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Sexually antagonistic "zygotic drive" of the sex chromosomes.

Rice WR, Gavrilets S, Friberg U - PLoS Genet. (2008)

Bottom Line: The phenomenon occurs because there is selection in the heterogametic sex for sex-linked mutations that harm the sex of offspring that does not carry them, whenever there is competition among siblings.This harmful phenotype can be expressed as an antagonistic green-beard effect that is mediated by epigenetic parental effects, parental investment, and/or interactions among siblings.A combination of mathematical modeling and a survey of empirical studies is used to show that sexually antagonistic zygotic drive is feasible, likely to be widespread in nature, and that it can promote a genetic "arms race" between the homo- and heteromorphic sex chromosomes.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology, Evolution, and Marine Biology, University of California Santa Barbara, Santa Barbara, CA, USA. rice@lifesci.ucsb.edu

ABSTRACT
Genomic conflict is perplexing because it causes the fitness of a species to decline rather than improve. Many diverse forms of genomic conflict have been identified, but this extant tally may be incomplete. Here, we show that the unusual characteristics of the sex chromosomes can, in principle, lead to a previously unappreciated form of sexual genomic conflict. The phenomenon occurs because there is selection in the heterogametic sex for sex-linked mutations that harm the sex of offspring that does not carry them, whenever there is competition among siblings. This harmful phenotype can be expressed as an antagonistic green-beard effect that is mediated by epigenetic parental effects, parental investment, and/or interactions among siblings. We call this form of genomic conflict sexually antagonistic "zygotic drive", because it is functionally equivalent to meiotic drive, except that it operates during the zygotic and postzygotic stages of the life cycle rather than the meiotic and gametic stages. A combination of mathematical modeling and a survey of empirical studies is used to show that sexually antagonistic zygotic drive is feasible, likely to be widespread in nature, and that it can promote a genetic "arms race" between the homo- and heteromorphic sex chromosomes. This new category of genomic conflict has the potential to strongly influence other fundamental evolutionary processes, such as speciation and the degeneration of the Y and W sex chromosomes. It also fosters a new genetic hypothesis for the evolution of enigmatic fitness-reducing traits like the high frequency of spontaneous abortion, sterility, and homosexuality observed in humans.

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Antagonistic coevolution between the X and Y leading to recurrent episodes of SA-zygotic drive.The autosomes will only evolve to block harmful phenotypes coded by the X and Y when SA-zygotic drive causes the average fitness of the brood to decline.
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pgen-1000313-g004: Antagonistic coevolution between the X and Y leading to recurrent episodes of SA-zygotic drive.The autosomes will only evolve to block harmful phenotypes coded by the X and Y when SA-zygotic drive causes the average fitness of the brood to decline.

Mentions: If a SA-GrBd-effect evolved that was coded by the Y and that favored sons at the expense of daughters, there would be counter-selection on the X to ameliorate this effect, and vice versa if a SA-GrBd-effect evolved that was coded by the X favoring daughters. Such selection and counter-selection could potentially lead to a genetic arms race (Figure 4) with the autosomes being selected to block X- and Y-coded antagonistic paternal effects only when the net fitness of the brood was reduced. Here we explore the fate of mutations located on the X and Y chromosome that code for i) paternal investment (PI) that is skewed toward the sex of offspring that carries them, ii) epigenetic paternal effects that interfere with the ontogeny of the sex of offspring that do not carry them (and thereby reduce their competitive ability during sibling competition), and iii) competitive sib-sib-interactions that reduce the competitive ability of the sex that does not carry them (by helping same sex siblings or harming opposite sex siblings).


Sexually antagonistic "zygotic drive" of the sex chromosomes.

Rice WR, Gavrilets S, Friberg U - PLoS Genet. (2008)

Antagonistic coevolution between the X and Y leading to recurrent episodes of SA-zygotic drive.The autosomes will only evolve to block harmful phenotypes coded by the X and Y when SA-zygotic drive causes the average fitness of the brood to decline.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2596966&req=5

pgen-1000313-g004: Antagonistic coevolution between the X and Y leading to recurrent episodes of SA-zygotic drive.The autosomes will only evolve to block harmful phenotypes coded by the X and Y when SA-zygotic drive causes the average fitness of the brood to decline.
Mentions: If a SA-GrBd-effect evolved that was coded by the Y and that favored sons at the expense of daughters, there would be counter-selection on the X to ameliorate this effect, and vice versa if a SA-GrBd-effect evolved that was coded by the X favoring daughters. Such selection and counter-selection could potentially lead to a genetic arms race (Figure 4) with the autosomes being selected to block X- and Y-coded antagonistic paternal effects only when the net fitness of the brood was reduced. Here we explore the fate of mutations located on the X and Y chromosome that code for i) paternal investment (PI) that is skewed toward the sex of offspring that carries them, ii) epigenetic paternal effects that interfere with the ontogeny of the sex of offspring that do not carry them (and thereby reduce their competitive ability during sibling competition), and iii) competitive sib-sib-interactions that reduce the competitive ability of the sex that does not carry them (by helping same sex siblings or harming opposite sex siblings).

Bottom Line: The phenomenon occurs because there is selection in the heterogametic sex for sex-linked mutations that harm the sex of offspring that does not carry them, whenever there is competition among siblings.This harmful phenotype can be expressed as an antagonistic green-beard effect that is mediated by epigenetic parental effects, parental investment, and/or interactions among siblings.A combination of mathematical modeling and a survey of empirical studies is used to show that sexually antagonistic zygotic drive is feasible, likely to be widespread in nature, and that it can promote a genetic "arms race" between the homo- and heteromorphic sex chromosomes.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology, Evolution, and Marine Biology, University of California Santa Barbara, Santa Barbara, CA, USA. rice@lifesci.ucsb.edu

ABSTRACT
Genomic conflict is perplexing because it causes the fitness of a species to decline rather than improve. Many diverse forms of genomic conflict have been identified, but this extant tally may be incomplete. Here, we show that the unusual characteristics of the sex chromosomes can, in principle, lead to a previously unappreciated form of sexual genomic conflict. The phenomenon occurs because there is selection in the heterogametic sex for sex-linked mutations that harm the sex of offspring that does not carry them, whenever there is competition among siblings. This harmful phenotype can be expressed as an antagonistic green-beard effect that is mediated by epigenetic parental effects, parental investment, and/or interactions among siblings. We call this form of genomic conflict sexually antagonistic "zygotic drive", because it is functionally equivalent to meiotic drive, except that it operates during the zygotic and postzygotic stages of the life cycle rather than the meiotic and gametic stages. A combination of mathematical modeling and a survey of empirical studies is used to show that sexually antagonistic zygotic drive is feasible, likely to be widespread in nature, and that it can promote a genetic "arms race" between the homo- and heteromorphic sex chromosomes. This new category of genomic conflict has the potential to strongly influence other fundamental evolutionary processes, such as speciation and the degeneration of the Y and W sex chromosomes. It also fosters a new genetic hypothesis for the evolution of enigmatic fitness-reducing traits like the high frequency of spontaneous abortion, sterility, and homosexuality observed in humans.

Show MeSH
Related in: MedlinePlus