Pink bollworm on (Bt) cotton: Spurious seed? Wrong gene? Evolution? Cultivation practices?

Keeping track of news on Bt cotton in India

Pectinophora gossypiella (pink bollworm) is one of the pests of cotton in India, but in the past >30 years has been less important than Helicoverpa armigera (American bollworm). Following sightings in 2010 on Bt cotton the incidence of this pest has been increasing, as described in by Dr Kanthi in this booklet on the pink bollworm. In December 2015, this came to a head with complete failure of the crop in Raichur district, Karnataka.

A team of experts looking into the failure concluded, probably correctly, that “It is clearly not the issue of seed adulteration.” They further concluded that it was due to “failure of Bt technology itself.” This is presumably based on the following: “When asked whether pink bollworm fell under Bt cotton seed producers’ pest-resistance claim-purview, Mr. Holalu showed the instruction manual supplied with Bt cotton seed packet and said that it did.”

It is not clear what experts meant by “pest-resistance claim,” but Monsanto (in their undated website) certainly states that Bollard II, containing two Bt genes, cry1Ac and cry2A confers protection against pink bollworm.

Perhaps the evolution of resistance in the pink bollworm is not so surprising a scenario, given that cry1A and cry2A  are known to be most effective against Heliothis, a common pest of cotton in America but not India, less effective against Helicoverpa, the most common pest in India, and least effective against Pectinophora. A study of the insects sampled in 2010-11 from Gujarat and MP (where resistance was observed) and Maharashtra (where it was not) showed clear genetic changes in a key protein, involved in the toxicity, that point to the mode of evolution of resistance.

Other than this factor, a complex set of agro-ecological factors contribute to selection pressure and the resurgence of the pink bollworm after an absence since the 1980’s should be seen in this light, according to Dr. Kanthi of CICR. These factors (long-duration hybrids, large number of hybrids with diverse flowering and fruiting periods, early sown-crops whose flowering period coincides with the peak of the insect’s life cycle, lack of refugia) lead to year-long persistence of the crop and insect, making possible build-up of resistance and outbreak of the disease. Apparently it is not just lack of refugia that contributes to evolution of resistant insects.

Major pests of cotton in India

Helicoverpa armigera (American boll worm)
Pectinophora gossypiella (pink boll worm)
Spodoptera litura (army worm)
Bemisia tabaci (white fly)

[Heliothis virescens (tobacco bud worm) a pest of the Americas; Bemisia not susceptible to Bt toxin]

Relative susceptibilities of cotton pests to Bt (Cry1A)

Lepidopterans are variably susceptible to Bt
Helicoverpa<Heliothis
Pectinophora<Helicoverpa
Spodoptera<Helicoverpa

i.e., Pectinophora<Helicoverpa<Heliothis (last not important in India)

Pink bollworm has evolved resistance in the field and in the laboratory is shown to evolve resistance to multiple toxins in crops engineered to produce more than one toxin.

Non-lepidopterans are not susceptible
Bemisia, Anthonomus

Variability of cotton pests to Bt (Cry1A)

High intraspecific variation [therefore likely to evolve resistance]
Helicoverpa, Spodoptera, Pectinophora

Low intraspecific variation
Heliothis

Sources:

2016. Mohan, K. S., Ravi, K. C., Suresh, P. J., Sumerford, D. & Head, G. P. Field resistance to the Bacillus thuringiensis protein Cry1Ac expressed in Bollgard® hybrid cotton in pink bollworm, Pectinophora gossypiella (Saunders), populations in India. Pest Manag. Sci. 72(4): 738–746. 10.1002/ps.4047 (2015)
2016. Nair, R., Kamath, S. P., Mohan, K. S., Head, G. & Sumerford, D. V. Inheritance of field-relevant resistance to the Bacillus thuringiensis protein Cry1Ac in Pectinophora gossypiella (Lepidoptera: Gelechiidae) collected from India. Pest Manag. Sci. 72(3): 558–565; 10.1002/ps.4023 (2015).
2015. Fabrick J. A. et al. Multi-toxin resistance enables pink bollworm survival on pyramided Bt cotton. Scientific Reports 5: 16554 doi:10.1038/srep16554
2014. Fabrick, J. A. et al. Alternative splicing and highly variable cadherin transcripts associated with field-evolved resistance of pink bollworm to Bt cotton in India. PLoS ONE 9(5), e97900. 10.1371/journal.pone.0097900.
2014. Ojha, A. et al. Analysis of resistance to Cry1Ac in field-collected pink bollworm, Pectinophora gossypiella (Lepidoptera:Gelechiidae), populations. GM Crops Food 5(4), 280–286.
2013. Tabashnik, B. E. Insect resistance to Bt crops: lessons from the first billion acres. Nature Biotechnology 31, 510–521 doi:10.1038/nbt.2597
2013. Choudhary, B. & Gaur, K. Bt Cotton in India: A Country Profile. ISAAA Series of Biotech Crop Profiles (ISAAA, Ithaca, NY).
2011. Dhurua, S. & Gujar, G. T. Field-evolved resistance to Bt toxin Cry1Ac in the pink bollworm, Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae), from India. Pest Manag. Sci. 67:898–903.
2010. Tabashnik B. E. and Carrière Y. Field-Evolved Resistance to Bt Cotton: Bollworm in the U.S. and Pink Bollworm in India. Southwestern Entomologist. 35(3):417-424 doi: 10.3958/059.035.0326
2000. Gujar, G. T., Kumari, A., Kalia, V., and Chandrashekar, K. Spatial and temporal variation in susceptibility of the American bollworm, Helicoverpa armigera (Huebner) to Bacillus thuringiensis var. kurstaki in India. Current Science 78:995-1001.
1999. de Maagd, R. A., Bosch, D., and Stiekema, W. Bacillus thuringiensis toxin mediated insect resistance in plants. Trends in Plant Science 4:9-13.
1999. Liu, Y-B, Tabashnik, B. E., Dennehy, T. J., Patin. A. L., Bartlett, A. C. Development time and resistance to Bt crops. Nature 400:519.
1999. Luttrell R. G, Wan L., Knighten K. J. Variation in susceptibility of noctuid (Lepidoptera) larvae attacking cotton and soybean to purified endotoxin proteins and commercial formulations of Bacillus thuringiensis. Economic Entomology 92:21-32.
1998. Adamczyk, J. J., Holloway, J. W., Church, G. E., Leonard, B. R., and Graves, J. B. Larval survival and development of the fall army worm (Lepidoptera : Noctuidae) on normal and transgenic cotton expressing the Bacillus thuringiensis CryIA(c) partial derivative-endotoxin. Journal of Economic Entomology 91:539-545.
1998. Chakrabarti, S. K., Mandaokar, A., Kumar, P. A., and Sharma, R. P. Efficacy of lepidopteran specific delta-endotoxins of Bacillus thuringiensis against Helicoverpa armigera. Journal of Invertebrate Pathology 72:336-7.
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