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Sexual conflict over the maintenance of sex: effects of sexually antagonistic coevolution for reproductive isolation of parthenogenesis.

Kawatsu K - PLoS ONE (2013)

Bottom Line: First, the model based on adaptive-dynamics theory demonstrates that the resultant antagonistic coevolution between male coercion and a female barrier fundamentally ends in either the prevalence of sex or the co-occurrence of two reproductive modes.Therefore, as shown by the individual-based model, the establishment of obligate parthenogenesis in the population requires the simultaneous evolution of strong reproductive isolation between males and parthenogens.These findings should shed light on the interspecific diversity of reproductive modes as well as help to explain the prevalence of sexual reproduction.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Insect Ecology, Graduate School of Agriculture, Kyoto University, Kitashirakawaoiwake-cho, Sakyo-ku, Kyoto, Japan. kazutakawatsu@gmail.com

ABSTRACT
Sexual reproduction involves many costs. Therefore, females acquiring a capacity for parthenogenetic (or asexual) reproduction will gain a reproductive advantage over obligately sexual females. In contrast, for males, any trait coercing parthenogens into sexual reproduction (male coercion) increases their fitness and should be under positive selection because parthenogenesis deprives them of their genetic contribution to future generations. Surprisingly, although such sexual conflict is a possible outcome whenever reproductive isolation is incomplete between parthenogens and the sexual ancestors, it has not been given much attention in the studies of the maintenance of sex. Using two mathematical models, I show here that the evolution of male coercion substantially favours the maintenance of sex even though a female barrier against the coercion can evolve. First, the model based on adaptive-dynamics theory demonstrates that the resultant antagonistic coevolution between male coercion and a female barrier fundamentally ends in either the prevalence of sex or the co-occurrence of two reproductive modes. This is because the coevolution between the two traits additionally involves sex-ratio selection, that is, an increase in parthenogenetic reproduction leads to a female-biased population sex ratio, which will enhance reproductive success of more coercive males and directly promotes the evolution of the coercion among males. Therefore, as shown by the individual-based model, the establishment of obligate parthenogenesis in the population requires the simultaneous evolution of strong reproductive isolation between males and parthenogens. These findings should shed light on the interspecific diversity of reproductive modes as well as help to explain the prevalence of sexual reproduction.

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Simulation results of the individual-based model in the case of no cost of parthenogenesis.A: Example dynamics of the degree of reproductive isolation for 10,000 generations in a single simulation run. Black and grey lined differ in the value of male PRR (the black line: μ = 1.25, the grey line: μ = 0.25). B: Mean frequency of parthenogenesis after 10,000 generations as a function of male PRR. Open-squares and filled-circles represent the frequency of females succeeding in parthenogenetic reproduction and the frequency of parthenogenetic alleles, respectively. Bars indicate standard deviation over 25 replicates. Other parameters are r = 10.0, h = 0.001, α  = 0.01, βm  = βf  = 0.0001.
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pone-0058141-g005: Simulation results of the individual-based model in the case of no cost of parthenogenesis.A: Example dynamics of the degree of reproductive isolation for 10,000 generations in a single simulation run. Black and grey lined differ in the value of male PRR (the black line: μ = 1.25, the grey line: μ = 0.25). B: Mean frequency of parthenogenesis after 10,000 generations as a function of male PRR. Open-squares and filled-circles represent the frequency of females succeeding in parthenogenetic reproduction and the frequency of parthenogenetic alleles, respectively. Bars indicate standard deviation over 25 replicates. Other parameters are r = 10.0, h = 0.001, α  = 0.01, βm  = βf  = 0.0001.

Mentions: As shown in examples of evolutionary dynamics of reproductive isolation for a single simulation run (Fig. 5A), the degree of reproductive isolation from males is initially high because of spreads of the invasive parthenogen. However, as generation proceeds, reproductive isolation vanishes from the population under the condition of higher male PRR (the black line), or approaches a fixed value under the condition of lower male PRR (the grey line). Therefore, the frequency of females that succeed in parthenogenetic reproduction decreases as s function of male PRR, and sexual reproduction is imposed on most females when μ≥1.0 (Fig. 5B; indicated by the open-squares). Moreover, I confirm that the IBM with the condition of facultative parthenogenesis yields results quantitatively similar to those of the adaptive-dynamics model under same parameter set (see Fig. S1). Therefore, the antagonistic coevolution for reproductive isolation works to maintain the male population under the assumption of the individual-based model, as in the adaptive-dynamics model.


Sexual conflict over the maintenance of sex: effects of sexually antagonistic coevolution for reproductive isolation of parthenogenesis.

Kawatsu K - PLoS ONE (2013)

Simulation results of the individual-based model in the case of no cost of parthenogenesis.A: Example dynamics of the degree of reproductive isolation for 10,000 generations in a single simulation run. Black and grey lined differ in the value of male PRR (the black line: μ = 1.25, the grey line: μ = 0.25). B: Mean frequency of parthenogenesis after 10,000 generations as a function of male PRR. Open-squares and filled-circles represent the frequency of females succeeding in parthenogenetic reproduction and the frequency of parthenogenetic alleles, respectively. Bars indicate standard deviation over 25 replicates. Other parameters are r = 10.0, h = 0.001, α  = 0.01, βm  = βf  = 0.0001.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3585248&req=5

pone-0058141-g005: Simulation results of the individual-based model in the case of no cost of parthenogenesis.A: Example dynamics of the degree of reproductive isolation for 10,000 generations in a single simulation run. Black and grey lined differ in the value of male PRR (the black line: μ = 1.25, the grey line: μ = 0.25). B: Mean frequency of parthenogenesis after 10,000 generations as a function of male PRR. Open-squares and filled-circles represent the frequency of females succeeding in parthenogenetic reproduction and the frequency of parthenogenetic alleles, respectively. Bars indicate standard deviation over 25 replicates. Other parameters are r = 10.0, h = 0.001, α  = 0.01, βm  = βf  = 0.0001.
Mentions: As shown in examples of evolutionary dynamics of reproductive isolation for a single simulation run (Fig. 5A), the degree of reproductive isolation from males is initially high because of spreads of the invasive parthenogen. However, as generation proceeds, reproductive isolation vanishes from the population under the condition of higher male PRR (the black line), or approaches a fixed value under the condition of lower male PRR (the grey line). Therefore, the frequency of females that succeed in parthenogenetic reproduction decreases as s function of male PRR, and sexual reproduction is imposed on most females when μ≥1.0 (Fig. 5B; indicated by the open-squares). Moreover, I confirm that the IBM with the condition of facultative parthenogenesis yields results quantitatively similar to those of the adaptive-dynamics model under same parameter set (see Fig. S1). Therefore, the antagonistic coevolution for reproductive isolation works to maintain the male population under the assumption of the individual-based model, as in the adaptive-dynamics model.

Bottom Line: First, the model based on adaptive-dynamics theory demonstrates that the resultant antagonistic coevolution between male coercion and a female barrier fundamentally ends in either the prevalence of sex or the co-occurrence of two reproductive modes.Therefore, as shown by the individual-based model, the establishment of obligate parthenogenesis in the population requires the simultaneous evolution of strong reproductive isolation between males and parthenogens.These findings should shed light on the interspecific diversity of reproductive modes as well as help to explain the prevalence of sexual reproduction.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Insect Ecology, Graduate School of Agriculture, Kyoto University, Kitashirakawaoiwake-cho, Sakyo-ku, Kyoto, Japan. kazutakawatsu@gmail.com

ABSTRACT
Sexual reproduction involves many costs. Therefore, females acquiring a capacity for parthenogenetic (or asexual) reproduction will gain a reproductive advantage over obligately sexual females. In contrast, for males, any trait coercing parthenogens into sexual reproduction (male coercion) increases their fitness and should be under positive selection because parthenogenesis deprives them of their genetic contribution to future generations. Surprisingly, although such sexual conflict is a possible outcome whenever reproductive isolation is incomplete between parthenogens and the sexual ancestors, it has not been given much attention in the studies of the maintenance of sex. Using two mathematical models, I show here that the evolution of male coercion substantially favours the maintenance of sex even though a female barrier against the coercion can evolve. First, the model based on adaptive-dynamics theory demonstrates that the resultant antagonistic coevolution between male coercion and a female barrier fundamentally ends in either the prevalence of sex or the co-occurrence of two reproductive modes. This is because the coevolution between the two traits additionally involves sex-ratio selection, that is, an increase in parthenogenetic reproduction leads to a female-biased population sex ratio, which will enhance reproductive success of more coercive males and directly promotes the evolution of the coercion among males. Therefore, as shown by the individual-based model, the establishment of obligate parthenogenesis in the population requires the simultaneous evolution of strong reproductive isolation between males and parthenogens. These findings should shed light on the interspecific diversity of reproductive modes as well as help to explain the prevalence of sexual reproduction.

Show MeSH