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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.

SUBMITTER: Casanovas P

PROVIDER: S-EPMC6300327 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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

Casanovas Paula P Goldson Stephen L SL Tylianakis Jason M JM

PloS one 20181219 12

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 ...[more]

PMID: 30566468

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Project description:There is growing interest in biological control as a sustainable and environmentally friendly way to control pest insects. Aphids are among the most detrimental agricultural pests worldwide, and parasitoid wasps are frequently employed for their control. The use of asexual parasitoids may improve the effectiveness of biological control because only females kill hosts and because asexual populations have a higher growth rate than sexuals. However, asexuals may have a reduced capacity to track evolutionary change in their host populations. We used a factorial experiment to compare the ability of sexual and asexual populations of the parasitoid Lysiphlebus fabarum to control caged populations of black bean aphids (Aphis fabae) of high and low clonal diversity. The aphids came from a natural population, and one-third of the aphid clones harbored Hamiltonella defensa, a heritable bacterial endosymbiont that increases resistance to parasitoids. We followed aphid and parasitoid population dynamics for 3 months but found no evidence that the reproductive mode of parasitoids affected their effectiveness as biocontrol agents, independent of host clonal diversity. Parasitoids failed to control aphids in most cases, because their introduction resulted in strong selection for clones protected by H. defensa. The increasingly resistant aphid populations escaped control by parasitoids, and we even observed parasitoid extinctions in many cages. The rapid evolution of symbiont-conferred resistance in turn imposed selection on parasitoids. In cages where asexual parasitoids persisted until the end of the experiment, they became dominated by a single genotype able to overcome the protection provided by H. defensa. Thus, there was evidence for parasitoid counteradaptation, but it was generally too slow for parasitoids to regain control over aphid populations. It appears that when pest aphids possess defensive symbionts, the presence of parasitoid genotypes able to overcome symbiont-conferred resistance is more important for biocontrol success than their reproductive mode.

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

Publications

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

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