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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 outcomes after 20,000 generations under various values of the reproductive barrier of the invasive parthenogens and the cost of parthenogenetic capacity.The two panels differ in the value of male PRR (A: μ = 2.00, B: μ = 0.50). Each box indicates the proportion of different outcomes over 25 replicates under its parameter set (white: the obligate-sex outcome; grey: the facultative-parthenogenesis outcome; black: the obligate-parthenogenesis outcome). The solid curves are the analytical threshold of cA for successful invasion by the invasive parthenogen (see Methods). Other parameters are as in Figure 5.
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pone-0058141-g006: Simulation outcomes after 20,000 generations under various values of the reproductive barrier of the invasive parthenogens and the cost of parthenogenetic capacity.The two panels differ in the value of male PRR (A: μ = 2.00, B: μ = 0.50). Each box indicates the proportion of different outcomes over 25 replicates under its parameter set (white: the obligate-sex outcome; grey: the facultative-parthenogenesis outcome; black: the obligate-parthenogenesis outcome). The solid curves are the analytical threshold of cA for successful invasion by the invasive parthenogen (see Methods). Other parameters are as in Figure 5.

Mentions: Figure 5B also demonstrates that the frequency of parthenogenetic alleles (the filled-circles) moderately decreases when μ>1.5. This is because the possibility that females succeed in parthenogenesis is strongly reduced, and selection for the parthenogenetic capacity becomes neutral. Thus, parthenogenetic alleles are predicted to be purged if they are deleterious for individual fitness. To verify this prediction, I incorporate a fitness cost cA into an allele for parthenogenetic capacity in the individual-based model (see Methods), and perform additional simulations under various costs of parthenogenesis cA and values of female barrier of the invasive parthenogen x'. The simulation run ends in one of the following three outcomes: in the first, parthenogenetic alleles go extinct and most of the population consists of only obligate sexuals (the obligate-sex outcome); in the second, the parthenogenetic allele becomes prevalent in the population but sexual reproduction is imposed on some proportion of females by coercive males (the facultative-parthenogenesis outcome); in the third, males are extinct and females reproduce only parthenogenetically (the obligate-parthenogenesis outcome). Specifically, under the condition of higher male PRR (Fig. 6A), the obligate-sex outcome dominates even with a small cost of parthenogenetic capacity, and occurs in broader regions than those which are expected by the analytical threshold (the solid curve; see Methods). When male PRR is lower than female PRR (Fig. 6B), the obligate-sex outcome occurs in limited regions with a large cost of parthenogenesis and/or a small value of female barrier of invasive parthenogen, which are qualitatively consistent to those of the analytical threshold. The simulation also demonstrates that the occurrence of the obligate-parthenogenesis outcome requires significantly larger reproductive barriers than those of the threshold for both conditions of male PRR (Fig. 6).


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

Kawatsu K - PLoS ONE (2013)

Simulation outcomes after 20,000 generations under various values of the reproductive barrier of the invasive parthenogens and the cost of parthenogenetic capacity.The two panels differ in the value of male PRR (A: μ = 2.00, B: μ = 0.50). Each box indicates the proportion of different outcomes over 25 replicates under its parameter set (white: the obligate-sex outcome; grey: the facultative-parthenogenesis outcome; black: the obligate-parthenogenesis outcome). The solid curves are the analytical threshold of cA for successful invasion by the invasive parthenogen (see Methods). Other parameters are as in Figure 5.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3585248&req=5

pone-0058141-g006: Simulation outcomes after 20,000 generations under various values of the reproductive barrier of the invasive parthenogens and the cost of parthenogenetic capacity.The two panels differ in the value of male PRR (A: μ = 2.00, B: μ = 0.50). Each box indicates the proportion of different outcomes over 25 replicates under its parameter set (white: the obligate-sex outcome; grey: the facultative-parthenogenesis outcome; black: the obligate-parthenogenesis outcome). The solid curves are the analytical threshold of cA for successful invasion by the invasive parthenogen (see Methods). Other parameters are as in Figure 5.
Mentions: Figure 5B also demonstrates that the frequency of parthenogenetic alleles (the filled-circles) moderately decreases when μ>1.5. This is because the possibility that females succeed in parthenogenesis is strongly reduced, and selection for the parthenogenetic capacity becomes neutral. Thus, parthenogenetic alleles are predicted to be purged if they are deleterious for individual fitness. To verify this prediction, I incorporate a fitness cost cA into an allele for parthenogenetic capacity in the individual-based model (see Methods), and perform additional simulations under various costs of parthenogenesis cA and values of female barrier of the invasive parthenogen x'. The simulation run ends in one of the following three outcomes: in the first, parthenogenetic alleles go extinct and most of the population consists of only obligate sexuals (the obligate-sex outcome); in the second, the parthenogenetic allele becomes prevalent in the population but sexual reproduction is imposed on some proportion of females by coercive males (the facultative-parthenogenesis outcome); in the third, males are extinct and females reproduce only parthenogenetically (the obligate-parthenogenesis outcome). Specifically, under the condition of higher male PRR (Fig. 6A), the obligate-sex outcome dominates even with a small cost of parthenogenetic capacity, and occurs in broader regions than those which are expected by the analytical threshold (the solid curve; see Methods). When male PRR is lower than female PRR (Fig. 6B), the obligate-sex outcome occurs in limited regions with a large cost of parthenogenesis and/or a small value of female barrier of invasive parthenogen, which are qualitatively consistent to those of the analytical threshold. The simulation also demonstrates that the occurrence of the obligate-parthenogenesis outcome requires significantly larger reproductive barriers than those of the threshold for both conditions of male PRR (Fig. 6).

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
Related in: MedlinePlus