The effect of disease on the evolution of females and the genetic basis of sex in populations with cytoplasmic male sterility

Abstract

The evolution of separate males and females is an important evolutionary transition that has occurred multiple times in flowering plants. While empirical studies have stressed the potential importance of natural enemies and organismal interactions in the evolution of separate sexes, there has been no treatment of natural enemies in the theoretical literature. We investigated the effects of disease on the evolution of females in gynodioecious populations composed of females and hermaphrodites, where sex is determined by the interaction of cytoplasmic male sterility (CMS) and nuclear restorer genes. When females are significantly more resistant than hermaphrodites, disease drives an increase in the frequency of females and sex determination becomes nuclear, creating the pre-conditions for the evolution of separate males and females. However, when females are only moderately more resistant, disease drives changes in the frequency of CMS and restorer alleles, but has little effect on the frequency of females. We discuss our results in the context of the evolution of mating systems and cyto-nuclear epistasis.

Keywords: cyto-nuclear epistasis; cytoplasmic male sterility; dioecy; disease; gynodioecy; sex-specific resistance.

Figure 1.

Level of female-specific disease resistance required for disease to drive the evolution of gynodioecy from hermaphroditism. A single diseased individual was introduced into a hermaphroditic population with a low starting CMS frequency (0.01), and no inherent female fertility advantage (a = 1). (a) Increase in the frequency of the CMS cytotype, (b) increase in the frequency of females. For both, darker colours indicate a larger increase. Wavy lines indicate parameter values that resulted in stable-limit cycles of CMS and females rather than stable point equilibria. (c) Genetic basis of sex H = hermaphroditism (loss of the CMS cytotype), C-N = cyto-nuclear sex-determination (maintenance of polymorphism in both the CMS and R loci), N = nuclear sex-determination (fixation of the CMS, and maintenance of polymorphism at the R locus). Disease transmission was frequency dependent. Disease was not maintained when β_H < 0.2. Other model parameters: cc = 0.9, a*cc = 0.9, cr = 0.25, μ = 0.2, k = 0.001.

Figure 2.

Effect of sex-specific disease resistance on the evolution of females and the genetic basis of sex in populations at stable cyto-nuclear gynodioecy. Top and bottom rows show the effect of introducing disease with different levels of sex-specific resistance into two populations with different pre-disease equilibrium levels. Females are more resistant to disease than hermaphrodites below the diagonal. (a–d) a = 1.5, a*cc = 1.35, initial CMS frequency = 0.31, female frequency = 0.068. (e–h) a = 2, a*cc = 1.8, CMS = 0.55, female = 0.061. (a,e) Change in the frequency of the equilibrium frequency of the CMS cytotype following the introduction of disease. (b,f) Change in the frequency of females. Red indicates an increase in frequency relative to disease-free equilibrium, and blue indicates a decrease in frequency relative to disease-free equilibrium. Darker shades correspond to a greater magnitude of change. (c,g) Change in the genetic basis of sex (figure 1). (d,h) Change in the frequency of the CMS cytotype (red lines), nuclear restorer (blue lines), and females (black lines) when females are 25% more resistant than hermaphrodites. Thin lines indicate pre-disease equilibrium; dotted grey line indicates disease prevalence. For all simulations, disease transmission was frequency dependent. Other model parameters: cc = 0.9, cr = 0.25, μ = 0.2, k = 0.001.

Figure 3.

Effect of selection on the heritability and evolution of females when sex determination is cyto-nuclear. (a) Frequency of the CMS cytotype before and after the introduction of disease. (b) Female heritability, measured as the proportion of female offspring that are female. (c) Change in female frequency. Black lines denote females are more resistant than hermaphrodites (β_H = 0.5, β_F = 0.3). Grey lines, females are more susceptible than hermaphrodites (β_H = 0.3, β_F = 0.5). Dashed grey lines, no sex-specific difference in resistance (β_H = β_F = 0.4). Other parameters: a = 1.5, cc = 0.9, a*cc = 1.35, cr = 0.25, μ = 0.2, k = 0.001.