Like many other transgenic crops, Bt maize synthesises its own pesticide: a toxic protein produced in its leaves and stems, which kills pests in a matter of days. Perfect… Except when insect populations develop resistance to the toxin! To date, management strategies implemented to delay the evolution of resistance have been successful. Notwithstanding the success of these strategies, IRD scientists and their South African partners have now revealed that a major pest of maize, the moth Busseola fusca, has developed an unusual defense mechanism against Bt toxin in South Africa. By contrast with the usual expectations, this resistance is inherited as a dominant trait, a characteristic that may have contributed to its rapid geographical expansion. This result recently published in the journal PLoS ONE, suggests that insect resistance management should be more finely tuned to local pests and should go beyond the simple implementation of refuges for Bt-susceptible moths.
Bt maize and resistance development
Genetically engineered maize is created by introducing a gene into the plant genome that expresses a toxic protein from a bacterium, i.e. Bacillus thuringiensis (Bt). Both the leaves and stems of Bt maize produce this toxin which destroys the gut of any moth larvae eating the plant. The technique is effective and unlike wide spectrum pesticides, it only targets larvae of moths. However, sooner or later, insect species may be able to develop a mechanism of resistance against any pesticides. Bt maize is not fundamentally different in this regard and in order to delay the evolution of resistance in pest populations, the concept of maintaining refuges for Bt susceptible moths was developed.
Non-Bt maize fields are protecting Bt maize fields
The refuge strategy consists of planting a small proportion of land with non-Bt maize; the aim being to maintain pockets of insects that remain susceptible to the toxin. In line with other known cases of Bt-resistance, resistance in Busseola fusca was expected to involve modification of the cells in the gut wall, which prevents the toxin from binding. Crucially, this type of adaptation is inherited recessively: both parents must be resistant to produce fully resistant offspring. Since the probability of resistant individuals arising in the field is low, any resistant insects surviving on Bt maize will mate with one of the many Bt-susceptible individuals originating from the refuge area and their progeny will not survive in the Bt-maize field. This tactic has been successful, especially in North America where the first Bt maize has been planted since 1995 with resistance yet to develop among lepidopteran pests.
The exception to the rule
However, about seven years after Bt maize was introduced to South Africa in the late 1990's, scientists observed resistant Busseola fusca caterpillars and, more importantly, these resistant insects seemed to reproduce and spread rapidly. To explain this phenomenon, scientists in South Africa, together with IRD researchers, crossed resistant South African moths with susceptible moths imported from Kenya, where Bt maize is not yet commercialized. The offspring developed perfectly on Bt maize and were as resistant as the South African resistant parents. Unlike everything known so far, this resistance evolved in the field was inherited as a dominant trait.
A likely new resistance mechanism
This result shows for the first time that resistance to Bt maize can be inherited in a dominant rather than recessive way. It also explains why resistance has spread rapidly. The moth does not seem to have followed the expected pattern of adaptation. At this stage, there are several hypotheses as to the nature of the mechanism, but it is very likely that Busseola fusca has developed an unconventional resistance mechanism yet to be identified.
In South Africa, most farmers are still cultivating single-toxin Bt maize. In many cases they need to apply at least one pesticide spray, which makes planting of Bt varieties less attractive. As a result of the study, the planting of refuges needs to be reconsidered in South Africa, and a possibility exists that the refuge strategy may totally change in the future. However these are very short term solutions. In the medium term, single-toxin Bt maize is being progressively replaced by a stacked variety producing two different toxins but, in a worst case scenario, one cannot exclude that Busseola fusca could also quickly adapt to varieties expressing more than one toxin. In the long term, new Insect Resistance Management strategies, likely more complex, should be developed against Busseola fusca. Such perspectives could include a more diverse array of toxins for the control of pest populations, possibly supplemented with a biological component such as pathogenic fungi or parasitic wasps.
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