Abstract

Beneficial alleles that spread rapidly as an adaptation to a new environment are often associated with costs that reduce the fitness of the population in the original environment. Several species of insect pests have evolved resistance to Bacillus thuringiensis (Bt) toxins in the field, jeopardizing its future use. This has most commonly occurred through the alteration of insect midgut binding sites specific for Bt toxins. While fitness costs related to Bt resistance alleles have often been recorded, the mechanisms behind them have remained obscure. We asked whether evolved resistance to Bt alters dietary nutrient intake, and if reduced efficiency of converting ingested nutrients to body growth are associated with fitness costs and variation in susceptibility to Bt. We fed the cabbage looper Trichoplusia ni artificial diets differing in levels of dietary imbalance in two major macronutrients, protein and digestible carbohydrate. By comparing a Bt-resistant T. ni strain with a susceptible strain we found that the mechanism behind reduced pupal weights and growth rates associated with Bt-resistance in T. ni was reduced consumption rather than impaired conversion of ingested nutrients to growth. In fact, Bt-resistant T. ni showed more efficient conversion of nutrients than the susceptible strain under certain dietary conditions. Although increasing levels of dietary protein prior to Bt challenge had a positive effect on larval survival, the LC50 of the resistant strain decreased when fed high levels of excess protein, whereas the LC50 of the susceptible strain continued to rise. Our study demonstrates that examining the nutritional basis of fitness costs may help elucidate the mechanisms underpinning them.

Highlights

  • Repeated use of chemical insecticides, as well as several microbial insecticides, has resulted in the evolution of resistance in numerous insect species [1,2,3,4,5]

  • Bacillus thuringiensis (Bt)-S pupae weighed more than Bt-RU on the three most balanced dietary P:C ratios, but the mass of Bt-susceptible line (Bt-S) pupae decreased on the two extreme P:C ratio diets, resulting in similar masses for both lines

  • Greater efficiency of converting protein into bodily nitrogen on the most protein-rich diet was associated with a significant increase in mortality compared to more balanced diets when challenged with Bt

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Summary

Introduction

Repeated use of chemical insecticides, as well as several microbial insecticides, has resulted in the evolution of resistance in numerous insect species [1,2,3,4,5]. The mutations that confer resistance often reduce fitness in the absence of the insecticide [6,7,8,9,10]. The evolution and stability of resistance to microbial and chemical insecticides is believed to be strongly influenced by fitness costs [11,12]. Repeated exposure to Bt has placed strong selection pressure on its target herbivores, resulting in some instances in the evolution of resistance [3,5,14]. Fitness costs associated with resistance to Bt sprays or Bt toxins have been found in representatives from one family of Coleoptera (Chrysomelidae [16]) and Diptera (Culicidae [17]), and four families of Lepidoptera (Noctuidae [18,19], Plutellidae [20,21], Pyralidae [22], and Gelechiidae [23])

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