Dominance and fitness costs of insect resistance to genetically modified Bacillus thuringiensis crops

Abstract

Evolution of resistance to genetically modified Bacillus thuringiensis (Bt) crops in pest populations is a major threat to the sustainability of the technology. Incidents of field resistance that have led to control problems of Bt crops or significantly reduced susceptibility of individual Bt proteins in pyramided plants have increased dramatically across the world, especially in recent years. Analysis of globally published data showed that 61.5% and 60.0% of the cases of resistance with major alleles that allowed homozygous resistant genotypes to survival on Bt crops were functionally non-recessive and did not involve fitness costs, respectively. Dominance levels (D FL s) measured on Bt plants ranged from −0.02 to 1.56 with a mean (± sem) of 0.35 ± 0.13 for the 13 cases of single-gene resistance to Bt plants that have been evaluated. Among these, all six cases with field control problems were functionally non-recessive with a mean D FL of 0.63 ± 0.24, which was significantly greater than the D FL (0.11 ± 0.07) of the seven cases without field resistance. In addition, index of fitness costs (IFC) of major resistance was calculated for each case based on the fitness of resistant (R’R’) and heterozygous (R’S’) genotypes on non-Bt plants divided by the fitness of their susceptible (S’S’) counterparts. The estimated IFCs for 15 cases of single-gene resistance were similar for R’R’ and R’S’, and for the cases with and without field resistance; and the values averaged 1.10 ± 0.12 for R’R’ and 1.20 ± 0.18 for R’S’. Limited published data suggest that resistance of insects to dual/multiple-gene Bt crops is likely to be more recessive than the related single-gene resistance, but their IFCs are similar. The quantitative analysis of the global data documents that the prevalence of non-recessive resistance has played an essential role in the widespread evolution of resistance to Bt crops, while the lack of fitness costs is apparently not as critical as the non-recessive resistance. The results suggest that planting of ‘high dose’ traits is an effective method for Bt crop IRM and more comprehensive management strategies that are also effective for functionally non-recessive resistance should be deployed.

Varied frequencies of resistance alleles to Cry1Ab and Cry1Ac among Brazilian populations of the sugarcane borer, Diatraea saccharalis (F.)

“…Published data have shown that nonrecessive resistance to Bt crops was common. 22 In particular, three previous studies have reported that a Cry1Ab resistance in D. saccharalis on Bt maize was nonrecessive with a dominance level ranging from 0.17 to 0.65. [55][56][57] Additional studies to measure the dominance levels of the Cry1Ab and Cry1Ac resistance in D. saccharalis on Bt sugarcane have been planned, and data generated from the proposed study should reveal the reasons that caused the high survival rates of PPLs in the F 2 screen.…”

“…More likely, the observed high survival rates in the F 2 screen were due to nonrecessive resistance associated with RAs that could allow some RS individuals also to survive in the screen. Published data have shown that nonrecessive resistance to Bt crops was common 22 . In particular, three previous studies have reported that a Cry1Ab resistance in D. saccharalis on Bt maize was nonrecessive with a dominance level ranging from 0.17 to 0.65 55–57 .…”

“…20 Lessons from the use of Bt maize and cotton have provided clear evidence that implementation of effective insect resistance management (IRM) plans is critical to delay the evolution of resistance. [20][21][22] IRM application relies on effective resistance monitoring that can provide information in early changes in the resistance allele frequency (RAF) in insect pest populations. [23][24][25] A phenotypic method called F 2 screen, 23 which can identify heterozygous genotypes in field insect populations, has been widely adopted to detect Bt resistance alleles (RAs) in pest populations.…”

Inheritance of Resistance to Cry1A.105 in Helicoverpa zea (Boddie) (Lepidoptera: Noctuidae)

“…In addition, Yang et al [ 20 ] reported that the D ML of a Texas Cry2Ab2-resistant population varied from incompletely dominant to incompletely recessive at selected concentrations from 1.0 to 31.6 µg/cm 2 , and the resistance was functionally dominant on Cry1Ab/Cry2Ae cotton leaf tissues. A recent analysis of globally published data showed that all six cases of practical resistance to Bt crops, where dominance levels on Bt plants had been evaluated, were associated with functionally nonrecessive resistance [ 25 ]. The functionally nonrecessive nature of the resistance to Cry1A.105 and Cry2Ab2 in H. zea observed here and by Yang et al [ 20 ] suggests that Bt maize-producing Cry1A.105 and Cry2Ab2 likely does not produce a ‘high dose’ for either of these toxins.…”

“…There was a concern that the genetic background of BZ-SS could be different from that of Cry1A.105-RR. Crosses between insect populations with different genetic backgrounds that are not related to the Bt resistance might cause hybrid vigor that could confound the assessment of Bt resistance [ 25 ]. Thus, in Test-II, to ensure a similar genetic background among the insect populations to be evaluated, the original Cry1A.105-RR was crossed and backcrossed with BZ-SS.…”