The  Western corn rootworm, known as “the billion-dollar beetle” because its larvae ravage America's corn crops to the economic tune of $1 billion a year, may need a new nickname. 

A team of nine researchers, including UC Davis biologist Scott Carroll, analyzed data over a six-year period and concluded that crop rotation works well in battling the notorious pest that annually causes $800 million in yield loss and $200 million in treatment costs. 

“Answering this question was important not only to grower success but the agricultural economy, said Carroll, an associate of the UC Davis Department of Entomology and Nematology and owner of the Davis-based Institute for Contemporary Evolution. “Bt crops are far-and-away the single most important factor reducing soil and crop insecticide applications in the United States at present.” 

When Bacillus thuringiensis (Bt) corn was introduced in 2003, the pest seemed under control. The genetically engineered corn is a transgenic, insecticidal crop that kills rootworm larvae but is harmless to humans. 

However, when the pest began developing resistance to the Bt corn toxins, the U.S. Department of Agriculture recommended crop rotation as a method of control. Crop rotation, an age-old agricultural tactic, is a consistent and economical means of controlling rootworms the season following an outbreak. It reduces rootworm densities, and is considered more effective than insecticides. 

With crop rotation, “the frequency of problem fields declined by 92 percent in 2014 to 2016 relative to 2011 to 2013,” the nine-member team wrote in the research article, “Crop Rotation Mitigates Impacts of Corn Rootworm Resistance to Transgenic BT Corn,” in the current edition of the Proceedings of the National Academy of Sciences. 

“Corn rootworm is one of the nation's most devastating pests, giving a sense of urgency to protecting the efficacy of industrial pest control approaches with reduced non-target effects,” said Carroll, who studies basic and applied aspects of evolutionary biology. “Transgenic insecticidal Bt crops in the United States are cultivated under a very interesting socio-evolutionary model of resistance management that is mandated by the U.S. Environmental Protection Agency. Individual growers must implement resistance management--usually by devoting a small acreage to planting a 'refuge' of non-Bt crops in order to nurture a local reservoir population of Bt-susceptible pest insects.” 

Carroll pointed out that the “outstanding productivity of Bt corn has led a portion of growers to reduce or eliminate their required refuge planting. Moreover, many time-tested practices for integrated pest management have fallen by the wayside as growers have found they could rely solely on the genetics of the seemingly invulnerable Bt varieties.”   

“As predicted, Bt resistance evolution in corn rootworm has accelerated. In response to this dire risk, in 2016 EPA began mandating crop rotation as a complementary means of reducing the damage to Bt corn fields caused by resistant corn rootworms. Our working group analyzed the success of this traditional agricultural tactic to help sustain the efficacy of the high-tech Bt tactic.” 

Carroll said that under the leadership of his colleague Yves Carrière at the University of Arizona, “our team analyzed six years of field data from 25 crop reporting districts in Illinois, Iowa and Minnesota—three states facing some of the most severe rootworm damage to Bt cornfields. 

“The answer we found is that traditional crop rotation is working to protect the Bt corn fields from rootworm damage, including in areas that have seen the evolution of behavioral resistance to crop-rotation by rootworms.” 

The bottom line, said Carrière, is this: "Farmers have to diversify their Bt crops and rotate. Diversify the landscape and the use of pest control methods. No one technology is the silver bullet.”

The project also included scientists from North Carolina State and McGill University, along with Carroll's colleague, Peter Jørgensen of the Stockholm Resistance Center.

While Jorgensen was pursuing his master's degree program at the University of Copenhagen and studying at UC Davis, he worked with Carroll and Sharon Strauss of the Department of Evolution and Ecology.

“This PNAS paper,” Carroll said, “is one of several that have developed from a pursuit Peter and I organized on 'Living with Resistance' at the National Socio-Environmental Synthesis Center in Annapolis, with the aim to explore more sustainable approaches to managing evolutionary challenges to health and food security.” 

The abstract:

"Transgenic crops that produce insecticidal proteins from Bacillus thuringiensis (Bt) can suppress pests and reduce insecticide sprays, but their efficacy is reduced when pests evolve resistance. Although farmers plant refuges of non-Bt host plants to delay pest resistance, this tactic has not been sufficient against the western corn rootworm, Diabrotica virgifera virgifera. In the United States, some populations of this devastating pest have rapidly evolved practical resistance to Cry3 toxins and Cry34/35Ab, the only Bt toxins in commercially available corn that kill rootworms. Here, we analyzed data from 2011 to 2016 on Bt corn fields producing Cry3Bb alone that were severely damaged by this pest in 25 crop reporting districts of Illinois, Iowa, and Minnesota. The annual mean frequency of these problem fields was 29 fields (range 7 to 70) per million acres of Cry3Bb corn in 2011 to 2013, with a cost of $163 to $227 per damaged acre. The frequency of problem fields declined by 92% in 2014 to 2016 relative to 2011 to 2013 and was negatively associated with rotation of corn with soybean. The effectiveness of corn rotation for mitigating Bt resistance problems did not differ significantly between crop-reporting districts with versus without prevalent rotation-resistant rootworm populations. In some analyses, the frequency of problem fields was positively associated with planting of Cry3 corn and negatively associated with planting of Bt corn producing both a Cry3 toxin and Cry34/35Ab. The results highlight the central role of crop rotation for mitigating impacts of D. v. virgifera resistance to Bt corn."

Antimicrobial drug resistance threatens both personal and planetary health and the issue is as crucial as the global threat of climate change, says UC Davis evolutionary ecologist Scott Carroll.

In a paper titled “Use Antimicrobials Wisely,” published in the current edition of Nature, a nine-member international research team, including Carroll, advocates that the United Nations reframe its action on antimicrobial resistance.

The United Nations is meeting in New York on Sept. 21 to discuss the global antimicrobial drug resistance (AMR) crisis.

“We're concerned about what will happen if the proposed UN solutions focus mainly on incentives for new drug development, at a time when the drug industry itself is abandoning those efforts against infectious disease due to AMR,” said Carroll, who co-leads the international group on resistance to pesticides and antimicrobial drugs. He founded and directs the Institute for Contemporary Evolution, Davis, and is a member of the Sharon Lawler lab, UC Davis Department of Entomology and Nematology.

The paper, published in the Comment section, is the first product from a two-year working group sponsored by the National Socio-Environmental Synthesis Center in Annapolis, Maryland. “We are taking a similar socio-environmental approach in our concurrent work on pesticide stewardship,” Carroll said.

“While new drugs have a role, we think it's more important for society to learn how to steward pathogen susceptibility, so we develop that theme in the paper,” Carroll said. “And because we also depend on microbes for digestion, immunity, and general health, and microbes support ecosystem functioning through nutrient cycles and the maintenance of soil and water quality, we further argue that our AM drug habits and waste streams threaten both personal and planetary health. “

Lead authors of the paper are Peter Jorgensen of Stockholm, Sweden, and Didier Wernli of Geneva Switzerland. Jørgensen, who spent part of his Danish graduate program working with Carroll in Davis, is now a postdoctoral researcher at the Royal Swedish Academy of Science, Stockholm.

“The effectiveness of antibiotics has been waning since they were introduced into modern medicine more than 70 years ago,” the research team wrote. “Today, our inability to treat infections ranks alongside climate change as a global threat. New classes of antimicrobial drugs are unlikely to become widely available any time soon; if and when they do, bacteria, viruses and other microbes will again evolve resistance.”

Carroll described AMR as more than a medical dilemma—it's a socio-ecological problem. “The vulnerability of pathogens to antimicrobial drugs is a communal resource, readily threatened by overuse, to be lost as a classic 'tragedy of the commons.' There is a lot of contemporary theory for social resilience in the face of socio-ecological challenges, and– linking to entomology– the early success of the pioneering management of Bt crop pest resistance evolution is an encouraging precedent.”

In its planetary health approach, the group seeks to be “more cognizant not only of preserving drug susceptibility in pathogenic microbes, but also protecting from wholesale destruction the community of microbes on which we depend for life,” Carroll said.

In the paper, the scientists pointed out that “Resistance affects animal and environmental health as well as human health, and so requires coordinated action across economic sectors. No single concern exemplifies this better than the high rate of antibiotic use in agriculture (largely as growth promoters or disease prevention).” They wrote that in the United States, 70 to 80 percent of all anti-microbials consumed are given to livestock.”

DAVIS--Soapberry bugs are a classic evolutionary example of how rapidly insects can switch hosts, adapting from a native to an invasive plant. 

Now newly published UC Davis research shows that soapberry bugs have not only lost adaptations to their native host plant but are regionally specializing on an invasive host.

 The work, "Adaptation to an Invasive Host Is Driving the Loss of a Native Ecotype," published in the current edition of the journal Evolution, “collapses a classic and well-documented example of local adaptation,” said doctoral candidate Meredith Cenzer of the Louie Yang lab, UC Davis Department of Entomology and Nematology. The plant-host switch can lead to disruption of native plant communities and a breakdown of the ecosystem.

The players involved are the soapberry bug (Jadera haematoloma), also known as “the red-shouldered bug”; its native host plant, the balloon vine (Cardiospermum corindum), and the invasive host,  the golden rain tree or Taiwanese rain tree (Koelreuteria elegans).

The study, which took place in Florida, expands on the 1989 groundbreaking research of UC Davis evolutionary ecologist and soapberry expert Scott Carroll, who documented local adaptation in beak length, survival, and development time and other traits between soapberry bugs, balloon vine and the golden rain tree in Florida.

Said Carroll: "Meredith Cenzer's findings carry an important message for those concerned with biodiversity conservation, because she shows that even highly distinct adaptive specializations can disappear rapidly due to human influence on the environment– even in cases where the key native habitat has not been lost."

The soapberry bug, which lives throughout the United States and much of the world, feeds on seeds within the soapberry plant family, Sapindaceae, which includes soapberries, boxelders and maples. Mostly black, it has red eyes, red lateral stripes on the sides of its head and red on its “shoulders” (pronotum).  It is often mistaken for the boxelder bug.

“As part of my doctoral dissertation, I documented that this pattern of local adaptation has been lost in the last 27 years,” Cenzer said, “and that all populations of soapberry bugs in Florida-- even those still found on the native --are now adapted only to the invasive host.“

“Locally adapted populations are often used as model systems for the early stages of  rccological speciation, but most of these young divergent populations will never become complete species,” Cenzer noted in her abstract. “The maintenance of locally adapted populations relies on the strength of natural selection overwhelming the homogenizing effects of gene flow; however, this balance may be readily upset in changing environments.”

 “All populations that were adapted to the native host--including those still found on that host today--are now better adapted to the invasive host in multiple phenotypes,” she wrote in her abstract.” Weak differentiation remains in two traits, suggesting that homogenization across the region is incomplete. This study highlights the potential for adaptation to invasive species to disrupt native communities by swamping adaptation to native conditions through maladaptive gene flow.”

Cenzer characterized local adaptation as “high performance in one habitat coming at the cost of performance in other habitat types, such that populations specialized on each habitat will have higher fitness in that environment than immigrants from other habitats.”

“This results directly in two types of ecological reproductive isolation between locally adapted populations: 1) selection against migrants, who will be outcompeted by residents, and 2) selection against hybridization (if hybrids show intermediate phenotypes), as hybrid offspring will be outcompeted in each habitat by one parental type,” she wrote in her research paper. “However, such reproductive isolation relies on ongoing differential selection balanced with low rates of gene flow between habitats. In most well studied systems demonstrating local adaptation, we do not know how perturbation – either to selection pressures or gene flow – will influence the long-term stability of differentiation.”

Carroll, who maintains a website, “Soapberries of the World,”  says the soapberry bugs are “very approachable native guides to how evolution is taking place on earth day.” His website shows “how evolution happens every day and why it matters.”

A native of Gainesville, Fla., Cenzer received her bachelor of science degree in entomology at the University of Florida in 2009.

“I am broadly interested in evolutionary ecology, particularly in plant-insect interactions, and the balancing roles of selection, gene flow, and plasticity on determining the phenotypes we see in nature,” she said. After receiving her doctorate in entomology from UC Davis in the fall, she will start a postdoctoral position at Florida State University with biology professor Leithen M'Gonigle, developing theory on the evolution of dispersal in patchy landscapes.

Evolutionary ecologist Scott Carroll, director of the Institute for Contemporary Evolution and a member of the Sharon Lawler lab, UC Davis Department of Entomology and Nematology, will speak on "Applied Evolutionary Biology to Address Global Changes" at a noon seminar on Thursday, Jan. 29 in the Center for Evolution and Medicine, Arizona State University.

"Two categories of evolutionary challenges result from escalating human impacts on the planet," Carroll says. "The first arises from cancers, pathogens and pests evolving too quickly, and the second from the inability of many valued species to adapt quickly enough."

Carroll says that applied evolutionary biology offers strategies to address these global challenges that threaten human health, food security and biodiversity and natural resources.

He will highlight both progress and gaps in evolutionary methods across the life sciences that either "target the rate and director of evolution or reduce the mismatch between organisms and human-altered environments."

"Refining and applying these underused tools will be vial for meeting current and future targets for sustainable development." 

Carroll does research on patterns of ongoing evolution in wild and anthropogenic environments. He is well-known for his studies on evolutionary changes in soapberry bugs in response to plant introductions.  His expertise includes behavioral and evolutionary aspects of adaptation to contemporary environmental change in insects and other organisms.

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