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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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Summary of how linkage to the sex chromosomes simplifies the requisite multifarious phenotype needed to produce a sexually antagonistic green-beard effects that fuel SA-zygotic drive.
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pgen-1000313-g002: Summary of how linkage to the sex chromosomes simplifies the requisite multifarious phenotype needed to produce a sexually antagonistic green-beard effects that fuel SA-zygotic drive.

Mentions: Sex chromosomes are predicted to evolve to code for SA-GrBd-effects, and the sexually antagonistic zygotic drive that they propel, for three reasons. First, all X- and Y-linked genes co-segregate during male meiosis like a single Mendelian gene that is highly pleiotropic. As a consequence, different genes on the same sex chromosome, rather than pleiotropy of a single gene, can code for the multifarious phenotypes required for green-beard effects to operate. A second feature promoting X- and Y-coded SA-GrBd-effects is the presence of the master sex-determining gene on one of these chromosomes. This linkage creates a perfect association between the presence or absence of a father's X and Y in his offspring and all sexually dimorphic phenotypes that are coded by any gene in the genome, i.e., within a family, all daughter-specific traits are effectively paternal X-tags and all son-specific traits are effectively Y-tags (Figure 2). The final feature contributing to sex chromosomes being hot-spots for SA-GrBd-effects is competition among siblings. In this case, any X- or Y-coded phenotype that differentially influences the competitive ability of the two sexes of offspring can cause a SA-GrBd-effect in three ways (Figure 3):


Sexually antagonistic "zygotic drive" of the sex chromosomes.

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

Summary of how linkage to the sex chromosomes simplifies the requisite multifarious phenotype needed to produce a sexually antagonistic green-beard effects that fuel SA-zygotic drive.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1000313-g002: Summary of how linkage to the sex chromosomes simplifies the requisite multifarious phenotype needed to produce a sexually antagonistic green-beard effects that fuel SA-zygotic drive.
Mentions: Sex chromosomes are predicted to evolve to code for SA-GrBd-effects, and the sexually antagonistic zygotic drive that they propel, for three reasons. First, all X- and Y-linked genes co-segregate during male meiosis like a single Mendelian gene that is highly pleiotropic. As a consequence, different genes on the same sex chromosome, rather than pleiotropy of a single gene, can code for the multifarious phenotypes required for green-beard effects to operate. A second feature promoting X- and Y-coded SA-GrBd-effects is the presence of the master sex-determining gene on one of these chromosomes. This linkage creates a perfect association between the presence or absence of a father's X and Y in his offspring and all sexually dimorphic phenotypes that are coded by any gene in the genome, i.e., within a family, all daughter-specific traits are effectively paternal X-tags and all son-specific traits are effectively Y-tags (Figure 2). The final feature contributing to sex chromosomes being hot-spots for SA-GrBd-effects is competition among siblings. In this case, any X- or Y-coded phenotype that differentially influences the competitive ability of the two sexes of offspring can cause a SA-GrBd-effect in three ways (Figure 3):

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