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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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Examples of evolutionary dynamics of male coercion and the female barrier over 25000 generations under the assumption of no mortality costs.A: The coevolutionary dynamics of the degree of reproductive isolation; B: The demographic dynamics of the population sex ratio. The solid line indicates the dynamics in a population with higher male PRR (μ = 1.5) that starts at (x, y)  =  (7.5, 0.0). The dashed line indicates the dynamics in a population with lower male PRR (μ  = 0.3) that starts at (x, y)  =  (1.0, 0.0). Other parameters are r = 2.5, h = 0.001, α = 0.01, and δ = 0.02.
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pone-0058141-g002: Examples of evolutionary dynamics of male coercion and the female barrier over 25000 generations under the assumption of no mortality costs.A: The coevolutionary dynamics of the degree of reproductive isolation; B: The demographic dynamics of the population sex ratio. The solid line indicates the dynamics in a population with higher male PRR (μ = 1.5) that starts at (x, y)  =  (7.5, 0.0). The dashed line indicates the dynamics in a population with lower male PRR (μ  = 0.3) that starts at (x, y)  =  (1.0, 0.0). Other parameters are r = 2.5, h = 0.001, α = 0.01, and δ = 0.02.

Mentions: Because it is hard to analytically obtain candidate equilibria of this system using full versions of equation (2), I first analyse the case of no mortality cost to trait investment (i.e., βm  =  βf  = 0.0). In this case, solving sf(x)  = 0 and sm(y)  = 0 yields an analytical solution in which values of the two traits are equal (i.e., x = y). Stability analysis [42] demonstrates that these equilibria are stable whenever the inequality μ≥1.0 is satisfied (see Methods for the detail of the analysis). The solid lines in figure 2 represent an example of coevolutionary dynamics of male coercion and the female barrier in this case; even if a mutant female with an enhanced reproductive barrier invades, reproductive isolation from males will be lost under conditions of higher male PRR (Fig. 2A). Thus, sexual reproduction is eventually imposed on all females and the population sex ratio becomes balanced (Fig. 2B). However, when μ<1.0, a different system arises. Evolutionary rates of the two traits necessarily become equal at a value of , which is obtained by solving sf(x)  =  sm(y), and thus the difference between the two traits approaches either the value D, depending on initial trait values (Fig. 2A; the dashed line). At this value, both traits keep changing in the same direction at a constant rate, and females reproduce parthenogenetically with a probability: the population sex ratio remains biased toward females (Fig. 2B; the dashed line). That is, in the case of no mortality cost, the coevolution between male coercion and the female barrier shows the following two dynamics depending on the value of male PRR: evolution to the line of equilibria x = y when μ≥1.0 and continuous increase in x and y at a constant rate when μ<1.0. These are similar to the dynamics shown in a previous study that investigated the sexually antagonistic coevolution of reproductive barrier in sexual species [34].The above analysis reveals that the antagonistic coevolution for reproductive isolation results in only two outcomes (i.e., the prevalence of sex and the co-occurrence of two reproductive modes) under the absence of natural selection on trait investment. Next, to investigate how the mortality costs of trait investment affect the frequency of parthenogenetic reproduction, I perform numerical calculations that track population densities and the degree of reproductive isolation based on equations (1) and (2), under various ratios of the mortality coefficients to the coefficient of female fertilisation (βm/α and βf/α). The numerical analysis indicates that additional mortality costs yield a new outcome of parthenogenesis: because both male coercion and the female barrier display periodic dynamics that are out of phase with each other (Fig. 3A), the frequency of parthenogenetic reproduction and the population sex ratio periodically oscillate (Fig. 3B; the solid line and dashed line, respectively). In the case of both lower and higher male PRR, this outcome arises under conditions where the mortality coefficient of the female barrier is moderately lower and that of male coercion is higher than the coefficient of female fertilisation (Fig. 4; indicated by the dark grey region). In addition, the co-occurrence outcome (the light grey region) arises for the first time under higher male PRR around oscillation outcome (see Fig 4A). These results also show that male population persists even under disadvantageous conditions for them, such as lower male PRRs and a larger mortality coefficient for male coercion than that for the female barrier (i.e., βf/α < βm/α). Please note that these oscillation dynamics emerging from interactions of sexual conflict and viability selection are similar to the dynamics in a previous study of sexual conflict in obligate sexuals [43].


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

Kawatsu K - PLoS ONE (2013)

Examples of evolutionary dynamics of male coercion and the female barrier over 25000 generations under the assumption of no mortality costs.A: The coevolutionary dynamics of the degree of reproductive isolation; B: The demographic dynamics of the population sex ratio. The solid line indicates the dynamics in a population with higher male PRR (μ = 1.5) that starts at (x, y)  =  (7.5, 0.0). The dashed line indicates the dynamics in a population with lower male PRR (μ  = 0.3) that starts at (x, y)  =  (1.0, 0.0). Other parameters are r = 2.5, h = 0.001, α = 0.01, and δ = 0.02.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3585248&req=5

pone-0058141-g002: Examples of evolutionary dynamics of male coercion and the female barrier over 25000 generations under the assumption of no mortality costs.A: The coevolutionary dynamics of the degree of reproductive isolation; B: The demographic dynamics of the population sex ratio. The solid line indicates the dynamics in a population with higher male PRR (μ = 1.5) that starts at (x, y)  =  (7.5, 0.0). The dashed line indicates the dynamics in a population with lower male PRR (μ  = 0.3) that starts at (x, y)  =  (1.0, 0.0). Other parameters are r = 2.5, h = 0.001, α = 0.01, and δ = 0.02.
Mentions: Because it is hard to analytically obtain candidate equilibria of this system using full versions of equation (2), I first analyse the case of no mortality cost to trait investment (i.e., βm  =  βf  = 0.0). In this case, solving sf(x)  = 0 and sm(y)  = 0 yields an analytical solution in which values of the two traits are equal (i.e., x = y). Stability analysis [42] demonstrates that these equilibria are stable whenever the inequality μ≥1.0 is satisfied (see Methods for the detail of the analysis). The solid lines in figure 2 represent an example of coevolutionary dynamics of male coercion and the female barrier in this case; even if a mutant female with an enhanced reproductive barrier invades, reproductive isolation from males will be lost under conditions of higher male PRR (Fig. 2A). Thus, sexual reproduction is eventually imposed on all females and the population sex ratio becomes balanced (Fig. 2B). However, when μ<1.0, a different system arises. Evolutionary rates of the two traits necessarily become equal at a value of , which is obtained by solving sf(x)  =  sm(y), and thus the difference between the two traits approaches either the value D, depending on initial trait values (Fig. 2A; the dashed line). At this value, both traits keep changing in the same direction at a constant rate, and females reproduce parthenogenetically with a probability: the population sex ratio remains biased toward females (Fig. 2B; the dashed line). That is, in the case of no mortality cost, the coevolution between male coercion and the female barrier shows the following two dynamics depending on the value of male PRR: evolution to the line of equilibria x = y when μ≥1.0 and continuous increase in x and y at a constant rate when μ<1.0. These are similar to the dynamics shown in a previous study that investigated the sexually antagonistic coevolution of reproductive barrier in sexual species [34].The above analysis reveals that the antagonistic coevolution for reproductive isolation results in only two outcomes (i.e., the prevalence of sex and the co-occurrence of two reproductive modes) under the absence of natural selection on trait investment. Next, to investigate how the mortality costs of trait investment affect the frequency of parthenogenetic reproduction, I perform numerical calculations that track population densities and the degree of reproductive isolation based on equations (1) and (2), under various ratios of the mortality coefficients to the coefficient of female fertilisation (βm/α and βf/α). The numerical analysis indicates that additional mortality costs yield a new outcome of parthenogenesis: because both male coercion and the female barrier display periodic dynamics that are out of phase with each other (Fig. 3A), the frequency of parthenogenetic reproduction and the population sex ratio periodically oscillate (Fig. 3B; the solid line and dashed line, respectively). In the case of both lower and higher male PRR, this outcome arises under conditions where the mortality coefficient of the female barrier is moderately lower and that of male coercion is higher than the coefficient of female fertilisation (Fig. 4; indicated by the dark grey region). In addition, the co-occurrence outcome (the light grey region) arises for the first time under higher male PRR around oscillation outcome (see Fig 4A). These results also show that male population persists even under disadvantageous conditions for them, such as lower male PRRs and a larger mortality coefficient for male coercion than that for the female barrier (i.e., βf/α < βm/α). Please note that these oscillation dynamics emerging from interactions of sexual conflict and viability selection are similar to the dynamics in a previous study of sexual conflict in obligate sexuals [43].

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