Insecticide resistance in arthropods is a serious problem that costs farmers millions, if not billions, of dollars each year. According to the online database maintained at the Michigan State University, worldwide resistance has been reported to 433 different insecticides. In the U.S. alone, 234 different insect, mite, and tick species became resistant to at least one chemical. Furthermore, these numbers, as impressive as they are, likely underestimate the true extent of the problem. Despite all the efforts of people who maintain the database, not every case gets entered into the database, or even becomes known to people outside of the farm where it happened.
Some pests are resistant to a single compound; however, many of them are simultaneously resistant to several related, or even unrelated chemicals. New cases of resistance are being continuously detected in a wide variety of crops, and commercial growers can never assume that it will not happen on their farms.
Practical significance of insecticide resistance is widely acknowledged. Numerous scientific papers and extension bulletins are published on the subject, presentations are being delivered at a variety of conferences, and grants are being awarded by government agencies in different jurisdictions. There is even a standing committee, comprised of the representatives of major pesticide companies and aptly named Insecticide Resistance Action Committee. Yet, the problem remains, and arguably even getting worse. So, what is going on?
What Is Insecticide Resistance?
To answer this question, it is important to first understand what insecticide resistance is. A good place to start is defining what we are trying to understand, an approach that is also helpful in many other situations in life. While this seems like a no-brainer, the issue was contentious for a while, and there are still some differences in opinion. An academic definition describes field-selected resistance as a genetically based decrease in susceptibility of a population to a toxin caused by exposure of the population to that toxin in the field. In other words, it is not the same population now than it used to be, and it is likely to stay this way at least in the near future.
A definition favored by pest control practitioners depicts field-selected resistance as a heritable change in the sensitivity of a pest population that is reflected in the repeated failure of a product to achieve the expected level of control when used according to the label recommendation for that pest species. In other words, a pesticide applicator seems to be doing everything right, but an insecticide does not work anymore.
The two definitions are not mutually exclusive. Both emphasize that members of a given insect population gain an ability to deal with an insecticide, and that ability is passed from parents to offspring. The academic definition is probably more appropriate if we are to take a proactive approach to resistance management instead of waiting for problems to show up in the field. However, the challenge is to detect when such a shift is beginning to occur, and to decide how much of a decline in susceptibility actually matters. Therefore, in real life people usually start calling a population resistant once they cannot control it as they did in the past.
Development of insecticide resistance in insect populations, whatever its true definition is, usually unfolds as a typical evolutionary process driven by survival of the fittest individuals. Initially, there are a few mutants that have somehow acquired an ability to avoid being poisoned. This ability may be due to digesting a toxin, quickly passing it through the system without letting it destroy anything, or recognizing its presence and avoiding treated surfaces.
Mutations responsible for insecticide resistance are usually randomly caused by some internal (e.g., various molecules bumping against DNA in their chromosomes) or external (e.g., solar radiation) factors. It has been hypothesized that they may also be caused by exposure to pesticides, some of which are known to have mutagenic properties. However, currently there is no hard evidence to support this suggestion.
As is usually the case for most oddball individuals, resistant mutants do not do very well among the general population under normal conditions. Their survivorship and reproductive success are usually lower than that of their susceptible peers. Therefore, relatively few of them persist in a population that is not exposed to a particular insecticide to which they have developed resistance.
Furthermore, resistant genes are usually incompletely dominant. In plain words, this means that the level of resistance in hybrid crosses between resistant and susceptible insects is somewhere in between that of their parents. Since mutations are rare, the probability of two resistant insects meeting each other is low. So, they will mate instead with susceptible insects, producing the offspring that is not likely to survive exposure to an insecticide that is applied at a reasonably high rate. This further declines the number of resistant individuals in a population.
As a result, most pests are susceptible to a new insecticide at the time of its introduction. They die following its application, thus demonstrating that this chemical is highly effective. This is usually enthusiastically highlighted in glossy booklets distributed at trade shows and grower meetings.
Situation changes dramatically, however, once an insecticide starts being applied on a regular basis. Resistant insects find themselves in a position of a class nerd who made a fortune in computer business at the Dawn of the Internet and flies a private jet to a high school reunion. The nerd is still the same; however, the surrounding world has changed dramatically, and a mindset that used to do little but provoke jokes of various degree of stupidity now helps making millions in salary and stock options. Similarly, resistant mutants survive and thrive in the treated areas, while their previously superior susceptible competitors are not doing very well anymore.
Most species of insect pests have high fecundity, with one female producing literally hundreds of offspring. Their generation times are also usually short. These two attributes are important for making them pests in the first place. As a result, it does not take much time for originally scarce resistant insects to reach population densities sufficient for causing economically significant damage.
In some cases, insecticide resistance may arise without a classical Darwinian selection that was described above. Instead of new mutations, genes already present in most members of a population kick in a high gear following insect exposure to an insecticide. As a result, individuals that somehow avoided ingesting a lethal dose of the toxin (perhaps they arrived at the field after most chemical was washed away by a rain, or something like that) start producing more detoxifying enzymes and digest the poison. This state of enzyme overproduction is inherited by their offspring, which is now better prepared to deal with the insecticide.
Instead of “survival of the fittest,” which currently remains a dominant paradigm in biology, such a strategy can be described as “forewarned means forearmed.” It allows for a quicker onset of resistance because several generations of selection are no longer necessary. Inheritance of traits acquired over lifetime of an individual organism is the subject of a relatively recent, but rapidly developing, scientific field of epigenetics.
Insecticide resistance is often considered to be one of the perils of industrial farming. While it is certainly true, it is also important to realize that adaptation to toxins is a perfectly natural process. Furthermore, it predates agriculture (and humans, and even dinosaurs for that matter) by hundreds of millions of years.
Nature is full of toxins. In particular, plants cannot run away from herbivores. Therefore, they often rely on the production of various toxins for protection. Insects have been feeding on plants for a very long time. To overcome these toxins, they had to develop effective physiological detoxification machinery directed against natural plant poisons. Relatively little change was needed to start using it against human-made insecticides. As a matter of fact, chemical structure of more than a few synthetic insecticides resembles that of natural compounds. The word neonicotinoids, for example, shares the same root with nicotine for a good reason. In other words, insects were already well-prepared by the time the first insecticides arrived at the marketplace.
The Risks and Rewards of the Insecticide Treadmill
Current approach to dealing with insecticide resistance has been dubbed as a “pesticide treadmill” – endless cycles of chemicals failing due to resistance and being replaced by newly developed chemicals. This word has a negative connotation, as it implies running hard without getting anywhere.
There is another side to this analogy, however. Running on a treadmill is convenient. It is often more comfortable than running outside (people who do not believe me are welcome to go for a jog in Maine in February or in Arizona in July). It also gets the job done, keeping a treadmill runner in shape. The same applies to insecticides – they provide a convenient and cost-effective way to control pest insects.
The insecticide treadmill has been working well so far. Failing chemicals are being reliably replaced with new ones, developed by R&D departments of pesticide companies. However, bringing a new insecticide to market is an increasingly long and expensive process. For one thing, most of the low-hanging fruit has been already picked – there is a limited number of things that a chemist can do, for example, to a nicotine molecule to make it into a different molecule that still kills insects.
For another thing, demands and regulations are much more stringent now. A chemical that would have been enthusiastically welcomed by the industry in 1960s cannot make it out of a test tube nowadays because of its potential effects on the environment.
In light of these challenges, preservation of effectiveness of existing insecticides is very important. The treadmill will probably continue spinning for a while, but it is risky to count on it. Therefore, managing of insecticide resistance is important for pretty much everybody who produces or consumes agricultural products (a group that encompasses the entire human population). Fortunately, there are ways to do it, which will be a topic of my next article.