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Citation Grant, Peter R., B. Rosemary Grant, Raymond B. Huey, Marc T. J.Johnson, Andrew H. Knoll, and Johanna Schmitt. 2017. EvolutionCaused by Extreme Events. Philosophical Transactions of the RoyalSociety B 373, no. 1723: 20160146.

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1

Evolutionary responses to extreme events 1

2

Peter R. Grant1, B. Rosemary Grant1, Raymond B. Huey2, Marc 3

T. J. Johnson3, Andrew H. Knoll4 and Johanna Schmitt5 4

5

1 Department of Ecology and Evolutionary Biology, Princeton 6

University, Princeton, N.J. 08544, USA 7

2 Department of Biology, University of Washington, Seattle, 8

WA 98195, USA 9

3 Department of Biology, University of Toronto-Mississauga, 10

Mississauga, ON L5L 1C6, Canada 11

4 Department of Organismic and Evolutionary Biology, 12

Harvard University, Cambridge, MA 02138, USA 13

5 Department of Evolution and Ecology, University of 14

California, Davis, CA 95616, USA 15

16

Extreme events can be a major driver of evolutionary change 17

over geological and contemporary timescales. Outstanding 18

examples are evolutionary diversification following mass 19

extinctions caused by extreme volcanism or asteroid impact. 20

The evolution of organisms in contemporary time is typically 21

viewed as a gradual and incremental process that results from 22

genetic change, environmental perturbation, or both. However, 23

2

contemporary environments occasionally experience strong 1

perturbations such as heat waves, floods, hurricanes, droughts 2

and pest outbreaks. These extreme events set up strong 3

selection pressures on organisms, and are small-scale 4

analogues of the dramatic changes documented in the fossil 5

record. Because extreme events are rare, almost by definition, 6

they are difficult to study. So far most attention has been given 7

to their ecological rather than to their evolutionary 8

consequences. We review several case studies of contemporary 9

evolution in response to two types of extreme environmental 10

perturbations, episodic (pulse) or prolonged (press). Evolution 11

is most likely to occur when extreme events alter community 12

composition. We encourage investigators to be prepared for 13

evolutionary change in response to rare events during long-14

term field studies. 15

16

Key words: adaptation; physiology; long-term studies; 17

extinction 18

19

1 Introduction 20

The history of life on Earth has been a series of evolutionary 21

expansions of biological diversity that were repeatedly 22

reversed by minor or major geophysical disturbances [1]. 23

3

Perturbations originated either endogenously within the Earth 1

(e.g. volcanoes) or exogenously from without (e.g. impacts of 2

extra-terrestrial bodies). Through direct and indirect (climatic) 3

effects these catastrophic events decimated communities in 4

often non-random ways, with the result that diversity renewal 5

began from compositionally altered communities and took new 6

evolutionary directions [2]. 7

Today human activities are causing increases in 8

atmospheric CO2 and global temperatures at a rate 9

unprecedented in recent geological history, with concomitant 10

shifts in rainfall patterns and species distributions. Climate 11

change, increased CO2 and its direct physiological effects, and 12

deoxygenation of subsurface water masses in the oceans are 13

tightly linked in the Earth system and influence populations of 14

organisms simultaneously and synergistically. 15

According to the Inter-Governmental Panel on Climate 16

Change (IPCC) the probability of extreme climatic events 17

associated with global warming is also increasing [3-4]. This 18

has alerted ecologists to the likelihood of more frequent or 19

more severe disturbances to ecological communities caused by 20

droughts, storms, exceptional rainfall, heat waves, fires and 21

abrupt changes in ocean circulation [3,5-8]. Indeed on a small 22

4

and local scale this has been quantified, following droughts [9] 1

and floods [10]. 2

The purpose of this article is to consider how extreme 3

contemporary events are responsible for evolutionary change 4

as well as ecological change [11,12]. We begin by discussing 5

the scale and scope of extreme events. We then review the role 6

of physiology, and studies of isolated fish populations, birds on 7

islands, plant populations and plant-animal interactions, 8

before returning to the really long-term context of geological 9

history. Contemporary evolution in response to extreme events 10

has been studied rarely simply because such events themselves 11

are rare. Understanding contemporary evolution will be 12

improved by a combination of short-term perturbation 13

experiments and long-term studies that opportunistically take 14

advantage of rare events. 15

16

2 Scope and scale 17

Our survey of contemporary evolution is concentrated on, but 18

not restricted to, climate and the effect of extreme events on 19

evolution. The scope is set by the way we treat the words 20

extreme and event. Extreme events are close to, at, or beyond 21

the limits of the normal range of phenomena experienced by 22

organisms, and are rare almost by definition. A high 23

5

temperature recorded only twice a century is both extreme 1

and rare. On the other hand the highest summer temperature 2

and the lowest winter temperature are extremes within a year, 3

but may not be exceptional in any one year when compared 4

with the long-term record of maxima and minima. So it is 5

important to place “extreme” in temporal context [13]. 6

We distinguish between a process and an event. A process 7

is continuous through time whereas an event is an occurrence. 8

Speciation is a process, whereas mutation is an event. A rise in 9

temperature is a process whereas a maximum temperature is a 10

single occurrence. Bender et al. [14] made a similar distinction 11

in describing natural or experimental perturbations to the 12

environment as either discrete (pulse) or prolonged (press). 13

The distinction between process and event, prolonged or 14

discrete, is blurred when an unusual event (e.g. 9 month-long 15

1982-83 El Niño event) lasts for an appreciably long time [15]. 16

This is another example of the importance of temporal scale 17

and context of the event. 18

Climate modelers predict that the frequency of climatic 19

extremes will increase as the Earth warms continuously. And, 20

as mean temperature rises, the maxima may become even 21

more extreme. Another possibility is they will become more 22

frequent {3,9,16] and hence less rare. Wherever we can make 23

6

the distinction we will focus on the extremes and not on the 1

mean, the variance or the process of gradual change and 2

trends: other articles in this issue attend to those. 3

It is natural to focus on physical phenomena as extreme 4

events. However biological events may also be extreme, and 5

these can have climatic or other causes as well as evolutionary 6

consequences. For example, colonization by an invading or 7

immigrating species results in new interactions among 8

members of a food web, potentially leading to new selection 9

pressures and evolutionary change in some of the residents as 10

well as the immigrants [17]. A second example is evolution that 11

is set in motion by extinction. Mass extinctions at the end of the 12

Permian due to exceptionally prolonged and extensive 13

volcanism, and additional extinctions at the end of the 14

Cretaceous, gave rise to strong evolutionary responses of the 15

survivors, with major new clades arising and proliferating [2]. 16

Extreme events themselves did not cause evolution -- they set 17

up the conditions that promoted evolution. Evolution 18

facilitated by extinction of some species may be an undetected 19

factor in modern communities subject to changing climate. 20

These extreme events in time may be coupled with 21

extremes in space. For example organisms encounter limits to 22

their physiological tolerance to water, heat, or chemical 23

7

environment when they enter new environments at or beyond 1

their normal geographical borders, and are then subject to 2

strong selection [18]. One example is the entry into freshwater 3

of marine-adapted fish, such as sticklebacks [19]. Another is 4

the reverse, invasion of the marine environment by freshwater 5

organisms [20]. A third example is the entry into arid 6

terrestrial environments by organisms adapted to mesic 7

conditions. This must have happened many times in the history 8

of arthropods, reptiles [21], plants [22] and other taxa. 9

Environmental conditions at the margins of geographical 10

distributions are likely to be extreme -- that is often why those 11

locations are margins. Diurnal, seasonal or annual fluctuations 12

in limiting factors in such environments put strong 13

evolutionary pressures on organisms that live at the 14

boundaries [23,24], and those pressures are expected to 15

increase in the future at some boundaries while being relaxed 16

at others. 17

How organisms respond to extreme environmental 18

conditions depends in part on their behavior, prior exposure to 19

extremes, how phenotypically plastic they are, the degree to 20

which they are genetically variable in fitness-related traits, and 21

demographic factors such as life-span and dispersal (gene 22

flow) [25], as well as the magnitude of deviations from average 23

8

environmental conditions, and on how long those conditions 1

persist relative to the life span of organisms. The rate and 2

duration of environmental change in extreme conditions may 3

be more important than the magnitude of change in 4

determining whether the outcome is extinction, a shift in 5

geographical distribution, or local evolution and persistence 6

[20, 26-28]. 7

We make the traditional distinction between an 8

environmental event and the response of a population to it. 9

Ecologists, especially those concerned with ecophysiological 10

[11] or ecosystem-level [29] effects of unusual weather on 11

plants, combine events and responses in a single definition of 12

extreme events. This has the advantage of avoiding the many 13

cases of normal responses to unusual events. Moreover 14

operational definitions are invaluable for comparative 15

purposes. Our task is to identify or anticipate any evolutionary 16

response to an unusual event. For this the general conception 17

as outlined above is more useful than a precise definition. In 18

the future extreme events might be defined as those with 19

magnitudes outside the 95 percentiles of long-term 20

measurements. 21

22

3 Evolution of physiology 23

9

The ecological and evolutionary impacts of extreme abiotic 1

events are often mediated through an organism’s behavior and 2

physiology [30,31]. Behavioral evasion is often a mobile 3

organism’s first line of defense against environmental 4

extremes [32], but physiology helps transduce environmental 5

variation – extreme or not – into performance and fitness. 6

Behavior and physiology are thus key filters and buffers of 7

environmental challenges. 8

Extreme events can affect physiological performance by 9

depleting environmental resources, altering physiological 10

rates, inducing stress, elevating mortality, or even reshuffling 11

community composition (§ 6). In so doing, they can alter 12

selective agents as well as the genetic composition of 13

populations. If associated mortality randomly reduces standing 14

genetic variation, the extreme event will retard future adaptive 15

evolution; but if mortality is selective, the event may enhance 16

future tolerance [31,33,34]. 17

Most field studies documenting rapid evolutionary shifts 18

in physiology involve responses to gradual and sustained 19

environmental change (e.g., climate warming), and so the 20

involvement of extreme events is unclear. Still, standing 21

genetic variation for physiological tolerance traits is evident 22

from numerous laboratory studies, implying evolutionary 23

10

responses to extreme events in nature are possible. For 1

example, laboratory (and mesocosm) selection experiments, 2

which force organisms to experience a sudden and permanent 3

change in environmental conditions, result in rapid 4

physiological shifts [35]: such protocols mimic perturbations 5

that are acute and permanent (e.g., island uplifts, § 4, or 6

myxoma virus, § 7). Similarly, artificial selection experiments, 7

which subject experimental lines to an extreme temperature 8

every generation, also typically lead to increased heat 9

tolerance [36]: however, these protocols are poor mimics of 10

most natural extremes, which are rare and episodic [33]. 11

Consequently, such protocols prevent reversion of the genetic 12

constitution of experimental lines towards the pre-extreme 13

state [34]. Most importantly, both types of experimental 14

evolution eliminate any option for behavioral evasion and also 15

generally eliminate involvement of other selective agents (e.g., 16

predators). Not surprisingly, the evolved phenotypes do have 17

enhanced tolerance but often would never survive in nature 18

[37]. Experimental evolution thus demonstrates that extreme-19

driven shifts in physiology are feasible, but more realistic 20

experimental designs are needed. 21

Field translocation studies also suggest that standing 22

genetic variation can be sufficient to permit a selective 23

11

physiological response to an extreme event. When lizards were 1

forcibly introduced onto a hot Caribbean island, survival was 2

highest in individuals that ran relatively quickly at high 3

temperature [38]. Similarly, when marine stickleback fish were 4

transferred to (relatively cold) freshwater ponds, their cold 5

tolerance evolved within three years [39]. 6

Potential physiological impacts of extreme events have 7

recently been explored with evolutionary models. One was 8

motivated by high mortality that intertidal limpets suffered on 9

days with high air temperatures, high solar radiation, plus low 10

wind speeds [33]: A statistical model (“environmental 11

bootstrap”) generated a time series with long periods of benign 12

conditions, punctuated with rare clusters of extreme events. 13

Next, heat-transfer models mapped environmental variations 14

onto body temperature and onto risk of heat stress, which 15

were used as input values for an allelic evolutionary model. 16

Simulations suggested that rare heat events will lead to the 17

evolution of upper lethal temperatures in limpets that are 5 to 18

7°C above the average annual maximum temperature: this 19

“thermal safety margin” in fact approximates that observed for 20

limpets. 21

A quantitative genetic model and an extension recently 22

explored impacts of extreme temperatures on overall thermal 23

12

sensitivity, not just extreme heat tolerance [31,34]: rare 1

extreme events (even only one every 20 years) shifted the 2

shape and position of thermal performance curves, especially 3

when extreme events cause death or persistent injury, or when 4

behavioral evasion and acclimation was blocked. This model 5

correctly predicted a shallow latitudinal gradient in heat 6

tolerance of Drosophila from eastern Australia, even though 7

mean temperature varies substantially with latitude. 8

Mass mortality following extreme events is commonly 9

reported and will deplete genetic variation (perhaps 10

selectively), but documented genetic shifts following such 11

events are rare. An extreme heat wave in Europe in spring 12

2011 caused frequencies of chromosome inversions of 13

Drosophila subobscura to shift transiently to summer-like 14

frequencies, implying survivors were relatively heat tolerant 15

[40]. Similarly, an algal bloom along the California coast in 16

2011 was implicated in causing mass mortality and genetic 17

shifts in abalone [41]. 18

An ideal design for a study of the evolutionary effects of 19

extreme events might adopt a factorial controlled experiment. 20

One would monitor physiological sensitivity, behavior, 21

demography, and the genetic underpinnings thereof, in 22

replicate populations, only some of which would experience 23

13

the extreme event. One would monitor all populations before, 1

during, and after an extreme event, and ideally then replicate 2

the entire “experiment” with another set of populations during 3

an independent extreme episode. Such an ideal study could be 4

approximated by intentionally collecting tissues at intervals in 5

sites where extreme events are likely to occur (and in 6

protected sites nearby): if an event occurs, then “forensic 7

genomics” could quantify genetic and likely physiological 8

impacts [41]. Alternatively, studies that have been repeatedly 9

sampling populations for unrelated reasons can take 10

advantage of an extreme event [40,42]. They would be most 11

useful if genetically informed. 12

13

4 Fish in a new environment 14

Our first example of evolution of a population in contemporary 15

time provides a link with geophysical perturbations in the past 16

(§ 8) and exemplifies evolution in response to a press 17

perturbation. The largest earthquake ever recorded in North 18

America occurred on 27 March 1964. It uplifted islands in 19

Prince William Sound and the Gulf of Alaska by as much as 20

3.4m, thereby creating freshwater ponds from marine habitat. 21

Sticklebacks (Gasterosteus aculeatus) colonized many of these 22

ponds from the marine environment. Their subsequent 23

14

evolution was documented by a detailed genomic study of 1

several populations from samples collected in 2005 and 2011, 2

that is 25-50 generations after the ponds were colonized. In 3

this short time the sticklebacks had diverged phenotypically 4

and genetically [43]. The environmental perturbation lasted a 5

day; the response took less than 50 years. 6

Genetic reconstruction confirmed that the freshwater 7

populations were derived several times from the marine 8

population and not from previously existing freshwater 9

populations on Middleton and Montague islands [43]. Six new 10

populations on Middleton Island rapidly diverged from each 11

other, and even more from a nearby marine population, 12

independently and in parallel. This happened despite recurring 13

gene exchange between freshwater populations, and between 14

them and the marine population, as indicated by some 15

discordant phenotypic and genetic variation. A repeated 16

reduction in lateral plate number was accompanied by shifts in 17

traits used in foraging, defense and swimming. Because all the 18

traits have a known genetic basis [44,45] the response to a 19

new environment was genetic and not solely phenotypic. These 20

traits have been well studied and the changes are in accord 21

with what is known about adaptation to the freshwater 22

environment [46,47]. 23

15

The rapidity and magnitude of the changes are striking. 1

Fst analysis showed that freshwater populations established 2

after 1964 have diverged from marine ancestors nearly as 3

much as have older post-glacial freshwater populations on the 4

mainland that were formed 13 thousand years ago [43]. The 5

new findings suggest that most evolution occurs rapidly in a 6

new habitat. This example can be considered a prolonged 7

process over a few decades, or a pulsed event on the scale of 8

millennia [14]. Proponents of punctuated equilibria in the 9

fossil record make a similar claim of rapid early evolution 10

followed by stasis [48]. 11

12

5 Demography of birds 13

Demographic studies are a powerful and direct way to 14

investigate evolution, but need to be long-term to have a 15

chance of assessing evolutionary consequences of extreme 16

environmental events [13]. Those events are pulsed 17

perturbations that punctuate long periods of comparative 18

stability or gradual environmental change [8]. 19

The first, opportunistic, and short-term study was carried 20

out by H.C. Bumpus [49] after an exceptional ice- and snow-21

storm hit Providence, Rhode Island in February 1898. Bumpus 22

collected 136 specimens of the introduced house sparrow 23

16

(Passer domesticus) that he found on the ground, and measured 1

72 that survived and 64 that died. Surviving males were 2

relatively large, while surviving females were of intermediate 3

size. Together with more recent studies of swallows [50], the 4

study suggests natural selection had occurred in response to 5

an extreme climatic event. However both expose the 6

difficulties of interpreting survival patterns from samples 7

taken at the same or different times [51,52]. Longitudinal 8

studies are needed to infer the role of selection, inheritance of 9

selected traits, and trans-generational evolutionary responses. 10

Two types of extreme climatic events occurred during a 11

40-year study of ground finches (Geospiza spp.) on the small 12

Galápagos island of Daphne Major (1973 - 2012): an 13

abundance of rain and two drought years in sequence. The first 14

was an extremely intense and prolonged El Niño event in 15

1982-83 resulting in 1.3 m of rain falling on the island. From 16

coral core data it was estimated to be the most severe such 17

event in more than 400 years [15]. The abundant rain caused a 18

change in the composition of the vegetation, which became 19

dominated by plants that produce small and soft seeds. The 20

change had a selective effect on medium ground finch (G. 21

fortis) survival during a drought in 1985 when only 4 mm of 22

rain fell and food became scarce: birds with small and pointed 23

17

beaks had a selective advantage. The second extreme event 1

was a two-year drought (2003-05). G. fortis with large beaks 2

were outcompeted by G. magnirostris, the large ground finch, 3

for a dwindling supply of large seeds. 4

Evolution occurred in response to natural selection each 5

time because morphological traits are highly heritable [54]. 6

Notably two variants of a gene (HMGA2) with major effects on 7

beak size changed in frequency in the expected direction as a 8

result of natural selection in 2004-05 [55]. Evolution was 9

genetically predictable but environmentally unpredictable 10

[56]. There is an element of chance in what constitutes the food 11

environment at any one time, and when major perturbations 12

occur; hence evolution is partly stochastic. An extreme event 13

can have mild or strong effects depending on the state of the 14

environment when it occurs. For example in 2003, when seeds 15

were abundant at the beginning of a drought, selection on beak 16

size did not occur despite high finch mortality. Natural 17

selection only occurred in 2004, the second year of a prolonged 18

drought and food scarcity [53]. Similarly, selection did not 19

occur in the only other two-year drought (1988-89) owing to 20

an abundant production of seeds in the strong El Niño event of 21

1987 [15]. 22

18

Combinations of extreme events [5,7], and not just the 1

single events themselves, may be unusually potent factors by 2

permitting or causing evolution. Two unrelated and 3

improbable events with long-term consequences occurred on 4

Daphne Major Island in the 1980s [15]. First, a single hybrid 5

male ground finch (G. fortis x G. scandens) immigrated in 1981. 6

It produced offspring by breeding with G. fortis. The drought of 7

2004-05 reduced this new lineage to two individuals, a brother 8

and a sister, which bred with each other in 2005 and in 9

subsequent years. The next two generations were entirely 10

endogamous, and hence the lineage was behaving as an 11

incipient species. Second, two female and three male G. 12

magnirostris immigrated to Daphne in 1982 and established a 13

breeding population at the end of the year. Both colonizations 14

are remarkable because none are known to have occurred 15

elsewhere in the archipelago since the end of the nineteenth 16

century when collectors for museums visited all islands in the 17

archipelago and documented the distributions of finch species. 18

Almost certainly an important factor in the success of both 19

colonizations was the unusually favorable ecological 20

conditions caused by the exceptionally prolonged El Niño 21

event in 1982-83. 22

19

The two colonization events were not initially connected. 1

Twenty years later a connection was made when G. 2

magnirostris determined the fate of the hybrid lineage by 3

competitively eliminating most of the large members of the G. 4

fortis population during the drought of 2003-05 [53]. The 5

hybrid lineage is ecologically similar to G. fortis. Without the El 6

Niño event and the population of G. magnirostris that it 7

fostered, the hybrid lineage may not have been able to persist 8

beyond 2004. Rare and extreme events need not be exactly 9

coincident to have profound and long-lasting effects, and the 10

consequences may emerge after a long delay, as these 11

examples illustrate [15]. 12

They also illustrate another principle of general 13

significance: a population that evolves as a result of a press 14

perturbation does not necessarily evolve back to its original 15

state. G. fortis remained small on average after 2005 because 16

the composition of the finch community had changed. The 17

agents of change --- G. magnirostris and the hybrid lineage --- 18

rapidly increased in numbers after the drought. 19

20

6 Evolutionary responses of plant populations 21

In many plant species, populations across the species range 22

exhibit the signature of past adaptation to climate. For these 23

20

species, a critical question is whether local populations will be 1

able to evolve fast enough in situ to survive extreme events, 2

track rapid climate change, and thus avoid extinction [57,58]. 3

This question is particularly important for long-lived species 4

such as forest trees, which are likely to experience rare 5

extreme events combined with rapid climate change over 6

decades within individual lifetimes. Relevant data are scarce. 7

Even less is known about how increasing atmospheric CO2 8

interacts with climate change to affect plant performance and 9

evolutionary potential in nature. A few studies have used 10

historical data and/or resurrection studies of banked seeds to 11

demonstrate rapid evolutionary response to extreme events or 12

the press of climate warming on decadal scales. However, 13

whether this rate of adaptation is sufficient to allow 14

evolutionary rescue remains an open question. 15

One of the best examples of plant evolutionary response 16

to an extreme climatic event comes from a resurrection study 17

of the annual field mustard Brassica rapa [42,59]. The 18

investigators collected a large sample of seeds from two 19

California populations in 1997, after several wet years, and 20

again in 2004 after several years of severe spring drought. 21

They then grew population samples of genotypes collected in 22

1997 and in 2004 together in a common garden. The 2004 23

21

genotypes flowered significantly earlier in the common garden 1

than the 1997 genotypes. Experimental water manipulations 2

showed that early drought onset strongly selected for earlier 3

flowering, evidence that the observed evolutionary change was 4

adaptive. 5

These B. rapa populations also display a genomic 6

signature of temporal drought adaptation [42]. A genome-wide 7

scan for Fst outlier-loci found 855 genes with significant 8

temporal differentiation in allele frequencies between the 9

1997 and 2004 samples. Many had annotations suggesting 10

involvement in flowering time and drought response. However, 11

only 11 genes exhibited parallel shifts in allele frequencies in 12

both populations. Thus, rapid adaptation to drought in the two 13

populations appears to have occurred along largely 14

independent trajectories. 15

Extreme climate events may also result in strong 16

selection episodes in longer-lived plants such as trees. For 17

example, a severe heat wave and drought in 2003 resulted in 18

selective mortality of Douglas fir trees in a common garden 19

experiment in France [60]. Surviving trees had higher stem 20

wood density, ring density, and latewood density than did 21

trees that died, probably because these traits conferred 22

drought-resistant hydraulic properties [60]. If these traits are 23

22

heritable then strong selection by this extreme event could 1

have produced rapid evolutionary response. Long-term 2

monitoring of forestry provenance trials, where tree genotypes 3

originating from multiple populations are grown in common 4

gardens in multiple sites, could provide an excellent 5

opportunity to investigate the genetic basis of selective 6

mortality in response to extreme climate events [61]. 7

Long-term studies have demonstrated phenological 8

changes in many plant species in response to the press of 9

climate change on a decadal scale. The question is how much 10

of this phenotypic change represents phenotypic plasticity vs. 11

adaptive evolution. Anderson et al. [62] combined data from 12

38 years of field observations of flowering phenology in the 13

Colorado Rocky Mountains with measurements of selection 14

and heritability in a quantitative genetic field experiment with 15

the perennial mustard Boechera stricta. They observed strong 16

selection for earlier flowering, and predicted that evolutionary 17

response to this selection could account for more than 20% of 18

the accelerated phenology observed in the long-term field 19

study. 20

A few other studies have documented contemporary 21

evolution in plant populations in apparent response to rapid 22

climate change. Nevo et al. [63] used a common garden 23

23

resurrection experiment to demonstrate rapid evolution of 1

earlier flowering from 1980 to 2008 in wild cereal populations 2

across Israel. Thompson et al. [64] observed an increase in 3

frequency of frost-sensitive but summer drought-tolerant 4

phenolic chemotypes, associated with a recent decline in the 5

frequency of severe freezing events in populations of 6

Mediterranean wild thyme (Thymus vulgaris). 7

Is adaptive evolution in plant populations fast enough to 8

keep up with the pace of contemporary climate change? This 9

question can be addressed by provenance trial experiments in 10

which accessions from a range of climates are planted into 11

common gardens across that climatic range. Wilczek et al. [65] 12

used banked seeds from geographically diverse accessions of 13

the annual plant Arabidopsis thaliana to establish common 14

garden experiments spanning the species’ European climate 15

range. Although they found evidence of historical adaptation 16

to local climate, the year of the field experiment was unusually 17

warm compared with historical averages. Consequently 18

accessions from lower latitudes with historically warmer 19

climates had higher fitness than did local genotypes- an 20

example of adaptational lag [57] in an extreme year. McGraw 21

et al. [66] also observed adaptational lag in a reciprocal 22

transplant experiment with the long-lived sedge Eriophorum 23

24

vaginatum across a climate gradient in Alaska. Seeds were 1

planted in 1980, and a 1993 census demonstrated local 2

adaptation: local genotypes had the highest fitness in each site. 3

However, when the experiment was recensused in 2010, 4

genotypes transplanted from the south had higher fitness than 5

local genotypes, suggesting that rapid warming has created a 6

mismatch between local genotypes and their new climate. 7

8

7 Species interactions and evolution 9

The evolutionary consequences of extreme events may 10

frequently be mediated indirectly via species interactions. Both 11

pulse and press extreme events frequently alter the abundance 12

of multiple species within communities [12]. These changes 13

can disrupt mutualisms, competition, and antagonistic 14

interactions. In this way, extreme events are expected to alter 15

the strength and direction of (co)evolutionary dynamics. 16

An example of how extreme events affect species 17

interactions is seen with herbivorous insects. Numerous 18

studies show that climatic extremes affect herbivore 19

performance and population dynamics. The most common 20

observation is that pulsed stresses, such as increased 21

temperature and drought, are associated with herbivore 22

population outbreaks [67]. For example, Europe experienced 23

25

an unprecedented heat wave and drought during 2003, which 1

was associated with outbreaks of multiple insect species [68]. 2

Similarly, population outbreaks of caterpillars in Nothofagus 3

forests in Patagonia have been associated with unusually warm 4

and dry periods over the last 155 years [69]. By contrast, 5

prolonged (press) climatic stresses frequently lead to 6

decreased performance and abundance of herbivores [67]. 7

Thus, pulse and press perturbations can both increase and 8

decrease the size of local herbivore populations. 9

Herbivores may also respond to extreme events by 10

expanding their range to form new populations and 11

associations with novel hosts [12]. In southern Europe, for 12

example, the pine processionary moth (Thaumetopoea 13

pityocampa, Lepidoptera, Notodontidae) expanded its 14

latitudinal range 87 km northward and its altitudinal range 15

230 m higher in response to climate warming between 1972 16

and 2004 [70]. In the record hot summer of 2003, this species 17

expanded its altitudinal range by an additional 33% on top of 18

all previous altitudinal range expansions [71]. This expanded 19

range persisted and facilitated T. pityocampa’s use of novel 20

host plants. These and similar results show that extreme 21

climate events can dramatically alter the ecology of plant-22

26

herbivore interactions, but how might this affect evolutionary 1

dynamics? 2

Recent experiments show that plant populations can 3

evolve rapidly in response to changes in herbivore 4

populations. Herbivores frequently impose strong selection on 5

plant traits [72], and most plant populations contain 6

substantial genetic variation in plant defenses against 7

herbivores [73]. Thus, any change in the abundance of 8

herbivore populations brought about by extreme events is 9

expected to alter subsequent selection on plant populations. 10

This prediction has been experimentally supported in recent 11

field experiments that manipulate the abundance of herbivores 12

as discussed below. 13

The first example of how extreme variation in herbivore 14

populations can affect plant evolution focuses on arthropod 15

populations. Agrawal et al. [74] used insecticides to manipulate 16

densities of arthropods feeding on genetically diverse 17

experimental field populations of evening primrose (Oenothera 18

biennis). They then followed the evolutionary dynamics of 19

these populations for four generations. Populations exhibited 20

rapid genetic and phenotypic divergence in response to the 21

manipulation of arthropod abundance, with the fastest changes 22

occurring in the first generation. In the presence of herbivores, 23

27

plant populations evolved by flowering later and producing 1

more chemical defenses against specialist seed predators. This 2

manipulation was not a direct result of an extreme climatic 3

event, but it clearly shows that large changes in herbivore 4

populations can cause rapid evolution in plants. 5

The second example involves rabbit grazers native to 6

Europe. Rabbits and other mammalian populations frequently 7

exhibit population cycles, but natural or human facilitated 8

disease represents an extreme event that causes drastic 9

population declines. In rabbits, such declines are caused by the 10

myxoma virus, which was introduced to rabbit populations in 11

Europe and Australia [75]. Recent evidence indicates that plant 12

populations can evolve in response to the loss of rabbit 13

grazers. Didiano et al. (76) experimentally manipulated the 14

presence or absence of rabbits in British grasslands for up to 15

34 years, approximating the timeframe of change that occurs 16

following the spread of myxoma virus. They found multiple 17

plant species evolved diverse morphological and life-history 18

responses to decreased grazing, including lower tolerance to 19

damage, slower growth and more upright growth forms. 20

Although these evolutionary changes happened simultaneously 21

across multiple species following the elimination of a grazer, 22

28

the evolutionary dynamics were species-specific and non-1

convergent. 2

Despite the evidence reviewed above, large gaps remain 3

in our understanding of how extreme events can affect 4

evolution via altered species interactions. In the case of plant-5

herbivore interactions, convincing evidence shows that 6

extreme events frequently lead to changes in the abundance of 7

species’ populations. Mounting evidence suggests that changes 8

in herbivore abundance can cause rapid evolution of plant 9

traits. However, no study has yet provided a complete 10

demonstration of the links between extreme events, herbivore 11

populations and plant evolution. All of the necessary 12

ingredients for these links are in place, but an explicit 13

demonstration represents an important avenue for future 14

research. 15

Although we have focused on plant-herbivore 16

interactions, extreme events can affect the evolution of any 17

type of species interaction. For example, endosymbionts 18

facilitate the evolution of increased heat tolerance of aphids 19

following a pulsed heat stress [77]. Competing microbes 20

rapidly use novel resources as a result of evolving when their 21

environment changes [78]. Similarly, beak shape of Darwin’s 22

finches evolves in response to drought, and the direction 23

29

depends on which competing finch species are present in the 1

community (§ 5). Such indirect effects of extreme events on 2

evolution have not been well studied owing to their inherent 3

complexity, and they represent an important frontier in linking 4

climate, community ecology and (co)evolution. 5

6

8 Lessons from the past 7

The geologic record makes it clear that humans have 8

experienced only a limited subset of the extreme climatic 9

events recorded through Earth history. What can we learn 10

from geologically extreme events? Does their sheer magnitude 11

limit their relevance to 21st century issues? Or, might they 12

underscore a continuity of pattern applicable to climatic 13

extremes at all scales? Indeed, might geologically extreme 14

events provide our best guide to predicting biological 15

responses to climate change at rates not previously 16

experienced by humans? 17

Extinction is the most commonly recorded response to 18

geologically extreme events. Extinction, of course, is inevitable 19

for eukaryotic species, and last appearances of fossil taxa occur 20

more or less continuously throughout the Phanerozoic Eon. 21

Such “background” extinctions probably reflect, at least in part, 22

minor climatic events not easily distinguished by geologists. At 23

30

rare moments, however, many species have gone extinct 1

simultaneously, disrupting ecosystem fabrics and, on million 2

year time scales, providing new evolutionary opportunities for 3

survivors. Paleontologists recognize five mass extinctions 4

during the past 500 million years, along with a dozen or more 5

lesser events of elevated extinction [79]. All reflect rapid and 6

transient environmental disruptions of global extent, but they 7

differ in terms of both causation and evolutionary 8

consequences. 9

Despite this, several features unite major extinction 10

events, and these are relevant to concerns about our 11

environmental future. First, enhanced rates of extinction 12

correspond to times of rapid climatic change, not to absolute 13

maxima and minima in temperature and precipitation. When 14

change is protracted, both physical and biological components 15

of the Earth system can accommodate. Populations respond 16

adaptively or migrate, while geophysical processes buffer 17

environmental effects. When change is rapid, however, 18

adaptation, migration and geophysical buffering are all 19

challenged. Although temperatures anticipated for the end of 20

the 21st century fall well below those characterizing much of 21

Earth history, the rates at which CO2 and, hence, temperature 22

are increasing are unique within the past 66 million years [80]. 23

31

The underlying state of the Earth system also appears to 1

influence the biological effects of rapid environmental 2

perturbation. For example, mass extinction near the end of the 3

Ordovician Period, some 445 million years ago, is associated 4

with a short-lived ice age [81]. Why did Ordovician ice sheets 5

result in widespread species loss, when relatively few marine 6

extinctions are associated with Pleistocene glaciation? A 7

reasonable answer is that Pleistocene ice sheets expanded in a 8

world in which continents were arrayed across wide stretches 9

of latitude, while sea level lay near its Phanerozoic minimum. 10

In contrast, the Ordovician ice age began in a world with 11

isolated, commonly equatorial continents inundated by 12

historically high levels of continental flooding. In consequence, 13

sea level drop associated with Ordovician ice sheets removed 14

much more habitable area for marine benthos than an 15

equivalent drop during the Pleistocene. At the same time, 16

Pleistocene continental distribution allowed more effective 17

migration in the face of climate change than was probable in 18

the Ordovician [81]. 19

Other extinction episodes also suggest the importance of 20

longer-term context of transient environmental perturbations 21

[82]. Relative to other times of enhanced volcanic activity, the 22

catastrophic biological consequences of end-Permian massive 23

32

volcanism may relate to both the state of late Permian oceans 1

(widespread subsurface dysoxia in the hemispheric 2

Panthalassic Ocean, amplifying the climatic and physiological 3

consequences of volcanism [83]; and the locus of volcanic 4

eruptions (Archean crust overlain by thick Proterozoic 5

carbonates [84]. And it may be that the uniquely disruptive 6

effects of end-Cretaceous bolide impact reflect a world already 7

stressed by Deccan Trap volcanism [85]. Indeed, the Holocene 8

extinction of large mammals in North America is thought to 9

reflect the combined influences of expanding human 10

populations and rapid environmental change characterized by 11

non-analog vegetation [86,87]. 12

It isn’t straightforward to align these one-two punches of 13

deep Earth history with press and pulse dynamics argued for 14

contemporary events, as the sustained stresses identified as 15

presses to ecologists may look like a pulse to geologists. 16

Nonetheless, the idea that longer-term context may condition 17

biological responses to short term events has relevance for 18

today. In the 21st century, “hit 1” is surely the direct effects of 19

humans on habitat disruption, pollution and overexploitation, 20

but the interaction of these processes with “hit 2” – global 21

warming – has yet to be fully explored or experienced. Geologic 22

history suggests that by mitigating the stresses of “hit 1” we 23

33

may minimize the biological consequences of emerging climate 1

stress. For better or worse, the coming century may prove a 2

unique moment when the large extremes recognized by 3

geologists and ecologically observed biological responses 4

coalesce. 5

The third commonality among mass extinctions lies in the 6

pattern and time scale of recovery. On million year timescales, 7

extinction pays an important evolutionary dividend: a 8

permissive ecology in which novel innovations fuel new 9

radiations. Mammals famously diversified in the wake of 10

dinosaur extinction, and marine teleosts radiated after end-11

Cretaceous extinction extirpated the ammonites [88]. More 12

generally, key Phanerozoic shifts in the structure and 13

composition of marine communities occurred during the 14

recovery intervals following mass extinctions [89]. 15

Unfortunately for us and for our grandchildren, the time scale 16

on which 21st century extinctions will pay evolutionary 17

dividends carries us a million years into the future. 18

19

9 Projections and conjectures for the future 20

Natural selection has been studied and quantified in numerous 21

species and environments but anticipating evolutionary 22

change in the future is still poorly grounded. The main reason 23

34

is that direct evidence for evolutionary responses of organisms 1

to extreme events in nature is almost entirely lacking, because 2

not enough information is available to distinguish between 3

genetic and non-genetic explanations for observed change in 4

use of habitats, morphology, physiology and diets. The scarcity 5

of genetic information is particularly acute in the marine 6

environment where calcareous organisms such as corals and 7

plankton are imperiled by increasing acidity arising from 8

elevated atmospheric CO2 levels [90]. Compounding the problem 9

for these organisms, extreme increases in sea surface 10

temperature associated with intense El Niño events cause mass 11

mortality of corals as well as fish (91). El Niño events are 12

expected to increase in intensity and frequency in the future 13

[16], and the unanswered question is whether marine 14

organisms are capable of an evolutionary response in the race 15

against extinction (reviewed in 89) 16

Attempts to predict evolutionary consequences of 17

extreme climatic events have languished, and few studies have 18

advanced beyond identifying factors promoting future 19

evolutionary change (rescue) in the face of gradual climate 20

change: reviewed by Bell [92] and Gomulkiewicz & Shaw [93]. 21

Three important factors are fluctuating climate, because 22

organisms that experience them are already adapted to 23

35

change; large, widespread and inter-connected populations, 1

because they have large amounts of standing genetic variation; 2

and short generation times because evolutionary responses 3

are potentially rapid. 4

How can we be prepared to take advantage of 5

opportunities arising unpredictably in the future to learn about 6

evolution caused by extreme events? Long-term field studies 7

offer the best prospects [11,13,29], opportunistically after the 8

event as in the case of new populations of sticklebacks (§ 4) or 9

prospectively in a suitable system with information prior to 10

the event, as in the case of Darwin’s finches (§ 5). A good 11

choice would be organisms amenable to trans-generational 12

study, known to have evolved rapidly in the past, and living in 13

environments known to change rapidly. Ex situ preservation of 14

genotypes sampled from present day populations, such as 15

seeds being banked by Project Baseline [61], will also be 16

important for resurrection studies of evolutionary change 17

during future extreme events. 18

19

10 Conclusions 20

There are few demonstrations of evolutionary change in 21

nature that can be tied to an extreme climatic event, yet many 22

reasons described in this article to suggest microevolutionary 23

36

responses are likely to be widespread. A combined ecological 1

and evolutionary research program is needed to anticipate the 2

potential resilience of populations that face both gradual 3

climatic change and extreme events. 4

5

Authors’ contributions. The authors contributed equally to 6

the design, content and writing of the article. P.R.G. 7

coordinated the sections and wrote the introduction. 8

Competing interests. We have no competing interests. 9

Funding. The authors were funded by NSF 1038016 RBH), the 10

NASA Astrobiology Institute (AHK), a NSERC Discovery grant 11

(MTJJ) and NSF DEB 1447203 (JS). 12

Acknowledgments. RBH thanks L Buckley, M Denny, A. 13

Hoffmann, LJ Ruiz-Jones, N Rose and M. Santos for discussion. 14

15

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