Understanding the Evolutionary Ecology of host–pathogen Interactions Provides Insights into the Outcomes of Insect Pest Biocontrol

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.

Identification of Diverse Toxin Complex Clusters and an eCIS Variant in Serratia proteamaculans Pathovars of the New Zealand Grass Grub ( Costelytra Giveni ) and Manuka Beetle ( Pyronota Spp.) Larvae

“…Accordingly, these isolates offer the potential for the development of biopesticides that are more active in specific environments. Further, combining isolates with different virulence properties, such as S. entomophila and the more rapid-killing S. proteamaculans isolates identified in this study, may afford greater control of the insect host ( 47 ). The isolation of new Pyronota -active Tc-encoding Serratia species offers additional measures for the control of this species.…”

“…The epidemiological aspects of non-amber-disease S. proteamaculans pathotypes remain undefined. It is likely that faster acting pathogens such as S. proteamaculans AGR96X may be predisposed to localized outbreaks characterized by a “boom to bust” life cycle ( 47 ) or, alternately, suited to cooler climes where reduced larval metabolism limits larval movement. This may mean that unlike amber-disease-causing isolates, rapid-killing pathogens have less capacity to spread and persist in subsequent years ( 47 , 48 ).…”

“…It is likely that faster acting pathogens such as S. proteamaculans AGR96X may be predisposed to localized outbreaks characterized by a “boom to bust” life cycle ( 47 ) or, alternately, suited to cooler climes where reduced larval metabolism limits larval movement. This may mean that unlike amber-disease-causing isolates, rapid-killing pathogens have less capacity to spread and persist in subsequent years ( 47 , 48 ). In addition to these variables, though it may reflect differences in larval physiology or genetics, the capacity of some of the Serratia isolates to cause disease in only 60 to 90% of the challenged larvae may ensure the long-term persistence of the pathogen by maintaining host availability in subsequent years.…”

Systematic shifts in the variation among host individuals must be considered in climate-disease theory

“…In such cases, eco-evolutionary dynamics have been proposed as a mechanism by which variation in susceptibility can be realistically high (C > 1) and the host population can still cycle. Specifically, if host susceptibility is heritable, under selection, and is costly to fecundity, then stable cycling can still occur when C > 1 [47,49,45,42]. Although this eco-evolutionary theory has some empirical support, our analysis introduces an alternative hypothesis: while C may be greater than 1 during parts of the epizootic, if temperature drives C lower than 1 during other parts, we may still expect cycling.…”

“…The simplified assumptions are thus that environmental conditions exist in each new host generation to generate an equivalent distribution of susceptibilities among host individuals and that the coefficient of variation in transmission rate, C, is constant through an epizootic. In addition to determining the number of individuals that become infected and die during an outbreak, the degree of host variation (i.e., the value of C) determines whether long-term fluctuations in population size follow point equilibrium dynamics or whether they cycle in a stable or an unstable manner [25,43,45]. Therefore, incorporating the effects of varying TPCs in the epizootic model are expected to result in different epidemic sizes and different long-term patterns of population cycling, even if the effect of temperature on C is transient.…”