Can an ambitious breeding effort save North America’s ash trees? | Science

Forest geneticist Jennifer Koch hopes her ash breeding strategy could save other threatened trees.

Maddie McGarvey

DELAWARE, OHIO—On a weekday morning in August, just one pickup truck sat in the sprawling visitors’ parking lot here at the U.S. Department of Agriculture’s (USDA’s) Forestry Sciences Laboratory. A decadeslong decline in research funding had been slowly quieting the place—and then came the pandemic.

But in a narrow strip of grass behind a homely, 1960s-era building, forest geneticist Jennifer Koch was overseeing a hive of activity. A team of seven technicians, researchers, and students—each masked and under their own blue pop-up tent—were systematically dissecting 3-meter-tall ash trees in a strange sort of arboreal disassembly line. Over 5 weeks, the researchers would take apart some 400 saplings, peeling wood back layer by layer in search of the maggotlike larvae of the emerald ash borer (Agrilus planipennis), the most devastating insect ever to strike a North American tree. Since the Asian beetle was first discovered in Michigan in 2002, it has killed hundreds of millions of ash trees across half the continent and caused tens of billions of dollars of damage.

“We have contests for who can successfully pull out the smallest larvae and the biggest larvae,” Koch says. “People get pretty excited and competitive about it. You have to do something, because it is very tedious—and [the larvae] are really gross.”

The larvae kill ash trees by burrowing into them to feed on bark and, fatally, the thin, pipelike tissues that transport water and nutrients. They then transform into iridescent green beetles about the size of a grain of rice that fly off to attack other trees. Dead larvae excite Koch and her team the most. Those finds signal trees that, through genetic luck, can kill emerald ash borers, rather than the other way around. Such rare resistant trees could ultimately help Koch achieve her ambitious goal: using time-tested plant-breeding techniques to create ash varieties that can fend off the borer and reclaim their historic place in North American forests.

Ash borer invasionSince slipping into the United States around the turn of the millennium,probably on a container ship, theemerald ash borer (EAB) has spreadto 35 states and killed hundreds ofmillions of trees. Scientists havecalled it the most destructive forestpest ever introduced to North America. Agrilus planipennis 7–13 mm Cooked rice grain A cornerstone treeComprising at least 16 species native to North America, ash trees are key components of wetland, mountain, and savanna ecosystems. They have also been heavily planted in cities. Cycle of destructionThe EAB completes its life cycle in 1 to 2 years. Along the way it exploits multiple parts of the tree. 1 MatingAdult EAB beetles feed on ash leaves and mate during the warmest parts of the summer. A female can mate multiple times during her short life. 2 Egg layingFemales lay eggs in crevices in ash bark. One female can lay up to 100 eggs, which hatch in 7 to 10 days. 3 Larva developmentMaggotlike larvae burrow into the tree and feed on wood and tissues that trees use to transport water and nutrients, creating squiggly galleries up to half a meter long. Larval feeding is what kills trees. 4 Adult developmentIn the fall, larvae create small chambers within the tree. They overwinter there and pupate in the spring. 5 EscapeBeetles bore out of the bark, creating characteristic D-shaped exit holes, and fly off in search of new trees to feed on. Adult beetles live about 3 weeks. They can fly up to 10 kilometers, but usually find a new tree much closer to home. Adult EABfeeds on leaves 1–2 yearcycle Larvagallery Larva Pupa D-shapedexit hole Frass View atright 1 2 3 4 5 D-shapedexit hole

C. Bickel/Science

Koch focuses mostly on the green ash, one of at least 16 native ash species in North America. “If we don’t intervene, there’s a good chance that green ash will go extinct,” she says. But she is also ramping up work on other ash species; none is safe from the borer. And ultimately, she hopes to expand her approach to other trees brought low by a foreign pest, in a bid to reverse the biological hollowing out of forests set in motion by the transcontinental swapping of species.

Since a devastating fungal blight popped up in the Bronx Zoo in 1904 and went on to kill at least 3 billion chestnut trees, North American forests have been swept by one plague after another, including a fungus that kills elms and an aphidlike insect that kills hemlocks. No tree has come back—but Koch hopes her approach can usher in an unprecedented era of tree revival. “We don’t think we have to lose any North American tree species to invasive pests and disease,” says plant geneticist Jeanne Romero-Severson of the University of Notre Dame, one of Koch’s collaborators.

Not all researchers share such faith in tree breeding. Many researchers believe identifying and releasing natural enemies of the ash borer, an approach called biological control, could help ash sooner. And some wonder whether, even if a better ash emerges, the trees will be able to muscle their way back into profoundly reshaped ecosystems. “It’s not like if we have a resistant ash tree, everything is going to be hunky dory,” says Deborah McCullough, a forest entomologist at Michigan State University.

Koch, however, feels certain that genes lurking among the billions of ash trees growing across the continent can save the species. “Genetic variation,” she says, “is a very powerful survival mechanism.” 

Koch’s quest has its origins in a humble place: parking lots around Detroit. That’s where, nearly 2 decades ago, experts gathered to examine ash trees that had suddenly died. “It was pretty obvious right away this was not something anybody had ever seen before,” recalls McCullough, who cut down some of those trees for study. “We just don’t have native insects that do that kind of stuff.”

Eventually Eduard Jendek, an entomologist in Bratislava, Slovakia, identified the culprit as the emerald ash borer, which had lived mostly unnoticed in its east Asian homeland. But the insect’s arrival in North America set off alarms. Ash is a key genus of temperate hardwood tree. Individuals soar to 35 meters, and species anchor critical ecosystems: black ash in soggy northern wetlands, green ash along Midwestern streams, blue ash in open savannas of Kentucky, white ash in dense mountain forests of Appalachia, and a half-dozen species in the Southwest. Resilient and stress-tolerant, ash was also heavily planted in cities.

Adult borers, scientists soon learned, feed on ash leaves and lay eggs on ash bark. Burrowing and feeding larvae eventually girdle trees, killing them. North American trees, separated from their Asian cousins by an ocean and millions of years of evolution, had never been exposed to the borer, and lacked chemicals to detect or defeat it. “It’s as if they don’t even know something is boring into their vascular system and killing them,” Romero-Severson says.

Michigan and USDA imposed quarantines on moving ash trees in a bid to contain the pest. But the beetle, an agile flier adept at sniffing out ash trees, slipped through with ease; it has now reached 35 states and Washington, D.C. (see map, below). Many Midwestern city streets became denuded dystopias of dead trees. Some experts predicted the borer could cause the extinction of ash species in North America and began to organize a response.

A beetle on the march

Since the emerald ash borer (EAB) was discovered in Michigan in 2002, it has spread widely into areas where ash trees grow.

0 500 km Range of ash in theUnited States and Canada Counties where EABdetected CANADA UNITED STATES MEXICO

A. Cuadra/Science

Koch, who had arrived at the USDA lab in the 1990s as a graduate student and stayed on as a staff scientist, was intrigued. Gregarious and impatient with dogmatic thinking, Koch is more motivated by solving real-world problems than by doing basic research on model organisms. In graduate school, she studied the genetics of air pollution resistance in poplar trees but then moved on to trying to breed resistance to a century-old debilitating bark disease of beech trees caused by a fungus-insect combination.

In 2003, Koch attended an early meeting on the forest pest du jour: the emerald ash borer. During the discussion, she wondered aloud whether some trees might harbor natural resistance to the beetle. “Everyone kind of looked at me like I was nuts,” she recalls. “Back then the big headline was: ‘Kiss your ash goodbye.’ People just didn’t believe that there could be resistance within native species.”

But Koch persisted. In cities, where the plague first emerged, trees tend to lack diversity, she reasoned; urban foresters tend to plant genetically similar strains widely, making street trees uniquely vulnerable to invasive pests. Trees growing in forests, by contrast, have had millions of years to mutate and mix genes into countless combinations.

The first step, Koch realized, was to survey that genetic diversity before the borer eliminated it. Starting in 2005, ecologist Kathleen Knight of the U.S. Forest Service and Koch set up 150 study plots in infested forests in Ohio, and then repeatedly revisited them, tracing how ash trees in the plots fared. It was “kind of boring” at first, Knight says, because almost all the ash trees simply died. But over time, she found that about one in 1000 green and white ash trees—the most common species in Ohio—produced flushes of new leaves even after borers had killed neighboring trees. Starting in 2008, Knight, Koch, and others cut branches from the biggest and healthiest of those trees, which they dubbed “lingering ash,” and grafted them onto root stock of healthy trees. “We try to look for the best of the best,” Knight says.

The researchers then developed a way to test for resistance under controlled conditions. Starting in late spring, Koch’s team receives coffee filters containing thousands of ash borer eggs reared by Forest Service entomologist Therese Poland in Lansing, Michigan. Researchers place 12 eggs on each stem of hundreds of ash saplings grown from cuttings. Eight weeks later, they dissect the trees and trace the fate of each hatched borer.

David Carey, a technician on Koch’s team, was performing that task in August. Sitting under his tent, he snapped green branches off a sapling and saved them for future grafting onto other trees, in case the sapling proved resistant. Then he deftly shaved the thin bark off the trunk, to expose evidence of feeding: “galleries,” or winding tunnels bored by the larvae that resemble a kindergartner’s marker squiggles.

Larvae of the emerald ash borer, an introduced beetle, have killed millions of ash trees in North America by tunneling beneath their bark.

Maddie McGarvey

Soon, Carey found a little yellow head poking out, the larva’s body still encased in the tree. He pulled the larva out with tweezers, placed it in a plastic tray with a growing pile of its compatriots, and cataloged its size and location. The tree’s failure to kill this larva was a strike against its future in the breeding program. Carey moved down a few centimeters along the tree trunk and started a new dissection.

In 2015, Koch’s team published its first major paper on ash, reporting that lingering green ash trees killed significantly more larvae than control trees. That, she says, convinced many who doubted that trees never exposed to an introduced insect could still resist it. But even lingering trees didn’t kill enough larvae to save themselves, the researchers found; they still died, just more slowly. So in 2010, Koch started to crossbreed her most resistant trees—the same basic technique used by plant breeders for 10,000 years to produce bigger grains, sweeter fruit, and countless other desired traits. In essence, one of Koch’s colleagues joked, they created “TreeHarmony”—a matchmaking service for durable trees. “We’re kind of pushing Mother Nature along by putting these trees together,” Koch says.

Such traditional breeding is a blunter tool than more fashionable genetic engineering techniques that can precisely transfer or alter single genes. But traits like insect resistance are typically controlled by many genes, not one—and in the case of ash trees, researchers don’t know which genes are important. Some may code for chemicals that kill feeding larvae or make wood less digestible; others may make leaves less detectable or palatable to adults. Several generations of breeding and selection will allow these genes to stack up over time, providing ever stronger defense, Koch hopes.

The efforts have borne some fruit. The top-performing offspring of two lingering ash trees kill up to four times as many larvae as their parents, Koch and colleagues have found. “Our best tree so far was 11 out of 11” larvae killed, Koch says; the 12th egg failed to hatch. Now, she’s planning to use those top performers to breed an even more resistant generation. If those trees consistently kill 80% to 90% of larvae that attack them in field trials, Koch says they can begin restoration efforts. She hopes restoration plantings could start in about 10 years.

Such a timeline would be fast by tree-breeding standards, but some fear it may be too slow to save the ash. Already, formerly ash-dominated sites now host other trees, grasses, or invasive plants. So, to restore ash, those newcomers would first need to be removed—a potentially expensive, labor-intensive process, McCullough says. “Nature doesn’t just sit there and wait for you to come along and plant a tree.”

Larvae of the emerald ash borer chew into trees, where they overwinter beneath the bark before pupating in the spring.

Maddie McGarvey

McCullough and others are more bullish on saving existing trees through biological control: identifying, rearing, and releasing insects or other species that kill unwanted pests. The concept has a long history of success in managed landscapes, such as farm fields and orchards. But its record in natural forests is less sterling. For example, biocontrol researchers have spent more than 3 decades seeking and rearing predators to curb the hemlock woolly adelgid, which kills eastern and Carolina hemlock trees; they’ve made progress but are still far from declaring victory.

Biocontrol researchers say the ash borer might be easier to defeat. In the insect’s home range in Asia, researchers have found three species of tiny wasps that lay eggs inside ash borer larvae, and one wasp the size of a grain of sand that parasitizes borer eggs. Parasitoids have often proved to be more successful biocontrol agents than predators, like those that might tame the woolly adelgid, because parasitoids are more likely to target a single species, causing less collateral damage.

In recent years, researchers have released wasps in forests in 30 states where the emerald ash borer is present. Follow-up studies have shown the wasps can find beetles, parasitize them, and reproduce; in some trees, up to 80% of ash borer larvae have wasps living inside them. “There’s a lot of data that suggest it’s promising,” says Poland, who leads the Forest Service’s research effort.

Biocontrol is now the “cornerstone” of antiborer efforts led by the Animal and Plant Health Inspection Service (APHIS), USDA’s primary agency for fighting plant pests. Through the end of 2019, APHIS had invested $13.2 million in emerald ash borer biocontrol research, versus $2.4 million in breeding resistant trees. Whereas breeding could pay off eventually, biocontrol may already be protecting regrowing ash trees in some places, says Scott Pfister, director of APHIS’s pest management division. “We tend to try to work towards shorter term solutions,” he says. “Breeding for resistance is a long-term research effort.”

But biological control faces its own limitation: There have to be enough borers in an area to sustain wasp populations. By the time borers have reached such densities, they will have likely already killed almost all large ash trees, experts say.

“Sometimes there’s an overexuberance towards the efficacy of biocontrol,” says Koch, who feels she has had to meet a higher bar to get her breeding research funded. Still, she hopes the wasps succeed. Effective parasitoids could complement her breeding efforts, she says, by lowering ash borer numbers enough to give partially resistant trees better odds of surviving to reproductive age. That’s what happens in Asia, Koch notes, where genes and ash borer enemies conspire to protect trees. The ultimate goal, she says, is “to mimic what happens in nature.”

In the meantime, Koch worries her funders—primarily USDA—will lose patience with her breeding efforts. So she has embarked on several efforts to speed up the process. In one, she’s testing whether ash seedlings grown in containers under artificial light and treated with hormones produce seeds in less than the normal 3 to 4 years. Another seeks to identify the specific compounds that resistant ash trees use to fight the borer. Robert Stanley, a graduate student in Romero-Severson’s group, grinds up samples from dissected saplings and analyzes the chemicals in the wood. This is no trivial task; ash, like other trees, is a sophisticated chemical factory, producing hundreds of compounds with structures and functions unknown to science. “Plants are just chemical geniuses,” Stanley says.

Most of these compounds probably provide no defense against ash borers. But a handful show up disproportionately in trees that kill the most borer larvae, Stanley has found. And if such compounds reliably predict longer survival in the forest, they could pave the way to rapid testing of wild trees for borer resistance, potentially speeding breeding efforts, Koch says. “We’re hoping for some way we can quickly test a tree and say, ‘OK, that one’s a dog.’”

Despite the progress she’s made, Koch says it sometimes “feels like the weight of the world is on us.” Hers remains the sole U.S.-based effort to revive ash trees through breeding. (Breeders in the United Kingdom are seeking genetic resistance to a fungus attacking ash trees there.) But she’s starting to recruit help by building a network of government and nonprofit organizations to grow and plant resistant ash trees. The collaboration—which includes the conservation organization American Forests; the Holden Arboretum in Kirtland, Ohio; and Fender Musical Instruments, which has long used ash wood for guitars—has plans to establish an ash tree nursery in Detroit. Some of Koch’s trees were supposed to be growing there by now, but the shipment was delayed by the pandemic and is now planned for spring.

Ash breeding may be just the beginning. Koch believes her approach could save other North American trees facing introduced threats. Researchers at the University of Rhode Island and North Carolina State University, for example, have reared lingering hemlock trees that may resist the adelgid; Koch hopes to start breeding the best performers. She’d also like to breed beech trees that can beat the bark disease and eventually add butternut, which is threatened by a fungus, as well as elm and chestnut trees. And she knows new diseases and insects will arrive. “My goal,” Koch says, “is that when I retire, I leave behind all the tools” that others might need to meet new threats to native trees.


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