Divergent Evolution of Duplicate Genes Leads to Genetic Incompatibilities Within
            <i>A. thaliana</i>

Bikard, David; Patel, Dhaval; Metté, Claire Le; Giorgi, Veronica; Camilleri, Christine; Bennett, Malcolm J.; Loudet, Olivier

doi:10.1126/science.1165917

Cited by 264 publications

(269 citation statements)

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“…Such Dobzhansky -Muller incompatibilities are thought to arise 'incidental' to evolutionary processes, such as genetic drift or directional selection, but a detailed understanding of the ecological and evolutionary mechanisms involved remains elusive. Examples of incompatibilities that are polymorphic within species have been identified in Drosophila (Reed & Markow 2004;Brideau et al 2006), Caenorhabditis (Seidel et al 2008), Arabidopsis (Bomblies et al 2007;Bikard et al 2009) and Mimulus (several studies reviewed below), and these offer unique opportunities for investigating early stages in the evolution of postzygotic isolation, and may even elucidate why such incompatibilities initially arose.…”

Section: Introductionmentioning

confidence: 99%

Geographical variation in postzygotic isolation and its genetic basis within and between twoMimulusspecies

Martin

Willis

2010

Phil. Trans. R. Soc. B

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The aim of this study is to investigate the evolution of intrinsic postzygotic isolation within and between populations of Mimulus guttatus and Mimulus nasutus. We made 17 intraspecific and interspecific crosses, across a wide geographical scale. We examined the seed germination success and pollen fertility of reciprocal F 1 and F 2 hybrids and their pure-species parents, and used biometrical genetic tests to distinguish among alternative models of inheritance. Hybrid seed inviability was sporadic in both interspecific and intraspecific crosses. For several crosses, Dobzhansky -Muller incompatibilities involving nuclear genes were implicated, while two interspecific crosses revealed evidence of cytonuclear interactions. Reduced hybrid pollen fertility was found to be greatly influenced by Dobzhansky -Muller incompatibilities in five out of six intraspecific crosses and nine out of 11 interspecific crosses. Cytonuclear incompatibilities reduced hybrid fitness in only one intraspecific and one interspecific cross. This study suggests that intrinsic postzygotic isolation is common in hybrids between these Mimulus species, yet the particular hybrid incompatibilities responsible for effecting this isolation differ among the populations tested. Hence, we conclude that they evolve and spread only at the local scale.

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Section: Introductionmentioning

confidence: 99%

Geographical variation in postzygotic isolation and its genetic basis within and between twoMimulusspecies

Martin

Willis

2010

Phil. Trans. R. Soc. B

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“…Segregation distortion in A. thaliana: In addition to the association of the early flowering-time phenotype to MAF2 insertion alleles, we observed segregation distortion favoring the MAF2 insertion alleles in BC 5 F 2 segregating lines. Segregation distortion has been widely reported in A. thaliana (Loudet et al 2002;Bikard et al 2009) and other plant species (Lu et al 2002;Park et al 2005;Koide et al 2008). In A. thaliana, chimeric genes, as well as duplicated genes that undergo divergent evolution, have been shown to lead to genetic incompatibilities (Bomblies et al 2007;Alcazar et al 2009;Bikard et al 2009).…”

Section: Discussionmentioning

confidence: 99%

“…Segregation distortion has been widely reported in A. thaliana (Loudet et al 2002;Bikard et al 2009) and other plant species (Lu et al 2002;Park et al 2005;Koide et al 2008). In A. thaliana, chimeric genes, as well as duplicated genes that undergo divergent evolution, have been shown to lead to genetic incompatibilities (Bomblies et al 2007;Alcazar et al 2009;Bikard et al 2009). We have repeatedly observed that segregation distortion favors the MAF2 insertion allele in the progeny of a single, selffertilized BC 5 heterozygote.…”

Section: Discussionmentioning

confidence: 99%

Natural Diversity in Flowering Responses of Arabidopsis thaliana Caused by Variation in a Tandem Gene Array

et al. 2010

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Tandemly arrayed genes that belong to gene families characterize genomes of many organisms. Gene duplication and subsequent relaxation of selection can lead to the establishment of paralogous cluster members that may evolve along different trajectories. Here, we report on the structural variation in MADS AFFECTING FLOWERING 2 (MAF2) gene, one member of the tandemly duplicated cluster of MADS-boxcontaining transcription factors in Arabidopsis thaliana. The altered gene structure at the MAF2 locus is present as a moderate-frequency polymorphism in Arabidopsis and leads to the extensive diversity in transcript patterns due to alternative splicing. Rearrangements at the MAF2 locus are associated with an early flowering phenotype in BC 5 lines. The lack of suppression of flowering time in a MAF2-insertion line expressing the MAF2-specific artificial miRNA suggests that these MAF2 variants are behaving as loss-offunction alleles. The variation in gene architecture is also associated with segregation distortion, which may have facilitated the spread and the establishment of the corresponding alleles throughout the Eurasian range of the A. thaliana population.

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“…The detection and functional analysis of such intraspecific incompatibilities could provide fundamental insights into the mechanisms that drive postzygotic reproductive isolation in the wild and thus represent a useful model for understanding the molecular basis of speciation (Bomblies and Weigel 2007). In plants, the clearest examples of intraspecific genetic incompatibilities come from experimental crosses of Arabidopsis thaliana (e.g., Bikard et al 2009;Durand et al 2012;Chae et al 2014). Arguably the best-studied case is the work of Bikard et al (2009), who examined F 2 progeny of selfed hybrids derived from the Columbia (Col) and the Cape Verde (Cvi) accessions.…”

mentioning

confidence: 99%

“…In plants, the clearest examples of intraspecific genetic incompatibilities come from experimental crosses of Arabidopsis thaliana (e.g., Bikard et al 2009;Durand et al 2012;Chae et al 2014). Arguably the best-studied case is the work of Bikard et al (2009), who examined F 2 progeny of selfed hybrids derived from the Columbia (Col) and the Cape Verde (Cvi) accessions. The authors found that a subset of the F 2 's had severely compromised fitness and demonstrated that this fitness loss is caused by a genetic incompatibility involving a reciprocal loss of duplicate genes on chromosome (chr) 1 and chr 5 ( Figure 1A).…”

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confidence: 99%

Signatures of Dobzhansky–Muller Incompatibilities in the Genomes of Recombinant Inbred Lines

Colomé-Tatché

Johannes

2015

Genetics

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In the construction of recombinant inbred lines (RILs) from two divergent inbred parents certain genotype (or epigenotype) combinations may be functionally "incompatible" when brought together in the genomes of the progeny, thus resulting in sterility or lower fertility. Natural selection against these epistatic combinations during inbreeding can change haplotype frequencies and distort linkage disequilibrium (LD) relations between loci on the same or on different chromosomes. These LD distortions have received increased experimental attention, because they point to genomic regions that may drive a Dobzhansky-Muller type of reproductive isolation and, ultimately, speciation in the wild. Here we study the selection signatures of two-locus epistatic incompatibility models and quantify their impact on the genetic composition of the genomes of two-way RILs obtained by selfing. We also consider the biases introduced by breeders when trying to counteract the loss of lines by selectively propagating only viable seeds. Building on our theoretical results, we develop model-based maximum-likelihood (ML) tests that can be applied to multilocus RIL genotype data to infer the precise mode of incompatibility as well as the relative fitness of incompatible loci. We illustrate this ML approach in the context of two published Arabidopsis thaliana RIL panels. Our work lays the theoretical foundation for studying more complex systems such as RILs obtained by sibling mating and/or from multiparental crosses.KEYWORDS genetic incompatibility; RIL; long-range LD; selection; epistasis; recombination; complex traits; Dobzhansky-Muller; inbreeding H YBRIDS from crosses between two divergent parental lines sometimes display low fertility and phenotypic abnormalities (Presgraves 2010). These effects are often attributable to combinations of parental genotypes (or epigenotypes) at two or more loci that are functionally incompatible when brought together into a single genome. This form of negative epistasis was originally invoked by Dobzhansky (1937) and Muller (1942) as a model for speciation. In the classical Dobzhansky-Muller (DM) model, a population splits into two subpopulations that become reproductively isolated through geographic or temporal mechanisms (i.e., prezygotically). Once separated, the two subpopulations acquire independent mutations that are incompatible upon hybridization, thus resulting in sterility or reduced fertility among offspring. This process prevents further mixing and reinforces the existing (prezygotic) reproductive isolation genetically (i.e., postzygotically). Additional independent mutations accumulate over time, causing further divergence between subpopulations and ultimately speciation. Empirical examples of interspecific genetic incompatibilities are well documented in the literature (Presgraves 2010) and have motivated extensive theoretical work in evolutionary genetics (e.g., Nei et al. 1983;Orr and Orr 1996;Turelli and Orr 2000;Barton 2001;Orr and Turelli 2001;Turelli et al. 2001;Welch 2004;Fi...

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Divergent Evolution of Duplicate Genes Leads to Genetic Incompatibilities Within A. thaliana

Cited by 264 publications

References 32 publications

Geographical variation in postzygotic isolation and its genetic basis within and between twoMimulusspecies

Geographical variation in postzygotic isolation and its genetic basis within and between twoMimulusspecies

Natural Diversity in Flowering Responses of Arabidopsis thaliana Caused by Variation in a Tandem Gene Array

Signatures of Dobzhansky–Muller Incompatibilities in the Genomes of Recombinant Inbred Lines

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