Pleiotropic Constraint Hampers the Resolution of Sexual Antagonism in Vertebrate Gene Expression

Mank, Judith E.; Hultin‐Rosenberg, Lina; Zwahlén, Martin; Ellegren, Hans

doi:10.1086/523954

Cited by 156 publications

(231 citation statements)

References 47 publications

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“…This observation agrees with a previous observation that malerelated genes on the X have significantly lower rates of protein evolution compared to those on the autosomes (Cutter and Ward 2005). Lower conservation of female-biased genes on the X chromosome (with respect to both chromosomal location and copy number) may be due to greater functional pleiotropy of female-biased genes compared to male-biased genes Mank et al 2008b;Mank and Ellegren 2009;Meiklejohn and Presgraves 2012). If an X-linked femalebiased gene has a non-sex-biased role in many different tissues, there may be pressure to undergo gene duplication to allow one copy to carry out the sex-biased function and the other the pleiotropic functions (Maciejowski et al 2005).…”

Section: Conservation Of Chromosomal Location and Sex Bias Of One-to-supporting

confidence: 92%

Sex-Biased Gene Expression and Evolution of the X Chromosome in Nematodes

et al. 2014

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Studies of X chromosome evolution in various organisms have indicated that sex-biased genes are nonrandomly distributed between the X and autosomes. Here, to extend these studies to nematodes, we annotated and analyzed X chromosome gene content in four Caenorhabditis species and in Pristionchus pacificus. Our gene expression analyses comparing young adult male and female mRNAseq data indicate that, in general, nematode X chromosomes are enriched for genes with high female-biased expression and depleted of genes with high male-biased expression. Genes with low sex-biased expression do not show the same trend of X chromosome enrichment and depletion. Combined with the observation that highly sex-biased genes are primarily expressed in the gonad, differential distribution of sex-biased genes reflects differences in evolutionary pressures linked to tissue-specific regulation of X chromosome transcription. Our data also indicate that X dosage imbalance between males (XO) and females (XX) is influential in shaping both expression and gene content of the X chromosome. Predicted upregulation of the single male X to match autosomal transcription (Ohno's hypothesis) is supported by our observation that overall transcript levels from the X and autosomes are similar for highly expressed genes. However, comparison of differentially located one-to-one orthologs between C. elegans and P. pacificus indicates lower expression of X-linked orthologs, arguing against X upregulation. These contradicting observations may be reconciled if X upregulation is not a global mechanism but instead acts locally on a subset of tissues and X-linked genes that are dosage sensitive. IN an XY sex-determination system, male and female genomes are identical with the exception of the male-specific Y chromosome, which bears few genes (Charlesworth et al. 2005). This is particularly true when the Y chromosome is thought to be completely lost, as is the case for C. elegans and many other nematodes (Walton 1940). Because gene content is the same, phenotypic differences between males and females, termed "sexual dimorphisms," must be caused by differential gene expression between the two sexes (Connallon and Knowles 2005;Ellegren and Parsch 2007). Throughout the article, such differentially expressed genes are referred to as "sex biased." As males and females have different fitness optima, a trait that is beneficial to one sex can be harmful to the other (termed sexual antagonism) (Rice and Chippindale 2001;Arnqvist 2004;Connallon and Knowles 2005;Ellegren and Parsch 2007;Mank et al. 2008a;Rice 1984). The evolution of sex-biased gene expression is thought to mediate the effects of sexual antagonism and allow for achievement of sex-specific fitness. Previous studies have indicated that anywhere between 30 and 60% of metazoan genes may be sex biased Parisi et al. 2004;Reinke et al. 2004;Yang et al. 2006;Reinius et al. 2008;Small et al. 2009;Innocenti and Morrow 2010;Assis et al. 2012;Reinius et al. 2012;Thomas et al. 2012). Genes with sex-biased exp...

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Section: Conservation Of Chromosomal Location and Sex Bias Of One-to-supporting

confidence: 92%

Sex-Biased Gene Expression and Evolution of the X Chromosome in Nematodes

et al. 2014

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“…For instance, pleiotropy would tend to obscure the relationship betweensex linkage and antagonist sexual selection (Fitzpatrick, 2004) usually going on when sexual selection on an ornament in one sex is stronger than natural selection acting against it in the other sex (Mank et al, 2008). Although not common in birds (O'Neill et al, 2000), genetic mechanisms as genomic imprinting for sex traits could be at work in the chromosomes of Ficedula flycatchers.…”

Section: Discussionmentioning

confidence: 99%

Heritability and genetic correlation between the sexes in a songbird sexual ornament

Potti

Cañal

2010

Heredity

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The genetic correlation between the sexes in the expression of secondary sex traits in wild vertebrate populations has attracted very few previous empirical efforts of field researchers. In southern European populations of pied flycatchers, a sexually selected male ornament is also expressed by a proportion of females. Additive genetic variances in ornament size and expression, transmission mechanisms (autosomal vs Z-linkage) and maternal effects are examined by looking at patterns of familial resemblance across three generations. Size of the secondary sex trait has a genetic basis common to both sexes, with estimated heritability being 0.5 under an autosomal model of inheritance. Significant additive genetic variance in males was also confirmed through a crossfostering experiment. Heritability analyses were only partially consistent with previous molecular genetics evidence, as only two out of the three predictions supported Z-linkage and lack of significant mother-daughter resemblance could be due to small sample sizes caused by limited female trait expression. Therefore, the evidence was mixed as to the contribution of the Z chromosome and autosomal genes to trait size. The threshold heritability of trait expression in females was lower, around 0.3, supporting autosomal-based trait expression in females. Environmental (birth date) and parental effects on ornament size mediated by the mother's condition after accounting for maternal and paternal genetic influences are also highlighted. The genetic correlation between the sexes did not differ from one, indicating that selection on the character on either sex entails a correlated response in the opposite sex.

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“…A growing body of evidence suggests that loci with SA alleles exist in the genomes of various organisms (reviewed by Mank et al 2008;Bonduriansky and Chenoweth 2009;Delcourt et al 2009;Stulp et al 2012). However, the only known SA polymorphisms are in fish, where male characters involved in attractiveness to females increase predation risk.…”

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confidence: 99%

Testing for the Footprint of Sexually Antagonistic Polymorphisms in the Pseudoautosomal Region of a Plant Sex Chromosome Pair

Qiu¹,

Bergero²,

Charlesworth

2013

Genetics

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The existence of sexually antagonistic (SA) polymorphism is widely considered the most likely explanation for the evolution of suppressed recombination of sex chromosome pairs. This explanation is largely untested empirically, and no such polymorphisms have been identified, other than in fish, where no evidence directly implicates these genes in events causing loss of recombination. We tested for the presence of loci with SA polymorphism in the plant Silene latifolia, which is dioecious (with separate male and female individuals) and has a pair of highly heteromorphic sex chromosomes, with XY males. Suppressed recombination between much of the Y and X sex chromosomes evolved in several steps, and the results in Bergero et al. (2013) show that it is still ongoing in the recombining or pseudoautosomal, regions (PARs) of these chromosomes. We used molecular evolutionary approaches to test for the footprints of SA polymorphisms, based on sequence diversity levels in S. latifolia PAR genes identified by genetic mapping. Nucleotide diversity is high for at least four of six PAR genes identified, and our data suggest the existence of polymorphisms maintained by balancing selection in this genome region, since molecular evolutionary (HKA) tests exclude an elevated mutation rate, and other tests also suggest balancing selection. The presence of sexually antagonistic alleles at a locus or loci in the PAR is suggested by the very different X and Y chromosome allele frequencies for at least one PAR gene.

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Pleiotropic Constraint Hampers the Resolution of Sexual Antagonism in Vertebrate Gene Expression

Cited by 156 publications

References 47 publications

Sex-Biased Gene Expression and Evolution of the X Chromosome in Nematodes

Sex-Biased Gene Expression and Evolution of the X Chromosome in Nematodes

Heritability and genetic correlation between the sexes in a songbird sexual ornament

Testing for the Footprint of Sexually Antagonistic Polymorphisms in the Pseudoautosomal Region of a Plant Sex Chromosome Pair

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