Population-genetic models of the fates of duplicate genes

Walsh, Bruce

doi:10.1007/978-94-010-0229-5_16

Cited by 56 publications

(70 citation statements)

References 28 publications

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“…All of the data presented here are consistent with the hypothesis that the preservation of duplicated yeast genes can be explained by duplication, degeneration, and complementation and that newly evolved functions have contributed little to the persistence of most duplicated genes in yeast. These data are fully consistent with theoretical and population genetic analyses of DDC models (e.g., Lynch and Force 2000;Walsh 2003) and offer strong experimental support for such models. One limitation of the population genetic analyses is that they require assumptions about the relative rate of different kinds of mutations.…”

Section: Discussionsupporting

confidence: 85%

“…Bias toward maintaining certain genes in duplicate is evident from the fact that 75% of ribosomal protein genes are duplicated as compared to 12% of all genes (Warner et al 2001;Kellis et al 2004; and data not shown). Genes that have more separable functions also may be more likely to be maintained after gene duplication (Lynch and Force 2000;Walsh 2003).…”

Section: Discussionmentioning

confidence: 99%

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Conserved Functions of Yeast Genes Support the Duplication, Degeneration and Complementation Model for Gene Duplication

Hoof

2005

Genetics

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Gene duplication is often cited as a potential mechanism for the evolution of new traits, but this hypothesis has not been thoroughly tested experimentally. A classical model of gene duplication states that after gene duplication one copy of the gene preserves the ancestral function, while the other copy is free to evolve a new function. In an alternative duplication, divergence, and complementation model, duplicated genes are preserved because each copy of the gene loses some, but not all, of its functions through degenerating mutations. This results in the degenerating mutations in one gene being complemented by the other and vice versa. These two models make very different predictions about the function of the preduplication orthologs in closely related species. These predictions have been tested here for several duplicated yeast genes that appeared to be the leading candidates to fit the classical model. Surprisingly, the results show that duplicated genes are maintained because each copy carries out a subset of the conserved functions that were already present in the preduplication gene. Therefore, the results are not consistent with the classical model, but instead fit the duplication, divergence, and complementation model.

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Section: Discussionsupporting

confidence: 85%

Section: Discussionmentioning

confidence: 99%

Conserved Functions of Yeast Genes Support the Duplication, Degeneration and Complementation Model for Gene Duplication

Hoof

2005

Genetics

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“…where r ¼ u b /u n , u n is the null mutation rate, and u b is the mutation rate between B f and B m (for a similar analysis, see Walsh 1995Walsh , 2003. Taking both steps into account (fixation of B f by drift and B m by selection), the expected waiting time until B m becomes fixed is approximately (Weissman et al 2009)], a B f allele that is otherwise destined to become lost from the population may alternatively become ''rescued'' by mutation to B m followed by positive selection.…”

Section: Invasionmentioning

confidence: 99%

“…Previous gene duplication models suggest that natural selection can immediately favor the evolutionary invasion of duplicates from a locus that is evolving by balancing selection (Spofford 1969;Otto and Yong 2002;Walsh 2003;Proulx and Phillips 2006;Innan and Kondrashov 2010). However, functional diversification by gene duplication is constrained for loci evolving under purifying selection (Walsh 1995(Walsh , 2003.…”

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confidence: 99%

The Resolution of Sexual Antagonism by Gene Duplication

2011

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Disruptive selection between males and females can generate sexual antagonism, where alleles improving fitness in one sex reduce fitness in the other. This type of genetic conflict arises because males and females carry nearly identical sets of genes: opposing selection, followed by genetic mixing during reproduction, generates a population genetic ''tug-of-war'' that constrains adaptation in either sex. Recent verbal models suggest that gene duplication and sex-specific cooption of paralogs might resolve sexual antagonism and facilitate evolutionary divergence between the sexes. However, this intuitive proximal solution for sexual dimorphism potentially belies a complex interaction between mutation, genetic drift, and positive selection during duplicate fixation and sex-specific paralog differentiation. The interaction of these processes-within the explicit context of duplication and sexual antagonism-has yet to be formally described by population genetics theory. Here, we develop and analyze models of gene duplication and sex-specific differentiation between paralogs. We show that sexual antagonism can favor the fixation and maintenance of gene duplicates, eventually leading to the evolution of sexually dimorphic genetic architectures for male and female traits. The timescale for these evolutionary transitions is sensitive to a suite of genetic and demographic variables, including allelic dominance, recombination, sex linkage, and population size. Interestingly, we find that female-beneficial duplicates preferentially accumulate on the X chromosome, whereas male-beneficial duplicates are biased toward autosomes, independent of the dominance parameters of sexually antagonistic alleles. Although this result differs from previous models of sexual antagonism, it is consistent with several findings from the empirical genomics literature.

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“…Finally, under specialization, subfunctionalization and neofunctionalization act in concert, producing two copies that are functionally distinct from each other and from the ancestral gene (11). Theoretical work has shown that different conditions can result in the retention of duplicate genes by any one of these processes (9,(12)(13)(14)(15)(16)(17), and empirical studies have uncovered numerous examples of each (11,(18)(19)(20)(21)(22)(23).…”

mentioning

confidence: 99%

Neofunctionalization of young duplicate genes in Drosophila

Assis

Bachtrog

2013

Proc. Natl. Acad. Sci. U.S.A.

186

332

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Gene duplication is a key source of genetic innovation that plays a role in the evolution of phenotypic complexity. Although several evolutionary processes can result in the long-term retention of duplicate genes, their relative contributions in nature are unknown. Here we develop a phylogenetic approach for comparing genome-wide expression profiles of closely related species to quantify the roles of conservation, neofunctionalization, subfunctionalization, and specialization in the preservation of duplicate genes. Application of our method to pairs of young duplicates in Drosophila shows that neofunctionalization, the gain of a novel function in one copy, accounts for the retention of almost twothirds of duplicate genes. Surprisingly, novel functions nearly always originate in younger (child) copies, whereas older (parent) copies possess functions similar to those of ancestral genes. Further examination of such pairs reveals a strong bias toward RNAmediated duplication events, implicating asymmetric duplication and positive selection in the evolution of new functions. Moreover, we show that young duplicate genes are expressed primarily in testes and that their expression breadth increases over evolutionary time. This finding supports the "out-of-testes" hypothesis, which posits that testes are a catalyst for the emergence of new genes that ultimately evolve functions in other tissues. Thus, our study highlights the importance of neofunctionalization and positive selection in the retention of young duplicates in Drosophila and illustrates how duplicates become incorporated into novel functional networks over evolutionary time.G ene duplication produces two copies of an existing gene.Evolutionary theory predicts that functional redundancy of duplicate genes causes one copy to undergo a brief period of relaxed selection after duplication (1). In nearly all cases, this should result in an accumulation of deleterious mutations and pseudogenization of the copy within a few million years (2). However, most sequenced eukaryotic genomes contain many functional duplicates, some of which are hundreds of millions of years old (3-8), suggesting that duplicate genes play important roles in evolution.Four processes can result in the evolutionary preservation of duplicate genes: conservation, neofunctionalization, subfunctionalization, and specialization. Under conservation, ancestral functions are maintained in both copies, likely because increased gene dosage is beneficial (1). Under neofunctionalization, one copy retains its ancestral functions, and the other acquires a novel function (1). Under subfunctionalization, mutations damage different functions of each copy, such that both copies are required to preserve all ancestral gene functions (9, 10). Finally, under specialization, subfunctionalization and neofunctionalization act in concert, producing two copies that are functionally distinct from each other and from the ancestral gene (11). Theoretical work has shown that different conditions can result in the retention of...

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Population-genetic models of the fates of duplicate genes

Cited by 56 publications

References 28 publications

Conserved Functions of Yeast Genes Support the Duplication, Degeneration and Complementation Model for Gene Duplication

Conserved Functions of Yeast Genes Support the Duplication, Degeneration and Complementation Model for Gene Duplication

The Resolution of Sexual Antagonism by Gene Duplication

Neofunctionalization of young duplicate genes in Drosophila

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