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NEWS FEATURE
NEWS FEATURE
Probing the limits of “evolutionary rescue”
Could species threatened by climate change and other stresses avoid extinction through
rapid evolution?
Amy McDermott, Science Writer
In the space of five years, the field crickets of Kauai fell chirping in the grass and drop their larvae onto his
silent. The quiet was deafening to evolutionary bi- back. The maggots burrow through his carapace and
ologist Marlene Zuk, who had spent a decade crawling eat his soft insides, bursting out to pupate in the soil
through Hawaii’s vacant lots and church lawns, collect- about a week later. The drama of the cricket and the
ing the insects for her research at the University of fly unfolded nightly in the front yards and hotel lawns
California, Riverside. When she started her work, Zuk of Hawaiian paradise, forcing a big trade-off for male
remembered males as always chirping. But beginning crickets: sing for sex and court a gruesome death.
in the 1990s, she saw and heard fewer crickets. It By the early 2000s, Zuk had all but stopped hearing
seemed Kauai’s population had careened off an eco- field crickets on Kauai. The roadsides she frequented
logical cliff toward extinction. to collect insects no longer thrummed with the
One obvious culprit, Zuk thought, was a small distinctive, nails-along-a-comb chirping of the males.
parasitoid fly with remarkable hearing (1). Female flies One night in 2003, she opened her car door to silence
use their fine-tuned ears to locate a male cricket on her field site. “I thought ‘that’s that, but you may as
“Evolutionary rescue” may effectively bring back some species from the brink of extinction. There’s evidence that
evolution can, at times, be surprisingly fast, as in the case of this cricket and fly interaction on Kauai, HI. Image credit:
Norman Lee (St. Olaf College, Northfield, MN).
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Published under the PNAS license.
12116–12120 | PNAS | June 18, 2019 | vol. 116 | no. 25 www.pnas.org/cgi/doi/10.1073/pnas.1907565116
well get out of the car’,” Zuk remembers. She stepped
out, clicked on her headlamp, “and all of a sudden I
started seeing all these crickets.”
“If you’re not a cricket person, you will not fully
appreciate the cognitive dissonance this generates,”
Zuk says emphatically. Chirping is a cricket’s sexual
signal. Losing it means males should not be able to
attract females or have offspring. Yet, here Zuk was,
seeing crickets, and not hearing a thing. “It was like,
what the hell?” she says. On closer inspection, the
Kauai males still rubbed their wings together. The
crickets were trying to sing; their wings had just stop-
ped making sound.
The silence turned out to be genetic (2). A muta-
tion in a single sex-linked gene had altered wing de-
velopment for some male field crickets, Zuk’s research
group found. Instead of growing the rough file and
scraper–like structures males usually rub together to
sing, their wings became smooth and soundless.
Normally, these flatwing males would face terrible
odds of reproducing because females find males by
localizing their calls. But with a sharp-eared fly hunting
singing crickets, silent males were much less likely to
be eaten inside-out. It seemed that their favorable
mutation had rescued the population, as their
genes spread.
The case of the quieted crickets offers up an
intriguing question: Can evolution act fast enough to
save a population plunging toward extinction under
the strain of environmental change? Researchers are
increasingly considering the possibility of recovery in
at least some species, a concept called evolutionary
rescue. The crickets’ silent-wing mutation could be
one example. It spread like wildfire because staying
quiet conferred a big advantage.
Normal male field crickets (A) use a comb-like file structure to chirp. It looks like a
And yet, detecting evolutionary rescue in wild
fine white stripe (a, Right). Silent males (B) have a much-reduced file (c, Right), so
populations is still hard to do with any certainty. Other their wings look similar to females’ (C). Even though silent males do rub their
factors can also rescue populations, such as changing wings together, they cannot sing. Republished with permission of Royal Society,
behavior or moving to a new habitat. Still, understanding from ref. 13; permission conveyed through Copyright Clearance Center, Inc.
when evolution can arrest and reverse population de-
cline has major implications for the field—and for the
size. One key assumption: the population is closed,
future of wildlife conservation policies.
meaning no individuals are migrating in or out. In
evolutionary rescue, as it was defined in 1995, natural
From Theory to Practice
selection acts on the pool of genes already present in
The classic graph in evolutionary rescue is a U-shaped
the population.
curve representing a population changing in size over
After Gomulkiewicz and Holt’s early work, the field
time after an abrupt shift in the environment. First, the
matured slowly. “Evolutionary rescue was a mid ’90s
population plummets, then bellies out, and finally re-
idea that sat around in the literature without taking off
bounds by evolving a trait that allows it to persist. The
first of these curves for evolutionary rescue appeared in a for quite a while,” says ecologist Andrew Gonzalez of
1995 article by theoretical population geneticist Richard McGill University and the Quebec Center for Bio-
Gomulkiewicz and theoretical ecologist and evolutionary diversity Science in Montreal. He and colleague Gra-
biologist Robert Holt (3). Why do some populations ham Bell were the first to demonstrate evolutionary
survive environmental change, the two men asked, while rescue in the lab using yeast. Bell and Gonzalez set up
others don’t? When does evolution intervene? hundreds of brewer’s yeast populations of varying sizes
Combining fundamental equations from pop- and stressed them with salt (4). Larger populations
ulation biology and genetics, Gomulkiewicz and Holt more readily adapted, they found, following Gomul-
calculated that a population was most likely to obey its kiewicz and Holt’s U-curve prediction.
U-curve and persist when it was initially large, with a But there were important caveats. Natural selec-
diverse pool of genes for natural selection to act on. tion on existing genes isn’t the only way to save a
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And it couldn’t go extinct so fast that evolution had no population. New individuals can migrate into a de-
time to kick in or dip below a critically low population clining population and keep it from shrinking further
McDermott PNAS | June 18, 2019 | vol. 116 | no. 25 | 12117just by showing up, even if they don’t breed (a phe-
nomenon known as ecological or demographic res-
cue), or they can bring in beneficial genes (genetic
rescue) by breeding. Genetic rescue can also happen
if new genetic material arrives by wind, water, or other
means—think pollen floating through the air (5–7).
Most of the time, the two concepts go hand in hand,
explains evolutionary ecologist Ruth Hufbauer. New
individuals migrate into a population and then breed,
facilitating gene flow and sometimes genetic rescue.
Hufbauer teased all three kinds of rescue apart in
experiments with red flour beetles in her lab at Colo-
rado State University in Fort Collins (8). Tiny denizens
of grain silos, the beetles live their lives immersed in
wheat flour: they eat it, live in it, and breed in it.
Hufbauer raised hundreds of beetle populations in
wheat flour enriched with nutritious yeast and then
dumped them into clear plastic boxes with corn flour
and a lower percentage of yeast, a less-nutritious en-
vironment. If the beetles didn’t adapt to their newfound
meal, they would die. Then Hufbauer encouraged them
to survive. To simulate demographic rescue, she added
extra beetles from the same stock to some of the
Mixed populations, as in the case of snowshoe hares,
populations. For other populations, she swapped out probably offer the best odds of evolutionary rescue,
just one beetle with an individual of a different genetic wildlife biologist Scott Mills argues, because they have
background, simulating genetic rescue. Sometimes she the most genetic raw material for natural selection to act
did both. Sometimes she did neither: her control pop- on. Image credit: Scott Mills (University of Montana,
Missoula, MT).
ulations didn’t receive any extra help. If they survived, it
would be through evolutionary rescue.
After six generations in the corn, across both the quickly, and have many young, studies suggest, are
experimental and control groups, some populations most likely to evolve their way out of extinction. New
had evolved and rebounded. Their bodies grew smaller, field studies hint at evolutionary rescue in wild pop-
and were likely to use fewer resources in a resource- ulations of rats, rabbits, phytoplankton, and minnows
poor environment. Genetically rescued populations— called Atlantic killifish (9–11). A 2016 study, for exam-
the ones with extra genes from one beetle—had the ple, found that killifish populations from filthy urban
largest population sizes at the end of the experiment, estuaries tolerate industrial chemical concentrations
compared with demographic rescue and control pop- hundreds to thousands of times higher than pop-
ulations. But surprisingly, Hufbauer says, even some of ulations from cleaner sites, thanks to rapid selection on
the control populations survived. “We fully expected,” a handful of genes (12). Such examples suggest evo-
she says, “that they would really go extinct,” but they lutionary rescue could be relevant to the real world—
“were able to adapt and rescue themselves, essentially.”
and that evolution may occasionally work fast enough in
Natural selection acted on the beetles’ existing genes, it
environments rapidly being degraded by people.
seemed, yielding the same U-curve predicted in 1995. It
But wild cases are hard to verify. Take Kauai’s field
was the telltale signature of evolutionary rescue.
crickets. Even such a suggestive case—with an iden-
Over the last 25 years, studies such as this one have
tified mutation, that’s beneficial and widespread—
taken evolutionary rescue from the realm of purely
isn’t definitively evolutionary rescue. Crickets and flies
theoretical to experiments with actual populations of
coexist on other Hawaiian islands too, where flatwing
multicellular organisms. “Now people have confidence
it’s not just in mathematicians’ brains and petri dishes,” males are much rarer, suggesting Kauai’s population
Gonzalez says. But making the leap from yeasts and might not have needed the mutation to avoid going
beetles in the lab to organisms in the wild has been extinct. If the crickets weren’t headed for oblivion,
much harder, researchers acknowledge. Even working then their rebound wouldn’t qualify as rescue.
with small laboratory critters means monitoring hundreds “There’s always some uncertainty,” Gonzalez says.
of replicate populations evolving over generations—a Real-world populations don’t live in the isolation of
feat of tracking that’s much harder in the bush. What a petri dish, and evolutionary adaptation isn’t their
can rapid evolution really do to prevent extinction in the only tool to deal with environmental change. New
wild, Gonzalez asks? “That turns out to be a question behaviors and migration can also help a population
of enormous applied value.” survive stressful situations.
In the cricket’s case, it seems a combination of ge-
Adaptive Flexibility netic change over time across the population, as well as
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Rescue favors the easily overlooked, smaller creatures. behavior, helped their populations rebound. A silent
Organisms that swarm in large numbers, reproduce male might be safe from the fly, but staying quiet
12118 | www.pnas.org/cgi/doi/10.1073/pnas.1907565116 McDermottpresents mating challenges. “How does a female find Mismatched hares can’t keep pace with warmer
you?” says Zuk, who’s now at the University of Minnesota winters and decreasing snow because their trigger to
in St. Paul. “And even if she finds you, what’s going to molt and shed isn’t temperature; it’s day length. Mills
make her mate without a song?” A behavior of the silent has found that hares don’t have much phenotypic
males may have been key. They hang around the few plasticity to change their coats, overriding day length
singing males in the grass and intercept females headed for another seasonal cue. “So then we have to ask,” he
the same way. All crickets will sometimes carry out this says, “is there a possibility to adapt fast enough, via
so-called satellite behavior, Zuk says, but it “seems to be
natural selection?”
more pronounced in places with the flatwings.” Zuk
The answer is: maybe. In more southerly parts of
thinks the mutation found a toehold because of sat-
the snowshoe hare range, such as coastal Oregon and
ellite behavior (13). Evolution alone didn’t save the
Washington, snow is unpredictable and rarely sticks.
crickets; behavior helped it along.
Hares there keep a brown coat year-round, molting
This sort of behavioral flexibility in a changing envi-
ronment is one example of phenotypic plasticity—the and shedding from brown to brown. A single gene is
ability to display different traits under different circum- responsible, which came from mating with black-tailed
stances. It can look a lot like evolution, but it’s not. Ants in jackrabbits, and spread through snowshoe hare pop-
the genus Pheidole, for example, carry genes for huge ulations living in low-snow conditions, Mills reported
heads and bodies, which most species normally don’t last June (16).
express. The genes can be expressed, however, in larvae Liaisons with another species can accelerate evolu-
exposed to a juvenile hormone, according to a 2012 tion, but unless they coincide with population declines
study in Science (14). Ants born after exposure to the
hormone grow into super-soldier–like adults with massive “The promise of evolutionary rescue, is that maybe some
heads. But the ants aren’t evolving. Huge-head genes
fraction will recover, maybe there is some hope.”
already existed in the population, sleeping in the genome.
Adaptation—becoming better suited to the envi- –Andrew Gonzalez
ronment—can happen by evolution (as in genetic
change over time) or by changing gene expression so and high-speed environmental change, they don’t
the same genotype shows a new phenotype (as in the qualify as rescue. In this case, the winter brown coats
ants). One reason that wild cases of evolutionary res- probably spread through Pacific Northwestern hares
cue are so hard to prove, Gonzalez says, is because between 3,000 and 15,000 years ago, so it’s hard to say
phenotypic plasticity and evolutionary adaptation can whether it initiated rescue or not in those populations.
look so alike. Pure plasticity, as in the ants’ case, isn’t But the adaptive brown gene showed Mills that climate
rescue. But when plasticity and genetic change are can shape coat color. “Not many traits are as de-
combined, as in the crickets, evolutionary rescue can finitively shaped by climate as this one,” Mills says.
occur. Zuk’s case seems to be rapid evolution made “Because whether you’re mismatched is 100% de-
possible by phenotypic plasticity; the silent-wing gene termined by the average persistence of snow.”
wouldn’t have spread without a way for males and When could a trait shaped by climate help species
females to find each other and mate.
survive the kind of rapid change Mills is seeing in
Montana? He figured that polymorphic populations—
A Natural Ally
where winter white and winter brown hares coexist—
So what can rapid evolution really do in the wild, and
would offer the richest palette for natural selection to
what are its limits? Scott Mills chuckled at that question,
act on and, therefore, the highest odds of evolutionary
on the phone from his office at the University of Mon-
rescue. In another 2018 article, Mills showed, using
tana in Missoula. “That’s it,” he says. “We don’t know.”
data from natural history collections, that polymorphic
Mills and other wildlife biologists want to make evolu-
populations of hares and other seasonally coat-
tion an ally in the race to conserve disappearing spe-
cies. Montana’s winter mountains give them a unique changing species pop up across the Northern Hemi-
vantage to ask how. sphere (17). In places such as Washington’s Cascade
On the hillsides there, a long list of predators prey Mountains, both hare color morphs hop between
on snowshoe hares—“the candy bar of the forest,” patches of snow and towering red cedars. Hares aren’t
Mills says. Camouflage is a hare’s best defense. The endangered, but they illustrate how conservation
animals blend in with the landscape by growing a might embrace polymorphic areas, such as the Cas-
brown coat in spring, which turns snowy white as the cades, where evolutionary rescue is most likely.
days grow short in fall. But as Montana’s climate Although Mills isn’t certain rescue can happen in
changes, snow is falling later, and melting earlier in this case, he sees the hare’s story as a metaphor for the
the season, leaving hares mismatched with their en- conservation community because evolutionary rescue
vironment and very visible to predators. Snowpack is is “nowhere on the radar of reserve design.” It’s been
expected to decrease by roughly 40 to 69 days in clear since the first theory article in 1995 that large
western Montana this century (15). “White animals on populations are more likely to rescue with a man-
brown ground stick out,” Mills says. “Our hares in ageable extent of environmental change. Subsequent
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Montana get clobbered in weeks where they’re white studies showed connected populations, with migra-
on brown background.” tion, gene flow, and some history of similar stress may
McDermott PNAS | June 18, 2019 | vol. 116 | no. 25 | 12119be the most likely to adapt and survive. But how ex- keep populations big and connected, he says, to
actly humans might foster rapid evolution is the next “allow evolutionary rescue to be a possibility, even if
unanswered question, Mills says—one that “goes to it’s not likely.”
the heart of climate resilience for wild species.” The next frontier for the field may be studying it at
How effective reserves could be depends heavily community levels. Individual populations are woven
on the rate of climate change, Gonzalez adds. into communities, so when one group rescues, there
Whether Earth sees 2 °C or 4 °C of warming and may be domino effects for the species it interacts with,
whether that’s in 50 years or 100 or 200 will decide Gonzalez explains. Stressing whole ecosystems—such
which populations are even candidates. Polar bears as small ponds teeming with bacteria, water bugs, and
and other charismatic mammals aren’t likely con- fish—and then watching as adaptation unfolds (or
tenders because their generation times are long. doesn’t) at multiple trophic levels could help clarify
Evolutionary rescue takes 10 to 100 generations, he community evolutionary rescue’s role in the fate of
says, meaning hundreds of years for large mammals. ecosystems themselves.
Rapid change will outpace them before rescue kicks Understanding rapid evolution may not stop many
in. Faster-breeding creatures, such as insects, are the extinctions, but it could lead to conservation policies that
better bet. Indeed, Kauai’s field crickets shifted from maximize the potential for rescue. Considering how bleak
chirping to 90% silent males in fewer than 20 genera- the story of man’s impact on wildlife can be, “the promise
tions, or about a decade. Even so, Gonzalez would still of evolutionary rescue,” Gonzalez says, “is that maybe
choose policies that slow down climate change and some fraction will recover, maybe there is some hope.”
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12120 | www.pnas.org/cgi/doi/10.1073/pnas.1907565116 McDermottYou can also read
