine functional differentiation. Alternatively, a duplicate locus can instead first fix a null allele, becoming a pseudogene.

WALSH 1995 (p. 426) Duplicated genes persist only if mutations create new and essential protein functions, an event that is predicted to occur rarely.

NADEAU and SANKOFF 1997 (p. 1259) Thus overall, with complex metazoans, the major mechanism for retention of ancient gene duplicates would appear to have been the acquisition of novel expression sites for developmental genes, with its accompanying opportunity for new gene roles underlying the progressive extension of development itself.

COOKE et al. 1997 (p. 362)

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				P. Labbe, A. Berthomieu, C. Berticat, H. Alout, M. Raymond, T. Lenormand, and M. Weill Independent Duplications of the Acetylcholinesterase Gene Conferring Insecticide Resistance in the Mosquito Culex pipiens Mol. Biol. Evol., April 1, 2007; 24(4): 1056 - 1067. [Abstract] [Full Text] [PDF]

				F. X. Cunningham Jr., H. Lee, and E. Gantt Carotenoid Biosynthesis in the Primitive Red Alga Cyanidioschyzon merolae Eukaryot. Cell, March 1, 2007; 6(3): 533 - 545. [Abstract] [Full Text] [PDF]

				E. M. Kramer, L. Holappa, B. Gould, M. A. Jaramillo, D. Setnikov, and P. M. Santiago Elaboration of B Gene Function to Include the Identity of Novel Floral Organs in the Lower Eudicot Aquilegia PLANT CELL, March 1, 2007; 19(3): 750 - 766. [Abstract] [Full Text] [PDF]

				K. P. Byrne and K. H. Wolfe Consistent Patterns of Rate Asymmetry and Gene Loss Indicate Widespread Neofunctionalization of Yeast Genes After Whole-Genome Duplication Genetics, March 1, 2007; 175(3): 1341 - 1350. [Abstract] [Full Text] [PDF]

				B. P. Cusack and K. H. Wolfe Not Born Equal: Increased Rate Asymmetry in Relocated and Retrotransposed Rodent Gene Duplicates Mol. Biol. Evol., March 1, 2007; 24(3): 679 - 686. [Abstract] [Full Text] [PDF]

				B. C. Thomas, L. Rapaka, E. Lyons, B. Pedersen, and M. Freeling Arabidopsis intragenomic conserved noncoding sequence PNAS, February 27, 2007; 104(9): 3348 - 3353. [Abstract] [Full Text] [PDF]