Cry1F Resistance in Fall Armyworm Spodoptera frugiperda: Single Gene versus Pyramided Bt Maize

Abstract

Evolution of insect resistance to transgenic crops containing Bacillus thuringiensis (Bt) genes is a serious threat to the sustainability of this technology. However, field resistance related to the reduced efficacy of Bt maize has not been documented in any lepidopteran pest in the mainland U.S. after 18 years of intensive Bt maize planting. Here we report compelling evidence of field resistance in the fall armyworm, Spodoptera frugiperda (J.E. Smith), to Cry1F maize (TC 3507) in the southeastern region of the U.S. An F2 screen showed a surprisingly high (0.293) Cry1F resistance allele frequency in a population collected in 2011 from non-Bt maize in south Florida. Field populations from non-Bt maize in 2012–2013 exhibited 18.8-fold to >85.4-fold resistance to purified Cry1F protein and those collected from unexpectedly damaged Bt maize plants at several locations in Florida and North Carolina had >85.4-fold resistance. In addition, reduced efficacy and control failure of Cry1F maize against natural populations of S. frugiperda were documented in field trials using Cry1F-based and pyramided Bt maize products in south Florida. The Cry1F-resistant S. frugiperda also showed a low level of cross-resistance to Cry1A.105 and related maize products, but not to Cry2Ab2 or Vip3A. The occurrence of Cry1F resistance in the U.S. mainland populations of S. frugiperda likely represents migration of insects from Puerto Rico, indicating the great challenges faced in achieving effective resistance management for long-distance migratory pests like S. frugiperda.

Bacterial Vegetative Insecticidal Proteins (Vip) from Entomopathogenic Bacteria

“…Cross-resistance to Vip3A has also been studied in two S. frugiperda Cry1F-resistant populations, one collected from Bt maize fields in Puerto Rico and the other collected from the southeast United States. Both populations were very susceptible to Vip3Aa, indicating the absence of cross-resistance between the Vip3Aa and Cry1F proteins (111,112). A study using a different Vip3A protein, Vip3Ac, showed that it was equally toxic to susceptible and Cry1Ac-resistant Trichoplusia ni (Lepidoptera: Noctuidae) strains (77).…”

Role of dispersal in resistance evolution and spread

“…frugiperda is a complicated case where the relative roles of spread of Bt resistance by migration or independent evolution in hotspots remains uncertain. Cry1F resistance was detected in Puerto Rico in 2006 [43], and has since been found in Brazil [44] and parts of Florida [45]. S. frugiperda is a strong migrant, and the spread of Cry1F resistance from Puerto Rico to Florida by dispersing adults is possible.…”

Field-Evolved Mode 1 Resistance of the Fall Armyworm to Transgenic Cry1Fa-Expressing Corn Associated with Reduced Cry1Fa Toxin Binding and Midgut Alkaline Phosphatase Expression

“…More specifically, high levels of S. frugiperda resistance to Bt corn event TC1507 in Puerto Rico represented the first case in a U.S. territory of practical resistance (7) in a lepidopteran pest resulting in withdrawal of the Bt crop event from the local market (5). Recent reports support the evolution of resistance to the Bt corn event TC1507 in S. frugiperda from Brazil (8) and suggest the possibility that Bt corn-resistant S. frugiperda strains may have migrated to the southeastern United States (9).…”