Yves Carriere

Interests

Research

Landscape Ecology for IPM; Resistance management for Bt crops; Environmental impacts of Bt crops; Insect Ecology

Teaching

Insect EcologyAgroEcology

Courses

Scholarly Contributions

Journals/Publications

• Carriere, Y., Degain, B., & Tabashnik, B. (2021). Effects of gene flow between Bt and non-Bt plants in a seed mixture of Cry1A.105 + Cry2Ab corn on performance of corn earworm in Arizona.. Pest Management Science, 77, 2106–2113.
• Fabrick, J. A., LeRoy, D. M., Mathew, L. G., Wu, Y., Unnithan, G. C., Yelich, A. J., Carrière, Y., Li, X., & Tabashnik, B. E. (2021). CRISPR-mediated mutations in the ABC transporter gene ABCA2 confer pink bollworm resistance to Bt toxin Cry2Ab. Scientific reports, 11(1), 10377.
  More info

  Crops genetically engineered to produce insecticidal proteins from Bacillus thuringiensis (Bt) have many benefits and are important globally for managing insect pests. However, the evolution of pest resistance to Bt crops reduces their benefits. Understanding the genetic basis of such resistance is needed to better monitor, manage, and counter pest resistance to Bt crops. Previous work shows that resistance to Bt toxin Cry2Ab is associated with mutations in the gene encoding the ATP-binding cassette protein ABCA2 in lab- and field-selected populations of the pink bollworm (Pectinophora gossypiella), one of the world's most destructive pests of cotton. Here we used CRISPR/Cas9 gene editing to test the hypothesis that mutations in the pink bollworm gene encoding ABCA2 (PgABCA2) can cause resistance to Cry2Ab. Consistent with this hypothesis, introduction of disruptive mutations in PgABCA2 in a susceptible strain of pink bollworm increased the frequency of resistance to Cry2Ab and facilitated creation of a Cry2Ab-resistant strain. All Cry2Ab-resistant individuals tested in this study had disruptive mutations in PgABCA2. Overall, we found 17 different disruptive mutations in PgABCA2 gDNA and 26 in PgABCA2 cDNA, including novel mutations corresponding precisely to single-guide (sgRNA) sites used for CRISPR/Cas9. Together with previous results, these findings provide the first case of practical resistance to Cry2Ab where evidence identifies a specific gene in which disruptive mutations can cause resistance and are associated with resistance in field-selected populations.
• Harrington, K., Carrière, Y., & Mostafa, A. M. (2021). Re-evaluating the Economic Injury Level for Alfalfa Weevil (Coleoptera: Curculionidae) Control in Low Desert Irrigated Alfalfa. Journal of economic entomology, 114(3), 1173-1179.
  More info

  Alfalfa (Medicago sativa L.) dominates cropping systems in the Western United States and is first in terms of acreage planted in Arizona. The alfalfa weevil, Hypera postica (Gylenhall) and/or Hypera brunneipennis (Boheman), respectively, is the most destructive pest in terms of yield loss in low desert-grown alfalfa hay. The current economic threshold of 15-20 larvae per sweep, established in California in 1975, is currently not suitable or adopted by growers in the western U.S. low desert. Here, we conducted 4 yr of field trials to re-evaluate this economic threshold. Supporting observations of agricultural growers and professionals in the region, our results indicate that the economic threshold established in 1975 is too high. Specifically, one to three large larvae often cause a significant decrease in yield justifying weevil control based on current hay prices and costs of insecticide application. These results are discussed in the context of sustainable alfalfa production in the western U.S. low desert.
• Tabashnik, B. E., Liesner, L. R., Ellsworth, P. C., Unnithan, G. C., Fabrick, J. A., Naranjo, S. E., Li, X., Dennehy, T. J., Antilla, L., Staten, R. T., & Carrière, Y. (2021). Transgenic cotton and sterile insect releases synergize eradication of pink bollworm a century after it invaded the United States. Proceedings of the National Academy of Sciences of the United States of America, 118(1).
  More info

  Invasive organisms pose a global threat and are exceptionally difficult to eradicate after they become abundant in their new habitats. We report a successful multitactic strategy for combating the pink bollworm (), one of the world's most invasive pests. A coordinated program in the southwestern United States and northern Mexico included releases of billions of sterile pink bollworm moths from airplanes and planting of cotton engineered to produce insecticidal proteins from the bacterium (Bt). An analysis of computer simulations and 21 y of field data from Arizona demonstrate that the transgenic Bt cotton and sterile insect releases interacted synergistically to reduce the pest's population size. In Arizona, the program started in 2006 and decreased the pest's estimated statewide population size from over 2 billion in 2005 to zero in 2013. Complementary regional efforts eradicated this pest throughout the cotton-growing areas of the continental United States and northern Mexico a century after it had invaded both countries. The removal of this pest saved farmers in the United States $192 million from 2014 to 2019. It also eliminated the environmental and safety hazards associated with insecticide sprays that had previously targeted the pink bollworm and facilitated an 82% reduction in insecticides used against all cotton pests in Arizona. The economic and social benefits achieved demonstrate the advantages of using agricultural biotechnology in concert with classical pest control tactics.
• Van den Berg, J., Prasanna, B. M., Midega, C. A., Ronald, P. C., Carrière, Y., & Tabashnik, B. E. (2021). Managing Fall Armyworm in Africa: Can Bt Maize Sustainably Improve Control?. Journal of economic entomology, 114(5), 1934-1949.
  More info

  The recent invasion of Africa by fall armyworm, Spodoptera frugiperda, a lepidopteran pest of maize and other crops, has heightened concerns about food security for millions of smallholder farmers. Maize genetically engineered to produce insecticidal proteins from the bacterium Bacillus thuringiensis (Bt) is a potentially useful tool for controlling fall armyworm and other lepidopteran pests of maize in Africa. In the Americas, however, fall armyworm rapidly evolved practical resistance to maize producing one Bt toxin (Cry1Ab or Cry1Fa). Also, aside from South Africa, Bt maize has not been approved for cultivation in Africa, where stakeholders in each nation will make decisions about its deployment. In the context of Africa, we address maize production and use; fall armyworm distribution, host range, and impact; fall armyworm control tactics other than Bt maize; and strategies to make Bt maize more sustainable and accessible to smallholders. We recommend mandated refuges of non-Bt maize or other non-Bt host plants of at least 50% of total maize hectares for single-toxin Bt maize and 20% for Bt maize producing two or more distinct toxins that are each highly effective against fall armyworm. The smallholder practices of planting more than one maize cultivar and intercropping maize with other fall armyworm host plants could facilitate compliance. We also propose creating and providing smallholder farmers access to Bt maize that produces four distinct Bt toxins encoded by linked genes in a single transgene cassette. Using this novel Bt maize as one component of integrated pest management could sustainably improve control of lepidopteran pests including fall armyworm.
• Carrière, Y., Brown, Z., Aglasan, S., Dutilleul, P., Carroll, M., Head, G., Tabashnik, B. E., Jørgensen, P. S., & Carroll, S. P. (2020). Crop rotation mitigates impacts of corn rootworm resistance to transgenic Bt corn. Proceedings of the National Academy of Sciences of the United States of America, 117(31), 18385-18392.
  More info

  Transgenic crops that produce insecticidal proteins from (Bt) can suppress pests and reduce insecticide sprays, but their efficacy is reduced when pests evolve resistance. Although farmers plant refuges of non-Bt host plants to delay pest resistance, this tactic has not been sufficient against the western corn rootworm, In the United States, some populations of this devastating pest have rapidly evolved practical resistance to Cry3 toxins and Cry34/35Ab, the only Bt toxins in commercially available corn that kill rootworms. Here, we analyzed data from 2011 to 2016 on Bt corn fields producing Cry3Bb alone that were severely damaged by this pest in 25 crop-reporting districts of Illinois, Iowa, and Minnesota. The annual mean frequency of these problem fields was 29 fields (range 7 to 70) per million acres of Cry3Bb corn in 2011 to 2013, with a cost of $163 to $227 per damaged acre. The frequency of problem fields declined by 92% in 2014 to 2016 relative to 2011 to 2013 and was negatively associated with rotation of corn with soybean. The effectiveness of corn rotation for mitigating Bt resistance problems did not differ significantly between crop-reporting districts with versus without prevalent rotation-resistant rootworm populations. In some analyses, the frequency of problem fields was positively associated with planting of Cry3 corn and negatively associated with planting of Bt corn producing both a Cry3 toxin and Cry34/35Ab. The results highlight the central role of crop rotation for mitigating impacts of resistance to Bt corn.
• Carrière, Y., Degain, B. A., & Tabashnik, B. E. (2020). Effects of gene flow between Bt and non-Bt plants in a seed mixture of Cry1A.105 + Cry2Ab corn on performance of corn earworm in Arizona. Pest management science.
  More info

  Using natural populations of Helicoverpa zea from Arizona, we tested the hypotheses that gene flow between Bt and non-Bt plants in a seed mixture of 10% non-Bt corn and 90% Bt corn producing Cry1A.105 and Cry2Ab reduces larval performance on ears from non-Bt plants, or increases performance on ears from Bt plants.
• Carrière, Y., Degain, B. A., Harpold, V. S., Unnithan, G. C., & Tabashnik, B. E. (2020). Gene Flow Between Bt and Non-Bt Plants in a Seed Mixture Increases Dominance of Resistance to Pyramided Bt Corn in Helicoverpa zea (Lepidoptera: Noctuidae). Journal of economic entomology, 113(5), 2041-2051.
  More info

  For delaying evolution of pest resistance to transgenic corn producing Bacillus thuringiensis (Bt) toxins, limited data are available to compare the effectiveness of refuges of non-Bt corn planted in seed mixtures versus blocks. Here we addressed this issue in the ear-feeding pest Helicoverpa zea Boddie by measuring its survival and development in the laboratory on ears from field plots with 90% Cry1A.105 + Cry2Ab corn and 10% non-Bt corn planted in a seed mixture or blocks. We compared a strain of H. zea selected for resistance to Cry1Ac in the laboratory, its parent strain not selected in the laboratory, and their F1 progeny. The relative survival of the F1 progeny and dominance of resistance were higher on ears from Bt plants in the seed mixture than the block. Half of the kernels in ears from non-Bt plants in the seed mixture produced both Cry1A.105 and Cry2Ab. However, survival on ears from non-Bt plants did not differ between the block and seed mixture. In simulations based on the observed survival, resistance to Cry1A.105 + Cry2Ab corn evolved faster with the seed mixture than the blocks, because of the higher dominance of resistance in the seed mixture. Increasing the refuge percentage improved durability of Cry1A.105 + Cry2Ab corn more for the blocks than the seed mixture. These findings imply that, for a given percentage of non-Bt corn, resistance of H. zea and other ear-feeding pests to multi-toxin Bt corn is likely to evolve faster for seed mixtures than blocks.
• Comeau, G., Zinna, R. A., Scott, T., Ernst, K., Walker, K., Carrière, Y., & Riehle, M. A. (2020). Vertical Transmission of Zika Virus in Produces Potentially Infectious Progeny. The American journal of tropical medicine and hygiene, 103(2), 876-883.
  More info

  Vertical transmission, or pathogen transfer from female to offspring, can facilitate the persistence of emerging arboviruses, such as Zika virus (ZIKV), through periods of low horizontal transmission or adverse environmental conditions. We aimed at determining the rate of vertical transmission for ZIKV in its principal vector, , and the vector competence of vertically infected progeny. females that consumed a blood meal provisioned with ZIKV were maintained under three temperature conditions (27°C, 30°C, and 33°C) following the infectious blood meal and allowed to complete three reproductive cycles. The overall vertical transmission rate was 6.5% (95% CI = 3.9-9.9). Vertical transmission of ZIKV was observed across all temperature conditions and virus detected in adult progeny up to 2 weeks postemergence. In total, 3.4% (95% CI = 1.6-6.2) of adult progeny produced saliva with ZIKV, indicating their vector competence. These results suggest the virus may be maintained in populations without a vertebrate host for short periods.
• Comeau, G., Zinna, R., Carriere, Y., Ernst, K. C., Walker, K. R., & Riehle, M. A. (2020). Impact of Zika virus vertical transmission in the mosquito Aedes aegypti. American Journal of Tropical Medicine and Hygiene, 103(2), 876-883. doi:10.4269/ajtmh.19-0698
• Fabrick, J. A., LeRoy, D. M., Unnithan, G. C., Yelich, A. J., Carrière, Y., Li, X., & Tabashnik, B. E. (2020). Shared and Independent Genetic Basis of Resistance to Bt Toxin Cry2Ab in Two Strains of Pink Bollworm. Scientific reports, 10(1), 7988.
  More info

  Evolution of pest resistance threatens the benefits of crops genetically engineered to produce insecticidal proteins from Bacillus thuringiensis (Bt). Field populations of the pink bollworm (Pectinophora gossypiella), a global pest of cotton, have evolved practical resistance to transgenic cotton producing Bt toxin Cry2Ab in India, but not in the United States. Previous results show that recessive mutations disrupting an autosomal ATP-binding cassette gene (PgABCA2) are associated with pink bollworm resistance to Cry2Ab in field-selected populations from India and in one lab-selected strain from the United States (Bt4-R2). Here we discovered that an independently derived, lab-selected Cry2Ab-resistant pink bollworm strain from the United States (BX-R) also harbors mutations that disrupt PgABCA2. Premature stop codons introduced by mis-splicing of PgABCA2 pre-mRNA were prevalent in field-selected larvae from India and in both lab-selected strains. The most common mutation in field-selected larvae from India was also detected in both lab-selected strains. Results from interstrain crosses indicate BX-R has at least one additional mechanism of resistance to Cry2Ab that does not involve PgABCA2 and is not completely recessive or autosomal. We conclude that recessive mutations disrupting PgABCA2 are the primary, but not the only, mechanism of resistance to Cry2Ab in pink bollworm.
• Fritz, M. L., Nunziata, S. O., Guo, R., Tabashnik, B. E., & Carrière, Y. (2020). Mutations in a Novel Cadherin Gene Associated with Bt Resistance in. G3 (Bethesda, Md.), 10(5), 1563-1574.
  More info

  Transgenic corn and cotton produce crystalline (Cry) proteins derived from the soil bacterium (Bt) that are toxic to lepidopteran larvae. , a key pest of corn and cotton in the U.S., has evolved widespread resistance to these proteins produced in Bt corn and cotton. While the genomic targets of Cry selection and the mutations that produce resistant phenotypes are known in other lepidopteran species, little is known about how selection by Cry proteins shape the genome of We scanned the genomes of Cry1Ac-selected and unselected lines, and identified twelve genes on five scaffolds that differed between lines, including (), a gene from a family that is involved in Cry1A resistance in other lepidopterans. Although this gene was expressed in the larval midgut, the protein it encodes has only 17 to 22% identity with cadherin proteins from other species previously reported to be involved in Bt resistance. An analysis of midgut-expressed cDNAs showed significant between-line differences in the frequencies of putative nonsynonymous substitutions (both SNPs and indels). Our results indicate that is a likely target of Cry1Ac selection in It remains unclear, however, whether genomic changes at this locus directly disrupt midgut binding of Cry1Ac and cause Bt resistance, or indirectly enhance fitness of in the presence of Cry1Ac by some other mechanism. Future work should investigate phenotypic effects of these nonsynonymous substitutions and their impact on fitness of larvae that ingest Cry1Ac.
• Jeff, F., & Carriere, Y. (2020). Reduced cadherin expression associated with resistance to Bt toxin Cry1Ac in pink bollworm.. Pest Management Science, 76, 67-74..
• Sherbrooke, S., Carrière, Y., & Palumbo, J. C. (2020). Evaluation of Trap Cropping for Control of Diamondback Moth (Lepidoptera: Plutellidae) in a Broccoli Production System. Journal of economic entomology, 113(4), 1864-1871.
  More info

  Trap cropping, in which a trap crop is planted near a cash crop, has been used successfully for reducing pest damage in some agricultural systems. We used a meta-analysis of extensive data on two trap cropping systems, diamondback moth, Plutella xylostella (Linnaeus), exploiting cabbage and Chilo partellus (Swinhoe) (Lepidoptera: Crambidae) exploiting maize, to show that oviposition preference for, and high larval mortality on trap crops are important indicators of effectiveness of trap cropping systems. We then evaluated Indian mustard (Brassica juncea var. juncea L. Czern.) (Capparidales: Brassicaceae) and yellow rocket (Barbarea vulgaris W. T. Aiton) (Brassicales: Brassicaceae) as trap crops for protecting broccoli (Brassica oleracea var. italica Plenck) (Capparidales: Brassicaceae) against diamondback moth in Yuma, AZ, using planting configurations compatible with current practices for commercial production and without use of insecticides. In oviposition choice tests, both yellow rocket and Indian mustard were highly preferred over broccoli in the field. Furthermore, the number of larvae and pupae was significantly lower on yellow rocket and Indian mustard compared to broccoli, indicating relatively high mortality on these trap crops. Nevertheless, during the fall and spring growing seasons, no significant differences in the number of individuals on broccoli or proportion of broccoli crowns infested at harvest occurred between plots with trap crops relative to plots exclusively planted to broccoli. Thus, with the plant density and planting patterns used and without use of insecticides, there was no evidence that trap cropping was effective for reducing diamondback moth infestation of broccoli.
• Søgaard Jørgensen, P., & Carriere, Y. (2020). Coevolutionary governance of antibiotic and pesticide resistance.. Trends in Ecology and Evolution, 35, 484-494..
• Tabashnik, B., & Carriere, Y. (2020). Evaluating cross-resistance between Vip and Cry Toxins of Bacillus thuringiensis.. Journal of Economic Entomology., 113:, 553-561..
• Carriere, Y., & al, e. (2019). Gossypol in cottonseed increases the fitness cost of resistance to Bt cotton in pink bollworm. Crop Protection.
• Carrière, Y., Brown, Z. S., Downes, S. J., Gujar, G., Epstein, G., Omoto, C., Storer, N. P., Mota-Sanchez, D., Søgaard Jørgensen, P., & Carroll, S. P. (2019). Governing evolution: A socioecological comparison of resistance management for insecticidal transgenic Bt crops among four countries. Ambio, 49(1), 1-16.
  More info

  Cooperative management of pest susceptibility to transgenic Bacillus thuringiensis (Bt) crops is pursued worldwide in a variety of forms and to varying degrees of success depending on context. We examine this context using a comparative socioecological analysis of resistance management in Australia, Brazil, India, and the United States. We find that a shared understanding of resistance risks among government regulators, growers, and other actors is critical for effective governance. Furthermore, monitoring of grower compliance with resistance management requirements, surveillance of resistance, and mechanisms to support rapid implementation of remedial actions are essential to achieve desirable outcomes. Mandated resistance management measures, strong coordination between actors, and direct linkages between the group that appraises resistance risks and growers also appear to enhance prospects for effective governance. Our analysis highlights factors that could improve current governance systems and inform other initiatives to conserve susceptibility as a contribution to the cause of public good.
• Carrière, Y., Degain, B., Unnithan, G. C., Harpold, V. S., Li, X., & Tabashnik, B. E. (2019). Seasonal Declines in Cry1Ac and Cry2Ab Concentration in Maturing Cotton Favor Faster Evolution of Resistance to Pyramided Bt Cotton in Helicoverpa zea (Lepidoptera: Noctuidae). Journal of economic entomology, 112(6), 2907-2914.
  More info

  Under ideal conditions, widely adopted transgenic crop pyramids producing two or more distinct insecticidal proteins from Bacillus thuringiensis (Bt) that kill the same pest can substantially delay evolution of resistance by pests. However, deviations from ideal conditions diminish the advantages of such pyramids. Here, we tested the hypothesis that changes in maturing cotton producing Cry1Ac and Cry2Ab affect evolution of resistance in Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae), a pest with low inherent susceptibility to both toxins. In terminal leaves of field-grown Bt cotton, the concentration of both toxins was significantly higher for young, squaring plants than for old, fruiting plants. We used laboratory bioassays with plant material from field-grown cotton to test H. zea larvae from a strain selected for resistance to Cry1Ac in the laboratory, its more susceptible parent strain, and their F1 progeny. On young Bt cotton, no individuals survived to pupation. On old Bt cotton, survival to pupation was significantly higher for the lab-selected strain and the F1 progeny relative to the unselected parent strain, indicating dominant inheritance of resistance. Redundant killing, the extent to which insects resistant to one toxin are killed by another toxin in a pyramid, was complete on young Bt cotton, but not on old Bt cotton. No significant fitness costs associated with resistance were detected on young or old non-Bt cotton. Incorporation of empirical data into simulations indicates the observed increased selection for resistance on old Bt cotton could accelerate evolution of resistance to cotton producing Cry1Ac and Cry2Ab in H. zea.
• Fabrick, J. A., Mathew, L. G., LeRoy, D. M., Hull, J. J., Unnithan, G. C., Yelich, A. J., Carrière, Y., Li, X., & Tabashnik, B. E. (2019). Reduced cadherin expression associated with resistance to Bt toxin Cry1Ac in pink bollworm. Pest management science, 76(1), 67-74.
  More info

  Better understanding of the molecular basis of resistance is needed to improve management of pest resistance to transgenic crops that produce insecticidal proteins from Bacillus thuringiensis (Bt). Here we analyzed resistance of the pink bollworm (Pectinophora gossypiella) to Bt toxin Cry1Ac, which is used widely in transgenic Bt cotton. Field-evolved practical resistance of pink bollworm to Cry1Ac is widespread in India, but not in China or the United States. Previous work with laboratory- and field-selected pink bollworm indicated that resistance to Cry1Ac is caused by changes in the amino acid sequence of a midgut cadherin protein (PgCad1) that binds Cry1Ac in susceptible larvae.
• Li, S., Hussain, F., Unnithan, G. C., Dong, S., UlAbdin, Z., Gu, S., Mathew, L. G., Fabrick, J. A., Ni, X., Carrière, Y., Tabashnik, B. E., & Li, X. (2019). A long non-coding RNA regulates cadherin transcription and susceptibility to Bt toxin Cry1Ac in pink bollworm, Pectinophora gossypiella. Pesticide biochemistry and physiology, 158, 54-60.
  More info

  Extensive planting of transgenic crops producing insecticidal proteins from the bacterium Bacillus thuringiensis (Bt) has spurred increasingly rapid evolution of resistance in pests. In the pink bollworm, Pectinophora gossypiella, a devastating global pest, resistance to Bt toxin Cry1Ac produced by transgenic cotton is linked with mutations in a gene (PgCad1) encoding a cadherin protein that binds Cry1Ac in the larval midgut. We previously reported a long non-coding RNA (lncRNA) in intron 20 of cadherin alleles associated with both resistance and susceptibility to Cry1Ac. Here we tested the hypothesis that reducing expression of this lncRNA decreases transcription of PgCad1 and susceptibility to Cry1Ac. Quantitative RT-PCR showed that feeding susceptible neonates small interfering RNAs (siRNAs) targeting this lncRNA but not PgCad1 decreased the abundance of transcripts of both the lncRNA and PgCad1. Moreover, neonates fed the siRNAs had lower susceptibility to Cry1Ac. The results imply that the lncRNA increases transcription of PgCad1 and susceptibility of pink bollworm to Cry1Ac. The results suggest that disruption of lncRNA expression could be a novel mechanism of pest resistance to Bt toxins.
• Tabashnik, B. E., & Carrière, Y. (2019). Evaluating Cross-resistance Between Vip and Cry Toxins of Bacillus thuringiensis. Journal of economic entomology.
  More info

  Crops genetically engineered to produce insecticidal proteins from the bacterium Bacillus thuringiensis (Bt) have revolutionized control of some major pests. Some recently introduced Bt crops make Vip3Aa, a vegetative insecticidal protein (Vip), which reportedly does not share binding sites or structural homology with the crystalline (Cry) proteins of Bt used widely in transgenic crops for more than two decades. Field-evolved resistance to Bt crops with practical consequences for pest control includes 21 cases that collectively reduce the efficacy of nine Cry proteins, but such practical resistance has not been reported yet for any Vip. Here, we review previously published data to evaluate cross-resistance between Vip and Cry toxins. We analyzed 31 cases based on 48 observations, with each case based on one to five observations assessing cross-resistance from pairwise comparisons between 21 resistant strains and 13 related susceptible strains of eight species of lepidopteran pests. Confirming results from previous analyses of smaller data sets, we found weak, statistically significant cross-resistance between Vip3 and Cry1 toxins, with a mean of 1.5-fold cross-resistance in 21 cases (range: 0.30-4.6-fold). Conversely, we did not detect significant positive cross-resistance between Vip3 toxins and Cry2Ab. Distinguishing between weak, significant cross-resistance, and no cross-resistance may be useful for better understanding mechanisms of resistance and effectively managing pest resistance to Bt crops.
• Tabashnik, B. E., & Carrière, Y. (2019). Global Patterns of Resistance to Bt Crops Highlighting Pink Bollworm in the United States, China, and India. Journal of economic entomology, 112(6), 2513-2523.
  More info

  Crops genetically engineered to produce insecticidal proteins from Bacillus thuringiensis (Bt) have advanced pest control, but their benefits have been reduced by evolution of resistance in pests. The global monitoring data reviewed here reveal 19 cases of practical resistance to Bt crops, which is field-evolved resistance that reduces Bt crop efficacy and has practical consequences for pest control. Each case represents the responses of one pest species in one country to one Bt toxin. The results with pink bollworm (Pectinophora gossypiella) and Bt cotton differ strikingly among the world's three leading cotton-producing nations. In the southwestern United States, farmers delayed resistance by planting non-Bt cotton refuges from 1996 to 2005, then cooperated in a program that used Bt cotton, mass releases of sterile moths, and other tactics to eradicate this pest from the region. In China, farmers reversed low levels of pink bollworm resistance to Bt cotton by planting second-generation hybrid seeds from crosses between Bt and non-Bt cotton. This approach yields a refuge of 25% non-Bt cotton plants randomly interspersed within fields of Bt cotton. Farmers adopted this tactic voluntarily and unknowingly, not to manage resistance, but apparently because of its perceived short-term agronomic and economic benefits. In India, where non-Bt cotton refuges have been scarce and pink bollworm resistance to pyramided Bt cotton producing Cry1Ac and Cry2Ab toxins is widespread, integrated pest management emphasizing shortening of the cotton season, destruction of crop residues, and other tactics is now essential.
• Zhang, M., & al., e. (2019). Decreased Cry1Ac activation by midgut proteases is associated with Cry1Ac resistance in Helicoverpa zea.. Pest Management Science, 75, 1099-1106.
• Carrière, Y., Degain, B. A., Unnithan, G. C., Harpold, V. S., Heuberger, S., Li, X., & Tabashnik, B. E. (2018). Effects of seasonal changes in cotton plants on the evolution of resistance to pyramided cotton producing the Bt toxins Cry1Ac and Cry1F in Helicoverpa zea. Pest management science, 74(3), 627-637.
  More info

  In pests with inherently low susceptibility to Bacillus thuringiensis (Bt) toxins, seasonal declines in the concentration of Bt toxins in transgenic crops could accelerate evolution of resistance by increasing the dominance of resistance. Here, we evaluated Helicoverpa zea survival on young and old cotton plants that produced the Bt toxins Cry1Ac and Cry1F or did not produce Bt toxins.
• Carrière, Y., Williams, J. L., Crowder, D. W., & Tabashnik, B. E. (2018). Genotype-specific fitness cost of resistance to Bt toxin Cry1Ac in pink bollworm. Pest management science, 74(11), 2496-2503.
  More info

  To improve resistance management strategies for Bacillus thuringiensis (Bt) crops, a better understanding of the relative fitness of pest genotypes with resistance alleles in the absence of Bt toxins is needed. Here, we evaluated the impact of costs of resistance to Bt toxin Cry1Ac on the relative fitness of specific pink bollworm (Pectinophora gossypiella) genotypes. We created two heterogeneous strains with an intermediate frequency of mutant cadherin alleles linked with resistance to Cry1Ac, reared the strains on diet without Bt and tracked the decline in frequency of resistant genotypes for 15-30 generations using polymerase chain reaction amplification. We used a population genetics model and sensitivity analyses to estimate the relative fitness of resistant genotypes.
• Jørgensen, P. S., & (21 authors), e. a. (2018). Antibiotic and pesticide susceptibility and the Anthropocene operating space. Nature Sustainability, 1, 632–641. doi:https://doi.org/10.1038/s41893-018-0164-3
  More info

  Rising levels of antimicrobial and pesticide resistance increasingly undermine human health and systems for biomass production, and emphasize the sustainability challenge of preserving organisms susceptible to these biocides. In this Review, we introduce key concepts and examine dynamics of biocide susceptibility that must be governed to address this challenge. We focus on the impact of biocides on the capacity of susceptible organisms to prevent spread of resistance, and we then review how biocide use affects a broader suite of ecosystem services. Finally, we introduce and assess the state of what we term the Anthropocene operating space of biocide susceptibility, a framework for assessing the potential of antibiotic and pesticide resistance to undermine key functions of human society. Based on current trends in antibiotic, insecticide and herbicide resistance, we conclude that the states of all six assessed variables are beyond safe zones, with three variables surpassed regionally or globally.
• Karp, D. S., Chaplin-Kramer, R., Meehan, T. D., Martin, E. A., DeClerck, F., Grab, H., Gratton, C., Hunt, L., Larsen, A. E., Martínez-Salinas, A., O'Rourke, M. E., Rusch, A., Poveda, K., Jonsson, M., Rosenheim, J. A., Schellhorn, N. A., Tscharntke, T., Wratten, S. D., Zhang, W., , Iverson, A. L., et al. (2018). Crop pests and predators exhibit inconsistent responses to surrounding landscape composition. Proceedings of the National Academy of Sciences of the United States of America, 115(33), E7863-E7870.
  More info

  The idea that noncrop habitat enhances pest control and represents a win-win opportunity to conserve biodiversity and bolster yields has emerged as an agroecological paradigm. However, while noncrop habitat in landscapes surrounding farms sometimes benefits pest predators, natural enemy responses remain heterogeneous across studies and effects on pests are inconclusive. The observed heterogeneity in species responses to noncrop habitat may be biological in origin or could result from variation in how habitat and biocontrol are measured. Here, we use a pest-control database encompassing 132 studies and 6,759 sites worldwide to model natural enemy and pest abundances, predation rates, and crop damage as a function of landscape composition. Our results showed that although landscape composition explained significant variation within studies, pest and enemy abundances, predation rates, crop damage, and yields each exhibited different responses across studies, sometimes increasing and sometimes decreasing in landscapes with more noncrop habitat but overall showing no consistent trend. Thus, models that used landscape-composition variables to predict pest-control dynamics demonstrated little potential to explain variation across studies, though prediction did improve when comparing studies with similar crop and landscape features. Overall, our work shows that surrounding noncrop habitat does not consistently improve pest management, meaning habitat conservation may bolster production in some systems and depress yields in others. Future efforts to develop tools that inform farmers when habitat conservation truly represents a win-win would benefit from increased understanding of how landscape effects are modulated by local farm management and the biology of pests and their enemies.
• Mathew, L. G., Ponnuraj, J., Mallappa, B., Chowdary, L. R., Zhang, J., Tay, W. T., Walsh, T. K., Gordon, K. H., Heckel, D. G., Downes, S., Carrière, Y., Li, X., Tabashnik, B. E., & Fabrick, J. A. (2018). ABC transporter mis-splicing associated with resistance to Bt toxin Cry2Ab in laboratory- and field-selected pink bollworm. Scientific reports, 8(1), 13531.
  More info

  Evolution of pest resistance threatens the benefits of genetically engineered crops that produce Bacillus thuringiensis (Bt) insecticidal proteins. Strategies intended to delay pest resistance are most effective when implemented proactively. Accordingly, researchers have selected for and analyzed resistance to Bt toxins in many laboratory strains of pests before resistance evolves in the field, but the utility of this approach depends on the largely untested assumption that laboratory- and field-selected resistance to Bt toxins are similar. Here we compared the genetic basis of resistance to Bt toxin Cry2Ab, which is widely deployed in transgenic crops, between laboratory- and field-selected populations of the pink bollworm (Pectinophora gossypiella), a global pest of cotton. We discovered that resistance to Cry2Ab is associated with mutations disrupting the same ATP-binding cassette transporter gene (PgABCA2) in a laboratory-selected strain from Arizona, USA, and in field-selected populations from India. The most common mutation, loss of exon 6 caused by alternative splicing, occurred in resistant larvae from both locations. Together with previous data, the results imply that mutations in the same gene confer Bt resistance in laboratory- and field-selected strains and suggest that focusing on ABCA2 genes may help to accelerate progress in monitoring and managing resistance to Cry2Ab.
• Moore Brusca, W., Carriere, Y., Smith, R. L., Papaj, D. R., Davidowitz, G., & Schaller, J. (2018). Molecular phylogeny, ecology and multispecies aggregation behaviour of bombardier beetles in Arizona. PLoS ONE, 13(10), e0205192.
• Schaller, J. C., Davidowitz, G., Papaj, D. R., Smith, R. L., Carrière, Y., & Moore, W. (2018). Molecular phylogeny, ecology and multispecies aggregation behaviour of bombardier beetles in Arizona. PloS one, 13(10), e0205192.
  More info

  Aggregations of conspecific animals are common and have been documented in most phyla. Multispecies aggregations are less common and less well studied. Eight species of Brachinus beetles -famous for their unique, highly effective, chemical defense-regularly settle together form large diurnal multispecies aggregations in dark, moist areas in riparian habitats in the Sonoran Desert Region. Here, we document these multispecies aggregations and investigate the incidence and dynamics of aggregation behavior. Analysis of species composition of 59 field-collected aggregations revealed that 71% contained more than one species, eight species regularly co-occurred in aggregations, and no two species showed a preference to aggregate with one another. We provide the first phylogenetic analyses of participants in multispecies aggregations, and find that Brachinus species found together in aggregations are not each other's closest relatives but rather are dispersed throughout the phylogeny of the genus. Further, we find no tendency for species to aggregate with close relatives more frequently than distant relatives. Laboratory experiments on B. elongatulus showed that it chose to settle in occupied shelters over empty shelters. Experiments with B. hirsutus and B. elongatulus showed that B. hirsutus prefers to settle under shelters housing heterospecifics over conspecifics. Our findings suggest that these multispecies aggregations do not form by chance, but rather are initiated by a genus-wide aggregation cue associated with the presence of individuals already in a shelter, which is likely to be chemical and potentially tactile in nature.
• Vandervoet, T. F., Ellsworth, P. C., Carrière, Y., & Naranjo, S. E. (2018). Quantifying Conservation Biological Control for Management of Bemisia tabaci (Hemiptera: Aleyrodidae) in Cotton. Journal of economic entomology, 111(3), 1056-1068.
  More info

  Conservation biological control can be an effective tactic for minimizing insect-induced damage to agricultural production. In the Arizona cotton system, a suite of generalist arthropod predators provides critical regulation of Bemisia tabaci Gennadius (MEAM1) (Hemiptera: Aleyrodidae) and other pests. Arthropod predator and B. tabaci populations were manipulated with a range of broad-spectrum and selective insecticide exclusions to vary predator to prey interactions in a 2-yr field study. Predator to prey ratios associated with B. tabaci densities near the existing action threshold were estimated for six predator species found to be negatively associated with either adult and/or large nymphs of B. tabaci [Misumenops celer (Hentz) (Araneae: Thomisidae), Drapetis nr divergens (Diptera: Empididae), Geocoris pallens Stäl (Hemiptera: Geocoridae), Orius tristicolor (White) (Hemiptera: Anthocoridae), Chrysoperla carnea s.l. (Neuroptera: Chrysopidae), and Collops spp. (Coleoptera: Melyridae)] with the first three most consistently associated with declining B. tabaci densities. Ratios ranged from 1 M. celer per 100 sweeps to 1 B. tabaci adult per leaf to 44 D. nr. divergens per 100 sweeps to 1 large nymph per leaf disk. These ratios represent biological control informed thresholds that might serve as simple-to-use decision tool for reducing risk in the current B. tabaci integrated pest management strategy. The identification of key predators within the large, flexible food web of the cotton agro-ecosystem and estimation of predator to B. tabaci ratios clarifies the role of key predators in B. tabaci suppression, yielding potential decision-making advantages that could contribute to further improving economic and environmental sustainability of insect management in the cotton system.
• Walker, K. R., Williamson, D., Carrière, Y., Reyes-Castro, P. A., Haenchen, S., Hayden, M. H., Jeffrey Gutierrez, E., & Ernst, K. C. (2018). Socioeconomic and Human Behavioral Factors Associated With Aedes aegypti (Diptera: Culicidae) Immature Habitat in Tucson, AZ. Journal of medical entomology, 55(4), 955-963.
  More info

  Aedes aegypti (L.; Diptera: Culicidae) has been established in the southwestern United States for several decades, but relationships between humans and mosquitoes in this arid region are not well-characterized. In August 2012, the outdoor premises of 355 houses within 20 neighborhoods in Tucson, Arizona were surveyed for containers that could provide larval habitat for Ae. aegypti mosquitoes. At the same time, a knowledge, attitudes and practices (KAP) questionnaire was administered to a resident of each house surveyed for immature mosquitoes. The KAP questionnaire assessed respondents' knowledge and concerns about vector-borne illnesses as well as practices they used to avoid mosquitoes. Of the houses surveyed, 91% had at least one container present, and 64% had at least one container with standing water. On average, each house had 2.2 containers with water at the time of the survey. The overall House Index (proportion of premises surveyed with at least one container with Ae. aegypti immatures present) was 13%. Based on questionnaire responses, there was a significant positive association between the number of residents in the home and the odds of finding Ae. aegypti positive containers on the premises, while household income showed a significant negative association. The reported frequency of checking for standing water was also significantly associated with the odds of finding immatures, although the nature of this association was ambiguous. Flower pots were the principal type of container with Ae. aegypti larvae. These findings show that larval habitat is widely available even in an arid environment and city with good housing and sanitation infrastructure.
• Zhang, M., Wei, J., Ni, X., Zhang, J., Jurat-Fuentes, J. L., Fabrick, J. A., Carrière, Y., Tabashnik, B. E., & Li, X. (2018). Decreased Cry1Ac activation by midgut proteases associated with Cry1Ac resistance in Helicoverpa zea. Pest management science.
  More info

  Field-evolved resistance of Helicoverpa zea to Bacillus thuringiensis (Bt) toxin Cry1Ac was first reported more than a decade ago, yet the underlying mechanisms remain elusive. Towards understanding the mechanisms of resistance to Cry1Ac, we analyzed a susceptible (LAB-S) and two resistant (GA and GA-R) strains of H. zea. The GA strain was derived from Georgia and exposed to Bt toxins only in the field. The GA-R strain was derived from the GA strain and selected for increased resistance to Cry1Ac in the laboratory.
• Orpet, R. J., Degain, B. A., Tabashnik, B. E., & Carriere, Y. (2015). Effects of dietary protein to carbohydrate ratio on Bt toxicity and fitness costs of resistance in Helicoverpa zea.. Entomol. Exp. Appl., 156, 28-36.
• Palumbo, J. C., & Carriere, Y. (2015). Association between Bagrada hilaris density and feeding damage in broccoli: Implications for pest management. Plant Health Progress, 16, 158-162. doi:doi:10.1094/PHP-RS-15-0024
• Carriere, Y. -., Nolte, K. D., Marsh, S. E., Degain, B., Hartfield, K. A., Ellers-Kirk, C., Dutilleul, L. P., van Leeuwen, W. J., & Palumbo, J. C. (2014). Assessing Transmission of Crop Diseases by Insect Vectors in a Landscape Context. Journal of Economic Entomology, 107(1), 10.

Presentations

• Carriere, Y. (2020, Fall). Plant-Insect Ecosystems (P-IE) Lifetime Achievement Award in Entomology. ESA Anual Meeting.
  More info

  Bruce E. Tabashnik has been awarded the Plant-Insect Ecosystems (P-IE) Lifetime Achievement Award in Entomology. During this presentation, I summarize Bruce’s lifetime accomplishments.
• Carriere, Y., & Tabashnik, B. (2019, November). Promises and Pitfalls of Bt Crop Pyramids for Managing Pest Resistance. ESA Annual meeting. St-Louis: ESA.
  More info

  Invited to present at ESA Member symposium “Population Genetics and Pest Control: Advocating a Leading Role for Entomologists.”
• Fabrick, J., Li, X., Carriere, Y., & Tabashnik, B. (2019, January). CRISPR/Cas9 gene editing confirms the function of a Bacillus thuringiensis resistance receptor gene. XXVIII Plant & Animal Genomics Conference. San Diego.
  More info

  Invited to present at workshop
• Carriere, Y., Tabashnik, B., Leisner, L., & Staten, B. (2018, November). Extreme resistance management: Eradication of Pink bollworm in the US and Northern Mexico.. ESA symposium. Vancouver..
• Dixon, W. A., Carriere, Y., Palumbo, J. C., Fournier, A. J., & Ellsworth, P. C. (2018, November). Proactive Resistance Management: Can We Predict, and Ultimately Delay, Resistance Development in Whiteflies Across the Agricultural Landscape?. IRAC Symposium: Impact of Borders on Managing Insect Resistance Management, Entomological Society of America Annual Meeting. Vancouver, British Columbia, Canada: USDA-National Institute of Food and Agriculture.
• Ellsworth, P., Fournier, A., Palumbo, J., Carriere, Y., Dixon, W., & Pier, N. (2018, November). Proactive resistance management: Can we predict, and ultimately delay, resistance development in whiteflies across the agricultural landscape?. ESA Symposium. Vancouver.
• Tabashnik, B., & Carriere, Y. (2018, November). Global surge in pest resistance to Bt crops and prospects for sustainability.. ESA symposium.. Vancouver..
• Carriere, Y. -., & Tabashnik, B. E. (2013, November). Invited symposium presentation: Landscape-based approach for sustaining efficacy of Bt crops (coauthor). Annual Meeting of the Entomological Society of America.
• Ellsworth, P. C., Li, X. -., Carriere, Y. -., Brown, L., & Nichols, R. L. (2013, March). Cotton Pest Management Research Update: Resistance & Resistance Management. Southwest Ag Summit. Arizona Western College, Yuma, AZ: 2013 Southwest Ag Summit.
  More info

  30 participants. 0.5 AZ CEU, 0.5 CA CEU, 0.5 CCA CEU
• Ellsworth, P. C., Palumbo, J. C., Carriere, Y. -., Fournier, A. J., & Dixon, W. A. (2013, August). Appropriate Use of Your Data? Mapping Chemical Use Patterns. Arizona Pest Management Center Pesticide Use Database Advisory Committee. Yuma, AZ: Arizona Pest Management Center.
  More info

  12 participants
• Ellsworth, P. C., Palumbo, J. C., Carriere, Y. -., Fournier, A. J., & Dixon, W. A. (2013, September). Chemical Use Data & Resistance. Useful?. Late Summer La Paz County Agronomic Workshop. Elks Lodge, Parker, AZ: University of Arizona Cooperative Extension.
  More info

  1 AZ CEU; 30 participants
• Tabashnik, B. E., & Carriere, Y. -. (2013, November). Invited syposium presentation: Where and why resistance management has and hasn't succeeded for Bt crops (speaker). Annual Meeting of the Entomological Society of America.

Poster Presentations

• Riehle, M. A., Joy, T., Ernst, K. C., Gouge, D. H., Carriere, Y., & Walker, K. R. (2020, November). How old is that mosquito? Age grading Aedes aegypti in the desert Southwest.. ESA National Meeting. Virtual.
• Ellsworth, P. C., Prabhaker, N. P., Castle, S. J., Brown, L. M., Dixon, W. A., Carriere, Y. P., Palumbo, J. C., Fournier, A. J., & Naomi, P. (2018, March). Adoption of Proactive Resistance Management Practices to Control Bemisia Tabaci in Arizona and California. 9th International IPM Symposium. Baltimore, MD: USDA-National Instituted of Food and Agriculture.
• Walker, K. R., Ernst, K. C., Joy, T., Reyes-Castro, P., Carriere, Y., Castro, L., Diaz-Cervantes, R., Gameros, M., Hayden, M., Monaghan, A., Haenchen, S., Guttierez-Jeffrey, E., & Riehle, M. A. (2015, September). Exploring differential emergence of dengue in two cities with established Aedes aegypti populations: A case study in Sonora, Mexico. 2015 Annual Meeting of the Society for Vector Ecology. Albuquerque, NM.