Asymmetry in reproduction strategies drives evolution of resistance in biological control systems

Abstract

The success of biological control may depend on the control agent co-evolving with its target pest species, precluding the emergence of resistance that often undermines chemical control. However, recent evidence of a decline in attack rates of a sexual pest weevil by its asexual parasitoid suggests that evolutionary arms races may not prevent the emergence of resistance if the host and parasitoid do not have reproductive strategies that generate equal amounts of genetic variation. To understand how these asymmetries in reproductive strategies may drive the emergence of resistance, we combined life history data from two pest weevils and their parasitoids (one sexual and one asexual) in the New Zealand pastoral ecosystem, with a population dynamic model that allows the coevolution of hosts and parasitoids. We found that the ratio of the genetic variance of hosts to parasitoids was a key determinant of the emergence of resistance. Host resistance eventually occurred unless the parasitoids had considerably greater additive genetic variance than their host. The higher reproductive rate of asexual parasitoids did little to offset the cost of reduced additive genetic variance. The model predictions were congruent with long-term parasitism rates observed in the field for both of the pests considered (one with a sexual and one with an asexual parasitoid). We then explored the consequences of introducing two parasitoids with different reproductive strategies that attack the same sexual host. The model showed that the sexually reproducing parasitoid always out-competed the asexually reproducing one. Our study shows that any asymmetry in reproductive strategies is extremely important for predicting the long-term success of biological control agents. Fortunately, introduction of sexually reproducing individuals after an initial introduction of asexual strains may overcome the problems of host resistance. We conclude that evolution must be considered when evaluating the long-term outcomes of importation biological control.

Fig 1. Effect of additive genetic variance on parasitism rates and resistance.

a) Proportion of parasitized and resistant weevils at 300 generations for different ratios between the additive genetic variance (AGV) of the parasitoid and the host. All parameters were kept constant, except for the parasitoid AGV. The dashed blue line and the blue arrows show resistance and parasitism rate of an asexual parasitoid interacting with a sexual host (parasitoid AGV = 0 and host AGV = 0.1). The dotted red line and the red arrows show resistance and parasitism rate of a sexual parasitoid interacting with a sexual host (parasitoid AGV = 0.1 and host AGV = 0.1). b) Examples of the parasitism rates over generation time for an asexual parasitoid (blue dashed line) and a sexual parasitoid (red dotted line).

Fig 2. Comparison between the field data and the model results for both systems.

a) L. bonariensis and M. hyperodae; b) S. discoideus and M. aethiopoides (Moroccan strain). The upper and lower "hinges" represent the first and third quartiles. The whiskers extend from the hinge to the highest and lowest value that is within 1.5 * distance between the first and third quartiles. The points beyond the end of the whiskers are outliers.

Fig 3. Four examples of parasitism rates and resistance over generation time for the three species model (two parasitoids and one host).

The y axis shows parasitism rate (a) and proportion of resistance (b). The blue line represents the parasitoid that was introduced first, and the red line represents the parasitoid introduced second (at 500 generations). The dashed line represents an asexual parasitoid, and the dotted line represents a sexual parasitoid. The dash-dotted line represents the sum of the parasitism rate of the two parasitoids. The inset graphs are expansions of the box where the second parasitoid was introduced (showing 50 generations before and after the introduction). Parasitoids are extinct when the parasitism rate equals 0 and the resistant proportion equals 1.