Abstract

The use of viral pathogens to control the population size of pest insects has produced both successful and unsuccessful outcomes. Here, we investigate whether those biocontrol successes and failures can be explained by key ecological and evolutionary processes between hosts and pathogens. Specifically, we examine how heterogeneity in pathogen transmission, ecological and evolutionary tradeoffs, and pathogen diversity affect insect population density and thus successful control. We first review the existing literature and then use numerical simulations of mathematical models to further explore these processes. Our results show that the control of insect densities using viruses depends strongly on the heterogeneity of virus transmission among insects. Overall, increased heterogeneity of transmission reduces the effect of viruses on insect densities and increases the long-term stability of insect populations. Lower equilibrium insect densities occur when transmission is heritable and when there is a tradeoff between mean transmission and insect fecundity compared to when the heterogeneity of transmission arises from non-genetic sources. Thus, the heterogeneity of transmission is a key parameter that regulates the long-term population dynamics of insects and their pathogens. We also show that both heterogeneity of transmission and life-history tradeoffs modulate characteristics of population dynamics such as the frequency and intensity of “boom–bust" population cycles. Furthermore, we show that because of life-history tradeoffs affecting the transmission rate, the use of multiple pathogen strains is more effective than the use of a single strain to control insect densities only when the pathogen strains differ considerably in their transmission characteristics. By quantifying the effects of ecology and evolution on population densities, we are able to offer recommendations to assess the long-term effects of classical biocontrol.

Highlights

  • Classical biocontrol refers to the control of pest species by the deliberate introduction of exotic or adapted natural enemies including pathogens, parasites, herbivores or predators [1]

  • The modelling results presented here suggest that heterogeneity in transmission and life-history tradeoffs, which are partly driven by evolutionary processes, are critical factors driving insect densities

  • For single-strain non-evolutionary models, increasing heterogeneity of transmission led to higher insect population densities if it was not constrained by the mean transmission rate

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Summary

Introduction

Classical biocontrol refers to the control of pest species by the deliberate introduction of exotic or adapted natural enemies including pathogens, parasites, herbivores or predators [1]. To assess the potential for long-term success of proposed control programs, this ecological knowledge is used to develop demographic predictions of the pest species by modeling the population dynamics of the insect pest and control agent [10] Most of these modeling efforts exclude evolutionary effects, as it is often assumed that evolutionary change occurs over much longer time-scales than ecological change. There is an increasing interest in understanding how ecology and evolution interact to mediate population dynamics of invertebrate hosts and their natural enemies [15,23,25], few efforts have been made to incorporate relevant evolutionary mechanisms to develop long-term predictions applicable to biological control (but see [26,27,28] ), making it difficult to evaluate whether such mechanisms should be considered during the development of control programs. We end with recommendations for using eco-evolutionary process models in classical biocontrol

Heterogeneity in Pathogen Transmission
Modeling Heterogeneity in Transmission in Insect–Pathogen Systems
Consequences of Heterogeneity in Transmission for Biocontrol
Ecological and Evolutionary Tradeoffs
Modeling Tradeoffs with Transmission in insect–pathogen Systems
Consequences of Tradeoffs for Biocontrol
Conclusions
Limitations and Need for Future Studies
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