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Evolution of dosage compensation under sexual selection differs between X and Z chromosomes.

Mullon C, Wright AE, Reuter M, Pomiankowski A, Mank JE - Nat Commun (2015)

Bottom Line: Sexual conflict over expression is inevitable when mutation effects are correlated across the sexes, as compensatory mutations in the heterogametic sex lead to hyperexpression in the homogametic sex.Coupled with stronger selection and greater reproductive variance in males, this results in slower and less complete evolution of Z compared with X dosage compensation.Our study explains the pattern of weak dosage compensation in ZW systems, and suggests that sexual selection plays a major role in shaping sex chromosome dosage compensation.

View Article: PubMed Central - PubMed

Affiliation: 1] Department of Genetics, Evolution and Environment, University College London, Gower Street, London WC1E 6BT, UK [2] CoMPLEX, University College London, Gower Street, London WC1E 6BT, UK [3] Department of Ecology and Evolution, Biophore, University of Lausanne, Ch-1015 Lausanne, Switzerland.

ABSTRACT
Complete sex chromosome dosage compensation has more often been observed in XY than ZW species. In this study, using a population genetic model and the chicken transcriptome, we assess whether sexual conflict can account for this difference. Sexual conflict over expression is inevitable when mutation effects are correlated across the sexes, as compensatory mutations in the heterogametic sex lead to hyperexpression in the homogametic sex. Coupled with stronger selection and greater reproductive variance in males, this results in slower and less complete evolution of Z compared with X dosage compensation. Using expression variance as a measure of selection strength, we find that, as predicted by the model, dosage compensation in the chicken is most pronounced in genes that are under strong selection biased towards females. Our study explains the pattern of weak dosage compensation in ZW systems, and suggests that sexual selection plays a major role in shaping sex chromosome dosage compensation.

No MeSH data available.


The evolution of dosage compensation on Z and X chromosomes.Expected gene expression is shown for males (blue) and females (red) under a very low (ρ=0.1, dotted line), intermediate (ρ=0.5, dashed line) and strong inter-sexual correlation (ρ=0.8, solid line)—(see equations (13) and (14) for dynamics). a,b show equal selection in males and females (Sm=Sf=0.5); c,d show stronger selection in males (Sm=1, Sf=0.1). Evolutionary time refers to the number of generations, ignoring the time taken by successive mutations to fix. Expression is scaled according to the initial degradation z0 of expression in the heterogametic sex due to the loss of one gene copy, which here is set at z0=1. Other parameters were also held equal across the two sex chromosome systems (NeX=NeZ=1125, μ=0.0003).
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f1: The evolution of dosage compensation on Z and X chromosomes.Expected gene expression is shown for males (blue) and females (red) under a very low (ρ=0.1, dotted line), intermediate (ρ=0.5, dashed line) and strong inter-sexual correlation (ρ=0.8, solid line)—(see equations (13) and (14) for dynamics). a,b show equal selection in males and females (Sm=Sf=0.5); c,d show stronger selection in males (Sm=1, Sf=0.1). Evolutionary time refers to the number of generations, ignoring the time taken by successive mutations to fix. Expression is scaled according to the initial degradation z0 of expression in the heterogametic sex due to the loss of one gene copy, which here is set at z0=1. Other parameters were also held equal across the two sex chromosome systems (NeX=NeZ=1125, μ=0.0003).

Mentions: The speed with which dosage compensation evolves is dramatically reduced under the more plausible assumption that mutations have correlated effects across the sexes (ρ≠0). When mutational effects are positively correlated (ρ>0), mutations that increase expression and improve dosage compensation in the heterogametic sex are associated with antagonistic fitness effects in the other sex, as they raise expression in the homogametic sex above the fitness optimum. As the homogametic sex carries more chromosomal copies, antagonistic effects impede selection in favour of dosage compensation in the heterogametic sex. If selection is equal between males and females (Sm=Sf), the expectation is that dosage compensation will be slow to evolve both for Z- (Fig. 1a) and X-linked genes (Fig. 1b).


Evolution of dosage compensation under sexual selection differs between X and Z chromosomes.

Mullon C, Wright AE, Reuter M, Pomiankowski A, Mank JE - Nat Commun (2015)

The evolution of dosage compensation on Z and X chromosomes.Expected gene expression is shown for males (blue) and females (red) under a very low (ρ=0.1, dotted line), intermediate (ρ=0.5, dashed line) and strong inter-sexual correlation (ρ=0.8, solid line)—(see equations (13) and (14) for dynamics). a,b show equal selection in males and females (Sm=Sf=0.5); c,d show stronger selection in males (Sm=1, Sf=0.1). Evolutionary time refers to the number of generations, ignoring the time taken by successive mutations to fix. Expression is scaled according to the initial degradation z0 of expression in the heterogametic sex due to the loss of one gene copy, which here is set at z0=1. Other parameters were also held equal across the two sex chromosome systems (NeX=NeZ=1125, μ=0.0003).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4525201&req=5

f1: The evolution of dosage compensation on Z and X chromosomes.Expected gene expression is shown for males (blue) and females (red) under a very low (ρ=0.1, dotted line), intermediate (ρ=0.5, dashed line) and strong inter-sexual correlation (ρ=0.8, solid line)—(see equations (13) and (14) for dynamics). a,b show equal selection in males and females (Sm=Sf=0.5); c,d show stronger selection in males (Sm=1, Sf=0.1). Evolutionary time refers to the number of generations, ignoring the time taken by successive mutations to fix. Expression is scaled according to the initial degradation z0 of expression in the heterogametic sex due to the loss of one gene copy, which here is set at z0=1. Other parameters were also held equal across the two sex chromosome systems (NeX=NeZ=1125, μ=0.0003).
Mentions: The speed with which dosage compensation evolves is dramatically reduced under the more plausible assumption that mutations have correlated effects across the sexes (ρ≠0). When mutational effects are positively correlated (ρ>0), mutations that increase expression and improve dosage compensation in the heterogametic sex are associated with antagonistic fitness effects in the other sex, as they raise expression in the homogametic sex above the fitness optimum. As the homogametic sex carries more chromosomal copies, antagonistic effects impede selection in favour of dosage compensation in the heterogametic sex. If selection is equal between males and females (Sm=Sf), the expectation is that dosage compensation will be slow to evolve both for Z- (Fig. 1a) and X-linked genes (Fig. 1b).

Bottom Line: Sexual conflict over expression is inevitable when mutation effects are correlated across the sexes, as compensatory mutations in the heterogametic sex lead to hyperexpression in the homogametic sex.Coupled with stronger selection and greater reproductive variance in males, this results in slower and less complete evolution of Z compared with X dosage compensation.Our study explains the pattern of weak dosage compensation in ZW systems, and suggests that sexual selection plays a major role in shaping sex chromosome dosage compensation.

View Article: PubMed Central - PubMed

Affiliation: 1] Department of Genetics, Evolution and Environment, University College London, Gower Street, London WC1E 6BT, UK [2] CoMPLEX, University College London, Gower Street, London WC1E 6BT, UK [3] Department of Ecology and Evolution, Biophore, University of Lausanne, Ch-1015 Lausanne, Switzerland.

ABSTRACT
Complete sex chromosome dosage compensation has more often been observed in XY than ZW species. In this study, using a population genetic model and the chicken transcriptome, we assess whether sexual conflict can account for this difference. Sexual conflict over expression is inevitable when mutation effects are correlated across the sexes, as compensatory mutations in the heterogametic sex lead to hyperexpression in the homogametic sex. Coupled with stronger selection and greater reproductive variance in males, this results in slower and less complete evolution of Z compared with X dosage compensation. Using expression variance as a measure of selection strength, we find that, as predicted by the model, dosage compensation in the chicken is most pronounced in genes that are under strong selection biased towards females. Our study explains the pattern of weak dosage compensation in ZW systems, and suggests that sexual selection plays a major role in shaping sex chromosome dosage compensation.

No MeSH data available.