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 fellsilent. The quiet was deafening to evolutionary bi-ologist Marlene Zuk, who had spent a decade crawlingthrough Hawaii’s vacant lots and church lawns, collect-ing the insects for her research at the University ofCalifornia, Riverside. When she started her work, Zukremembered males as always chirping. But beginningin the 1990s, she saw and heard fewer crickets. Itseemed Kauai’s population had careened off an eco-logical cliff toward extinction.

One obvious culprit, Zuk thought, was a smallparasitoid fly with remarkable hearing (1). Female fliesuse their fine-tuned ears to locate a male cricket

chirping in the grass and drop their larvae onto hisback. The maggots burrow through his carapace andeat his soft insides, bursting out to pupate in the soilabout a week later. The drama of the cricket and thefly unfolded nightly in the front yards and hotel lawnsof Hawaiian paradise, forcing a big trade-off for malecrickets: sing for sex and court a gruesome death.

By the early 2000s, Zuk had all but stopped hearingfield crickets on Kauai. The roadsides she frequentedto collect insects no longer thrummed with thedistinctive, nails-along-a-comb chirping of the males.One night in 2003, she opened her car door to silenceon 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 thatevolution 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).

Published under the PNAS license.

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well get out of the car’,” Zuk remembers. She steppedout, clicked on her headlamp, “and all of a sudden Istarted seeing all these crickets.”

“If you’re not a cricket person, you will not fullyappreciate the cognitive dissonance this generates,”Zuk says emphatically. Chirping is a cricket’s sexualsignal. Losing it means males should not be able toattract 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, theKauai males still rubbed their wings together. Thecrickets 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 researchgroup found. Instead of growing the rough file andscraper–like structures males usually rub together tosing, their wings became smooth and soundless.Normally, these flatwing males would face terribleodds of reproducing because females find males bylocalizing their calls. But with a sharp-eared fly huntingsinging crickets, silent males were much less likely tobe eaten inside-out. It seemed that their favorablemutation had rescued the population, as theirgenes spread.

The case of the quieted crickets offers up anintriguing question: Can evolution act fast enough tosave a population plunging toward extinction underthe strain of environmental change? Researchers areincreasingly considering the possibility of recovery inat least some species, a concept called evolutionaryrescue. The crickets’ silent-wing mutation could beone example. It spread like wildfire because stayingquiet conferred a big advantage.

And yet, detecting evolutionary rescue in wildpopulations is still hard to do with any certainty. Otherfactors can also rescue populations, such as changingbehavior or moving to a new habitat. Still, understandingwhen evolution can arrest and reverse population de-cline has major implications for the field—and for thefuture of wildlife conservation policies.

From Theory to PracticeThe classic graph in evolutionary rescue is a U-shapedcurve representing a population changing in size overtime after an abrupt shift in the environment. First, thepopulation plummets, then bellies out, and finally re-bounds by evolving a trait that allows it to persist. Thefirst of these curves for evolutionary rescue appeared in a1995 article by theoretical population geneticist RichardGomulkiewicz and theoretical ecologist and evolutionarybiologist Robert Holt (3). Why do some populationssurvive environmental change, the twomen asked, whileothers don’t? When does evolution intervene?

Combining fundamental equations from pop-ulation biology and genetics, Gomulkiewicz and Holtcalculated that a population was most likely to obey itsU-curve and persist when it was initially large, with adiverse pool of genes for natural selection to act on.And it couldn’t go extinct so fast that evolution had notime to kick in or dip below a critically low population

size. One key assumption: the population is closed,meaning no individuals are migrating in or out. Inevolutionary rescue, as it was defined in 1995, naturalselection acts on the pool of genes already present inthe population.

After Gomulkiewicz and Holt’s early work, the fieldmatured slowly. “Evolutionary rescue was a mid ’90sidea that sat around in the literature without taking offfor quite a while,” says ecologist Andrew Gonzalez ofMcGill University and the Quebec Center for Bio-diversity Science in Montreal. He and colleague Gra-ham Bell were the first to demonstrate evolutionaryrescue in the lab using yeast. Bell and Gonzalez set uphundreds of brewer’s yeast populations of varying sizesand stressed them with salt (4). Larger populationsmore readily adapted, they found, following Gomul-kiewicz and Holt’s U-curve prediction.

But there were important caveats. Natural selec-tion on existing genes isn’t the only way to save apopulation. New individuals can migrate into a de-clining population and keep it from shrinking further

Normal male field crickets (A) use a comb-like file structure to chirp. It looks like afine white stripe (a, Right). Silent males (B) have a much-reduced file (c, Right), sotheir wings look similar to females’ (C). Even though silent males do rub theirwings together, they cannot sing. Republished with permission of Royal Society,from ref. 13; permission conveyed through Copyright Clearance Center, Inc.

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just 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 (geneticrescue) by breeding. Genetic rescue can also happenif new genetic material arrives by wind, water, or othermeans—think pollen floating through the air (5–7).Most of the time, the two concepts go hand in hand,explains evolutionary ecologist Ruth Hufbauer. Newindividuals migrate into a population and then breed,facilitating gene flow and sometimes genetic rescue.

Hufbauer teased all three kinds of rescue apart inexperiments with red flour beetles in her lab at Colo-rado State University in Fort Collins (8). Tiny denizensof grain silos, the beetles live their lives immersed inwheat flour: they eat it, live in it, and breed in it.Hufbauer raised hundreds of beetle populations inwheat flour enriched with nutritious yeast and thendumped them into clear plastic boxes with corn flourand a lower percentage of yeast, a less-nutritious en-vironment. If the beetles didn’t adapt to their newfoundmeal, they would die. Then Hufbauer encouraged themto survive. To simulate demographic rescue, she addedextra beetles from the same stock to some of thepopulations. For other populations, she swapped outjust one beetle with an individual of a different geneticbackground, simulating genetic rescue. Sometimes shedid both. Sometimes she did neither: her control pop-ulations didn’t receive any extra help. If they survived, itwould be through evolutionary rescue.

After six generations in the corn, across both theexperimental and control groups, some populationshad evolved and rebounded. Their bodies grew smaller,and were likely to use fewer resources in a resource-poor environment. Genetically rescued populations—the ones with extra genes from one beetle—had thelargest population sizes at the end of the experiment,compared with demographic rescue and control pop-ulations. But surprisingly, Hufbauer says, even some ofthe control populations survived. “We fully expected,”she says, “that they would really go extinct,” but they“were able to adapt and rescue themselves, essentially.”Natural selection acted on the beetles’ existing genes, itseemed, yielding the same U-curve predicted in 1995. Itwas the telltale signature of evolutionary rescue.

Over the last 25 years, studies such as this one havetaken evolutionary rescue from the realm of purelytheoretical to experiments with actual populations ofmulticellular organisms. “Now people have confidenceit’s not just in mathematicians’ brains and petri dishes,”Gonzalez says. But making the leap from yeasts andbeetles in the lab to organisms in the wild has beenmuch harder, researchers acknowledge. Even workingwith small laboratory critters means monitoring hundredsof replicate populations evolving over generations—afeat of tracking that’s much harder in the bush. Whatcan rapid evolution really do to prevent extinction in thewild, Gonzalez asks? “That turns out to be a questionof enormous applied value.”

Adaptive FlexibilityRescue favors the easily overlooked, smaller creatures.Organisms that swarm in large numbers, reproduce

quickly, and have many young, studies suggest, aremost likely to evolve their way out of extinction. Newfield studies hint at evolutionary rescue in wild pop-ulations of rats, rabbits, phytoplankton, and minnowscalled Atlantic killifish (9–11). A 2016 study, for exam-ple, found that killifish populations from filthy urbanestuaries tolerate industrial chemical concentrationshundreds to thousands of times higher than pop-ulations from cleaner sites, thanks to rapid selection ona handful of genes (12). Such examples suggest evo-lutionary rescue could be relevant to the real world—and that evolutionmay occasionally work fast enough inenvironments rapidly being degraded by people.

But wild cases are hard to verify. Take Kauai’s fieldcrickets. Even such a suggestive case—with an iden-tified mutation, that’s beneficial and widespread—isn’t definitively evolutionary rescue. Crickets and fliescoexist on other Hawaiian islands too, where flatwingmales are much rarer, suggesting Kauai’s populationmight not have needed the mutation to avoid goingextinct. If the crickets weren’t headed for oblivion,then their rebound wouldn’t qualify as rescue.“There’s always some uncertainty,” Gonzalez says.

Real-world populations don’t live in the isolation ofa petri dish, and evolutionary adaptation isn’t theironly tool to deal with environmental change. Newbehaviors and migration can also help a populationsurvive stressful situations.

In the cricket’s case, it seems a combination of ge-netic change over time across the population, as well asbehavior, helped their populations rebound. A silentmale might be safe from the fly, but staying quiet

Mixed populations, as in the case of snowshoe hares,probably offer the best odds of evolutionary rescue,wildlife biologist Scott Mills argues, because they havethe most genetic raw material for natural selection to acton. Image credit: Scott Mills (University of Montana,Missoula, MT).

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presents mating challenges. “How does a female findyou?” says Zuk, who’s now at the University ofMinnesotain St. Paul. “And even if she finds you, what’s going tomake her mate without a song?” A behavior of the silentmales may have been key. They hang around the fewsinging males in the grass and intercept females headedthe same way. All crickets will sometimes carry out thisso-called satellite behavior, Zuk says, but it “seems to bemore pronounced in places with the flatwings.” Zukthinks the mutation found a toehold because of sat-ellite behavior (13). Evolution alone didn’t save thecrickets; behavior helped it along.

This sort of behavioral flexibility in a changing envi-ronment is one example of phenotypic plasticity—theability to display different traits under different circum-stances. It can look a lot like evolution, but it’s not. Ants inthe genus Pheidole, for example, carry genes for hugeheads and bodies, which most species normally don’texpress. The genes can be expressed, however, in larvaeexposed to a juvenile hormone, according to a 2012study in Science (14). Ants born after exposure to thehormone grow into super-soldier–like adults with massiveheads. But the ants aren’t evolving. Huge-head genesalready existed in the population, sleeping in the genome.

Adaptation—becoming better suited to the envi-ronment—can happen by evolution (as in geneticchange over time) or by changing gene expression sothe same genotype shows a new phenotype (as in theants). One reason that wild cases of evolutionary res-cue are so hard to prove, Gonzalez says, is becausephenotypic plasticity and evolutionary adaptation canlook so alike. Pure plasticity, as in the ants’ case, isn’trescue. But when plasticity and genetic change arecombined, as in the crickets, evolutionary rescue canoccur. Zuk’s case seems to be rapid evolution madepossible by phenotypic plasticity; the silent-wing genewouldn’t have spread without a way for males andfemales to find each other and mate.

A Natural AllySo what can rapid evolution really do in the wild, andwhat are its limits? Scott Mills chuckled at that question,on the phone from his office at the University of Mon-tana in Missoula. “That’s it,” he says. “We don’t know.”Mills and other wildlife biologists want to make evolu-tion an ally in the race to conserve disappearing spe-cies. Montana’s winter mountains give them a uniquevantage to ask how.

On the hillsides there, a long list of predators preyon snowshoe hares—“the candy bar of the forest,”Mills says. Camouflage is a hare’s best defense. Theanimals blend in with the landscape by growing abrown coat in spring, which turns snowy white as thedays grow short in fall. But as Montana’s climatechanges, snow is falling later, and melting earlier inthe season, leaving hares mismatched with their en-vironment and very visible to predators. Snowpack isexpected to decrease by roughly 40 to 69 days inwestern Montana this century (15). “White animals onbrown ground stick out,” Mills says. “Our hares inMontana get clobbered in weeks where they’re whiteon brown background.”

Mismatched hares can’t keep pace with warmerwinters and decreasing snow because their trigger tomolt and shed isn’t temperature; it’s day length. Millshas found that hares don’t have much phenotypicplasticity to change their coats, overriding day lengthfor another seasonal cue. “So then we have to ask,” hesays, “is there a possibility to adapt fast enough, vianatural selection?”

The answer is: maybe. In more southerly parts ofthe snowshoe hare range, such as coastal Oregon andWashington, snow is unpredictable and rarely sticks.Hares there keep a brown coat year-round, moltingand shedding from brown to brown. A single gene isresponsible, which came frommating with black-tailedjackrabbits, and spread through snowshoe hare pop-ulations living in low-snow conditions, Mills reportedlast June (16).

Liaisons with another species can accelerate evolu-tion, but unless they coincide with population declines

and high-speed environmental change, they don’tqualify as rescue. In this case, the winter brown coatsprobably spread through Pacific Northwestern haresbetween 3,000 and 15,000 years ago, so it’s hard to saywhether it initiated rescue or not in those populations.But the adaptive brown gene showedMills that climatecan shape coat color. “Not many traits are as de-finitively shaped by climate as this one,” Mills says.“Because whether you’re mismatched is 100% de-termined by the average persistence of snow.”

When could a trait shaped by climate help speciessurvive the kind of rapid change Mills is seeing inMontana? He figured that polymorphic populations—where winter white and winter brown hares coexist—would offer the richest palette for natural selection toact on and, therefore, the highest odds of evolutionaryrescue. In another 2018 article, Mills showed, usingdata from natural history collections, that polymorphicpopulations of hares and other seasonally coat-changing species pop up across the Northern Hemi-sphere (17). In places such as Washington’s CascadeMountains, both hare color morphs hop betweenpatches of snow and towering red cedars. Hares aren’tendangered, but they illustrate how conservationmight embrace polymorphic areas, such as the Cas-cades, where evolutionary rescue is most likely.

Although Mills isn’t certain rescue can happen inthis case, he sees the hare’s story as a metaphor for theconservation community because evolutionary rescueis “nowhere on the radar of reserve design.” It’s beenclear since the first theory article in 1995 that largepopulations are more likely to rescue with a man-ageable extent of environmental change. Subsequentstudies showed connected populations, with migra-tion, gene flow, and some history of similar stress may

“The promise of evolutionary rescue, is that maybe somefraction will recover, maybe there is some hope.”

–Andrew Gonzalez

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be the most likely to adapt and survive. But how ex-actly humans might foster rapid evolution is the nextunanswered question, Mills says—one that “goes tothe heart of climate resilience for wild species.”

How effective reserves could be depends heavilyon the rate of climate change, Gonzalez adds.Whether Earth sees 2 °C or 4 °C of warming andwhether that’s in 50 years or 100 or 200 will decidewhich populations are even candidates. Polar bearsand other charismatic mammals aren’t likely con-tenders because their generation times are long.Evolutionary rescue takes 10 to 100 generations, hesays, meaning hundreds of years for large mammals.Rapid change will outpace them before rescue kicksin. Faster-breeding creatures, such as insects, are thebetter bet. Indeed, Kauai’s field crickets shifted fromchirping to 90% silent males in fewer than 20 genera-tions, or about a decade. Even so, Gonzalez would stillchoose policies that slow down climate change and

keep populations big and connected, he says, to“allow evolutionary rescue to be a possibility, even ifit’s not likely.”

The next frontier for the field may be studying it atcommunity levels. Individual populations are woveninto communities, so when one group rescues, theremay be domino effects for the species it interacts with,Gonzalez explains. Stressing whole ecosystems—suchas small ponds teeming with bacteria, water bugs, andfish—and then watching as adaptation unfolds (ordoesn’t) at multiple trophic levels could help clarifycommunity evolutionary rescue’s role in the fate ofecosystems themselves.

Understanding rapid evolution may not stop manyextinctions, but it could lead to conservation policies thatmaximize the potential for rescue. Considering howbleakthe story ofman’s impact onwildlife can be, “the promiseof evolutionary rescue,” Gonzalez says, “is that maybesome fraction will recover, maybe there is some hope.”

1 A. C. Mason, M. L. Oshinsky, R. R. Hoy, Hyperacute directional hearing in a microscale auditory system. Nature 410, 686–690 (2001).2 R. M. Tinghitella Rapid evolutionary change in a sexual signal: Genetic control of the mutation ‘flatwing’ that renders male fieldcrickets (Teleogryllus oceanicus) mute. Heredity 100, 261–267 (2008).

3 R. Gomulkiewicz, R. D. Holt, When does evolution by natural selection prevent extinction? Evolution 49, 201–207 (1995).4 G. Bell, A. Gonzalez, Evolutionary rescue can prevent extinction following environmental change. Ecol. Lett. 12, 942–948 (2009).5 S.M. Carlson, C. J. Cunningham, P. A. H.Westley, Evolutionary rescue in a changingworld. Trends Ecol. Evol. (Amst.) 29, 521–530 (2014).6 P. W. Hedrick, R. Fredrickson, Genetic rescue guidelines with examples from Mexican wolves and Florida panthers. Conserv. Genet.11, 615–626 (2010).

7 J. H. Brown, A. Kodric-Brown, Turnover rates in insular biogeography: Effect of immigration on extinction. Ecology 58, 445–449 (1977).8 R. A. Hufbauer et al., Three types of rescue can avert extinction in a changing environment. Proc. Natl. Acad. Sci. U.S.A. 112, 10557–10562 (2015).

9 E. Vander Wal, D. Garant, M. Festa-Bianchet, F. Pelletier, Evolutionary rescue in vertebrates: Evidence, applications and uncertainty.Philos. Trans. R. Soc. Lond. B Biol. Sci. 368, 20120090 (2013).

10 G. Bell Evolutionary rescue and the limits of adaptation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 368, 20120080 (2013).11 A. Whitehead, B. W. Clark, N. M. Reid, M. E. Hahn, D. Nacci, When evolution is the solution to pollution: Key principles, and lessons

from rapid repeated adaptation of killifish (Fundulus heteroclitus) populations. Evol. Appl. 10, 762–783 (2017).12 N. M. Reid et al., The genomic landscape of rapid repeated evolutionary adaptation to toxic pollution in wild fish. Science 354, 1305–

1308 (2016).13 M. Zuk, J. T. Rotenberry, R. M. Tinghitella, Silent night: Adaptive disappearance of a sexual signal in a parasitized population of field

crickets. Biol. Lett. 2, 521–524 (2006).14 R. Rajakumar et al., Ancestral developmental potential facilitates parallel evolution in ants. Science 335, 79–82 (2012).15 L. S. Mills et al., Camouflage mismatch in seasonal coat color due to decreased snow duration. Proc. Natl. Acad. Sci. U.S.A. 110,

7360–7365 (2013).16 M. R. Jones et al., Adaptive introgression underlies polymorphic seasonal camouflage in snowshoe hares. Science 360, 1355–1358 (2018).17 L. S. Mills et al., Winter color polymorphisms identify global hot spots for evolutionary rescue from climate change. Science 359,

1033–1036 (2018).

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