Hilda L. Collins

North Carolina State University

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Anthony M. Shelton

Children's Hospital of Oklahoma

Yun Zhao

East China Normal University

Elizabeth D. Earle

Cornell University

R. T. Roush

Pennsylvania State University

Neil I. Morrison

Oxitec (United Kingdom)

Michael Bolton

Our Lady of the Lake Children's Hospital

Jun Cao

Jiangsu University

Rick Roush

Pennsylvania State University

Stefan J. Long

Cornell University

David W. Onstad

Health Affairs

Cooperative Institutions

Cornell University

New York State Department of Agriculture and Markets

Oxitec (United Kingdom)

North Carolina State University

Agricultural Research Service

Chinese Academy of Agricultural Sciences

University of California, Davis

AgResearch

United States Department of Agriculture

Southern Research Station

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First Field Release of a Genetically Engineered, Self-Limiting Agricultural Pest Insect: Evaluating Its Potential for Future Crop Protection

Frontiers in Bioengineering and Biotechnology (2020)

Anthony M. Shelton Stefan J. Long Adam S. Walker Michael Bolton Hilda L. Collins

Alternative, biologically-based approaches for pest management are sorely needed and one approach is to use genetically engineered insects. Herein we describe a series of integrated field, laboratory and modeling studies with the diamondback moth, Plutella xylostella, a serious global pest of crucifers. A "self-limiting" strain of Plutella xylostella (OX4319L), genetically engineered to allow the production of male-only cohorts of moths for field releases, was developed as a novel approach to protect crucifer crops. Wild-type females that mate with these self-limiting males will not produce viable female progeny. Our previous greenhouse studies demonstrated that releases of OX4319L males lead to suppression of the target pest population and dilution of insecticide-resistance genes. We report results of the first open-field release of a non-irradiated, genetically engineered self-limiting strain of an agricultural pest insect. In a series of mark-release-recapture field studies with co-releases of adult OX4319L males and wild-type counterparts, the dispersal, persistence and field survival of each strain were measured in a 2.83 ha cabbage field. In most cases, no differences were detected in these parameters. Overall, 97.8% of the wild-type males and 95.4% of the OX4319L males recaptured dispersed <35 m from the release point. The predicted persistence did not differ between strains regardless of release rate. With 95% confidence, 75% of OX4319L males released at a rate of 1,500 could be expected to live between 3.5 and 5.4 days and 95% of these males could be expected to be detected within 25.8-34.9 m from the release point. Moth strain had no effect on field survival but release rate did. Collectively, these results suggest similar field behavior of OX4319L males compared to its wild-type counterpart. Laboratory studies revealed no differences in mating competitiveness or intrinsic growth rates between the strains and small differences in longevity. Using results from these studies, mathematical models were developed that indicate release of OX4319L males should offer efficacious pest management of P. xylostella. Further field studies are recommended to demonstrate the potential for this self-limiting P. xylostella to provide pest suppression and resistance management benefits, as was previously demonstrated in greenhouse studies.

Limiting

Crop Protection

Insect pest

Genetically engineered

10.3389/fbioe.2019.00482

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Citations (48)

Response to a Synthetic Pheromone Source by OX4319L, a Self-Limiting Diamondback Moth (Lepidoptera: Plutellidae) Strain, and Field Dispersal Characteristics of Its Progenitor Strain

bioRxiv (Cold Spring Harbor Laboratory) (2018)

Michael Bolton Hilda L. Collins Tracey Chapman Neil I. Morrison Stefan J. Long

The Diamondback Moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae), is a global pest that infests vegetable and field crops within the Brassica family. A genetically engineered strain of P. xylostella, OX4319L, carrying a self-limiting gene, has shown potential for managing P. xylostella populations, using sustained releases of OX4319L male moths. In order for such a strain to provide control, the transgenic individuals must exhibit attraction to female P. xylostella sex pheromone and adequate dispersal in the field. In this study, we tested these key traits. First, we compared the responses of the OX4319L male moths to a synthetic female sex pheromone source in wind tunnel trials to those of males from three other strains. We found that OX4319L males responded comparably to strains of non-engineered males, with all males flying upwind towards the pheromone source. Second, we used mark-release-recapture studies of a wildtype P. xylostella strain, from which the OX4319L strain was originally developed, to assess dispersal under field conditions. Released males were recaptured using both pheromone-baited and passive traps within a 2.83 ha circular cabbage field, with a recapture rate of 7.93 percent. Males were recaptured up to the boundary of the field at 95 m from the central release point. The median dispersal of males was 14 m. These results showed the progenitor strain of OX4319L retained its ability to disperse within a host field. The results of these experiments are discussed in relation to the potential for the effective use of engineered male-selecting P. xylostella strains under field conditions.

Plutellidae

Strain (injury)

Pink bollworm

10.1101/501924

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Citations (0)

DOES INTEGRATING A DIVERSITY, EQUITY, AND INCLUSION CURRICULUM INCREASE PEDIATRIC RESIDENTS’ CONFIDENCE IN TREATING PATIENTS FROM DIFFERENT BACKGROUNDS AT OUR LADY OF THE LAKE CHILDREN’S HOSPITAL?

Academic Pediatrics (2025)

Christina Abi Kheir Kyra Stepney Hilda L. Collins Christine L.M. Joseph Pramod Upadhyay

Equity

10.1016/j.acap.2024.102686

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Natural Enemies Delay Insect Resistance to Bt Crops

PLoS ONE (2014)

Xiaoxia Liu Chen Mao Hilda L. Collins David W. Onstad R. T. Roush

We investigated whether development of resistance to a Bt crop in the presence of a natural enemy would be slower than without the natural enemy and whether biological control, in conjunction with a Bt crop, could effectively suppress the pest population. Additionally, we investigated whether insecticide-sprayed refuges of non-Bt crops would delay or accelerate resistance to the Bt crop. We used a system of Bt broccoli expressing Cry1Ac, a population of the pest Plutella xylostella with a low frequency of individuals resistant to Cry1Ac and the insecticide spinosad, and a natural enemy, Coleomegilla maculata, to conduct experiments over multiple generations. The results demonstrated that after 6 generations P. xylostella populations were very low in the treatment containing C. maculata and unsprayed non-Bt refuge plants. Furthermore, resistance to Bt plants evolved significantly slower in this treatment. In contrast, Bt plants with no refuge were completely defoliated in treatments without C. maculata after 4–5 generations. In the treatment containing sprayed non-Bt refuge plants and C. maculata, the P. xylostella population was low, although the speed of resistance selection to Cry1Ac was significantly increased. These data demonstrate that natural enemies can delay resistance to Bt plants and have significant implications for integrated pest management (IPM) with Bt crops.

Cry1Ac

Bt Cotton

Bacillus thuringiensis

10.1371/journal.pone.0090366

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Citations (74)

Using field-evolved resistance to Cry1F maize in a lepidopteran pest to demonstrate no adverse effects of Cry1F on one of its major predators

Transgenic Research (2012)

Jun‐Ce Tian Hilda L. Collins Jörg Romeis Steven E. Naranjo Richard L. Hellmich

Spodoptera frugiperda (JE Smith) represents the first documented case of field-evolved resistance to a genetically engineered crop expressing an insecticidal protein from Bacillus thuringiensis (Bt). In this case it was Cry1F-expressing maize (Mycogen 2A517). The ladybird beetle, Coleomegilla maculata, is a common and abundant predator that suppresses pest populations in maize and many other cropping systems. Its larvae and adults are polyphagous, feeding on aphids, thrips, lepidopteran eggs and larvae, as well as plant tissues. Thus, C. maculata may be exposed to Bt proteins expressed in genetically engineered crops by several pathways. Using Cry1F-resistant S. frugiperda larvae as prey, we evaluated the potential impact of Cry1F-expressing maize on several fitness parameters of C. maculata over two generations. Using Cry1F resistant prey removed any potential prey-mediated effects. Duration of larval and pupal stages, adult weight and female fecundity of C. maculata were not different when they were fed resistant S. frugiperda larvae reared on either Bt or control maize leaves during both generations. ELISA and insect-sensitive bioassays showed C. maculata were exposed to bioactive Cry1F protein. The insecticidal protein had no effect on C. maculata larvae, even though larvae contained 20-32 ng of Cry1F/g by fresh weight. Over all, our results demonstrated that the Cry1F protein did not affect important fitness parameters of one of S. frugiperda's major predators and that Cry1F protein did not accumulate but was strongly diluted when transferred during trophic interactions.

Bacillus thuringiensis

Genetically modified maize

10.1007/s11248-012-9604-4

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Citations (37)

Effect of Insecticides and Plutella xylostella (Lepidoptera: Plutellidae) Genotype on a Predator and Parasitoid and Implications for the Evolution of Insecticide Resistance

Journal of Economic Entomology (2012)

Xiaoxia Liu Chen Mao Hilda L. Collins David W. Onstad Rick Roush

In the laboratory and in cages in the greenhouse, we evaluated the toxicity of two insecticides (lambda-cyhalothrin and spinosad) on the parasitoid, Diadegma insulare (Cresson), and the predator, Coleomegilla maculate (DeGeer), both natural enemies of the diamondback moth, Plutella xylostella (L.). Lambda-cyhalothrin was very toxic to both natural enemies. Spinosad was less toxic to C. maculata adults and larvae, and slightly toxic to D. insulare. Both natural enemies suppressed P. xylostella populations in cages with 80% spinosad-treated and 20% nontreated plants; such suppression was not seen when lambda-cyhalothrin was used. Using broccoli, Brassica oleracea L. variety italica, a common host for P. xylostella, we also studied direct and indirect effects of both natural enemies in the presence and absence of the two insecticides and to different P. xylostella genotypes: resistant to the insecticide, susceptible, or heterozygous. Neither natural enemy could distinguish host genotype if P. xylostella were feeding on nontreated plants. They could also not distinguish between larvae feeding on spinosad-treated plants and nontreated plants, but D. insulare could distinguish between larvae feeding on lambda-cyhalothrin treated and nontreated plants. Our studies suggest that lambda-cyhalothrin has direct toxicity to these two natural enemies, can affect their host foraging and acceptance of P. xylostella and consequently would not be compatible in conserving these natural enemies in a program for suppression of P. xylostella. In contrast, our studies suggest that treatment with spinosad has much less effect on these natural enemies and would allow them to help suppress populations of P. xylostella. These findings are discussed in relation to the evolution of insecticide resistance and suppression of the pest populations.

Plutellidae

Cyhalothrin

Indoxacarb

Bacillus thuringiensis

10.1603/ec11299

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Citations (19)

Monitoring and Characterization of Diamondback Moth (Lepidoptera: Plutellidae) Resistance to Spinosad

Journal of Economic Entomology (2002)

Yun Zhao Y. -X. Li Hilda L. Collins L. R. Gusukuma-Minuto Ronald F. L. Mau

Fourteen populations of the diamondback moth, Plutella xylostella (L.), were collected from fields of crucifer vegetables in the United States, Mexico, and Thailand in 1999 and 2000 for susceptibility tests with spinosad. Most populations were susceptible to spinosad and similar to earlier baseline values, but populations from Thailand and Hawaii showed high levels of tolerance. A statewide survey in Hawaii in 2000 and 2001 indicated resistance problems on several islands. One colony collected in October 2000 from Pearl City, HI, was subjected to further selection pressure, using spinosad in the laboratory, and then was used as the resistant strain (Pearl-Sel) for other tests. Spray tests using the recommended field rates of spinosad on potted broccoli plants in the greenhouse confirmed that field control failures due to resistance were possible in the areas of these collections. Analysis of probit lines from F1 reciprocal crosses between the Pearl-Sel and S strain indicated that resistance to spinosad was inherited autosomally and was incompletely recessive. A direct test of monogenic inheritance based on the F1 × Pearl-Sel backcrosses suggested that resistance to spinosad was probably controlled by one locus. The synergists S,S,S-tributyl phosphorotrithioate and piperonyl butoxide did not enhance the toxicity of spinosad to the resistant colony, indicating metabolic mediated detoxification was probably not responsible for the spinosad resistance. Two field colonies in Hawaii that were resistant to spinosad were not cross-resistant to emamectin benzoate or indoxacarb. Resistance developed in Hawaii due to the continuous cultivation of crucifers in which as many as 50 applications of spinosad per year may have been made to a common population of P. xylostella in sequential plantings, although each grower might have used the labeled restrictions for resistance management. Resistance management strategies will need to address such cropping and pest management practices.

Indoxacarb

Plutellidae

Piperonyl butoxide

Pesticide resistance

Chlorfenapyr

10.1603/0022-0493-95.2.430

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Citations (278)

Transgenic plants expressing two Bacillus thuringiensis toxins delay insect resistance evolution

Nature Biotechnology (2003)

Yun Zhao Jun Cao Yaxin Li Hilda L. Collins R. T. Roush

Bacillus thuringiensis

Cry1Ac

10.1038/nbt907

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Citations (417)

Examination of the F<SUB>2</SUB> Screen for Rare Resistance Alleles to <I>Bacillus thuringiensis</I> Toxins in the Diamondback Moth (Lepidoptera: Plutellidae)

Journal of Economic Entomology (2002)

Yun Zhao Yaxin Li Hilda L. Collins Anthony M. Shelton

Journal Article Examination of the F2 Screen for Rare Resistance Alleles to Bacillus thuringiensis Toxins in the Diamondback Moth (Lepidoptera: Plutellidae) Get access Jian-Zhou Zhao, Jian-Zhou Zhao Department of Entomology, Cornell University, New York State Agricultural Experiment Station, Geneva, NY 14456 Search for other works by this author on: Oxford Academic PubMed Google Scholar Ya-Xin Li, Ya-Xin Li Department of Entomology, Cornell University, New York State Agricultural Experiment Station, Geneva, NY 14456 Search for other works by this author on: Oxford Academic PubMed Google Scholar Hilda L. Collins, Hilda L. Collins Department of Entomology, Cornell University, New York State Agricultural Experiment Station, Geneva, NY 14456 Search for other works by this author on: Oxford Academic PubMed Google Scholar Anthony M. Shelton Anthony M. Shelton 1 Department of Entomology, Cornell University, New York State Agricultural Experiment Station, Geneva, NY 14456 1E-mail: ams5@cornell.edu. Search for other works by this author on: Oxford Academic PubMed Google Scholar Journal of Economic Entomology, Volume 95, Issue 1, 1 February 2002, Pages 14–21, https://doi.org/10.1603/0022-0493-95.1.14 Published: 01 February 2002

Plutellidae

Agricultural experiment station

Entomology

10.1603/0022-0493-95.1.14

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Citations (64)

Evaluation of foliar sprays for control of adult Diaprepes abbreviatus L. on Florida citrus.

The Journal of the Georgia Entomological Society (1976)

Hilda L. Collins C. L. Mangum D. E. Hendricks

Source

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Citations (1)