Faster‐X evolution: Theory and evidence from <i>Drosophila</i>

Charlesworth, Brian; Campos, José Luis; Jackson, Benjamin C.

doi:10.1111/mec.14534

Cited by 105 publications

(154 citation statements)

References 167 publications

(337 reference statements)

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“…http://dx.doi.org/10.1101/358309 doi: bioRxiv preprint first posted online Jun. 29, 2018; In addition to the simulations of autosomes, we ran simulations that were intended to represent X chromosomal mutations with equal fitness effects in the two sexes, but with stronger selection than autosomal mutations, as is expected on both theoretical and empirical grounds (Charlesworth et al 2018). X-linked loci spend two-thirds of their time in females where they can recombine (Campos et al 2013), so that the effective rates of crossing over and initiation of gene conversion events for Xlinked loci should be 4/3 times the autosomal values for X-linked genes with similar parameter values in females to the autosomal ones.…”

Section: Methodsmentioning

confidence: 99%

“…All sites in UTRs were assumed to be subject to selection; 5´and 3´UTRs were assigned the same parameters, with most mutations being deleterious, with selective effective following a gamma DFE with shape parameter 0.3 and mean scaled selection coefficient γ UT = 110, as suggested by the population genomic estimates (Campos et al 2017 In addition to the simulations of autosomes, we ran simulations that were intended to represent X chromosomal mutations with equal fitness effects in the two sexes, but with stronger selection than autosomal mutations, as is expected on both theoretical and empirical grounds (Charlesworth et al 2018). X-linked loci spend two-thirds of their time in females where they can recombine (Campos et al 2013), so that the effective rates of crossing over and initiation of gene conversion events for Xlinked loci should be 4/3 times the autosomal values for X-linked genes with similar parameter values in females to the autosomal ones.…”

Section: Methodsmentioning

confidence: 99%

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The effects on neutral variability of recurrent selective sweeps and background selection

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Charlesworth

2018

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Levels of variability and rates of adaptive evolution can be affected by hitchhiking, the effect of selection on variants at linked sites. Hitchhiking can be caused either by selective sweeps or by background selection, involving the spread of new favorable alleles or the elimination of deleterious mutations, respectively. Recent analyses of population genomic data have fitted models where both these processes act simultaneously, in order to infer the parameters of selection. Here, we investigate the consequences of relaxing a key assumption of some of these studies -that neutral variability at a site affected by recurrent selective sweeps fully recovers between successive sweeps. We derive a simple expression for the expected level of neutral variability in the presence of recurrent selective sweeps and background selection.We also derive approximate integral expressions for the effects of recurrent selective sweeps on a given gene. The accuracy of the theoretical predictions was tested against multilocus simulations, using the software SLiM with selection, recombination and mutation parameters that are realistic for Drosophila melanogaster. We find good agreement between the simulation results and predictions from the integral approximations, except when rates of crossing over are close to zero. We show that the observed relations between the rate of crossing over and the level of synonymous site diversity and rate of adaptive evolution largely reflect background selection, whereas selective sweeps are needed to produce substantial distortions of the site frequency spectrum.All rights reserved. No reuse allowed without permission.(which was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.The copyright holder for this preprint . http://dx.doi.org/10.1101/358309 doi: bioRxiv preprint first posted online Jun. 29, 2018; 3 The effect of selection at a given locus on the properties of neutral variability at linked sites is a classic problem in population genetics, first studied by Sved (1968) and Ohta and Kimura (1970) in the context of associative overdominance -the apparent heterozygote advantage induced at a neutral locus by variants at linked loci, maintained by heterozygote advantage or by mutation to partially recessive deleterious alleles. This early work was followed by the classic paper of Maynard Smith and Haigh (1974) on the hitchhiking effect, whereby the spread of a favorable mutation reduces the level of neutral variability at a linked locus; this process has come to be termed a 'selective sweep ' (Berry et al. 1991). It was later shown that selection against recurrent deleterious mutations also reduces neutral variability at linked sites by a hitchhiking process, known as background selection (Charlesworth et al. 1993). The same basic equation that describes the effect of selection at one locus on the allele frequency at a linked neutral locus has recently been shown to underlie all three of these processes (Zhao and Charlewor...

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

The effects on neutral variability of recurrent selective sweeps and background selection

Parada

Charlesworth

2018

Preprint

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“…Under a secondary contact model, and assuming adaptation from new mutations, locally adaptive alleles can accumulate faster on the X chromosome than on autosomes during the allopatric divergence phase (Charlesworth et al., ). This faster‐X evolution occurs when the average dominance of newly arising beneficial mutations is sufficiently small: making the standard assumption that the ratio of effective population sizes for the X to that for the autosomes is N X / N A = 3/4, then faster‐X evolution will occur when

\overset{h}{true}

< 0.5 (Charlesworth et al., ); if N X / N A > 3/4, however, the conditions for faster‐X evolution are more permissive (

\overset{h}{true}

> 0.5; Charlesworth et al., ; Vicoso & Charlesworth, ). Adaptation from standing genetic variation, on the other hand, results in faster evolution at autosomal loci (Charlesworth et al., ; Connallon, Singh, & Clark, ; Orr & Betancourt, ).…”

Section: Sex Chromosome Differentiation With Selection and Gene Flowmentioning

confidence: 99%

Evaluating genomic signatures of “the large X‐effect” during complex speciation

2018

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The ubiquity of the "two rules of speciation"-Haldane's rule and the large X-effect-implies a general, special role for sex chromosomes in the evolution of intrinsic postzygotic reproductive isolation. The recent proliferation of genome-scale analyses has revealed two further general observations: (a) complex speciation involving some form of gene flow is not uncommon, and (b) sex chromosomes in male- and in female-heterogametic taxa tend to show elevated differentiation relative to autosomes. Together, these observations are consistent with speciation histories in which population genetic differentiation at autosomal loci is reduced by gene flow while natural selection against hybrid incompatibilities renders sex chromosomes relatively refractory to gene flow. Here, I summarize multilocus population genetic and population genomic evidence for greater differentiation on the X (or Z) vs. the autosomes and consider the possible causes. I review common population genetic circumstances involving no selection and/or no interspecific gene flow that are nevertheless expected to elevate differentiation on sex chromosomes relative to autosomes. I then review theory for why large X-effects exist for hybrid incompatibilities and, more generally, for loci mediating local adaptation. The observed levels of sex chromosome vs. autosomal differentiation, in many cases, appear consistent with simple explanations requiring neither large X-effects nor gene flow. Discerning signatures of large X-effects during complex speciation will therefore require analyses that go beyond chromosome-scale summaries of population genetic differentiation, explicitly test for differential introgression, and/or integrate experimental genetic data.

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“…Such movement could cause aneuploidy in species hybrids, leading to sterility or inviability that would often involve the X. Theories based on the faster evolution of genes on the X. These theories (see Charlesworth, Campos, & Jackson, ) are independent of gene action or gene density, positing that genes on the X (or Z) chromosome simply evolve faster than those on autosomes and that such evolution could cause both large X effects and Haldane's Rule as a by‐product. This can occur when advantageous alleles within a species—though not necessarily their effects on postzygotic isolation—are partly recessive.…”

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confidence: 99%