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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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A pedigree analysis of female homosexuality.The focal homosexual individual is highlighted in yellow. Relatives expressing elevated rates of homosexuality are shown in red (based on Table 6 of Pattatucci and Hamer (1995) [41]).
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pgen-1000313-g006: A pedigree analysis of female homosexuality.The focal homosexual individual is highlighted in yellow. Relatives expressing elevated rates of homosexuality are shown in red (based on Table 6 of Pattatucci and Hamer (1995) [41]).

Mentions: SA-zygotic drive provides a previously unexplored genetic model for the evolution of traits, such as sterility and homosexuality, which reduce Darwinian fitness, but yet can attain appreciable frequency in natural populations. We illustrate the heuristic potential of the concept of SA-zygotic drive by applying this genetic model to the unusual distribution of female homosexuality in human pedigrees (Figure 6, drawn from the data presented in Table 6 of [41]). We do not claim that this phenotype represents an established example of SA-zygotic drive, only that SA-zygotic drive provides a new functional form of hypothesis that can be tested to account for this – and other enigmatic – phenotypes that presently have no other genetic explanation.


Sexually antagonistic "zygotic drive" of the sex chromosomes.

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

A pedigree analysis of female homosexuality.The focal homosexual individual is highlighted in yellow. Relatives expressing elevated rates of homosexuality are shown in red (based on Table 6 of Pattatucci and Hamer (1995) [41]).
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1000313-g006: A pedigree analysis of female homosexuality.The focal homosexual individual is highlighted in yellow. Relatives expressing elevated rates of homosexuality are shown in red (based on Table 6 of Pattatucci and Hamer (1995) [41]).
Mentions: SA-zygotic drive provides a previously unexplored genetic model for the evolution of traits, such as sterility and homosexuality, which reduce Darwinian fitness, but yet can attain appreciable frequency in natural populations. We illustrate the heuristic potential of the concept of SA-zygotic drive by applying this genetic model to the unusual distribution of female homosexuality in human pedigrees (Figure 6, drawn from the data presented in Table 6 of [41]). We do not claim that this phenotype represents an established example of SA-zygotic drive, only that SA-zygotic drive provides a new functional form of hypothesis that can be tested to account for this – and other enigmatic – phenotypes that presently have no other genetic explanation.

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