Dietary antioxidant vitamin C influences the evolutionary path of insecticide resistance in Drosophila melanogaster

Authors: HUANG, JINGFEI - Fujian Agriculture And Forest University; SUN, WEILIN - Michigan State University; SEONG, KEON - Michigan State University; MITTAPALLI, OMPRAKASH - Omics Services Inc; OJO, JAMES - Kwara State University; Coates, Brad; PAIGE, KEN - University Of Illinois; CLARK, JOHN - University Of Massachusetts, Amherst; PITTENDRIGH, BARRY - University Of Michigan

Submitted to: Pesticide Biochemistry and Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/9/2020
Publication Date: 6/12/2020
Citation: Huang, J., Sun, W., Seong, K.M., Mittapalli, O., Ojo, J., Coates, B.S., Paige, K.N., Clark, J.M., Pittendrigh, B.R. 2020. Dietary antioxidant vitamin C influences the evolutionary path of insecticide resistance in Drosophila melanogaster. Pesticide Biochemistry and Physiology. 168. Article 104631. https://doi.org/10.1016/j.pestbp.2020.104631.
DOI: https://doi.org/10.1016/j.pestbp.2020.104631

Interpretive Summary: Resistance to chemical insecticides among agricultural pest insect species has led to increased difficulties controlling damage to agricultural crops leading to reduced quantity, quality and profitability of farm outputs. Insecticide applications result in adaptive changes within insect populations, including the development of insecticide resistance. Low-dose exposures to chemical insecticides cause insect cells to generate reactive oxygen species. High levels of reactive oxygen species in turn lead to DNA damage and the accumulation of random changes. Interestingly, vitamin C can prevent cells from damage caused by reactive oxygen species. An ARS researcher and university collaborators used fruit flies to test the effect of vitamin C on the development of insecticide resistance following insecticide (DDT) exposure in the laboratory. Fruit flies were either fed vitamin C and exposed multiple times to the insecticide DDT, received no vitamin C but were exposed to DDT multiple times, or received no vitamin C and no DDT exposure. It was found that only fruit flies receiving no vitamin C and DDT exposure showed an increase in resistance, and vitamin C appeared to prevent resistance when flies were similarly exposed to DDT. The scientists then examined the DNA sequences of the fruit flies to look for changes. They found frequent exposure to DDT increased the number of DNA changes relative to insects not exposed to DDT. Interestingly, feeding the fruit flies vitamin C appeared to protect them from the changes caused by DDT. Although performed under laboratory conditions, this research may suggest that low-dose exposures in the environment may speed up the development of insecticide resistance within insect populations in the field, and antioxidants may prevent these changes by reducing the level of changes (damage) reactive oxygen species cause to DNA. This research is of interest to university, federal research, regulatory, and industry stakeholders interested in the sustainability of insecticide use for the control of insect populations, and will likely benefit producers by increasing the understanding of how insects adapt to current control technologies.

Technical Abstract: Herbivorous insects encounter a variety of toxic environmental substances, ranging from ingested plant defensive compounds to human-introduced insecticidal agents. Dietary antioxidants are known to reduce the negative physiological impacts of toxins in mammalian systems through amelioration of reactive oxygen–related cellular damage; however, the analogous impacts to insects caused by multigenerational exposure to pesticides and the effects on adaptive responses within insect populations were hitherto unknown. To begin to address these research gaps, we used Drosophila as a model system to explore adaptive phenotypic responses to dichlorodiphenyltrichloroethane (DDT) exposure in the presence of the dietary antioxidant vitamin C and to examine the structural genomic consequences of this exposure. DDT tolerance increased significantly among four replicates exposed to a low dose of DDT for 10 generations. In contrast, tolerance was lower among replicates exposed to low-dose DDT plus dietary vitamin C, vitamin C alone, and the untreated control. No significant differences were predicted in overall nucleotide substitution rates across the genome between any of the treatments. Despite this, Drosophila replicates exposed to low-dose DDT without vitamin C showed the highest number of synonymous and non-synonymous variants, followed by the DDT plus vitamin C and vitamin C treatments. This study demonstrates the potential role of diet (specifically, antioxidant intake) on adaptive genome responses, and thus on the evolution of pesticide tolerance within insect populations.