Positive feedback in the transition from sexual reproduction to parthenogenesis

Abstract

Understanding how new phenotypes evolve is challenging because intermediate stages in transitions from ancestral to derived phenotypes often remain elusive. Here we describe and evaluate a new mechanism facilitating the transition from sexual reproduction to parthenogenesis. In many sexually reproducing species, a small proportion of unfertilized eggs can hatch spontaneously ('tychoparthenogenesis') and develop into females. Using an analytical model, we show that if females are mate-limited, tychoparthenogenesis can result in the loss of males through a positive feedback mechanism whereby tychoparthenogenesis generates female-biased sex ratios and increasing mate limitation. As a result, the strength of selection for tychoparthenogenesis increases in concert with the proportion of tychoparthenogenetic offspring in the sexual population. We then tested the hypothesis that mate limitation selects for tychoparthenogenesis and generates female-biased sex ratios, using data from natural populations of sexually reproducing Timema stick insects. Across 41 populations, both the tychoparthenogenesis rates and the proportions of females increased exponentially as the density of individuals decreased, consistent with the idea that low densities of individuals result in mate limitation and selection for reproductive insurance through tychoparthenogenesis. Our model and data from Timema populations provide evidence for a simple mechanism through which parthenogenesis can evolve rapidly in a sexual population.

Figure 1.

The stable proportion of females, p_F^*, depending on the tychoparthenogenesis rate (proportion v of unfertilized eggs that develop into females) and the mating probability of females, α, as predicted by our analytical model. (a) Including the feedback between population sex ratio and female mating probability, α = βp_M in equation (2.1); (b) with female mating probability independent of the population sex ratio, α = β in equation (2.1).

Figure 2.

The rate of tychoparthenogenesis is positively correlated with female bias across 41 populations of sexually reproducing Timema stick insects.

Figure 3.

(a) Sex ratios (proportion of females) and (b) tychoparthenogenesis rates across Timema populations with variable densities of individuals. The level of mate limitation is assumed to increase as the density of individuals in the population decreases.