Heterosis and the Evolution of Duplications

Spofford, Janice B.

doi:10.1086/282611

Cited by 106 publications

(81 citation statements)

References 21 publications

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“…Heterozygote advantage readily favors the invasion of duplicate genes (Spofford 1969;Otto and Yong 2002;Proulx and Phillips 2006). Similarly, sexual antagonism with a dominance reversal generates a form of overdominant selection (with fitness averaged across the sexes) that maintains ancestral genetic variation and favors the invasion of gene duplications.…”

Section: Discussionmentioning

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%

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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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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

The Resolution of Sexual Antagonism by Gene Duplication

2011

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“…The role of selective forces in the early evolutionary divergence of progenitor genes after a duplication event should depend on the specific functional features associated with the presence of the duplicate loci. Concurrent selection on progenitor and duplicate copies, as observed in the GD1 gene pair, is predicted by early studies that indicate that positive selection on both copies can occur simultaneously if the ancestral gene is segregating for selectively maintained alleles (32,33). Furthermore, the incipient pseudogenization of the neutrally evolving GD3-A locus suggests that gene loss may occur early in the process of duplicate gene evolution.…”

Section: Evidence For Positive Selection At Progenitor Locimentioning

confidence: 94%

The early stages of duplicate gene evolution

Moore

Purugganan

2003

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

487

307

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Gene duplications are one of the primary driving forces in the evolution of genomes and genetic systems. Gene duplicates account for 8 -20% of the genes in eukaryotic genomes, and the rates of gene duplication are estimated at between 0.2% and 2% per gene per million years. Duplicate genes are believed to be a major mechanism for the establishment of new gene functions and the generation of evolutionary novelty, yet very little is known about the early stages of the evolution of duplicated gene pairs. It is unclear, for example, to what extent selection, rather than neutral genetic drift, drives the fixation and early evolution of duplicate loci. Analysis of recently duplicated genes in the Arabidopsis thaliana genome reveals significantly reduced species-wide levels of nucleotide polymorphisms in the progenitor and͞or duplicate gene copies, suggesting that selective sweeps accompany the initial stages of the evolution of these duplicated gene pairs. Our results support recent theoretical work that indicates that fates of duplicate gene pairs may be determined in the initial phases of duplicate gene evolution and that positive selection plays a prominent role in the evolutionary dynamics of the very early histories of duplicate nuclear genes.G ene duplications are one of the primary driving forces in the evolution of genomes and genetic systems (1, 2). Duplicate genes are believed to be a major mechanism for the establishment of new gene functions (3) and the generation of evolutionary novelty (4). Around 15% of genes in the human genome are believed to arise from duplication events, whereas gene duplicates account for 8-20% of the Drosophila melanogaster, Caenorhabditis elegans, and Saccharomyces cervisiae genomes (5, 6). The rates of gene duplication in these model species are estimated at between 0.2% and 2% per gene per million years (5, 6).Most studies on the evolution of gene duplications examine the macroevolutionary patterns of gene diversification (7-9) and focus on the fates of duplicate loci long after their establishment and fixation within species. In contrast, we know very little about the initial stages of duplicate gene evolution. For example, it is unclear whether the process of evolutionary fixation of duplicate loci from a single individual to the entire species is governed by random genetic drift or through the action of positive selection acting on an adaptive phenotype associated with the gene duplication event (10, 11). We simply do not know which of these two evolutionary forces govern the critical early phases of duplicate gene evolution.Theoretical studies suggest that the relative importance of these two evolutionary forces, neutral genetic drift and positive selection, differs depending on the ultimate functional fate of the duplicate gene pair (10). Gene duplication can lead to one of several functional relationships between duplicate gene copies, including (i) loss of gene function by pseudogene formation, (ii) the establishment of redundant loci (12), (iii) the evolutionary diversi...

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“…The quantitative advantage of the first, that is, the increased protein production, is well documented: for example, homogeneous gene duplications have been reported in cases of resistance to insecticides through increased detoxification (Raymond, Chevillon, Guillemaud, Lenormand, & Pasteur, 1998) or in adaptation to a starch‐rich diet in humans and dogs through greater amylase production (Axelsson et al., 2013; Perry et al., 2007). On the contrary, heterogeneous duplications seem to be selected because the two alleles they carry can perform two different functions, by fixing the heterozygote advantage without segregation cost (Haldane, 1932; Milesi, Weill et al., 2017; Spofford, 1969). Such duplications have been documented in a few cases of insecticide resistance, the Rdl gene in Drosophila melanogaster (Remnant et al., 2013), or the ace‐1 gene in Anopheles gambiae and Culex pipiens (Assogba et al., 2016; Labbé, Berthomieu et al., 2007; Milesi, Assogba et al., 2017), where they associate one resistance and one susceptible copy of the gene.…”

Section: Introductionmentioning

confidence: 99%

Adaptive deletion in resistance gene duplications in the malaria vector Anopheles gambiae

Assogba

Alout

Koffi

et al. 2018

Evolutionary Applications

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While gene copy‐number variations play major roles in long‐term evolution, their early dynamics remains largely unknown. However, examples of their role in short‐term adaptation are accumulating: identical repetitions of a locus (homogeneous duplications) can provide a quantitative advantage, while the association of differing alleles (heterogeneous duplications) allows carrying two functions simultaneously. Such duplications often result from rearrangements of sometimes relatively large chromosome fragments, and even when adaptive, they can be associated with deleterious side effects that should, however, be reduced by subsequent evolution. Here, we took advantage of the unique model provided by the malaria mosquito Anopheles gambiae s.l. to investigate the early evolution of several duplications, heterogeneous and homogeneous, segregating in natural populations from West Africa. These duplications encompass ~200 kb and 11 genes, including the adaptive insecticide resistance ace‐1 locus. Through the survey of several populations from three countries over 3–4 years, we showed that an internal deletion of all coamplified genes except ace‐1 is currently spreading in West Africa and introgressing from An. gambiae s.s. to An. coluzzii. Both observations provide evidences of its selection, most likely due to reducing the gene‐dosage disturbances caused by the excessive copies of the nonadaptive genes. Our study thus provides a unique example of the early adaptive trajectory of duplications and underlines the role of the environmental conditions (insecticide treatment practices and species ecology). It also emphasizes the striking diversity of adaptive responses in these mosquitoes and reveals a worrisome process of resistance/cost trade‐off evolution that could impact the control of malaria vectors in Africa.

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Heterosis and the Evolution of Duplications

Cited by 106 publications

References 21 publications

The Resolution of Sexual Antagonism by Gene Duplication

The Resolution of Sexual Antagonism by Gene Duplication

The early stages of duplicate gene evolution

Adaptive deletion in resistance gene duplications in the malaria vector Anopheles gambiae

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