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Research unravels how spider mites quickly evolve resistance to toxins

As a generalist herbivore, the two-spotted spider mite is a destructive pest in global agriculture, especially in arid regions. It is known to infest more than 100 crop plants and hundreds of non-crop species.

This mite also demonstrates resistance to a wide variety of chemical toxins, such as those that plants produce, as well as human-made pesticides used to control arthropods (like insects and mites), thus making these pests extra hard to evict from the garden.

University of Utah biologist Richard Clark has published research this month that sheds new light on how this mite, known to science as Tetranychus urticae, quickly evolves resistance to foreign compounds, known as xenobiotics.

PHOTO CREDIT: Brian Maffly, University of Utah

Spider mites don’t eat leaves, but rather suck out the fluids in their cells, leaving the leaves desiccated, as shown here in biology professor Richard Clark’s greenhouse lab at the University of Utah. Credit: Brian Maffly

Although mites are arthropods, like insects, they differ by having eight legs (instead of six) and are more closely related to ticks, spiders and scorpions. The two-spotted spider mite is tiny, hardly half a millimeter long, and is named for the pair of black spots on either side of its partially translucent body. These spots are actually the digestive contents of its gut.

A ubiquitous inhabitant of greenhouses across the United States, it is equipped with needlelike mouthparts that both pierce and suck nutrients from leaves, leaving them a desiccated shell and killing the plant. They also deposit a silky webbing across the host plant, hence the second half of this mite’s common name.

“Arthropod pests have been responsible for historic famines and food shortages, and continue to impact human welfare today by reducing crop yields. So there’s been an interest in developing plant varieties which are more resistant to insects or mites,” said Clark, a professor in the School of Biological Sciences.

Working with then-U graduate student and lead author Meiyuan Ji, as well as colleagues from Belgium, Clark’s lab identified a mechanism by which spider mites “express” genes involved in the detoxification [inactivation] of xenobiotics, as is commonly observed in pesticide-resistant spider mites, according to research published this month. The findings could help scientists develop more effective ways to control this pest.

Two-spotted spider mites. Credit: Richard Clark, University of Utah

An evolutionary arms race

“If you have a large field of maize, in Utah or somewhere in the Midwest, and you have potentially millions of mites eating them, and you spray with pesticides, genetic variants that are present may allow some of the mites to detoxify the pesticides and survive,” Clark said. “These selected mites will then reproduce and can take over. “Pretty soon, the pesticide is no longer effective, or maybe your genetically resistant variety of maize is no longer resistant,” he continued. “That’s because there’s been genetic adaptation, similar to how some bacterial pathogens have adapted to defeat human-produced antibiotics. From a human perspective in agriculture that’s a problem.”

For hundreds of millions of years, a kind of genetic arms race has been quietly raging between plants and the creatures that eat them. In response to unrelenting herbivory, plant species evolved to produce compounds that are toxic to insects and other mites, and the animals in turn evolved the countervailing ability to tolerate these toxic xenobiotic compounds. This is why you should never randomly pick leaves of unknown plants to put in your salad.

While plants usually produce complex mixes of different xenobiotic toxins, an agricultural pesticide is typically a single toxic organic molecule (a potentially easier task to overcome). Spider mites have been champions, for better or worse, at evolving resistance to the chemicals farmers throw at pests—sometimes in as few as several tens of generations.

How does the spider mite do it so quickly?

PHOTO CREDIT: Brian Maffly, University of Utah

Biology professor Richard Clark inspects maize plants that are infested with mites at his greenhouse lab. Clark studies how two-spotted spider mites are able to quickly evolve resistance to pesticides.

While Clark says that the genetic basis for the two-spotted spider mite’s xenobiotic resistance evolution is not fully understood, one major route involves the metabolism, sequestration or transport of toxic compounds away from sensitive tissues. In fact, Clark said, “The species has many copies of detoxification genes that aid in overcoming foreign compounds, and  the mite’s ability to safely eat more than 1,100 different plant species demonstrates that it has the ability to detoxify or otherwise overcome the chemical defenses of a broad range of natural compounds in addition to pesticides.”

Has this trait supercharged the mite’s ability to survive chemical pesticide assaults?

“That’s what we suspect, but it’s still somewhat debated in the field,” Clark said. “A number of factors like population size and geographical distribution influence the possibility for chemical exposure. Anytime you have exposure to a foreign compound, there’ll be natural genetic variations that exist in the population and that can be selected. So the bigger opportunity you give, the more likely you are to see resistance evolve.”

In their experiments, Clark’s team studied mite strains that were both xenobiotic resistant and susceptible in search of elements in their genomes that could explain the difference in levels of resistance. Clark suspected the resistant mite strain was better equipped to metabolize the pesticide toxins it was resistant to, and his analyses brought the answer into sharper focus.

“We found that in this generalist mite [a mite species with many hosts] genetic variation in a regulatory gene in the resistant strain led to the upregulation of a whole bunch of detoxification genes,” he said. “Therefore, our findings suggest that genetic variation in genes that control the detoxification capacity of arthropods can be important targets of selection leading to high levels of resistance to plant-produced compounds or pesticides. That presumably is what’s leading to a greater ability of the resistant mite strain we studied to detoxify some of the multiple pesticides to which it is highly resistant.”

Learn more about insect and arthropod herbivory, and how plant evolution responds to this pressure, by exploring the Genetic Science Learning Center.

The Clark lab’s exploration of spider mites’ complicated relationship with corn was featured by the Genetic Science Learning Center.

The study was a collaboration between the Clark laboratory and that of Dr. Thomas Van Leeuwen at Ghent University, Belgium, and was published Aug. 17 in Nature Communications under the title, “A nuclear receptor HR96-related gene underlies large trans-driven differences in detoxification gene expression in a generalist herbivore.” Funding came from the European Research Council, Ghent University, and the Research Foundation Flanders.