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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.


Variance in male reproductive success and the evolution of dosage compensation.Stochastic evolutionary trajectories of male (blue) and female (red) expression for (a) Z-linked and (b) X-linked genes (see equations (11) and (12) for dynamics). Levels of expression are shown for low (η=1, light shade), intermediate (η=3, intermediate shade) or high (η=10, dark shade) degrees of male reproductive variance (the number of successful breeding females is set at 1,000). A sample of 5 trajectories is shown for each parameter value. Variance in heterogametic sex expression for (c) Z-linked and (d) X-linked genes after the end of the simulation is shown as a frequency distribution for 1,000 replicates. Selection is stronger on males than on females (Sm=1, Sf=0.2), inter-sexual correlation is relatively strong (ρ=0.6) and the mutation rate is μ=0.0003.
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f2: Variance in male reproductive success and the evolution of dosage compensation.Stochastic evolutionary trajectories of male (blue) and female (red) expression for (a) Z-linked and (b) X-linked genes (see equations (11) and (12) for dynamics). Levels of expression are shown for low (η=1, light shade), intermediate (η=3, intermediate shade) or high (η=10, dark shade) degrees of male reproductive variance (the number of successful breeding females is set at 1,000). A sample of 5 trajectories is shown for each parameter value. Variance in heterogametic sex expression for (c) Z-linked and (d) X-linked genes after the end of the simulation is shown as a frequency distribution for 1,000 replicates. Selection is stronger on males than on females (Sm=1, Sf=0.2), inter-sexual correlation is relatively strong (ρ=0.6) and the mutation rate is μ=0.0003.

Mentions: The evolutionary dynamics at Z- and X-linked genes also depend on the chromosomes' effective population sizes NeZ and NeX in equations (1)–(4), , , . Larger Ne results in faster evolution of dosage compensation, due to the more reliable fixation of positively selected mutations and elimination of negatively selected mutations (Fig. 2). With effective population size inversely proportional to the stochasticity in replicate evolutionary paths, small values of Ne not only slow down the evolution of dosage compensation but also result in more variable expression levels across replicate evolutionary trajectories. This effect is observed both during adaptation (Fig. 2), as well as at the evolutionary equilibrium (equation (15)).


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)

Variance in male reproductive success and the evolution of dosage compensation.Stochastic evolutionary trajectories of male (blue) and female (red) expression for (a) Z-linked and (b) X-linked genes (see equations (11) and (12) for dynamics). Levels of expression are shown for low (η=1, light shade), intermediate (η=3, intermediate shade) or high (η=10, dark shade) degrees of male reproductive variance (the number of successful breeding females is set at 1,000). A sample of 5 trajectories is shown for each parameter value. Variance in heterogametic sex expression for (c) Z-linked and (d) X-linked genes after the end of the simulation is shown as a frequency distribution for 1,000 replicates. Selection is stronger on males than on females (Sm=1, Sf=0.2), inter-sexual correlation is relatively strong (ρ=0.6) and the mutation rate is μ=0.0003.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f2: Variance in male reproductive success and the evolution of dosage compensation.Stochastic evolutionary trajectories of male (blue) and female (red) expression for (a) Z-linked and (b) X-linked genes (see equations (11) and (12) for dynamics). Levels of expression are shown for low (η=1, light shade), intermediate (η=3, intermediate shade) or high (η=10, dark shade) degrees of male reproductive variance (the number of successful breeding females is set at 1,000). A sample of 5 trajectories is shown for each parameter value. Variance in heterogametic sex expression for (c) Z-linked and (d) X-linked genes after the end of the simulation is shown as a frequency distribution for 1,000 replicates. Selection is stronger on males than on females (Sm=1, Sf=0.2), inter-sexual correlation is relatively strong (ρ=0.6) and the mutation rate is μ=0.0003.
Mentions: The evolutionary dynamics at Z- and X-linked genes also depend on the chromosomes' effective population sizes NeZ and NeX in equations (1)–(4), , , . Larger Ne results in faster evolution of dosage compensation, due to the more reliable fixation of positively selected mutations and elimination of negatively selected mutations (Fig. 2). With effective population size inversely proportional to the stochasticity in replicate evolutionary paths, small values of Ne not only slow down the evolution of dosage compensation but also result in more variable expression levels across replicate evolutionary trajectories. This effect is observed both during adaptation (Fig. 2), as well as at the evolutionary equilibrium (equation (15)).

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.