Life-History Traits of Spodoptera frugiperda Populations Exposed to Low-Dose Bt Maize

Abstract

Exposure to Bacillus thuringiensis (Bt) toxins in low- and moderate-dose transgenic crops may induce sublethal effects and increase the rate of Bt resistance evolution, potentially compromising control efficacy against target pests. We tested this hypothesis using the fall armyworm Spodoptera frugiperda, a major polyphagous lepidopteran pest relatively tolerant to Bt notorious for evolving field-relevant resistance to single-gene Bt maize. Late-instar larvae were collected from Bt Cry1Ab and non-Bt maize fields in five locations in Brazil, and their offspring was compared for survival, development, and population growth in rearing environment without and with Cry1Ab throughout larval development. Larval survival on Cry1Ab maize leaves varied from 20 to 80% among the populations. Larvae reared on Cry1Ab maize had seven-day delay in development time in relation to control larvae, and such delay was shorter in offspring of armyworms from Cry1Ab maize. Population growth rates were 50-70% lower for insects continuously exposed to Cry1Ab maize relative to controls, showing the population-level effect of Cry1Ab, which varied among the populations and prior exposure to Cry1Ab maize in the field. In three out of five populations, armyworms derived from Bt maize reared on Cry1Ab maize showed higher larval weight, faster larval development and better reproductive performance than the armyworms derived from non-Bt maize, and one of these populations showed better performance on both Cry1Ab and control diets, indicating no fitness cost of the resistance trait. Altogether, these results indicate that offspring of armyworms that developed on field-grown, single-gene Bt Cry1Ab maize had reduced performance on Cry1Ab maize foliage in two populations studied, but in other three populations, these offspring had better overall performance on the Bt maize foliage than that of the armyworms from non-Bt maize fields, possibly because of Cry1Ab resistance alleles in these populations. Implications of these findings for resistance management of S. frugiperda in Bt crops are discussed.

Fig 1. Sampling sites of the field populations of the fall armyworm, Spodoptera frugiperda.

Shown is the graphical representation of Minas Gerais state, Brazil, with the locations of the counties where fall armyworms were collected. Eugenio E. Oliveira, co-author of this work, made the figure himself using a vector graphics editor. The authors are not aware of any previous copyrights on this figure, and it does not contain any proprietary data.

Fig 2. Survival rates for larvae of Spodoptera frugiperda from five populations chronically exposed to Cry1Ab throughout larval development.

Insects were collected from conventional non-Bt (black bars) or Cry1Ab maize fields (grays bars) and their progeny reared on leaves of non-Bt isoline or Bt Cry1Ab maize in the laboratory. Survival on Cry1Ab maize foliage was adjusted (normalized) for natural mortality on non-Cry1Ab isoline (control) maize. A) Survival at 48h. B) Survival to adulthood. Means ± standard errors with the same line do not differ (P > 0.05) by Fisher’s protected Least Significant Difference procedure. Asterisk indicates significant difference (P < 0.05) between insects from Cry1Ab or non-Bt (conventional) maize fields.

Fig 3. Survival plots of five populations of Spodoptera frugiperda chronically exposed to Bt Cry1Ab maize throughout larval development.

Insects were collected from conventional (non-Bt) or Cry1Ab maize fields and their progeny reared on leaves of non-Bt maize (i.e., control diet) or Bt Cry1Ab maize (i.e., Cry1Ab diet) in the laboratory. Survival curves that do not significantly differ (P > 0.05) were coded with the same letter.

Fig 4. Body size of Spodoptera frugiperda from five populations chronically exposed Bt Cry1Ab maize throughout larval development.

Insects were collected from conventional (non-Bt) or Cry1Ab maize fields and their progeny were reared on leaves of isoline or Cry1Ab maize in the laboratory. A) Larval weight gain 14 days after hatching. B) Pupal weight 24 h after pupation. While means ± standard error with asterisk differ significantly (P < 0.05, Fisher’s protected Least Significant Difference procedure) between insects of the same population reared on non-Bt (i.e., control diet) or Bt Cry1Ab maize foliage, means ± standard error with ns indicate no significant difference.

Fig 5. Increase in the developmental time of five Spodoptera frugiperda populations caused by continuous exposure to Bt Cry1Ab maize foliage throughout larval development.

Data are mean time to develop from neonate to pupa for five populations of fall armyworm collected from conventional (non-Bt) or Cry1Ab maize fields and reared on leaves of non-Bt isoline (i.e., control diet) or Bt Cry1Ab maize (i.e., Cry1Ab diet) in the laboratory. While means ± standard errors with asterisk significantly differ (P < 0.05, Fisher’s protected Least Significant Difference procedure) between insects of the same population fed non-Bt isoline or Cry1Ab maize leaves as diet, means ± standard errors with ns indicate no significant difference.

Fig 6. Fitness index for five Spodoptera frugiperda populations exposed to Bt Cry1Ab maize.

Insects were collected from conventional non-Bt or Cry1Ab maize fields and their progeny were reared on leaves of non-Bt isoline (i.e. control diet) or Cry1Ab maize foliage (i.e., Cry1Ab diet) in the laboratory. Data are estimates of intrinsic rate of population growth obtained using the life table format, and error bars are 95% confidence intervals. While asterisk indicates significant difference (P < 0.05) by one-tailed t-test using variances estimated by the jackknife technique in SAS [42], ns indicate no significant difference.