Effective population size does not predict codon usage bias in mammals

Kessler, Michael; Dean, Matthew D.

doi:10.1002/ece3.1249

Cited by 18 publications

(18 citation statements)

References 151 publications

(184 reference statements)

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“…However, the two intermediate taxa do not follow the predictions of weak selection. Thus, there is no consistent relationship between inferred effective population size and codon usage bias estimated from our exomes, as observed by Kessler and Dean (2014).…”

Section: Resultscontrasting

confidence: 51%

“…2). Natural selection shapes codon usage bias across mammals, but shows no consistent correlation to proxies of effective population size (Kessler and Dean 2014). The effective population sizes of M. m. castaneus , M. m. domesticus , and M. m. musculus have been genetically estimated at 220K, 100K, and 60K, respectively (Geraldes et al 2008; Geraldes et al 2011; Phifer-Rixey et al 2012).…”

Section: Resultsmentioning

confidence: 99%

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Whole exome sequencing of wild-derived inbred strains of mice improves power to link phenotype and genotype

et al. 2017

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The house mouse is a powerful model to dissect the genetic basis of phenotypic variation, and serves as a model to study human diseases. Despite a wealth of discoveries, most classical laboratory strains have captured only a small fraction of genetic variation known to segregate in their wild progenitors, and existing strains are often related to each other. Inbred strains of mice independently derived from natural populations have the potential to increase power in genetic studies with the addition of novel genetic variation. Here, we perform exome-enrichment and high-throughput sequencing (~8X coverage) of 26 wild-derived strains known in the mouse research community as the “Montpellier strains”. We identified 1.46 million SNPs in our dataset, approximately 19% of which have not been detected from other inbred strains. This novel genetic variation is expected to contribute to phenotypic variation, as they include 18,496 nonsynonymous variants and 262 early stop codons. Simulations demonstrate that the higher density of genetic variation in the Montpellier strains provides increased power for quantitative genetic studies. Inasmuch as the power to connect genotype to phenotype depends on genetic variation, it is important to incorporate these additional genetic strains into future research programs.

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Section: Resultscontrasting

confidence: 51%

Section: Resultsmentioning

confidence: 99%

Whole exome sequencing of wild-derived inbred strains of mice improves power to link phenotype and genotype

et al. 2017

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“…In contrast, the ENC is independent of adult vertebrate body mass, consistent with past reports that effective population size does not predict codon usage in mammals (Figure 2C) (Kessler and Dean 2014). Note that a high ENC value means more codons are being used in the genome of the given species, so that the given species is less codon adapted, while a high CAIS value means that a species is more codon adapted.…”

Section: Resultssupporting

confidence: 91%

The protein domains of vertebrate species in which selection is more effective have greater intrinsic structural disorder

Weibel

James

Willis

et al. 2020

Preprint

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The effectiveness of selection varies among species. It is often estimated by means of an 'effective population size' based on neutral polymorphism, but this is confounded in complex ways with demography. The strength of codon bias more directly pertains to how well adaptation at many sites can be maintained in the face of deleterious mutations, but past metrics that compare codon bias across species are confounded by among-species variation in %GC content and/or amino acid composition. Here we propose a new Codon Adaptation Index of Species (CAIS) that corrects for both confounders. Unlike previous metrics, CAIS yields the expected relationship with adult vertebrate body mass. As an example of the use of CAIS, we ask whether protein domains evolve lower intrinsic structural disorder (ISD) when present in more exquisitely adapted species, as expected given that ISD is higher in eukaryotic proteomes than prokaryotic proteomes. Using phylogenetically corrected linear models, we find, contrary to expectations, that the ISD of a given protein domain evolves to be higher when in well-adapted species. This effect is stronger in young protein domains but is also present in ancient domains.

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“…For example, the X chromosome shows stronger codon usage bias in Drosophila (Singh et al 2005), which in turn may inflate X-linked estimates of v (Campos et al 2013). There is also weak codon usage bias in mice, but unlike Drosophila, it is significantly weaker on the X chromosome (Kessler and Dean 2014) and therefore conservative with respect to the observation of faster-X protein evolution. Further, both lower mutation rates and shallower coalescent times likely contribute to less nucleotide divergence on the mouse X chromosome (Table S2), making the observation of higher X-linked d N conservative.…”

Section: Protein Evolution and Spermatogenesismentioning

confidence: 99%

Contrasting Levels of Molecular Evolution on the Mouse X Chromosome

et al. 2016

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The mammalian X chromosome has unusual evolutionary dynamics compared to autosomes. Faster-X evolution of spermatogenic protein-coding genes is known to be most pronounced for genes expressed late in spermatogenesis, but it is unclear if these patterns extend to other forms of molecular divergence. We tested for faster-X evolution in mice spanning three different forms of molecular evolution-divergence in protein sequence, gene expression, and DNA methylation-across different developmental stages of spermatogenesis. We used FACS to isolate individual cell populations and then generated cell-specific transcriptome profiles across different stages of spermatogenesis in two subspecies of house mice (Mus musculus), thereby overcoming a fundamental limitation of previous studies on whole tissues. We found faster-X protein evolution at all stages of spermatogenesis and faster-late protein evolution for both X-linked and autosomal genes. In contrast, there was less expression divergence late in spermatogenesis (slower late) on the X chromosome and for autosomal genes expressed primarily in testis (testis-biased). We argue that slower-late expression divergence reflects strong regulatory constraints imposed during this critical stage of sperm development and that these constraints are particularly acute on the tightly regulated sex chromosomes. We also found slower-X DNA methylation divergence based on genome-wide bisulfite sequencing of sperm from two species of mice (M. musculus and M. spretus), although it is unclear whether slower-X DNA methylation reflects development constraints in sperm or other X-linked phenomena. Our study clarifies key differences in patterns of regulatory and protein evolution across spermatogenesis that are likely to have important consequences for mammalian sex chromosome evolution, male fertility, and speciation.KEYWORDS faster X evolution; gene expression; DNA methylation; fluorescence-activated cell sorting; postmeiotic sex chromosome repression (PSCR) T HE X chromosome plays a disproportionately large role in adaptation and speciation (Bachtrog et al. 2011;Ellegren 2011;Charlesworth 2013), but the underlying molecular and evolutionary drivers of these patterns remain unclear. On one hand, the X chromosome often shows strong signatures of evolutionary constraint. For example, the evolution of dosage compensation via epigenetic X-chromosome inactivation (XCI) in females (Lyon 1961(Lyon , 1962 imposes regulatory constraints that select for strong conservation of X-linked gene content in placental mammals (Ohno 1967;Kohn et al. 2004). On the other hand, these inherent constraints are punctuated by strong specialization in X-linked gene content (Emerson et al. 2004;Mueller et al. 2008Mueller et al. , 2013Potrzebowski et al. 2008;Zhang et al. 2010;Sin et al. 2012) and numerous examples of rapid X-linked evolution Singh 2003, 2006;Baines and Harr 2007;Kousathanas et al. 2014;Nam et al. 2015).The X chromosome is predicted to evolve faster than the autosomes if beneficial mutations...

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Effective population size does not predict codon usage bias in mammals

Cited by 18 publications

References 151 publications

Whole exome sequencing of wild-derived inbred strains of mice improves power to link phenotype and genotype

Whole exome sequencing of wild-derived inbred strains of mice improves power to link phenotype and genotype

The protein domains of vertebrate species in which selection is more effective have greater intrinsic structural disorder

Contrasting Levels of Molecular Evolution on the Mouse X Chromosome

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