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Rapid evolution of symbiont-mediated resistance compromises biological control of aphids by parasitoids.

ABSTRACT: 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.

SUBMITTER: Kach H

PROVIDER: S-EPMC5775498 | biostudies-literature | 2018 Feb

REPOSITORIES: biostudies-literature

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Rapid evolution of symbiont-mediated resistance compromises biological control of aphids by parasitoids.

Käch Heidi H Mathé-Hubert Hugo H Dennis Alice B AB Vorburger Christoph C

Evolutionary applications 20170903 2

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 evo ...[more]

PMID: 29387157

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Project description:BackgroundAphids are serious pest on crops. By probing with their stylets, they interact with the plant, they vector viruses and when they reach the phloem they start a continuous ingestion. Many plant resistances to aphids have been identified, several have been deployed. However, some resistances breaking down have been observed. In the melon, a gene that confers resistance to aphids has been deployed in some melon-producing areas, and aphid colony development on Vat-carrying plants has been observed in certain agrosystems. The Vat gene is a NBS-LRR gene that confers resistance to the aphid species Aphis gossypii and exhibits the unusual characteristic of also conferring resistance to non-persistently transmitted viruses when they are inoculated by the aphid. Thus, we characterized patterns of resistance to aphid and virus using the aphid diversity and we investigated the mechanisms by which aphids and viruses may adapt to the Vat gene.ResultsUsing a Vat-transgenic line built in a susceptible background, we described the Vat- spectrum of resistance to aphids, and resistance to viruses triggered by aphids using a set of six A. gossypii biotypes. Discrepancies between both resistance phenotypes revealed that aphid adaptation to Vat-mediated resistance does not occur only via avirulence factor alterations but also via adaptation to elicited defenses. In experiments conducted with three virus species serially inoculated by aphids from and to Vat plants, the viruses did not evolve to circumvent Vat-mediated resistance. We confirmed discrepancies between both resistance phenotypes by testing each aphid biotype with a set of thirteen melon accessions chosen to reflect the natural diversity of the melon. Inheritance studies revealed that patterns of resistance to virus triggered by aphids are controlled by different alleles at the Vat locus and at least another locus located at a short genetic distance. Therefore, resistance to viruses triggered by aphids is controlled by a gene cluster.ConclusionsUnder the Flor model, changes in the avirulence gene determine the ability of the pathogen to overcome the resistance conferred by a plant gene. The Vat gene belongs to a resistance gene family that fits this pest/pathogen-plant interaction, and we revealed an additional mechanism of aphid adaptation that potentially exists in other interactions between plants and pests or pathogens.

Project description: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.

Project description:Maize, Zea mays L., is the most abundant field crop in China. Aphids are the most economically damaging pest on maize, particularly in the maize agri-ecosystems of Jilin Province, northeastern China. Parasitic wasps are important natural enemies of aphids, but limited information exists about their species composition, richness and seasonal dynamics in northeastern China. In this study, the population dynamics of maize aphids and parasitoid wasps were assessed in relation to each other during the summer seasons of two consecutive years, 2018 and 2019. We selected maize fields in the Changchun, Songyuan, Huinan and Gongzhuling areas of Jilin Province. Four species of aphids were recorded from these maize fields: Rhopalosiphum padi (L), Rhopalosiphum maidis (Fitch), Aphis gossypii Glover and Macrosiphum miscanthi (Takahashi). The dominant species in each of the four areas were R. maids (Filch) and R. padi in Changchun, R. padi in Songyuan, A. gossypii and R. padi in Huinan, and A.gossypii and R. padi in Gongzhuling. We delineated a species complex made up of primary parasitoids and hyperparasitoids associated with maize aphids. The primary parasitoids Lysiphlebus testaceipes, Binodoxys communis and Aphelinus albipodus together formed approximately 85.3% of the parasitoid complex. Pachyneuron aphidis, Phaenoglyphis villosa, Syrphophagus taeniatus and Asaphes suspensus made up the hyperparasitoids. Of the primary parasitoids, L. testaceipes was the dominant species (81.31%). Of the hyperparasitoid group, P. villosa was the dominant species (68.42%). Parasitism rates followed the fluctuation of the aphid population. The highest parasitic rate was observed during the peak period of cotton aphids. In this paper, the occurrence dynamics and dominant species of aphids and the dynamics of parasitic natural enemies of aphids in maize fields in Jilin Province are, for the first time, systematically reported. This study provides important information for the establishment and promotion of aphid biological control in maize fields.

Project description:BackgroundControl and prevention of dengue relies heavily on the application of insecticides to control dengue vector mosquitoes. In Colombia, application of the larvicide temephos to the aquatic breeding sites of Aedes aegypti is a key part of the dengue control strategy. Resistance to temephos was recently detected in the dengue-endemic city of Cucuta, leading to questions about its efficacy as a control tool. Here, we characterize the underlying mechanisms and estimate the operational impact of this resistance.Methodology/principal findingsLarval bioassays of Ae. aegypti larvae from Cucuta determined the temephos LC50 to be 0.066 ppm (95% CI 0.06-0.074), approximately 15× higher than the value obtained from a susceptible laboratory colony. The efficacy of the field dose of temephos at killing this resistant Cucuta population was greatly reduced, with mortality rates <80% two weeks after application and <50% after 4 weeks. Neither biochemical assays nor partial sequencing of the ace-1 gene implicated target site resistance as the primary resistance mechanism. Synergism assays and microarray analysis suggested that metabolic mechanisms were most likely responsible for the temephos resistance. Interestingly, although the greatest synergism was observed with the carboxylesterase inhibitor, DEF, the primary candidate genes from the microarray analysis, and confirmed by quantitative PCR, were cytochrome P450 oxidases, notably CYP6N12, CYP6F3 and CYP6M11.Conclusions/significanceIn Colombia, resistance to temephos in Ae. aegypti compromises the duration of its effect as a vector control tool. Several candidate genes potentially responsible for metabolic resistance to temephos were identified. Given the limited number of insecticides that are approved for vector control, future chemical-based control strategies should take into account the mechanisms underlying the resistance to discern which insecticides would likely lead to the greatest control efficacy while minimizing further selection of resistant phenotypes.

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Rapid evolution of symbiont-mediated resistance compromises biological control of aphids by parasitoids.

Publications

Rapid evolution of symbiont-mediated resistance compromises biological control of aphids by parasitoids.

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