The advantage of sex: Reinserting fluctuating selection in the pluralist approach

Abstract

The advantage of sex, and its fixation in some clades and species all over the eukaryote tree of life, is considered an evolutionary enigma, especially regarding its assumed two-fold cost. Several likely hypotheses have been proposed such as (1) a better response to the negative frequency-dependent selection imposed by the "Red Queen" hypothesis; (2) the competition between siblings induced by the Tangled Bank hypothesis; (3) the existence of genetic and of (4) ecological factors that can diminish the cost of sex to less than the standard assumed two-fold; and (5) a better maintenance of genetic diversity and its resulting phenotypic variation, providing a selective advantage in randomly fluctuating environments. While these hypotheses have mostly been studied separately, they can also act simultaneously. This was advocated by several studies which presented a pluralist point of view. Only three among the five causes cited above were considered yet in such a framework: the Red Queen hypothesis, the Tangled Bank and the genetic factors lowering the cost of sex. We thus simulated the evolution of a finite mutating population undergoing negative frequency-dependent selection on phenotypes and a two-fold (or less) cost of sexuality, experiencing randomly fluctuating selection along generations. The individuals inherited their reproductive modes, either clonal or sexual. We found that exclusive sexuality begins to fix in populations exposed to environmental variation that exceeds the width of one ecological niche (twice the standard deviation of a Gaussian response to environment). This threshold was lowered by increasing negative frequency-dependent selection and when reducing the two-fold cost of sex. It contributes advocating that the different processes involved in a short-term advantage of sex and recombination can act in combination to favor the fixation of sexual reproduction in populations.

Fig 1. Proportion of populations where sexual reproduction fixed as a function of the variance of random environmental fluctuations.

In this example, a SD of 8 resulted in the fixation of sex in more than 5% of the populations, corresponding to the case with no negative frequency-dependent selection resulting from the Red Queen Hypothesis and with no inter-generational autocorrelation in environmental fluctuations. In these simulations, ecological niche width was defined as 2ω = 8.

Fig 2. Standard deviation (± SE) of random environmental fluctuations resulting in the fixation of sex in more than 50% of the populations.

Results are shown as a function of the negative frequency-dependent selection resulting from the Red Queen Hypothesis (inverse of parameter m) and inter-generational autocorrelation in environmental fluctuations. Closed dots: uncorrelated fluctuations, Open dots: auto-correlated fluctuations of 0.6.

Fig 3. Standard deviation (± SE) of random environmental fluctuations resulting in the fixation of sex in more than 50% of the populations.

Results are shown as a as a function of the intensity of the negative frequency-dependent selection resulting from the Red Queen Hypothesis (inverse of parameter m) and for different levels of the cost of sex. Open dots and solid lines: cost of sexual reproduction of 2.0; closed dots and solid lines: cost of sexual reproduction of 1.8; open dots and dashed lines: cost of sexual reproduction of 1.6; closed dots and dashed lines: cost of sexual reproduction of 1.2. The single point in the lower left part of the plot corresponds to no cost of sex and no negative frequency-dependent selection, allowing comparison with the previous prediction of [54] (see text).