The Importance of Genetic Redundancy in Evolution

Láruson, Áki J.; Yeaman, Sam; Lotterhos, Katie E.

doi:10.1016/j.tree.2020.04.009

Cited by 115 publications

(114 citation statements)

References 61 publications

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“…Driven by genetic drift and guided by selection, many GRNs that satisfied the same viability function were sorted into parallel lineages, whereas mixing edges between them can lead to fatal pathways and inviable offspring. These results highlight the importance of "functional redundancy" in evolution (Nowak et al, 1997;Láruson et al, 2020) and agree with earlier studies that suggested alternative regulatory structures can achieve the same phenotype (True and Haag, 2001;Wagner and Wright, 2007;Schiffman and Ralph, 2018;Tkačik and Walczak, 2011). Indeed, both theoretical and empirical studies increasingly support the role of parallel trajectories through fitness landscapes in evolution (Elmer and Meyer, 2011;Bank et al, 2016;Ogbunugafor and Eppstein, 2016;Langerhans, 2018).…”

Section: Discussionsupporting

confidence: 89%

“…Our pathway framework not only resonates with existing studies of the functional redundancy of GRNs (True and Haag, 2001;Wagner and Wright, 2007;Schiffman and Ralph, 2018;Láruson et al, 2020), but it also estimates how many GRNs generate a given phenotype under the Boolean-state assumption. Here we consider an extreme case where every protein is either required present or absent, except those that are stimulated by the environment.…”

Section: S2 Estimating Functional Redundancy Of Grns Under Extreme Sesupporting

confidence: 53%

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Reproductive barriers as a byproduct of gene network evolution

Yang

Scarpino

2020

Preprint

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Molecular analyses of closely related taxa have increasingly revealed the importance of 10 higher-order genetic interactions in explaining the observed pattern of reproductive isolation 11 between populations. Indeed, both empirical and theoretical studies have linked the process of 12 speciation to complex genetic interactions. Gene Regulatory Networks (GRNs) capture the 13 inter-dependencies of gene expression and encode information about an individual's phenotype 14 and development at the molecular level. As a result, GRNs can-in principle-evolve via natural 15 selection and play a role in non-selective, evolutionary forces. Here, we develop a network-based 16 model, termed the pathway framework, that considers GRNs as a functional representation of 17 coding sequences. We then simulated the dynamics of GRNs using a simple model that included 18 natural selection, genetic drift, and sexual reproduction and found that reproductive barriers can 19 develop rapidly between allopatric populations experiencing identical selection pressure. Further, 20 we show that alleles involved in reproductive isolation can predate the allopatric separation of 21 populations and that the number of interacting loci involved in genetic incompatibilities, i.e., the 22 order, is often high simply as a by-product of the networked structure of GRNs. Finally, we discuss 23 how results from the pathway framework are consistent with observed empirical patterns for 24 genes putatively involved in post-zygotic isolation. Taken together, this study adds support for the 25 central role of gene networks in speciation and in evolution more broadly. 26 27 31Through this work, it is widely accepted that divergent selection on de novo mutations in geo-32 graphically isolated populations can facilitate speciation, as originally theorized by (Bateson, 1909; 33 Dobzhansky, 1936; Muller, 1942). Despite well-established examples from Drosophila (Brideau34 et al., 2006), Xiphophorus (Wittbrodt et al., 1989; Powell et al., 2020), Oryza (Yamamoto et al., 35 2010), Arabidopsis (Bikard et al., 2009), and Mus (Davies et al., 2016), the genetics and evolutionary 36 history of incompatibilities are typically far more complex and/or less well understood than what 37 is suggested by classical models (Noor and Feder, 2006; Lowry et al., 2008; Presgraves, 2010; Wolf 38 et al., 2010; Nosil and Schluter, 2011; Seehausen et al., 2014; Marques et al., 2019; Dagilis and 39Matute, 2020). 40 Post-zygotic, genetic isolation is thought to occur due to epistatic interaction between loci, where 41 alleles arise and fix in allopatry prior to secondary contact, e.g., the Bateson-Dobzhansky-Muller 42 1 of 26 Manuscript submitted to eLife (BDM) model (Bateson, 1909; Dobzhansky, 1936; Muller, 1942). However, many incompatibilities 43 uncovered using high-throughput molecular analyses (Castillo and Barbash, 2017; Kuzmin et al., 44 2018; Vaid and Laitinen, 2019) and quantitative trait locus (QTL) mapping (Moyle and Nakazato, 45 2008; Turner et al., 2014; Ch...

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Section: Discussionsupporting

confidence: 89%

Section: S2 Estimating Functional Redundancy Of Grns Under Extreme Sesupporting

confidence: 53%

Reproductive barriers as a byproduct of gene network evolution

Yang

Scarpino

2020

Preprint

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“…In the case of plastic polygenic traits, the magnitude of response of individual genes may be relatively small and, therefore, not detectable via differential expression analysis. In the case of redundant genetic architecture, theory predicts that high genetic redundancy in a population occurs when individuals can reach a phenotypic outcome by a wide range of genes and pathways (see topic reviewed in Láruson et al, 2020) , which could result in very large residual error and limited statistical power to detect differences amongst treatment (i.e., lack of a clear significant response because every individual does something different to achieve the same phenotype).…”

Section: Subtle Shifts and Constraintsmentioning

confidence: 99%

Ocean acidification induces subtle shifts in gene expression and DNA methylation in mantle tissue of the Eastern oyster (Crassostrea virginica)

Downey-Wall

Cameron

Ford

et al. 2020

Preprint

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Word Count: 350 Manuscript Word Count: 15658 1 Abstract Early evidence suggests that DNA methylation can mediate phenotypic responses of marine calcifying species to ocean acidification (OA). Few studies, however, have explicitly studied DNA methylation in calcifying tissues through time. Here, we examined the phenotypic and molecular responses in the extrapallial fluid and mantle (fluid and tissue at the calcification site) in the Eastern oyster ( Crassostrea virginica ) exposed to experimental OA over 80 days. Oysters were reared under three experimental pCO 2 treatments ('control', 580 μatm; 'moderate OA', 1000 uatm; 'high OA', 2800 μatm) and sampled at 6 time points (24 hours -80 days). We found that high OA initially induced changes in the pH of the extrapallial fluid (pH EPF ) relative to the external seawater, but the magnitude of this difference was highest at 9 days and diminished over time. Calcification rates were significantly lower in the high OA treatment compared to the other treatments. To explore how oysters regulate their extrapallial fluid, gene expression and DNA methylation were examined in the mantle-edge tissue of oysters from day 9 and 80 in the control and high OA treatments. Mantle tissue mounted a significant global molecular response (both in the transcriptome and methylome) to OA that shifted through time. Although we did not find individual genes that were significantly differentially expressed to OA, the pH EPF was correlated with the eigengene expression of several co-expressed gene clusters. A small number of OA-induced differentially methylated loci were discovered, which corresponded with a weak association between OA-induced changes in genome-wide gene body DNA methylation and gene expression. Gene body methylation, however, was not significantly correlated with the eigengene expression of pH EPF correlated gene clusters. These results suggest that in C. virginica , OA induces a subtle response in a large number of genes, but also indicates that plasticity at the molecular level may be limited. Our study highlights the need to re-assess the plasticity of tissue-specific molecular responses in marine calcifiers , as well as the role of DNA methylation and gene expression in mediating physiological and biomineralization responses to OA.

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“…Theory suggests that the number of genotypes that, at a given time, segregate in a population and are phenotypically redundant, so called segregating redundancy, is a critical parameter governing both the predictability of evolution (18,19) and the consequences of locally heterogenous selection for maintaining different adaptive phenotypes (20). The level of segregating (genotypic) redundancy determines the intensity of selection on individual alleles.…”

Section: Introductionmentioning

confidence: 99%

“…Higher redundancy (several different genotypes can produce the same phenotype) makes it more difficult to either fix or eliminate individual alleles compared to situations where alternative phenotypes are determined by one or a few genotypes. Redundancy may also help maintain phenotypic differentiation in the face of high gene-flow, as several genotypes producing the same adapted phenotype can contribute to withstand swamping due to the immigration of divergent alleles (20).…”

Section: Introductionmentioning

confidence: 99%

From genotype to phenotype: maintenance of a chemical polymorphism in the context of high geneflow

Ehlers

Gauthier²,

Villesen

et al. 2020

Preprint

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A major question in evolution is how to maintain many adaptive phenotypes within a species. In Mediterranean wild thyme, a staggering number of discrete chemical phenotypes (chemotypes) coexist in close geographic proximity. Plant chemotypes are defined by the dominant monoterpene produced in their essential oil. We study the genetics of six distinct chemotypes nested within two well established ecotypes. Ecotypes, and chemotypes within ecotypes, are spatially segregated, and their distribution tracks local differences in the abiotic environment. The ecotypes have undergone a rapid shift in distribution associated with current climate change. Here, combining genomic, phenotypic, and environmental data, we show how the genetics of ecotype determination can allow for such rapid evolutionary response despite high gene flow among ecotypes. Variation in three terpene-synthase loci explains almost all variation in ecotype identity, with one single locus accounting for as much as 78% of it. Phenotypic selection on ecotypes combined with low segregating genotypic redundancy and tight genetic determination leaves a clear footprint at the genomic level: alleles associated with ecotype identity track environmental variation despite extensive gene flow. Different chemotypes, nested within each ecotype, also track environmental variation. However, in contrast to ecotypes, chemotype identity is determined by more loci and show a wider range of genotypic redundancy, which dilutes the impact of phenotypic selection on alleles associated with different chemotypes. Identifying the genetics behind this polymorphism in thyme is a crucial step towards understanding the maintenance of this widespread chemical polymorphism found in many aromatic Lamiaceae.

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The Importance of Genetic Redundancy in Evolution

Cited by 115 publications

References 61 publications

Reproductive barriers as a byproduct of gene network evolution

Reproductive barriers as a byproduct of gene network evolution

Ocean acidification induces subtle shifts in gene expression and DNA methylation in mantle tissue of the Eastern oyster (Crassostrea virginica)

From genotype to phenotype: maintenance of a chemical polymorphism in the context of high geneflow

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