The Evolutionary Context Of Insecticide Resistance

From The National Geographic to The Wall Street Journal, popular media are fond of stories on how insects have ruled the Earth from the Dawn of Time, and how their rule will continue well into the distant future. Indeed, insects and their relatives, such as centipedes, springtails, mites, and spiders, were among the first organisms to colonize terrestrial habitats.

Since then, they have successfully survived all the major extinction events and, as a group, prosper in a wide variety of rather diverse environments. Unfortunately, quite commonly such a high adaptability represents a serious problem to humans.

As a professional entomologist, I find it borderline offensive that all-too-many people consider every insect to be a disgusting and vaguely dangerous creature that should be stepped on, smashed with a folded paper version of The National Geographic or The Wall Street Journal, or, even worse, sprayed with insecticide from a bright and shiny aerosol can. In fact, most insects are highly beneficial. Without them, we would not have most fruits and vegetables in our daily diets (if you eat a cucumber, thank a pollinator), drowned in refuse, and could not have received a gift of real silk pajamas for Valentine’s Day. Furthermore, there would be no honey to put in a cup of tea to combat a common cold contracted while volunteering for Read-a-Loud Day at a local children’s library.

Having said that, many insect species are indeed pests. Not because they are evil or malicious, but because they happen to utilize the same resources – food, fiber, construction materials, or recreational facilities – as we do. This creates understandable tensions, and we are trying to use our highly evolved human brains to do something about it. Despite the size of our brains, however, we eventually settled on a single most common solution: to produce some poisons and use them to kill the little buggers as quickly as possible. Such an approach comes with a considerable environmental price tag attached, but it works. Until it doesn’t.

Repeated applications of insecticides lead to resistance development in exposed insect populations. It is a typical selection process. With uncountable billions of insects out in the field, a few of them develop random mutations allowing to deal with insecticides in one way or another. Some of the resistant individuals get a capability to digest toxic compounds and break them down into harmless molecules. Others become able to pass poisons through their bodies without having them stuck to any internal tissues. Still others start avoiding exposure to toxic chemicals by changing their behaviors.

Without insecticides in the environment, such mutations usually come at a cost. Resistant mutants often have a shorter lifespan, lower reproductive success, and suffer high mortality. As a result, they are being outcompeted by their susceptible counterparts, and their numbers remain low. After an insecticide is applied, however, only resistant organisms can survive a toxic onslaught, while their susceptible competitors are removed from the population. Resistant survivors quickly build up in numbers and prosper, often to a great detriment to human well-being.

Insecticide resistance is a very serious problem in agriculture. For example, the Colorado potato beetle, an important pest of potatoes, tomatoes, and eggplant, has become resistant to at least 56 different chemicals. The diamondback moth, which is a real curse for growers of cabbage, broccoli, and related crops, can withstand a whopping 95 insecticidal compounds. Not every population is resistant to every chemical, but the number of failures still speaks for itself.

As frustrating as it is, insecticide resistance should not be much of a surprise to anyone familiar with the basic concepts of the theory of evolution. This point often escapes common discourse, but toxic environments are not limited to agricultural fields or faculty meetings. Herbivorous insects have been likely exposed to insecticides for about 420 million of years, which predates not just our species, but mammals in general. Back then, those insecticides originated from plants. Not from human-built chemical plants with smokestacks and loading docks like now, but from living, photosynthesizing plants.

Many insect-plant interactions, such as pollination or seed dispersal, are mutually beneficial to the parties involved. However, many insect species eat plants. In response, plants develop defenses against being eaten. Synthesizing toxic chemicals is a very common approach to protection against herbivores.  Many insecticidal compounds produced by plants affect their insect targets in similar ways to insecticidal compounds produced by humans: disrupt cell membranes, inhibit metabolism, suppress nutrient and ion transport, inhibit transduction of nerve impulses, and disrupt hormonal regulation. Some chemical groups of synthetic insecticides are even modeled after natural molecules. For example, pyrethroids are similar in structure to pyrehtrum produced by daisies, and neonicotinoids are similar to nicotine produced by tobacco.

Not surprisingly, exposure to plant toxins triggered the evolutionary process described above for synthetic insecticides: only resistant mutants survived and reproduced. Those mutants became capable of devouring previously protected host plants, except for a few mutant plants that produced a different toxin still effective against the mutant population of herbivores. Those mutant plants survived and reproduced, until a new mutation in the insect population rendered their defenses obsolete. And so on, and so forth.

Such a sequence of reciprocal changes is known as co-evolution, and it is likely to be responsible for a large portion of the diversity of life on Earth. It is also no different from the “pesticide treadmill” of insecticide/resistance/new insecticide/new resistance sequence of events that is taking place in agricultural pest management. Even underlying biochemical mechanisms may have considerable similarities. In particular, a family of enzymes known as P450s is extremely important for detoxifying chemicals of both plant and human origin. Changes in the amount and structure of those enzymes have been shown to be instrumental both for adaptation to new host plants, as well as for resistance to a number of synthetic chemicals.

Insecticide resistance should be treated as a specific case of co-evolution, not as some kind of a new phenomenon unique to industrialized pest control. This is not a very comforting thought because pest control practitioners have to combat resistance mechanisms that are well entrenched over hundreds of millions of years of evolution. However, our ability to continue overcoming pest problems depends on our ability to understand their evolutionary origins. While many plant species successfully adapted to withstand insect herbivory, more than a few went extinct since early Devonian. If we do not want to join the latter, we should be able to reconstruct evolutionary history, learn its lessons, and act accordingly.

These thoughts are described in the article Adaptation to toxic hosts as a factor in the evolution of insecticide resistance, recently published in the journal Current Opinion in Insect Science. That article was authored by Andrei Alyokhin from the University of Maine and Yolanda H. Chen from the University of Vermont.

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