Experimental mutation-accumulation on the X chromosome of Drosophila melanogaster reveals stronger selection on males than females

Mallet, Martin A.; Bouchard, Jessica M; Kimber, Christopher M; Chippindale, Adam K.

doi:10.1186/1471-2148-11-156

Cited by 70 publications

(100 citation statements)

References 48 publications

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“…For lifespan, the picture is complicated by the fact that autosomal variation is larger in males. Why males show more variation than females in general is not obvious, but could be related to deleterious mutations having a generally larger effect on fitness in males (Mallet et al 2011; Sharp and Agrawal 2013), and thus generate more variation in this sex. If this effect carries over to traits closely connected to fitness, such as lifespan, this could potentially generate more variation for lifespan in males than females ( e.g.…”

Section: Discussionmentioning

confidence: 99%

Autosomal and X-Linked Additive Genetic Variation for Lifespan and Aging: Comparisons Within and Between the Sexes in Drosophila melanogaster

Griffin

Schielzeth

Friberg

2016

G3 Genes|Genomes|Genetics

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Theory makes several predictions concerning differences in genetic variation between the X chromosome and the autosomes due to male X hemizygosity. The X chromosome should: (i) typically show relatively less standing genetic variation than the autosomes, (ii) exhibit more variation in males compared to females because of dosage compensation, and (iii) potentially be enriched with sex-specific genetic variation. Here, we address each of these predictions for lifespan and aging in Drosophila melanogaster. To achieve unbiased estimates of X and autosomal additive genetic variance, we use 80 chromosome substitution lines; 40 for the X chromosome and 40 combining the two major autosomes, which we assay for sex-specific and cross-sex genetic (co)variation. We find significant X and autosomal additive genetic variance for both traits in both sexes (with reservation for X-linked variation of aging in females), but no conclusive evidence for depletion of X-linked variation (measured through females). Males display more X-linked variation for lifespan than females, but it is unclear if this is due to dosage compensation since also autosomal variation is larger in males. Finally, our results suggest that the X chromosome is enriched for sex-specific genetic variation in lifespan but results were less conclusive for aging overall. Collectively, these results suggest that the X chromosome has reduced capacity to respond to sexually concordant selection on lifespan from standing genetic variation, while its ability to respond to sexually antagonistic selection may be augmented.

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Section: Discussionmentioning

confidence: 99%

Autosomal and X-Linked Additive Genetic Variation for Lifespan and Aging: Comparisons Within and Between the Sexes in Drosophila melanogaster

Griffin

Schielzeth

Friberg

2016

G3 Genes|Genomes|Genetics

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“…Unfortunately, the results for detrimental mutations have been rather discordant, even for D. melanogaster (Halligan and Keightley 2009;Mallet et al 2011Mallet et al , 2012. Overall, there is evidence in this species for a detectable DM for fitness (equal to Us ) of 1-2%.…”

Section: The Properties Of Deleterious Mutationsmentioning

confidence: 97%

The Effects of Deleterious Mutations on Evolution at Linked Sites

2012

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The process of evolution at a given site in the genome can be influenced by the action of selection at other sites, especially when these are closely linked to it. Such selection reduces the effective population size experienced by the site in question (the HillRobertson effect), reducing the level of variability and the efficacy of selection. In particular, deleterious variants are continually being produced by mutation and then eliminated by selection at sites throughout the genome. The resulting reduction in variability at linked neutral or nearly neutral sites can be predicted from the theory of background selection, which assumes that deleterious mutations have such large effects that their behavior in the population is effectively deterministic. More weakly selected mutations can accumulate by Muller's ratchet after a shutdown of recombination, as in an evolving Y chromosome. Many functionally significant sites are probably so weakly selected that Hill-Robertson interference undermines the effective strength of selection upon them, when recombination is rare or absent. This leads to large departures from deterministic equilibrium and smaller effects on linked neutral sites than under background selection or Muller's ratchet. Evidence is discussed that is consistent with the action of these processes in shaping genome-wide patterns of variation and evolution. MUTATIONS that increase the fitness of their carriers are, of course, the basis of adaptive evolution. For this reason, the literature on evolutionary genetics is full of studies that document "positive" selection on genetic variants in natural populations-with the advent of data on the resequencing of numerous whole genomes from the same species, we can expect a tidal wave of such examples. But, as was pointed out long ago by geneticists such as TimofeeffRessovsky (1940) and Muller (1949Muller ( , 1950, most mutations that affect the phenotype must be deleterious, because biological machinery has been subject to billions of years of selection to improve its performance. Because the nucleotide sites at which deleterious mutations can arise are numerous and distributed throughout the genome, the constant mutational production of deleterious variants and their elimination by "purifying" selection have major effects on the mean fitness of a population, its level of inbreeding depression, and its genetic variability with respect to fitness components.These properties of populations have important consequences for the evolution of such fundamental features of organisms as sex and genetic recombination, diploidy vs. haploidy, outbreeding vs. inbreeding, mate choice, and aging. Jim Crow, a great admirer of Muller (Crow 2005), has devoted much of his career both to improving our theoretical understanding of the population consequences of deleterious mutations and to documenting their rates of occurrence and their effects on fitness, summed up in several masterly reviews (Crow 1970(Crow , 1993(Crow , 2000Simmons and Crow 1977;Crow and Simmons 1983). T...

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“…Within this framework, numerous studies have tested the efficacy of sexual selection in aiding adaptation by modifying the strength of sexual selection to study evolutionary responses from standing genetic variation (e.g., Holland and Rice 1999;Holland 2002;Martin and Hosken 2003;Rundle et al 2006;Fricke and Arnqvist 2007;Morrow et al 2008;Jarzebowska and Radwan 2010;Maklakov et al 2010;Plesnar-Bielak et al 2012;Chenoweth et al 2015;Lumley et al 2015) or purging naturally accumulated (e.g., Radwan et al 2004;Rundle et al 2006;Mallet et al 2011;McGuigan et al 2011;Sharp and Agrawal 2013) or artificially induced/introduced deleterious mutations (e.g., Radwan 2004;Sharp and Agrawal 2008;Hollis and Houle 2011;Plesnar et al 2011;Arbuthnott and Rundle 2012;Clark et al 2012;Almbro and Simmons 2013;Power and Holman 2015;Grieshop et al 2016). The results of these studies have been inconsistent, which allows several insights.…”

Section: Introductionmentioning

confidence: 99%

Intralocus Sexual Conflict and the Tragedy of the Commons in Seed Beetles

Berger

Martinossi‐Allibert

Grieshop

et al. 2016

The American Naturalist

128

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Online enhancements: appendixes, supplemental PDF. Dryad data: http://dx.doi.org/10.5061/dryad.bc94c.abstract: The evolution of male traits that inflict direct harm on females during mating interactions can result in a so-called tragedy of the commons, where selfish male strategies depress population viability. This tragedy of the commons can be magnified by intralocus sexual conflict (IaSC) whenever alleles that reduce fecundity when expressed in females spread in the population because of their benefits in males. We evaluated this prediction by detailed phenotyping of 73 isofemale lines of the seed beetle Callosobruchus maculatus. We quantified genetic variation in life history and morphology, as well as associated covariance in male and female adult reproductive success. In parallel, we created replicated artificial populations of each line and measured their productivity. Genetic constraints limited independent trait expression in the sexes, and we identified several instances of sexually antagonistic covariance between traits and fitness, signifying IaSC. Population productivity was strongly positively correlated to female adult reproductive success but uncorrelated with male reproductive success. Moreover, male (female) phenotypic optima for several traits under sexually antagonistic selection were exhibited by the genotypes with the lowest (highest) population productivity. Our study forms a direct link between individuallevel sex-specific selection and population demography and places lifehistory traits at the epicenter of these dynamics.

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Experimental mutation-accumulation on the X chromosome of Drosophila melanogaster reveals stronger selection on males than females

Cited by 70 publications

References 48 publications

Autosomal and X-Linked Additive Genetic Variation for Lifespan and Aging: Comparisons Within and Between the Sexes in Drosophila melanogaster

Autosomal and X-Linked Additive Genetic Variation for Lifespan and Aging: Comparisons Within and Between the Sexes in Drosophila melanogaster

The Effects of Deleterious Mutations on Evolution at Linked Sites

Intralocus Sexual Conflict and the Tragedy of the Commons in Seed Beetles

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