Developmental Penalties Associated with Inducible Tolerance in Helicoverpa armigera to Insecticidal Toxins from Bacillus thuringiensis

Abstract

Exposure of insect larvae to sublethal concentrations of crystal toxins from the soil bacterium Bacillus thuringiensis (Bt toxins) causes the induction of immune and metabolic responses that can be transmitted to offspring by epigenetic inheritance mechanisms. Given that the elevated immune status carries significant developmental penalties, we wanted to establish the relationships between immune induction, tolerance to the toxin and developmental penalties. A laboratory culture of Helicoverpa armigera was induced by a sublethal bacterial suspension containing crystal toxin Cry1Ac in one generation and maintained in the presence of toxin, acquiring significant levels of tolerance to the toxin within 12 generations of continuous exposure. Comparing tolerant and susceptible insects, we show that the induction of larval immune response and the coincident alteration of development-related metabolic activities by elicitors in the larval gut (larval induction) differs from the elevated immune status transmitted by epigenetic mechanisms (embryonic induction). Because the damaging effects of larval induction processes are higher compared to embryonic induction, it is likely that overall developmental penalties depend on the relative contribution of the two induction processes. When insects are kept with the same amount of toxin in the diet for subsequent generations, the embryonic induction process increases its contribution compared to the larval induction, resulting in reduced overall developmental penalty, while tolerance to the toxin is maintained.

Interactions between evolved pesticide resistance and pesticide exposure influence immunity against pathogens

“…Oral Btt infection did not decrease survival in our study but was associated with slower development in T. castaneum larvae, indicating a direct cost of infection or an indirect cost from mounting an immune response, as previously observed in the same system (Tate & Graham, 2015) and in other insects challenged with Bt toxins (Hernández-Martínez et al, 2017; Rahman et al, 2011). Previously documented variation in resistance in T. castaneum against Cry3 proteins effective against other Tenebrionid beetles may explain why Btt had negative effects on development but did not instigate high mortality (Milutinović et al, 2013; Oppert et al, 2011).…”

Effect of induced tolerance toBttoxin on the egg size ofHelicoverpa armigeraand parasitism byTrichogramma pretiosum

“…A Cry1Ac tolerant strain of H. armigera was produced in 2009 (Rahman et al ., ) by culturing the larval stages of susceptible insects on the artificial diet with the surface coated (using a pipette) with 0.1 mg mL −1 HD73 bacterial lysate (see above) to provide exposure to a sub‐lethal dose of Cry1Ac toxin. During establishment of the tolerant population, bioassays were performed every five generations to confirm and measure the level of tolerance.…”

“…A bacterial lysate containing Cry1Ac toxin produced from B. thuringiensis strain kurstaki HD73 was supplied by John L. Reichelt (Bacterial Fermentation Pty Ltd, Australia) and was prepared and assessed as described by Rahman et al (2011). The suspension was stored at −20 ∘ C and was thawed before dilution with sterile ultrapure water (Milli-Q; Merk Millipore, Germany) to produce a 20 mg mL −1 protein suspension, which was stored for short periods at 4 ∘ C prior to use.…”

“…The culture of H. armigera used in the present study was descended from the culture described in Rahman et al (2011). The susceptible culture of H. armigera was established by combining moths from the susceptible ANGR strain and a susceptible field strain collected in Queensland, Australia (provided by CSIRO, Australia).…”

Which Is Stronger? A Continuing Battle Between Cry Toxins and Insects

“…It is found that the levels of DNA methylation and histone acetylation of this resistant strain are increased, with the expression levels of some conserved miRNAs and their target mRNAs significantly changed, indicating that epigenetic mechanisms mediate the evolution of G. mellonella resistance to Bt at pre-transcriptional and posttranscriptional levels ( Mukherjee et al, 2017 ). Another evidence comes from the cotton bollworm ( Helicoverpa armigera ), which, when continuously exposed to Cry1Ac toxin for 12 generations, reveals tolerance to Cry1Ac with enhanced immune status through an epigenetic mechanism from a strong maternal effect, which can be passed to its offspring ( Rahman et al, 2011 ). Besides, the red flour beetle ( Tribolium castaneum ) exhibits an increased survival rate after exposure to Bt in a short time that can be directly transmitted to the first (F1) and second filial (F2) generations, called paternal trans-generational immune priming, which may be regulated by epigenetic mechanisms too ( Eggert et al, 2014 ; Schulz et al, 2019 ).…”