The Red Queen comes to Ordway

Alice and the Red Queen running to stay in place. Credit:  Rachel Nabors, Dribble.com

They say it's a curse to live in historically interesting times. 'They' were talking about human history, of course. But the same wisdom applies to evolutionary history. Perhaps even more so.

Recent ecological events at Ordway have me thinking a lot about the current moment, in the context of evolutionary time. Specifically, my thoughts keep coming back to the Red Queen Hypothesis (RQH). Like many biology students, I first encountered the idea in an undergraduate course on evolutionary biology. It's a bit esoteric, but the details are important. Bear with me. 

Leigh Van Valen proposed the RQH in the 1970's to explain an unexpected pattern he had found in the fossil record. Van Valen was interested in how long species tended to last over geological time scales. He examined data spanning tens to hundreds of millions of years, from a wide range of organisms:  single-celled protists to mammals. He found that the extinction probability for most species at any one point in time was almost always constant. This was surprising because it was widely assumed that natural selection tended to improve species over time, in the sense that they got better adapted to their environment. If that was true, then species that had been around for more time should be less likely to go extinct, on average, than younger species. Why would the age of a species not matter? 

Van Valen's hypothesis was that, for most species, the environment was constantly 'degrading' in some way. In other words, for any given species, the environment was always, in a sense, trying to kill them. To keep from going extinct, species had to constantly evolve new ways to manage their ever-worsening environment. As soon as it failed to do so, a species was extinguished. This constant evolution reminded Van Valen of the Red Queen from Lewis Carroll's Through the Looking Glass, who had to run as fast as she could just to stay in the same place. Thus, the 'Red Queen' Hypothesis.

What could account for such environmental degradation? Van Valen had some ideas there, too. His hypothesis highlighted a crucial difference between the kinds of environment that surrounds every species. One kind is the abiotic environment, made up of the non-living components that surround a species:  air, water, average temperature, precipitation, etc. Over geological time, such components change, of course, exerting pressure on a species to adapt. Importantly, however, once a species is adapted to the new conditions, the abiotic environment does not change in response to that evolution. 

That is very different in the case of a species' biotic, or living, environment:  the other organisms with which a species interacts. Unlike the non-living environment, a species' living one is able to evolve, too. This difference is particularly important in the case of a species' antagonists:  i.e., organisms that harm the species in some way, like parasites, diseases, predators, etc. These will often kill an organism, unless it evolves some kind of protective trait(s). Evolution has produced a wide range of these:  behaviors that help avoid antagonists, physiological mechanisms that isolate and/or kill infectious organisms, tissue repair processes that mitigate physical damage. But evolution acts on the antagonists, too:  every protective trait that a species might evolve against its enemies creates reciprocal selection pressure that favors the evolution of counter-measures in those enemies. Thus, a species' biotic environment is always degrading in precisely a Red Queen-like way, requiring constant evolutionary 'running' for a species to stay in the same place:  alive.

It's a bit embarrassing to admit now, but when I first learned about the RQH in that undergrad evolution course, it sounded far-fetched to me. The professor, a parasitologist, had emphasized the role of parasites as antagonists. To me, a lifelong citizen of an industrialized country with a temperate climate and a long history of effective public health and hygiene programs, that had seemed very counter-intuitive. I mean, I could count my encounters with parasites on one hand. It was hard for me to imagine that parasites could be widespread and damaging enough to drive any species - much less most species - to extinction should they slip up just once in the evolutionary race.

That naive intuition flipped over the course of my further studies. My graduate work focused on the evolutionary consequences of interactions between organisms, a field you cannot study very long without developing a deep appreciation of the significance of negative interactions like parasitism. Nevertheless, twenty-five years late, I feel like I am receiving an object lesson in the potential extinctive power of parasites. Emerald ash borer has come to Ordway. 

Emerald ash borer (Agrilus planipennis) - or EAB, for short - is a beetle native to portions of China, Korea and Russia, where it feeds on species of ash (Fraxinus) trees native to those regions. Since it was first detected in the Detroit metro in 2001, EAB has spread to 36 US states and 5 Canadian provinces, killing enough North American ash trees along the way to become the most damaging and costly wood-boring insect in US history. That cost reflects not only the destructiveness of the beetle, but also the importance of ash trees in North American ecosystems and cities. Minnesota alone has an estimated 1 billion ash trees belonging to three native species. Black ash (F. nigra), the most numerous, is a keystone species in several kinds of wetland ecosystem, particularly in the northern half of the state. Green ash (F. pennsylvanica) and white ash (F. americana) are important components of a wider range of forest ecosystems across the entire state, and are among the most numerous of urban trees in Minnesotan cities. Since the arrival of EAB into the state in 2009, every one of Minnesota's ash trees is now under serious threat.

For something so destructive, EAB is surprisingly beautiful. It belongs to the family Buprestidae, aka the 'jewel beetles' or 'metallic wood-boring beetles', named for the bright colors and metallic iridescence of their exoskeletons. This unique visual effect is not actually based on metal - or jewels, for that matter - but on the way their exquisitely microtextured surfaces scatter and reflect light. Surprisingly, their eye-catching display actually seems to help jewel beetles hide from predators, at least when it is viewed against the waxy, reflective backdrop of the leaves that most jewel beetles feed on. This unusual camouflage probably helps hide EAB adults while they feed on the ash leaves that sustain them. While this likely increases the harm that adult EAB are able to inflict on ash trees, it is far from the worst damage done by EAB.

 

Adult emerald ash borer. Photo credit:  UMN.

A far bigger issue is the beetles' larvae. Baby EAB do not feed on ash leaves like adults do. Instead, they eat the vascular tissue beneath the bark, and the stem cells that give rise to it. Together these two tissues make up the thin layer of a tree's trunk that is actually alive:  both the outermost bark and the innermost wood of the trunk are actually non-living material. Feeding larvae create empty tunnels that wind their way through the living sheath, interrupting movement of the resources the tree needs to survive. Worse:  while adult EAB feed for a few weeks at most before they mate and die, larva do so for many months at a time, and can remain in a tree for up to two years.  The longer this goes on, the more impaired the tree's living vascular tissue becomes. Beyond a certain point, the tree can no longer survive. 

In many North American ash species, that point of no return is almost guaranteed to be reached, once a tree becomes infested with EAB. That's because, unlike the species of ash native to EAB's home range, which have coevolved with EAB for millennia, North American ash species have few-to-no defenses against the beetle. Asian ash species make EAB's life difficult. In Manchurian ash (F. mandschurica), for example, leaves produce repellant chemicals to discourage adults from feeding, and the vascular cells targeted by EAB larvae contain chemicals known to act as low grade toxins. Likely for such reasons, EAB larvae are much more likely to survive to adulthood in North American than Asian species of ash. One study (Showalter et al. 2019) found that eggs laid in black ash (a North American species) were, on average, about 6 times more likely to survive to later stages than in Manchurian ash (an Asian species). Once larvae started to feed, more than 80% of them survived to later growth stages in the average black ash tree tested, compared to about 15% in Manchurian ash.

Perhaps as compensation for the defenses of Asian ash species, EAB are prolific reproducers. Mating occurs just a few days after adults emerge from host trees. Around 10 days after emergence, the average female is ready to lay her eggs - usually between 40 and 70 of them, but occasionally up to 200. In North American ash species, likely due to the trees' lack of defenses, female beetles can often lay their eggs right back into same tree they emerged from. It does not take many such intergenerational recursions to doom even a very large tree, especially when survival rates of larvae are so high.

EAB larval feeding tunnels beneath the peeled bark of a dead ash tree.

EAB larva within a feeding tunnel. Photo: PA Department of Conservation and Natural Resources - Forestry, Bugwood.org.

At Ordway we have been watching for EAB to show up for several years. Given that our location is only 13 miles from where the beetle was first detected in Minnesota, there was obvious cause for concern. During our annual surveys of the oak forest for the past decade, we have examined ash trees for EAB signs:  canopy thinning, exit holes, bark splitting to reveal larval tunnels beneath. For years we found no definitive signs. But EAB is tricky. Infestations begin in the canopy, and can take several years to spread down the trunk to eye level. And the signs left by the beetles can look very different from tree to tree.

As it turns out, the first definitive appearance of EAB at Ordway was not in our oak forest, but in the floodplain forest adjacent to the Mississippi River. In October 2022, during a survey of the trees on the floodplain, I took the photo below, adding it to our field notes with the caption 'WTF?'. I had never seen bark peeling in this way before. The answer to my abbreviated question is that, as the bark of an ash tree fills with EAB larvae, they come to the attention of local woodpeckers, which peel the bark from the tree in this pattern (called 'blonding') in order to get to the tasty grubs beneath. That photo was the first time I had ever seen ash blonding. The very next year, it seemed to be everywhere.     

   

This summer I repeated the tree inventory we had conducted in 2022. In the original survey, ash trees were the most frequently encountered taxonomic group of canopy trees; we located and measured 100 living ones. This year I relocated each of them, to check its status at year 3 of our study. As it turns out, that status was 'bad'. Every single tree had been top killed:  their trunks lacked live leaves from the canopy all the way to the ground. In every case the evidence pointed to EAB:  trunks were blonded, bark was split and shedding, and larval tunnels were clearly visible in the barkless gaps. The speed and scale of the outbreak has been humbling. To convey a sense of the loss, I have added a few sets of paired photos below. They are from the portion of our project that measures changes in light availability across the forest, using photos of the canopy. The left hand photo in each pair is from 2022; the right hand photo is from this summer. We did not set out to document the loss of ash with these photos, we just happened to capture it.

Canopy photo from 2022 (left) and the same spot in 2025 (right).

Canopy photo from 2022 (left) and the same spot in 2025 (right).

Canopy photo from 2022 (left) and the same spot in 2025 (right).

Canopy photo from 2022 (left) and the same spot in 2025 (right).

The situation for ash trees at Ordway is a microcosm of the situation across Minnesota. The most common species of ash at Ordway - green ash and black ash - are also the most common in the state. As it happens, they are also the two species most susceptible to EAB. Since Minnesota has the highest volume of ash trees of any state in the US, it is poised to be the center of destruction of the beetle. The map on the left below, generated by Minnesota's Department of Agriculture, illustrates the predicted vulnerability of different portions of the state, based on the number and species of ash that live there. At the risk of being overly sensationalistic, think of it as the distribution of oily rags in a garage that is already on fire. The map on the right is the Minnesota Department of Natural Resources real-time interactive map of the spread of EAB (the green shaded counties), accessed September 9th 2025. Think of it as the flames. The worst impacts of EAB in Minnesota are probably yet to come.  

 

But there are a couple glimmers of hope. First - at Ordway, nearly two-thirds of the top killed ash trees I observed this summer were resprouting at the base. Some trees, including many ash species, employ this as a bet-hedging strategy:  they maintain a collection of buds at the base of the trunk, usually belowground, that are able to become new stems if the original trunk should die. An additional strategy ash species use is establishing dense 'banks' of seedlings. Large portions of the ground in Ordway's floodplain forest are covered by a virtual carpet of ash seedlings. When the adults in the forest canopy die, the increased light to the forest floor supports the growth of this next generation. Both resprouting and seedling banking strategies have been found to support the recovery of ash populations after outbreaks of EAB near the epicenter of the beetle's invasion in Michigan.   

Resprouts arising from base of top-killed ash tree (background), and dense 'seedling bank' (fore- and mid-ground) of green ash (F. pennsylvanica).

The second glimmer is - perhaps unexpectedly - the Red Queen, herself. Species that are resistant to parasites - like Asian species of ash are to EAB - owe that resistance to an invisible history of death and reproductive failure of poorly-defended individuals. If we could see that history, it might look very much like what is happening to green and black ash in North America right now. Of course, for resistance to evolve in this way requires genetic variation in those vulnerable ash populations; i.e., some trees need to possess some degree of genetically-determined resistance. There may be some hope on that front, too. Green, black, and white ash actually possess chemical defenses that are effective against EAB. The reason for their vulnerability appears to be that they fail to activate those defenses when attacked by the beetle. That is actually good news. Gaining the ability to switch those genes on in the presence of EAB is a much smaller coevolutionary move than gaining an entire chemical defense system. Even that small change is far from guaranteed, of course, but there are indications that it may already be happening. In the wake of some of the worst local outbreaks of EAB in North America, a small proportion of 'lingering ash' have remained unharmed. The jury is still out on whether these individuals are, as one paper put it, "simply the last to die", or perhaps their species' next stumbling step forward in the evolutionary sprint to keep up with the Red Queen.

References and Further Reading

Emerald Ash Borer. Minnesota Department of Natural Resources website. Accessed 9-6-2025. https://www.dnr.state.mn.us/invasives/terrestrialanimals/eab/index.html

Herms & McCullough. 2014. Emerald ash borer invasion in North America: history, biology, ecology, impacts and management. Annual Review of Entomology 59:13-30.

Huff et al. 2022. A high-quality reference genome for Fraxinus pennsylvanica for ash species restoration and research. Molecular Ecology Resources 22:1284-1302.

Kashian. 2016. Sprouting and seed production may promote persistence of green ash in the presence of the emerald ash borer. Ecosphere 7:e01332.

Knight et al. 2011. Lingering ash population dynamics in Michigan and Ohio. Emerald Ash Borer National Research and Technology Development Meeting.

Showalter et al. 2020. Resistance of European ash (Fraxinus excelsior) saplings to larval feeding by emerald ash borer (Agrilus planipennis). Plants, People, Planet 2:41-46.

Sun et al. 2024. Emerald ash borer management and research: decades of damage and still expanding. Annual Review of Entomology 69:239-258.

Van Valen. 1973. A new evolutionary law. Evolutionary Theory 1:1.

Villari et al. 2016. Progress and gaps in understanding mechanisms of ash tree resistance to emerald ash borer, a model for wood-boring insects that kill angiosperms. New Phytologist 209:63-79.

Wang et al. 2010. The biology and ecology of the emerald ash borer, Agrilus planipennis, in China. Journal of Insect Science 10:128.

Wilson et al. 2025. Ongoing regeneration of ash and co-occurring species 20 years following invasion by emerald ash borer. Forest Ecology and Management 580:122546.