Functional dominance of different aged larvae of Bt-resistant Spodoptera frugiperda (Lepidoptera: Noctuidae) on transgenic maize expressing Vip3Aa20 protein
Introduction
Transgenic maize (Zea mays L.) plants expressing vegetative insecticidal (Vip) proteins from Bacillus thuringiensis Berliner (Bt) were released for commercial use in Brazil in 2009 (CTNBio, 2009). A Vip protein is expressed in maize plants with MIR162 (expressing Vip3Aa20 protein) or Bt11 × MIR162 × GA21 (expressing Cry1Ab and Vip3Aa20 proteins and glyphosate-tolerant EPSP synthase) events and has fall armyworm (FAW), Spodoptera frugiperda (J. E. Smith) as one of the main target pests. FAW is considered the major pest of several important agricultural crops, mainly in Central and South American countries (Pogue, 2002). In Brazil, this species is the most destructive pest of maize, causing severe yield reduction that can reach 60% (Barros et al., 2010).
Once Bt maize became available, the main control strategy of FAW in maize has been the use of hybrids that express Bt proteins, which are currently cultivated on more than 80% of the maize-growing area in Brazil (Céleres, 2015). However, MIR162 and Bt11 × MIR162 × GA21 maize were used in less than 10% of the maize-growing area during the 2014–15 cropping season. Maize technologies expressing Bt proteins have been successful in controlling FAW (Okumura et al., 2013, Bernardi et al., 2015a). However, the continuous expression of insecticidal proteins in Bt plants imposes a strong selection pressure on target pest populations, favoring resistance evolution (McGaughey and Whalon, 1992). In Brazil, FAW has evolved resistance to Cry1F-maize (Farias et al., 2014) and to Cry1Ab-maize (Omoto et al., 2016). This species has also developed resistance to Cry1F maize in Puerto Rico (Storer et al., 2010), and some areas of the southeastern region of the mainland United States (Huang et al., 2014).
A strategy currently used to delay or prevent insect resistance evolution to Bt plants is the high-dose/refuge strategy (Tabashnik et al., 2009, Huang et al., 2011, Jin et al., 2015). The success of this strategy depends, among other factors, on the use of large structured refuge areas (Gould, 1994, Tabashnik et al., 2009). In the Brazilian crop production system, there is a low adoption of refuge areas. An alternative to the structured refuge strategy would be the use of seed mixes that contain non-Bt seeds (“refuge-in-a-bag”), thus transferring the responsibility of refuge implementation to the company providing the technology (Carroll et al., 2012). This ensures that a refuge will be present within every Bt crop field (Head et al., 2014).
The seed mix strategy assumes a recessive inheritance of resistance and that larval mobility of target insects is negligible (Mallet and Porter, 1992, Tabashnik, 1994, Carroll et al., 2012, Carrière et al., 2016). For the Vip3Aa20 protein, recessive inheritance was reported for a laboratory-selected strain of FAW (Bernardi et al., 2016). This species also exhibited significant larval dispersion among maize plants (Pannuti et al., 2016). This behavior can expose the target pests to sublethal doses of Bt proteins through initial feeding in the Bt plant and subsequent feeding in the non-Bt plant (Andow, 2008). In addition, several studies showed that susceptibility of target pests to Bt proteins decreases throughout larval development (Ashfaq et al., 2001, Walker et al., 2000, Li et al., 2006, Armstrong et al., 2011). In this context, to optimize resistance management strategies, we evaluated the functional dominance of different aged larvae of Bt-resistant Spodoptera frugiperda in Bt maize expressing Vip3Aa20 protein.
Section snippets
FAW strains
A Vip3Aa20-resistant colony of FAW (called Vip-R) was selected from positive F2 tests (containing resistance alleles) using a field population collected in Correntina, Bahia, Brazil, as described in details by Bernardi et al. (2015b). After selection, the Vip-R strain was reared for nine generations from neonate to third instar in leaves of MIR162 maize (expressing Vip3Aa20 protein) and transferred to an artificial diet (Kasten et al., 1978), where they remained until the pupal stage (Bernardi
Results
No significant interactions between Bt maize and FAW strain for larval survival, number of pupae, adults, and neonate-to-adult period were detected (Table 1). There were also no significant effects of Bt maize on larval survival, number of pupae, adults, and neonate-to-adult period of FAW strains (Table 1). In contrast, FAW strains showed significant differences in larval survival, number of pupae and adults when fed in Bt maize; however, the neonate-to-adult period was similar among strains (
Discussion
The Vip-R strain of FAW showed high larval survival at different ages in MIR162 and Bt11 × MIR162 × GA21 maize, producing high number of adults. In contrast, few surviving larvae in fifth and sixth instars from heterozygote and Sus strains completed the life cycle feeding on these Bt maize plants. This is indicative that a short exposure of FAW larvae from heterozygote and Sus strains on Vip3Aa20 maize was sufficient to produce a high development arrestment, suggesting that this species in
Acknowledgments
We thank the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (Project number 2011/22743-0) for a postdoctoral scholarship to O.B., Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (Project number 475748/2011-5) for partial financial support, and Syngenta for providing maize seeds.
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