During the past decade the pesticidal bacterium Bacillus thuringiensis has been the subject of intensive research. These efforts have yielded considerable data about the complex relationships between the structure, mechanism of action, and genetics of the organism’s pesticidal crystal proteins, and a coherent picture of these relationships is beginning to emerge. Other studies have focused on the ecological role of the B. thuringiensis crystal proteins, their performance in agricultural and other natural settings, and the evolution of resistance mechanisms in target pests. Armed with this knowledge base and with the tools of modern biotechnology, researchers are now reporting promising results in engineering more-useful toxins and formulations, in creating transgenic plants that express pesticidal activity, and in constructing integrated management strategies to insure that these products are utilized with maximum efficiency and benefit.

Bacillus thuringiensis and Its Pesticidal Crystal Proteins

▪ Abstract This review examines potential impacts of transgenic cultivars on insect population dynamics and evolution. Experience with classically bred, insecticidal cultivars has demonstrated that a solid understanding of both the target insect's ecology and the cultivar's performance under varied field conditions will be essential for predicting area-wide effects of transgenic cultivars on pest and natural enemy dynamics. This experience has also demonstrated the evolutionary capacity of pests for adaptive response to insecticidal traits in crops. Biochemical and genetic studies of insect adaptation to the Bacillus thuringiensis (Bt) toxins expressed by currently marketed transgenic cultivars indicate a high risk for rapid adaptation if these cultivars are misused. Theoretical and practical issues involved in implementing strategies to delay pest adaptation to insecticidal cultivars are reviewed. Emphasis is placed on examining the “high dose”/refuge strategy that has become the goal of industry and reg...

Sustainability of Transgenic Insecticidal Cultivars: Integrating Pest Genetics and Ecology

In addition to altering global ecology, technology and human population growth also affect evolutionary trajectories, dramatically accelerating evolutionary change in other species, especially in commercially important, pest, and disease organisms. Such changes are apparent in antibiotic and human immunodeficiency virus (HIV) resistance to drugs, plant and insect resistance to pesticides, rapid changes in invasive species, life-history change in commercial fisheries, and pest adaptation to biological engineering products. This accelerated evolution costs at least $33 billion to $50 billion a year in the United States. Slowing and controlling arms races in disease and pest management have been successful in diverse ecological and economic systems, illustrating how applied evolutionary principles can help reduce the impact of human-kind on evolution.

https://science.sciencemag.org/content/sci/293/5536/1786.full.pdf

Humans as the World's Greatest Evolutionary Force

Insecticides derived from the common soil bacterium Bacillus thuringiensis (Bt) are becoming increasingly important for pest management. Insecticidal crystal proteins (also called 8-endotoxins) from Bt are extremely toxic to certain pests, yet cause little or no hann to humans, most beneficial insects, and other nontarget organisms (19, 40). After proteolytic activation in the insect midgut, Bt toxins bind to the brush border membrane of the midgut epithelium and create pores that cause cells to swell and lyse (55). Technical innovations, including expression of Bt toxin genes in transgenic crop plants and transgenic bacteria, should increase the usefulness of Bt (6, 12, 35, 46, 91, 94, 109, 116). At the same time, mounting concerns about environmental hazards and widespread resistance in pest populations are reducing the value of conventional synthetic insecticides. Because Bt had been used commercially for more than two decades without reports of substantial resistance development in open field popu­ lations, some scientists had presumed that evolution of resistance was unlikely (21, 89). However, resistance to Bt was documented recently in field populations of diamondback moth in Hawaii, the continental US, and Asia (36, 42, 92a, 128, 129, 131, 138, 146, 148, 151). These reports confirmed suspicions raised by the results of laboratory selection for resistance to Bt in several major pests (102, 104, 135). Scientists in industry, government, and academia now recognize evolution of resistance to Bt in pests as the greatest threat to the continued success of Bt (18, 44, 58, 59, lOla, 108). To delay or reverse resistance to Bt in pests, we must first understand

Evolution of Resistance to Bacillus Thuringiensis

Transgenic maize, Zea mays L., event TC1507 produces the Cry1F protein to provide protection from feeding by several important lepidopteran pests, including Spodoptera frugiperda (J.E. Smith) (Lepidoptera: Noctuidae). Reports of reduced field performance against this species in Puerto Rico were investigated, and laboratory bioassays showed that S. frugiperda collected from the affected area exhibited lower sensitivity to the Cry1F protein compared with typical colonies from other regions. The resistance was shown to be autosomally inherited and highly recessive. The Puerto Rico colony was shown to be moderately less sensitive than susceptible laboratory strains to Cry1Ab and Cry1Ac, but the differences in sensitivity were dramatically smaller than for Cry1F. Potential contributory factors to the emergence of resistance to Cry1F in Puerto Rico populations of S. frugiperda include the tropical island geography, unusually large population sizes in 2006, and drought conditions reducing the availability of alternative hosts. In response to this resistance incident, the technology providers have stopped commercial sales of TC1507 maize in Puerto Rico pending potential reversion to susceptibility.

https://bioone.org/journals/Journal-of-Economic-Entomology/volume-103/issue-4/EC10040/Discovery-and-Characterization-of-Field-Resistance-to-Bt-Maize/10.1603/EC10040.pdf

Discovery and Characterization of Field Resistance to Bt Maize: Spodoptera frugiperda (Lepidoptera: Noctuidae) in Puerto Rico

Transgenic crops expressing insecticidal toxins could soon provide safe, clean and effective means of pest control, but their usefulness will be short-lived if insects adapt to the toxins. Two planting strategies are among those that have been recommended to delay crop failure: susceptible insects could be conserved by planting either ‘refugia’, i.e. separate fields of toxic and toxin-free crop, or ‘seed mixtures’ of toxic and toxin-free plants in the same fields. However, we show that if insects can move from plant to plant, seed mixtures may actually hasten insect resistance compared with pure stands of toxic plants. Insect movement causes an increase in effective genetic dominance which can counteract reduced selection due to the mixture. This failure of seed mixtures is likely under just those conditions, low genetic dominance of resistance, which predict a good chance for resistance to the toxin to evolve slowly. Seed mixtures, unlike refugia, are therefore failure prone. This result also suggests potential problems with a third strategy, tissue-specific expression of toxins, which essentially provides a mixture of toxin-free and toxin-containing tissues on the same plant. However, better information and modelling are urgently required to evaluate alternative means of slowing insect adaptation to resistant crop plants. Legislation for toxinfree refugia may provide one of the best available means for conserving insect susceptibility.

Preventing Insect Adaptation to Insect-Resistant Crops: Are Seed Mixtures or Refugia the Best Strategy?

Abstract Speciation is the process through which reproductive isolation develops between distinct populations. Because this process takes time, speciation studies often necessarily examine populations within a species that are at various stages of divergence. The fall armyworm, Spodoptera frugiperda (J.E. Smith), is comprised of two strains (R = Rice & C = Corn) that serve as a novel system to explore population divergence in sympatry. Here, we use ddRADSeq data to show that fall armyworm strains in the field are largely genetically distinct, but some interstrain hybridization occurs. Although we detected F1 hybrids of both R‐ and C‐strain maternal origin, only hybrids with R‐strain mtDNA were found to contribute to subsequent generations, possibly indicating a unidirectional barrier to gene flow. Although these strains have been previously defined as “host plant‐associated,” we recovered an equal proportion of R‐ and C‐strain moths in fields dominated by C‐strain host plants. As an alternative to host‐associated divergence, we tested the hypothesis that differences in nightly activity patterns could account for reproductive isolation by genotyping temporally collected moths. Our data indicates that strains exhibit a significant shift in the timing of their nightly activities in the field. This divergence in phenology creates a prezygotic reproductive barrier that likely maintains the genetic isolation between strains. Thus, we conclude that it may be ecologically inaccurate to refer to the C‐ and R‐ strain as “host‐associated” and they should more appropriately be considered “allochronic strains.”

https://onlinelibrary.wiley.com/doi/pdfdirect/10.1002/ece3.8706

Patterns of genomic and allochronic strain divergence in the fall armyworm, Spodoptera frugiperda (J.E. Smith)

Transgenic corn and cotton that produce Cry and Vip3Aa toxins derived from Bacillus thuringiensis (Bt) are widely planted in the United States to control lepidopteran pests. The sustainability of these Bt crops is threatened because the corn earworm/bollworm, Helicoverpa zea (Boddie), is evolving a resistance to these toxins. Using Bt sweet corn as a sentinel plant to monitor the evolution of resistance, collaborators established 146 trials in twenty-five states and five Canadian provinces during 2020–2022. The study evaluated overall changes in the phenotypic frequency of resistance (the ratio of larval densities in Bt ears relative to densities in non-Bt ears) in H. zea populations and the range of resistance allele frequencies for Cry1Ab and Vip3Aa. The results revealed a widespread resistance to Cry1Ab, Cry2Ab2, and Cry1A.105 Cry toxins, with higher numbers of larvae surviving in Bt ears than in non-Bt ears at many trial locations. Depending on assumptions about the inheritance of resistance, allele frequencies for Cry1Ab ranged from 0.465 (dominant resistance) to 0.995 (recessive resistance). Although Vip3Aa provided high control efficacy against H. zea, the results show a notable increase in ear damage and a number of surviving older larvae, particularly at southern locations. Assuming recessive resistance, the estimated resistance allele frequencies for Vip3Aa ranged from 0.115 in the Gulf states to 0.032 at more northern locations. These findings indicate that better resistance management practices are urgently needed to sustain efficacy the of corn and cotton that produce Vip3Aa.

/pdf/extended-sentinel-monitoring-of-helicoverpa-zea-resistance-19jmx8xg.pdf

Extended Sentinel Monitoring of Helicoverpa zea Resistance to Cry and Vip3Aa Toxins in Bt Sweet Corn: Assessing Changes in Phenotypic and Allele Frequencies of Resistance

Patrick Porter

Papers

Preventing Insect Adaptation to Insect-Resistant Crops: Are Seed Mixtures or Refugia the Best Strategy?

Patterns of genomic and allochronic strain divergence in the fall armyworm, Spodoptera frugiperda (J.E. Smith)

Extended Sentinel Monitoring of Helicoverpa zea Resistance to Cry and Vip3Aa Toxins in Bt Sweet Corn: Assessing Changes in Phenotypic and Allele Frequencies of Resistance