Rapid spread of a densovirus in a major crop pest following wide-scale adoption of Bt-cotton in China
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Evaluation Summary:
This manuscript will be of interest to a broad audience of researchers interested in microbe-insect interactions and how they may affect adaptation to pesticides. It presents data supporting that infection with a mutualistic virus enhances fitness in a moth, and that selection pressure represented by transgenic crops may be driving the spread of this mutualistic infection in Chinese moth populations. Specificially, infection with a densovirus appears to improve the ability of the cotton bollworm to survive on transgenic cotton expressing insecticidal proteins from Bacillus thuringiensis (Bt). The widely-grown Bt-transgenic crops control insect pests with great reductions in chemical insecticides, and anything that could reduce their efficacy is of relevance to the agricultural biotechnology community and to growers. This work suggests that virus infection of the insect pest can have unexpected interactions with the ongoing selection for Bt resistance that threatens the sustainability of Bt-transgenic crops. The impact of the work would be clearer if there was a better distinction between pest resistance (the evolution of increased tolerance due to genetic changes in the pest population) and other mechanisms of increased pest tolerance (e.g., virus infection).
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
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Abstract
Bacillus thuringiensis (Bt) crops have been widely planted and the effects of Bt-crops on populations of the target and non-target insect pests have been well studied. However, the effects of Bt-crops exposure on microorganisms that interact with crop pests have not previously been quantified. Here, we use laboratory and field data to show that infection of Helicoverpa armigera with a densovirus (HaDV2) is associated with its enhanced growth and tolerance to Bt-cotton. Moreover, field monitoring showed a much higher incidence of cotton bollworm infection with HaDV2 in regions cultivated with Bt-cotton than in regions without it, with the rate of densovirus infection increasing with increasing use of Bt-cotton. RNA-seq suggested tolerance to both baculovirus and Cry1Ac were enhanced via the immune-related pathways. These findings suggest that exposure to Bt-crops has selected for beneficial interactions between the target pest and a mutualistic microorganism that enhances its performance on Bt-crops under field conditions.
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Reviewer #2 (Public Review):
The various pathogenic, parasitic, symbiotic, and mutualistic interactions between insects and the microbes they interact with represents a rich area of research. This study by Xiao et al. represents a very interesting example of such a relationship. Overall the study is well designed and executed. The approach they utilize to test their hypothesis is valid and they combined both laboratory and field collected insects to address the question. The RNAseq analysis also provides potential insights into possible mechanisms by which the virus HaDV2 enables enhanced resistance to Bt Cry1Ac. The RNAseq data also represent one of the minor issues. The authors focused on analyzing only development and immune systems, however, they do not report on any other significantly different changes in gene expression other …
Reviewer #2 (Public Review):
The various pathogenic, parasitic, symbiotic, and mutualistic interactions between insects and the microbes they interact with represents a rich area of research. This study by Xiao et al. represents a very interesting example of such a relationship. Overall the study is well designed and executed. The approach they utilize to test their hypothesis is valid and they combined both laboratory and field collected insects to address the question. The RNAseq analysis also provides potential insights into possible mechanisms by which the virus HaDV2 enables enhanced resistance to Bt Cry1Ac. The RNAseq data also represent one of the minor issues. The authors focused on analyzing only development and immune systems, however, they do not report on any other significantly different changes in gene expression other than reporting that there were 1573 significant differences. The authors should at least provide some holistic analysis and report the data in the supplemental results. Focusing on development and immune systems is valid and rationally supported but a complete analysis should be presented. The relationship between H. armigera and HaDV2 is more a mutualistic relationship, thus, the authors should consider changing the titles of the manuscript and the supplementary data. This is an exciting study and is well written and will be of general interest to the field.
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Reviewer #1 (Public Review):
Previous reports have provided evidence identifying infection of cotton bollworm with a densovirus as resulting in increased fitness. In the current manuscript, the relevance of this infection towards field resistance to transgenic Bt corn is evaluated by comparing its incidence between regions in China growing non-Bt versus Bt cotton. A clear correlation emerges with infection rates being higher in Bt versus non-Bt cotton growing areas, although its effect on resistance to Cry1Ac and Bt cotton is not as clear.
Strengths:
The manuscript presents evidence for the spread of densovirus infection in field bollworm populations, and that this spread seems to occur at a faster rate in areas of China where Bt cotton is grown versus non-Bt cotton areas. Life table comparisons clearly show increased fitness in …
Reviewer #1 (Public Review):
Previous reports have provided evidence identifying infection of cotton bollworm with a densovirus as resulting in increased fitness. In the current manuscript, the relevance of this infection towards field resistance to transgenic Bt corn is evaluated by comparing its incidence between regions in China growing non-Bt versus Bt cotton. A clear correlation emerges with infection rates being higher in Bt versus non-Bt cotton growing areas, although its effect on resistance to Cry1Ac and Bt cotton is not as clear.
Strengths:
The manuscript presents evidence for the spread of densovirus infection in field bollworm populations, and that this spread seems to occur at a faster rate in areas of China where Bt cotton is grown versus non-Bt cotton areas. Life table comparisons clearly show increased fitness in bollworms infected with the virus. The study capitalizes on availability of an impressive collection of samples with distinct geographic and historic origin to address relevant evolutionary questions.
Weaknesses:
The suggested role for densovirus infection in resistance to Cry1Ac and Bt cotton is supported by association and the data presented does not necessarily support causation. In fact, the confidence intervals in all the comparisons from bioassays overlap substantially and the resulting resistance ratio is not a good estimate of any significant differences the infection may have on ability to survive Cry1Ac. Infection by a virus is expected to activate the immune system, so the larvae used in bioassays should be considered as "primed" and the slight reduction in susceptibility should not be considered as an effect of the virus itself. The life table data clearly shows that fertility and fecundity are probably the most relevant aspects affecting fitness of infected insects. These differences in reproduction (even more than differences in larval growth) could explain why infection is rapidly spreading in the wild. However, most of the research and analyses are focused on the possibility that the viral infection may make the insects more able to survive Cry1Ac or Bt cotton. There are no conclusive data supporting this hypothesis in the current version, other than increased infection rates in Bt-cotton growing areas. This could be explained by effects on reproduction rather than enhanced survival. Related to this aspect, there should be a more clear distinction between the densovirus increasing fitness versus increasing resistance, the data supports the former but is not so clear in the later. It would be useful to provide a map detailing regions were moths were collected.
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Evaluation Summary:
This manuscript will be of interest to a broad audience of researchers interested in microbe-insect interactions and how they may affect adaptation to pesticides. It presents data supporting that infection with a mutualistic virus enhances fitness in a moth, and that selection pressure represented by transgenic crops may be driving the spread of this mutualistic infection in Chinese moth populations. Specificially, infection with a densovirus appears to improve the ability of the cotton bollworm to survive on transgenic cotton expressing insecticidal proteins from Bacillus thuringiensis (Bt). The widely-grown Bt-transgenic crops control insect pests with great reductions in chemical insecticides, and anything that could reduce their efficacy is of relevance to the agricultural biotechnology community and to growers. …
Evaluation Summary:
This manuscript will be of interest to a broad audience of researchers interested in microbe-insect interactions and how they may affect adaptation to pesticides. It presents data supporting that infection with a mutualistic virus enhances fitness in a moth, and that selection pressure represented by transgenic crops may be driving the spread of this mutualistic infection in Chinese moth populations. Specificially, infection with a densovirus appears to improve the ability of the cotton bollworm to survive on transgenic cotton expressing insecticidal proteins from Bacillus thuringiensis (Bt). The widely-grown Bt-transgenic crops control insect pests with great reductions in chemical insecticides, and anything that could reduce their efficacy is of relevance to the agricultural biotechnology community and to growers. This work suggests that virus infection of the insect pest can have unexpected interactions with the ongoing selection for Bt resistance that threatens the sustainability of Bt-transgenic crops. The impact of the work would be clearer if there was a better distinction between pest resistance (the evolution of increased tolerance due to genetic changes in the pest population) and other mechanisms of increased pest tolerance (e.g., virus infection).
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
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