Evolution in an acidifying ocean

Jennifer M. Sunday
1,2
, Piero Calosi
3
, Sam Dupont
4
, Philip L. Munday
5,6
,
Jonathon H. Stillman
7,8
, and Thorsten B.H. Reusch
9
1
Department of Biological Sciences, Simon Fraser University, Burnaby, British Columbia, V5A 1S6, Canada
2
Biodiversity Research Centre, University of British Columbia, Vancouver, British Columbia, V6T 1Z4, Canada
3
Marine Biology and Ecology Research Centre, School of Marine Science and Engineering, Plymouth University, Drake Circus,
Plymouth PL4 8AA, UK
4
Department of Biological and Environmental Sciences, University of Gothenburg, The Sven Love n Centre for Marine Sciences,
Kristineberg, 45178, Fiskeba ckskil, Sweden
5
ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville, Queensland 4811, Australia
6
School of Marine and Tropical Biology, James Cook University, Townsville, Queensland 4811, Australia
7
Romberg Tiburon Center and Department of Biology, San Francisco State University, Tiburon, CA 94920, USA
8
Department of Integrative Biology, University of California Berkeley, Valley Life Sciences Building, Berkeley, CA 94720, USA
9
GEOMAR Helmholtz Centre for Ocean Research Kiel, Evolutionary Ecology of Marine Fishes, Du sternbrooker Weg 20, D-24105
Kiel, Germany
Ocean acidication poses a global threat to biodiversity,
yet species might have the capacity to adapt through
evolutionary change. Here we summarize tools available
to determine species capacity for evolutionary adapta-
tion to future ocean change and review the progress
made to date with respect to ocean acidication. We
focus on two key approaches: measuring standing ge-
netic variation within populations and experimental
evolution. We highlight benets and challenges of each
approach and recommend future research directions for
understanding the modulating role of evolution in a
changing ocean.
Bringing evolution into the forecast of an acidied
ocean
The ocean environment is changing rapidly, with surface
waters changing in temperature and acidity at geologi-
cally unprecedented rates [1]. Projecting the fate of ma-
rine biodiversity requires not only understanding how
these changes will affect populations, but also how popu-
lations will respond via acclimation and adaptive evolu-
tion (Box 1). A global research effort is underway to
understand the potential impacts of global change on
species physiology and overall tness and to consider
the broader impacts for biodiversity, ecosystem function,
and ecosystem services, including food security [2]. Yet
most experiments assess phenotypic responses in rela-
tively short-term, single-generation, experiments under
future ocean conditions projected to occur within 100200
years, and fall short of considering the potential for
evolutionary adaptation[3].
Ocean acidication the increase in partial pressure of
CO
2
( pCO
2
) and reduction in pH associated with uptake of
fossil fuel-derived CO
2
from the atmosphere profoundly
alters the inorganic conditions of the oceans. Although
increased pCO
2
can enhance photosynthesis and growth
of photoautotrophic organisms, ocean acidication is a
stressor for many organisms (i.e., decreases tness,
reviewed in [4]). Because spatial gradients in pCO
2
are
relatively low and unstructured relative to the temporal
change predicted [5], species are less likely to nd refuge
through migration (as has been observed across thermal
gradients [6]). Evolutionary adaptation could hence be a
particularly important response to this widespread change.
Although the possibility for evolutionary adaptation to
ocean acidication is increasingly recognized [79], the
eld is at a nascent stage. Here we summarize approaches
that can be used to address the potential for evolutionary
adaptation in order to guide future work with an evolu-
tionary focus. Although we use ocean acidication as a case
study, the methods reviewed are equally applicable to
other aspects of ocean change and we highlight the utility
of considering multiple drivers simultaneously (see [10]
and [11] for reviews that focus on broader aspects of ocean
change). We rst review two key methodologies for asses-
sing the potential for future adaptation: measuring stand-
ing genetic variation in climate-sensitive traits and
conducting evolution experiments in real time. We next
consider how past adaptation can be inferred from com-
parisons across space and time. We discuss the limitations
of these methodologies, consider how these data will be
useful for understanding the fate of marine biodiversity
and the potential emergent changes in ecosystem function,
and highlight the most promising paths toward that un-
derstanding.
Measuring standing genetic diversity in response traits
Using quantitative genetics
Present-day populations might harbour phenotypic varia-
tion in responses to ocean acidication. The extent to which
this variation has a heritable, genetic basis can indicate
Review
0169-5347/$ see front matter
2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tree.2013.11.001
Corresponding author: Sunday, J.M. (sunday@zoology.ubc.ca).
Keywords: ocean acidification; climate change; evolutionary potential; adaptation;
quantitative genetics; experimental evolution.
Trends in Ecology & Evolution, February 2014, Vol. 29, No. 2 117
the potential for an evolutionary response [12]. Quantita-
tive genetics approaches use comparisons among relatives
with known genetic relatedness to partition observed phe-
notypic variance into their environmental and genetic
components [13]. The advantage of these methods is that
they can be applied to a range of organisms without
requiring prior molecular genetic information and they
can focus directly on tness traits with no need to identify
the specic genes involved.
Quantitative genetics approaches have been used in a
handful of ocean acidication studies. These focus either on
variation in acidication-sensitive phenotypes in the elevat-
ed pCO
2
condition or on variation in reaction norms of
phenotypes across present and future ocean conditions
(identifying a genotype-by-environment interaction, see
Figure 1A). The use of clonal organisms provides the sim-
plest study design. Because all variation within cloned
individuals is assumed to be environmental, heritability
Box 1. Acclimation or adaptation?
Organisms might be able to maintain their performance in a future
acidified ocean through acclimation or adaptation. Acclimation (here
meaning both natural acclimatization and laboratory-based acclima-
tion sensu [71]) involves phenotypically plastic responses in physiol-
ogy, morphology, or behaviour that can help maintain fitness in a new
environment. By contrast, adaptation involves selection on genetic
variation that shifts the average phenotype toward the fitness peak.
Under acclimation, we might observe no difference in a trait response
of interest between environments because of plasticity in underlying
processes, called phenotypic buffering [72,73]. For example, an
organism might maintain a similar growth rate in acidified conditions
compared with current-day controls because of plasticity in metabolic
processes that support growth (Figure I).
Acclimation is categorized into three types: reversible, develop-
mental, and transgenerational (Figure IB). Reversible acclimation
occurs over days to months, often within a life stage [71], such as
physiological adjustment to seasonal change [74]. Developmental
acclimation occurs when exposure to a novel environment early in life
enhances performance in that environment later in life [75]. Transge-
nerational acclimation occurs when the environment experienced by
parents influences the performance of offspring in the same environ-
ment through nutritional, somatic, cytoplasmic, or epigenetic transfer
between generations [76]. This can prime offspring for improved
performance in a stressful environment [77] (Figure IC). Consequently,
it might take two generations for the full extent of environmental
acclimation to be expressed.
All forms of acclimation can interact with genetic adaptation.
Acclimation can buffer populations against immediate impacts of
ocean acidification and provide time for adaptation to catch up [20],
which could be especially important for organisms with long
generation times. However, acclimation could also retard genetic
adaptation by shifting the mean phenotype closer to the fitness peak,
weakening the selection gradient, without changing allelic frequen-
cies. Acclimation can also come at a cost. For example, maintenance
of ion balance in acidified conditions can divert energy from other
activities [78,79]. Such a cost can influence adaptive responses in an
environment-specific manner (e.g., energetic costs might not matter if
food availability is high). Finally, acclimation might enhance genetic
adaptation if the new phenotype is favourably selected (genetic
assimilation [80]), although the occurrence of this process remains
highly uncertain. Both acclimation and adaptation can help organisms
persist in the face of environmental change and understanding the
links between these processes will be critical for predicting evolu-
tionary responses to ocean acidification.
8.0
8.2
8.4
8.6
8.8
9.0
9.2
9.4
low low mod high
low high mod high
Parent environment:
Ospring environment:
Reversible
Transgeneraonal
Developmental
T
r
a
i
t

v
a
l
u
e

Phenotypic buering Selecon in a populaon
M
e
a
n

t
r
a
i
t

v
a
l
u
e
Observed
funconal
phenotype
Underlying
mechanism
G
e
n
e

e
x
p
r
e
s
s
i
o
n

l
e
v
e
l
,
m
o
r
p
h
o
l
o
g
i
c
a
l

c
h
a
n
g
e
,
e
n
e
r
g
y

a
l
l
o
c
a

o
n
pCO
2
pCO
2
pCO
pCO
2
pCO
2
pCO
F
r
e
q
u
e
n
c
y

o
f

p
C
O
2
-
t
o
l
e
r
a
n
t

i
n
d
i
v
i
d
u
a
l
s
pCO
2
(A)
O

s
p
r
i
n
g

l
e
n
g
t
h

(
m
m
)
(C)
(B)
TRENDS in Ecology & Evolution
Figure I. (A) Two processes by which a functional phenotype might be similar across partial pressure of CO
2
( pCO
2
) treatments despite underlying mechanistic
changes. Left: if phenotypic plasticity exists, we might observe no change in a functional phenotype of interest despite underlying changes in gene expression,
morphological change, or energy allocation. Right: in experiments using populations of individuals, mortality selection removing pCO
2
-intolerant phenotypes at high
pCO
2
treatments can lead to no mean functional trait response despite underlying changes in phenotypic frequencies (e.g., [26]). (B) Three categories of acclimation.
(C) The effect of parental environment on standard length of juvenile anemonefish exposed to low, medium, and high pCO
2
[77]. The negative effect of pCO
2
on
offspring length was erased when both parents and offspring were reared at higher pCO
2
levels, showing transgenerational acclimation.
Review
Trends in Ecology & Evolution February 2014, Vol. 29, No. 2
118
in the broad sense (H
2
, see below) can be estimated by
partitioning variance within and between clones [13]. In
the bryozoan Celleporella hyalina, the response of colony
growth rate, reproductive investment, and colony condition
to elevated pCO
2
and temperature differed across clones,
demonstrating that heritable variation exists in tness-
related traits inuenced by ocean acidication, ocean warm-
ing, and their interaction [14]. Clonal strains of the cocco-
lithophore Emiliania huxleyi [15] collected from different
regions and grown in a common environment differed in
their growth rate and carbon content responses to elevated
pCO
2
. Likewise, tness, photosynthesis, carboncontent, and
size responses differed among isolated ecotypes of the pico-
plankton Ostreococcus tauri [16]. These clonal studies dem-
onstrate the existence of heritability for pCO
2
-related traits,
but only in the broad sense, meaning they include heritable
plastic, epigenetic, or genetic components of variation in
pCO
2
responses. Nevertheless they suggest that lineages
with less adverse responses (or greater positive responses)
will increase in frequency, at least in the short term [16].
In non-clonal organisms, single-generation breeding
designs and parentoffspring comparisons can be used
to estimate additive genetic variance (h
2
), the variance
component that can readily respond to selection (variance
due to heritable, genetic variation that is additive in
nature) [13]. Factorial breeding designs are particularly
useful for broadcast-spawning species in which both male
and female gametes can be isolated (Figure 1) and allow
additive genetic variance, maternal effects, and narrow-
sense heritability (i.e., the proportion of phenotypic vari-
ance that is additive genetic, denoted h
2
) to be estimated
[13]. Using factorial breeding designs, the size of early
pluteus larvae in sea urchins at elevated pCO
2
was shown
to have high heritability in Strongylocentrotus purpuratus
(h
2
= 0.5 [17]), but lower heritability in Strongylocentrotus
franciscanus (h
2
= 0.09 [18]). Interestingly, there were
similar levels of additive genetic variation for larval length
in these two studies (350 and 248 mm, respectively), indi-
cating that differences in the heritability estimates were
possibly driven by differences in phenotypic variance, a
feature that can differ according to experimental condi-
tions [17]. By contrast, in larvae of the mussel Mytilus
trossulus, there was additive genetic variance for larval
size at low pCO
2
, but none detected at high pCO
2
and hence
a diminishing scope for an evolutionary response [18].
Although the sea urchin Centrostephanus rodgersii did
not show signicant genetic variation for gastrulation
success with varying pCO
2
treatments, there was genetic
variation at varying temperatures and a signicant genetic
correlation between the two responses, indicating a poten-
tial for correlated responses to selection imposed by the
two stressors [19] (Box 2). In all of these examples, much of
the observed variation was attributed to maternal effects
at high- and low-pCO
2
conditions, indicating differences
in maternal provisioning that are expected at early em-
bryonic stages.
Control pCO
2
Future pCO
2
Mean
tness
by sire
(A) (B)
Test for adaptaon
Correlated response
Ancestral
populaon
Populaon
size
Replicaon
Selecon
environment
Control
environment
n generaons of
experimental evoluon
Assay
experiment 1
Assay experiment 2...m
F
i
t
n
e
s
s

Correlated
response
Test for
adaptaon
TRENDS in Ecology & Evolution
Figure 1. (A) Illustration of a factorial fertilization cross with a blocked design to estimate standing genetic variation using nine dams and sires. Inset shows idealized data
showing mean responses by individual sire. Phenotypic variation in experimental partial pressure of CO
2
( pCO
2
) conditions (height of points in grey box) or variation in
phenotype reaction norms between control and experimental pCO
2
conditions (slope of response curves in inset) can be attributed to sire effects, dam effects, sire dam
interaction effects, and culture effects. Using the sire model [13], additive genetic variation is derived from the sire effects and maternal effects are derived from the
difference between sire and dam effects. (B) Important elements of an experimental evolution experiment. Critical steps are the choice of the ancestral or base population
with its initial genetic diversity, the number and population size of the independently evolving population replicates, the number of generations of experimental evolution,
and the choice of the selection treatment, always compared with a laboratory selection control. The critical test for adaptation is conducted via a reciprocal assay
experiment in which selection and control treatments are exposed to both conditions after appropriate acclimation. The full-factorial assay experiments have to be repeated
over the course of the experiment. The hypothetical bar diagram indicates the evolutionary adaptation of the adapted populations as well as a decline of fitness due to
trade-offs when exposing adapted lines back to the ancestral conditions.
Review Trends in Ecology & Evolution February 2014, Vol. 29, No. 2
119
Although these studies demonstrate the advantage of
using breeding designs to estimate heritable variation,
they each focused on growth during early development,
the tness consequences of which are difcult to ascertain.
Estimating evolutionary potential requires knowledge of
genetic variance as well as the strength of selection toward
a tness optimum [20]. Future work must focus on surviv-
al, reproduction, or other ecologically important traits
affecting population growth to improve the utility of quan-
titative genetics studies, so that selection responses can be
better estimated.
Using genomics to identify pCO
2
-responsive loci
Recent advances in next-generation DNA sequencing have
made it possible and cost-effective to develop genome-scale
data that can be useful toward identifying standing genetic
variation at multiple loci responsive to pCO
2
change.
Transcriptomics proles have been useful for identifying
genes that vary in gene expression levels in future ocean
environments, indicating a plastic response at a cellular
level (e.g., [21,22]). However, to show a potential for evolu-
tionary adaptation, heritable variation in expression level
responses or allelic variation in the coding genes them-
selves must be demonstrated [23].
Once such loci are identied, it will be critical to relate
genetic variation directly to tness [24,25]. This was
recently achieved in a study of S. purpuratus urchin
larvae in which allele frequencies changed differentially
over 7 days in a high- versus low-pCO
2
regime, suggesting
allele-specic survival [26]. The changes in the high-pCO
2
treatment occurred at loci of known functional protein
classes. Furthermore, among those genes related to
biomineralization, lipid metabolism, and ion homeostasis,
surviving alleles had greater-than-expected differences at
amino acid-changing nucleotide sites compared with the
original pool, supporting the interpretation that selection
acted on functional proteins. These underlying allelic
changes occurred despite little change in development
and morphology between the high and low treatments,
suggesting that the underlying population genetic change
was responsible for the population resilience observed
(Box 1).
Although sequencing projects remain simplest in mod-
el organisms with existing genomic data (Box 3), recent
bioinformatics advances are facilitating the use of next-
generation sequencing in non-model organisms, opening
use of this technology for a broader scope of organisms
[27].
Box 2. Correlated traits and fitness trade-offs
Genetic correlations among traits might increase [81] or decrease
[82,83] the rate of adaptive evolution, depending on whether they are
positively or negatively correlated with respect to the fitness
landscape (Figure IIA,B). The basis for such correlations can be
genetic pleiotropy (single genes conferring multiple traits) or linkage
disequilibrium (non-random association of alleles at different loci)
[84,85], such that selection on one trait will elicit a response in
another in the direction of the correlation (e.g., [86]). If the
correlation exists because of gene linkage, it can be broken up by
recombination [87].
In the Sydney rock oyster, ten years of artificial selection for faster
growth and disease resistance inadvertently resulted in increased
resilience to pCO
2
stress [88]. This suggests a positive genetic
correlation between growth or disease resistance under ambient
conditions and growth rate responses to pCO
2
[88]. Likewise, in
developing sea urchin larvae, genotypes that performed well in high
temperatures also performed well at low pH [89], which should
accelerate the rate of evolution (Figure IIB).
The adaptive landscape itself might lead to unexpected responses to
selection because of fitness trade-offs. For example, greater survival
under ocean acidificationmight occur at a cost toreproductive output, to
performance of other life-history stages, or to fitness when multiple
drivers are considered (e.g., warming, anoxia, predation, competition;
Figure IIC). Recent evidence showing that pCO
2
resilience in calcifiers
comes at a metabolic cost [19,90] suggests energy allocation trade-offs
between pCO
2
resilience and other energetically maintained fitness
traits. Many taxa (but not all) also show negative synergistic responses
to acidification and warming (reviewed in [50,51]). This suggests a
common, nonlinear physiological mechanism linking an organisms
response to either an environmental driver, such as mutual effects on
aerobic scope [85,91], or a previous fitness trade-off in tolerating both
variables, such that few individuals have cotolerance [92]. There is also
evidence that greater resilience to pCO
2
comes at a competitive cost. In
two species of marine microalga, slow-growing strains had greater
resilience to pCO
2
than fast-growing strains [93], suggesting that
selection for fast growth, and hence competitive ability in phytoplank-
ton, might counter selection for pCO
2
resilience (Figure IIC). Where
possible, understanding the physiological mechanisms of pCO
2
responses will help in anticipating genetic correlations and fitness
trade-offs.
+
pCO
2
tolerance
T
e
m
p
e
r
a
t
u
r
e

t
o
l
e
r
a
n
c
e
+
pCO
2
tolerance
T
e
m
p
e
r
a
t
u
r
e

t
o
l
e
r
a
n
c
e
pCO
2
tolerance
+
C
o
m
p
e

v
e

a
b
i
l
i
t
y
(A) (B) (C)
TRENDS in Ecology & Evolution
Figure II. Genetic variance and fitness landscapes across two phenotypic dimensions. Coloured lines show isopleths in the fitness landscape leading up to a local
maximum (+), black dots and grey regions show mean and variation in 2D phenotype before selection, arrows show direction of selection, and broken lines show
direction of maximal genetic variance. A positive genetic correlation between two traits [e.g., partial pressure of CO
2
( pCO
2
) tolerance and temperature tolerance] will
accelerate adaptive evolution (A), whereas a negative genetic correlation will slow adaptive evolution (B). Even without genetic correlations, fitness trade-offs, such as
between pCO
2
tolerance and competitive ability, can constrain evolution along a maximal fitness ridge (C).
Review
Trends in Ecology & Evolution February 2014, Vol. 29, No. 2
120
Experimental evolution
Experimental evolution has only recently been used to
study processes of adaptation to ocean acidication. Two
basic designs can be distinguished. In experimental natu-
ral selection, the experimenter alters the environment and
selection occurs by a mixture of mortality and fecundity
selection of genotypes during the multigeneration experi-
ment (Figure 1). In articial selection, individuals with
specic trait values such as large body size or heat-shock
tolerance are selected by the experimenter to found the
next generation [28]. Articial selection is informative for
unravelling trait correlations and fundamental limits to
adaptive evolution [29]. Important considerations for both
designs are the diversity in the starting population and the
effective population size during the experiment, particu-
larly in experiments with metazoa, to avoid genetic drift
overriding selection [8]. The salient test for adaptation
always needs to include control populations for unwanted
laboratory selection, which (after appropriate acclimation
time to the stressor) are compared with populations that
evolved under the novel condition.
Owing to their short generation time, marine unicellu-
lar plankton were the rst targets for experimental evolu-
tion in ocean acidication research [8]. Important ndings
are that, in two species of phytoplankton (coccolithophores,
Haptophyta) exposed to elevated pCO
2
for hundreds of
asexual generations, adverse ocean acidication effects
declined. In a non-calcifying strain of Gephyrocapsa ocea-
nica [30], growth rates, particulate organic carbon content,
and photosynthesis rate increased due to adaptation after
approximately 670 generations, and in E. huxleyi growth
and calcication rates were partly restored after approxi-
mately 500 asexual generations [31]. In each of these
experiments, the initial population comprised only a single
genotype, highlighting the role of de novo mutations in
large plankton populations. In the E. huxleyi case, the
genetic basis of the observed phenotypic change was found
to differ among replicate populations [32]. When starting
cultures contained a mix of several E. huxleyi genotypes,
rapid and consistent genotypic sorting specic to pCO
2
treatment was observed [31]. In another long-term experi-
ment with E. huxleyi (703 generations), particulate inor-
ganic carbon and calcication rate increased after 214
generations with elevated pCO
2
and temperature [22],
which was in contrast to the response of the same E.
huxleyi strain in a short-term study (seven generations
[33]), indicating a change in response probably due to
adaptation.
In contrast to the experiments with coccolithophores,
no phenotypic changes were observed in a diatom species
in an experimental evolution experiment simulating end-
of the-century pCO
2
values [34]. This might be due to
either the relatively short duration (only 100 genera-
tions) or the selection regime, in which increased pCO
2
created a more benign growth condition for the non-calci-
fying diatom, relaxing the need for physiological concen-
tration of carbon molecules. Hence carbon concentration
mechanisms appeared to degenerate in the high-pCO
2
regime, a response that only becomes visible when
adapted lineages are back-exposed to ambient conditions
[35].
Adaptive responses might also affect community com-
position in mixed assemblages. This was recently ex-
plored in assemblages of dinoagellates [36] and
diatoms [37], where, after 1 year of isolated conditioning
in elevated pCO
2
(dinoagellates, 48126 generations) or
elevated pCO
2
and temperature (diatoms, 169229 gen-
erations), the relative dominance of species did not change
in a manner specic to their conditioning environment
(although for dinoagellates, assemblage composition
changed over time, apparantly in response to culture
conditions). These studies represent important forays
in focus from single species performance to community
composition and may be particularly interesting if applied
to communities with calcifying taxa.
Experimental evolution offers great potential for
addressing adaptation in species with short generation
times and is currently underused in marine metazoans
[8]. Because experimental natural selection directly
favours individuals with high Darwinian tness, the need
to mechanistically associate pCO
2
-sensitive traits with
survival and reproduction is alleviated. In addition, evolu-
tionary constraints (Box 4) are directly evident from ex-
perimental results and pleiotropic effects (Box 2) can be
experimentally tested [32].
Experimental challenges in assessing adaptive potential
Although these experimental approaches have demon-
strated the potential for evolution in principle, there are
several complexities that confound the predictive ability of
laboratory results. We summarize four surmountable chal-
lenges for future work.
Box 3. Utility of model organisms
Due to the inherent challenges of assessing evolutionary potential,
we have neither the time nor the resources to study every species
with the required level of detail, and many species are not amenable
for evolutionary experiments. One strategy is to use established
model organisms (e.g., the sea urchin Strongylocentrotus purpur-
atus, the polychaete worm Platynereis dumerilii, and the cocco-
lithophore Emiliania huxleyi) to prove concepts and dissect
underlying evolutionary mechanisms behind responses to ocean
acidification. For example, the developmental biology model sea
urchin species S. purpuratus has been used to demonstrate the key
role of existing genetic diversity in population responses to ocean
acidification [17,26].
Drawing generalizable inferences frommodel organisms, however,
is not without limitations. Model organisms are often selected for
their utility in mechanistic physiological or cellular studies, not their
ecological relevance. As such, they tend to have high accessibility,
small body size, and easy culturing for use in experimental laboratory
research. The transferability of stress-response findings using these
species might be limited because they are potentially more resilient to
environmental changes, leading to underestimation of the more
general impacts of a stressor. Because the impact of ocean
acidification appears to be highly taxon specific, even in closely
related species [51], care should be taken when extrapolating
responses from one species to another.
Democratization of new technologies, including genomics, has
allowed the emergence of new model organisms and transfer of
technology to non-model species. This is of great interest for
evolutionary ocean change research because it is now possible to
use genomics methods previously limited to model organisms
[70]. Research should now include a wide range of species with
various life-history strategies, habitats, physiology, and evolu-
tionary potential.
Review Trends in Ecology & Evolution February 2014, Vol. 29, No. 2
121
First, ocean acidication does not exist in isolation of
other changing abiotic parameters and we are only begin-
ning to understand the role of pCO
2
in modulating how
organisms simultaneously respond and potentially evolve
to changes in other key drivers such as temperature or
oxidative stress [7,14,19,3840]. Genetic correlations and
evolutionary trade-offs between environmental drivers can
greatly modify how evolution proceeds (Box 2); thus multi-
ple drivers need to be investigated.
Second, species interactions within ecosystems can be
affected by changing abiotic drivers and such indirect
effects are likely to play a key role in many ecosystems
[9]. For example, copepods, which are key players in the
marine ecosystem and a major food source for sh, seem
resilient to ocean acidication but can be indirectly impact-
ed by the negative effects observed on the quality of the
phytoplankton on which they feed [41]. By contrast, marine
bivalves can thrive in high-pCO
2
environments when
abundant food is available to offset the increased metabolic
costs associated with ocean acidication [19]. Thus the
selective landscape differs when species interactions are
included. In situ changes in community composition across
spatial or temporal gradients are to likely yield important
insight into pCO
2
-mediated species interactions (see be-
low), as well as experimental evolution studies that explic-
itly consider community composition in mesocosms (e.g.,
[36,37]).
Third, many marine species have complex life histories
and each life stage can respond differently to selection
pressures or live in a different selective environment (e.g.,
pelagic larvae, benthic adults) [42,43]. Exposure at one life-
history stage can also affect phenotypes at another through
phenotypic carry-over effects [44] (Box 1). For example, sea
urchin larvae exposed to elevated pCO
2
sea water produce
juveniles that are ten times more sensitive to ocean acidi-
cation than those produced from non-exposed larvae [45].
Whereas experimental evolutionintegrates selection across
entire lifespans of experimental organisms, assessments of
standing genetic variation tend to focus on onlyone lifestage
at a time. Longer experimental durations are thus needed to
integrate responses over a larger proportion of an organ-
isms lifespan or (ideally) across generations.
Fourth, experiments on ocean acidication have tradi-
tionally been approached as a comparison between pres-
ent-day and near-future average conditions, without
taking into account short-term pCO
2
variability or gradual
change. Yet temporal variability can be high within specic
locations [46] and mean future scenarios can be within the
range of variability presently experienced by populations
[47], with variability itself expected to increase [48]. Two
experimental approaches can help to improve this: (i)
imposing variable conditions around a present-day and
future pCO
2
mean; and (ii) changing the selection condition
during experimental evolution as a rate and not abruptly,
which may change the rate of adaptation [49].
These complexities are by no means trivial. Yet already
studies of multiple environmental drivers and their inter-
actions have become more prominent in non-evolutionary
research [50,51]. Improving our understanding of the
mechanisms that underlie how pCO
2
affects species per-
formance and their responses to other variables will allow
research on evolutionary potential that is more targeted to
the most salient aspects of ocean change. We might also
turn to comparative studies in natural settings, where
these complexities are left intact (see below).
Evidence of evolution in nature
Comparing phenotypes of species, populations, or strains
living along spatial or temporal environmental gradients
can inform our understanding of how adaptation has oc-
curred in the past. We explore rst spatial, then temporal,
approaches for understanding adaptation to ocean acidi-
cation. Although stable spatial gradients in pCO
2
and pH
are less evident or available than spatial gradients in tem-
perature, examples do exist along bathymetrical gradients
[52], around natural underwater CO
2
vents [53,54], along
fjords [19], and along coastal upwelling zones [55]. However,
these tend to occur on relatively small spatial scales with
often high temporal variability of pCO
2
, so local adaptation
may be limited by continuous input of genetic material from
the surrounding ambient-pCO
2
environment.
Box 4. Constraints on adaptive evolution
Adaptive evolution can be restricted by rate-limiting or fundamental
evolutionary constraints. Rate-limiting constraints can slow the rate
of adaptive evolution and fundamental constraints can prevent key
innovations because they are simply not available within a realistic
timeframe.
Rates of adaptive evolution can be influenced by the amount of
genetic variation in a population, the extent and frequency of
recombination, the rate of genetic drift, the strength of selection,
and the genetic architecture of a trait. Many marine populations
display large census sizes, which are likely to translate into large
effective population sizes (N
e
) [94] and thus a high rate of new
mutations and a predominance of selection over genetic drift. This
suggests a high potential for rapid evolutionary responses. How-
ever, N
e
tends to decline with body size among unicellular,
invertebrate, and vertebrate taxa [69] and further declines with
geographic substructuring of marine populations [95]. Sexual
reproduction increases the population-level variance available to
selection and joins separate beneficial mutations within the same
genotype via recombination [96]. By contrast, in asexual microbial
populations mutations have to occur sequentially, although the
same taxa tend to have very large population sizes and hence
represent enormous mutational targets [8].
Stronger selection increases the rate of adaptive evolution and can
be conceptualized as the rate of fitness decline from a phenotypic
optimum. Although the fitness optimum can be influenced by a
changing environment, so can phenotypes, via phenotypic plasticity;
hence both are important for estimating the strength of selection in a
changing environment [20]. The multidimensional fitness landscape
and genetic correlations between traits under selection can also
influence the rate of adaptation (Box 2).
Fundamental constraints on adaptive evolution are suggested by
the fossil record. For example, four of five coral mass extinctions
from the geological record were governed at least partly by ocean
acidification periods [97]. At contemporary time scales, stasis in
evolution experiments can indicate the presence of fundamental
constraints on global change-associated selection [98].
Extreme environments might also shed light on the presence of
fundamental evolutionary constraints. For example, the calcifying
deep-sea bivalves Bathymodiolus spp. thrive in the vicinity of hot
vents at pH values of 6 [99], suggesting that predicted ocean
acidification levels are not beyond the capacity of some mytilid
bivalves. By contrast, although limpets (Patella spp.) can calcify
below pH 7.0 [100], their shells are not protected by a protein shield
(periostracum) as in mussels; thus their shells will dissolve in these
environments.
Review
Trends in Ecology & Evolution February 2014, Vol. 29, No. 2
122
The critical test for local adaptation is to show site-
specic variation in responses to pCO
2
when individuals
are raised in a common environment and to show that this
variation is locally adaptive and heritable [56]. For exam-
ple, spatial variation in pCO
2
responses was detected in S.
purpuratus sea urchins collected from regions of California
with different amounts of pCO
2
-rich upwelling water ap-
proximately 700 km apart [17]. A factorial breeding design
showed lower sensitivity to high pCO
2
among larvae sired
by urchins from northern California, where pCO
2
-rich
upwelling is stronger and more persistent, compared with
larvae sired by urchins from southern California.
A less direct approach is to show population genetic
variation associated with different responses to pCO
2
. For
example, an increase in mass of a coccolithophore along a
pH gradient off the coast of Chile was coincident with a
change in frequency in two mitochondrial haplotypes
across a few hundred kilometres of open ocean [57]. Like-
wise, strong genetic structure in the polychaete Platynereis
dumerilii across a pCO
2
gradient formed by natural CO
2
vents in Ischia, Italy was associated with greater metabolic
rates and smaller body sizes in individuals from within the
CO
2
vent that were robust to single-generation acclimation
(using reciprocal transplants) [53]. However, given the
amount of genetic divergence, it remains to be determined
whether rapid local adaptation occurred in situ or the two
lineages represent cryptic species (one being a high pCO
2
specialist) separated from a common ancestor before colo-
nizing the vents. Furthermore, multigenerational studies
or breeding designs are required to attribute these pat-
terns to genetic adaptation as opposed to developmental or
trans-generational acclimation (Box 1).
Once demonstrated, using local adaptation for predict-
ing evolution into the future assumes that space can be
substituted for time (the synchronic approach sensu [58]).
This approach assumes that other environmental drivers
(e.g., temperature, salinity) covary across space as they
would across time [59] and that the evolutionary diver-
gence time between samples along the gradient mimics the
rate of environmental change into the future. Although
these assumptions are limiting, the space-for-time ap-
proach can at least demonstrate the potential for evolution
in complex natural environments.
Comparison of phenotypes across time coincident with
changing environmental pCO
2
conditions can more directly
demonstrate adaptation (the allochronic approach [58]). For
example, morphological change in preserved specimens of
coccolithophores has been associated with historical
changes in pCO
2
[57,60,61]. However, demonstrating that
phenotypic change(or a lackthereof) is a result of adaptation
is problematic. A potentially viable approach that has not
yet been applied to ocean acidication is to trace genetic
change over time in pCO
2
-sensitive loci. This might poten-
tiallybe done by storingor resurrectingdormant propagules
(e.g., of diatoms [62]) from historical times and comparing
their performance in a common garden [63].
Projecting evolutionary outcomes
The work done to date has shown that evolutionary adap-
tation to ocean acidication is possible in principle. In most
studies where it has been investigated, standing genetic
variation in pCO
2
-sensitive traits has been observed. Like-
wise, in all experimental evolution studies in which pCO
2
was a stressor, there was an adaptive response. The critical
question therefore must move beyond whether adaptation
can occur in principle, toward whether evolution can occur
rapidly enough to maintain populations and their ecosys-
tem services and how future communities will be assem-
bled.
For organisms with generation times too long for exper-
imental evolution, several modelling approaches are avail-
able to estimate the rate of adaptation and risk of
extinction within a changing environment [20,6466]. Al-
though models vary in complexity, they minimally require
knowledge of both genetic variation and the strength of
selection on a key trait. Despite this, most studies of
genetic variation to date use traits (such as growth rate)
with unknown effects on survival and reproduction. Kelly
et al. [17] used a model developed by Lande and Shannon
[66] to project evolutionary changes in larval size and
associated declines in population growth rates in S. pur-
puratus, based on experimentally estimated genetic vari-
ance of larval size at high pCO
2
. Although the strength of
selection on this trait was unknown, the authors explored a
small range of selection strengths using the assumption
that strength of selection would be negatively correlated
with genetic variance (because selection erodes genetic
variance) with a product <1 [66]. However, this assump-
tion might be tenuous for novel stressors like ocean acidi-
cation and remains to be demonstrated. Selection
strength on pCO
2
-sensitive phenotypes has been recently
empirically measured in larval sh by observing pCO
2
-
impacted larval sh in the wild [67]. We strongly recom-
mend that studies of genetic variation focus on traits with
either more straightforward or measurable relationships
to Darwinian tness [20].
Concluding remarks: where to focus efforts
Because evolutionary potential cannot be assessed in all
species, future work must strategically concentrate efforts
toward taxa and systems from which we can glean the most
critical or generalizable information. One approach is to
focus on species related to societal or ecosystem services, in
anticipation that these case studies will be most useful to
modellers and managers. For example, coccolithophores
play a disproportionately large role in the marine carbon
cycle, so evolution in their responses to pCO
2
represents
change in a major ecosystem service that can feed back and
alter the process of ocean acidication itself [68].
Another approach is to correlate evolutionary capacity
with parameters of ecology, physiology, or taxonomy. Dif-
ferent taxonomic or functional groups of species are likely
to have different evolutionary responses based on charac-
teristics of population size and recombination rates. For
example, phytoplankton with large population sizes and
fast turnover rates are likely to adapt quickly, and experi-
mental evolution has already demonstrated their ability to
adapt quickly via de novo mutations [31]. By contrast, in
larger organisms withsmaller effective population sizes and
with genomes that can harbour more degenerative or con-
ditionally neutral variation [69], adaptation from standing
genetic variation will probably be more commonplace [70].
Review Trends in Ecology & Evolution February 2014, Vol. 29, No. 2
123
Meanwhile, species in environments historically exposed to
unpredictable changes of pCO
2
might have greater standing
variation and adaptability than those living in a more
predictable pCO
2
regime. Toward this goal, signatures of
local adaptation as well as estimates of future evolutionary
potential can be useful.
Acknowledgements
This reviewgreatly beneted fromthe CeMEBAdvanced Course on Marine
Evolution Under Climate Change, funded by the Swedish Royal Academy
of Science and organized by S.D., P.C., and J.M.S., as well as the Workshop
on Evolutionary Potential in Marine Populations organized by Lisa Shama,
Mathias Wegner, the Alfred Wegener Institute Helmholtz Center for
Polar and Marine Research, and the Helmholtz Center for Ocean Research
Kiel (GEOMAR). J.M.S. was supported by an NSERC postdoctoral
fellowship and the UBC Biodiversity Centre. P.C. was supported by NERC
(grant no. NE/H017127/1 563) and the EU (grant no. 265103). S.D. was
supported by the Linnaeus Centre for Marine Evolutionary Biology at the
University of Gothenburg and a Linnaeus grant fromthe Swedish Research
Councils VR and Formas. P.L.M. was supported by the Australian
Research Council and the ARC Centre of Excellence for Coral Reef Studies.
J.H.S. was supported by the National Science Foundation (grant no.
1041225). T.B.H.R. was supported by the BMBF programme BIOACIDand
by the German Science Foundation (excellence cluster The Future Ocean).
The authors thank to the Earth
2
Ocean laboratory at Simon Fraser
University for early feedback on the manuscript.
References
1 Honisch, B. et al. (2012) The geological record of ocean acidication.
Science 335, 10581063
2 Branch, T.A. et al. (2013) Impacts of ocean acidication on marine
seafood. Trends Ecol. Evol. 28, 178185
3 Stockwell, C.A. et al. (2003) Contemporary evolution meets
conservation biology. Trends Ecol. Evol. 18, 94101
4 Kroeker, K.J. et al. (2010) Meta-analysis reveals negative yet variable
effects of ocean acidication on marine organisms. Ecol. Lett. 13,
14191434
5 Kelly, M.W. and Hofmann, G.E. (2013) Adaptation and the physiology
of ocean acidication. Funct. Ecol. 27, 980990
6 Perry, A.L. et al. (2005) Climate change and distribution shifts in
marine shes. Science 308, 19121915
7 Pandol, J.M. et al. (2012) Projecting coral reef futures under global
warming and ocean acidication. Science 333, 418422
8 Reusch, T.B.H. and Boyd, P.W. (2013) Experimental evolution meets
marine phytoplankton. Evolution 67, 18491859
9 Dupont, S. and Portner, H. (2013) Marine science: get ready for ocean
acidication. Nature 498, 429
10 Munday, P.L. et al. (2013) Predicting evolutionary responses to
climate change in the sea. Ecol. Lett. 16, 14881500
11 Reusch, T.B.H. (2013) Climate change in the oceans: evolutionary
versus phenotypically plastic responses of marine animals and plants.
Evol. Appl. http://dx.doi.org/10.1111/eva.12109
12 Shaw, R.G. and Etterson, J.R. (2012) Rapid climate change and the
rate of adaptation: insight from experimental quantitative genetics.
New Phytol. 195, 752765
13 Lynch, M. and Walsh, B. (1998) Genetics and Analysis of Quantitative
Traits, Sinauer Associates
14 Pistevos, J.C.A. et al. (2011) Will variation among genetic individuals
inuence species responses to global climate change? Oikos 120, 675
689
15 Langer, G. et al. (2009) Strain-specic responses of Emiliania huxleyi
to changing seawater carbonate chemistry. Biogeosciences 6, 2637
2646
16 Schaum, E. et al. (2013) Variation in plastic responses of a globally
distributed picoplankton species to ocean acidication. Nat. Clim.
Change 3, 298302
17 Kelly, M.W. et al. (2013) Natural variation, and the capacity to adapt
to ocean acidication in the sea urchin Strongylocentrotus purpuratus.
Global Change Biol. 19, 25362546
18 Sunday, J.M. et al. (2011) Quantifying rates of evolutionary
adaptation in response to ocean acidication. PLos ONE 6, e22881
19 Thomsen, J. et al. (2012) Food availability outweighs ocean
acidication effects in juvenile Mytilus edulis: laboratory and eld
experiments. Global Change Biol. 19, 10171027
20 Chevin, L.M. et al. (2010) Adaptation, plasticity, and extinction in a
changing environment: towards a predictive theory. PLoS Biol. 8,
e1000357
21 Todgham, A.E. and Hofmann, G.E. (2009) Transcriptomic response of
sea urchin larvae Strongylocentrotus purpuratus to CO
2
-driven
seawater acidication. J. Exp. Biol. 212, 25792594
22 Benner, I. et al. (2013) Emiliania huxleyi increases calcication but not
expression of calcication related genes in long-term exposure to
elevatedtemperature andpCO
2
. Philos. Trans. R. Soc. B368, 20130049
23 Wray, G.A. (2007) The evolutionary signicance of cis-regulatory
mutations. Nat. Rev. Genet. 8, 206216
24 Barrett, R. and Hoekstra, H. (2011) Molecular spandrels: tests of
adaptation at the genetic level. Nat. Rev. Genet. 12, 767780
25 Davidson, W.S. (2012) Adaptation genomics: next generation
sequencing reveals a shared haplotype for rapid early development
in geographically and genetically distant populations of rainbow
trout. Mol. Ecol. 21, 219222
26 Pespeni, M.H. et al. (2013) Evolutionary change during experimental
ocean acidication. Proc. Natl. Acad. Sci. U.S.A. 110, 69379642
27 Arnold, M.L. et al. (2012) The genomics of natural selection and
adaptation: Christmas past, present and future(?). Plant Ecol.
Divers. 5, 451456
28 Conner, J.K. (2003) Articial selection: a powerful tool for ecologists.
Ecology 84, 16501660
29 Fry, J.D. (2003) Detecting ecological trade-offs using selection
experiments. Ecology 84, 16721678
30 Jin, P. et al. (2013) Evolutionary responses of a coccolithophorid
Gephyrocapsa oceanica to ocean acidication. Evolution 67, 1869
1878
31 Lohbeck, K.T. et al. (2012) Adaptive evolution of a key phytoplankton
species to ocean acidication. Nat. Geosci. 5, 346351
32 Lohbeck, K.T. et al. (2013) Functional genetic divergence in high CO
2
adapted Emiliania huxleyi populations. Evolution 67, 8921900
33 Feng, Y. et al. (2008) Interactive effects of increased pCO
2
,
temperature and irradiance on the marine coccolithophore
Emiliania huxleyi (Prymnesiophyceae). Eur. J. Phycol. 43, 8798
34 Crawfurd, K.J. et al. (2011) The response of Thalassiosira pseudonana
to long-termexposure to increased CO
2
and decreased pH. PLoS ONE
6, e26695
35 Collins, S.L. and Bell, G. (2004) Phenotypic consequences of 1,000
generations of selection at elevated CO
2
in a green alga. Nature 431,
566569
36 Tatters, A.O. et al. (2013) Short- versus long-term responses to
changing CO
2
in a coastal dinoagellate bloom: implications for
interspecic competitive interactions and community structure.
Evolution 67, 18791891
37 Tatters, A.O. et al. (2013) Short- and long-term conditioning of a
temperate marine diatom community to acidication and warming.
Philos. Trans. R. Soc. B 368, 20120437
38 Lefebvre, S.C. et al. (2012) Nitrogen source and pCO
2
synergistically
affect carbon allocation, growth and morphology of the
coccolithophore Emiliania huxleyi: potential implications of ocean
acidication for the carbon cycle. Global Change Biol. 18, 493503
39 Boyd, P.W. (2011) Beyond ocean acidication. Nat. Geosci. 4, 273274
40 Byrne, M. et al. (2013) Effects of ocean warming and acidication on
embryos and non-calcifying larvae of the invasive sea star Patiriella
regularis. Mar. Ecol. Prog. Ser. 473, 235246
41 Rossoll, D. et al. (2012) Ocean acidication-induced food quality
deterioration constrains trophic transfer. PLoS ONE 7, e34737
42 Werner, E. and Gilliam, J. (1984) The ontogenetic niche and species
interactions in size-structured populations. Annu. Rev. Ecol. Syst. 15,
393425
43 Miller, N.A. et al. (2013) Differential thermal tolerance and energetic
trajectories during ontogeny in porcelain crabs, genus Petrolisthes. J.
Therm. Biol. 38, 7985
44 Podolsky, R. and Moran, L. (2006) Integrating function across marine
life cycles. Integr. Comp. Biol. 46, 577586
45 Dupont, S. et al. (2013) Long-term and trans-life-cycle effects of
exposure to ocean acidication in the green sea urchin
Strongylocentrotus droebachiensis. Mar. Biol. 8, 18351843
Review
Trends in Ecology & Evolution February 2014, Vol. 29, No. 2
124
46 Hofmann, G.E. et al. (2011) High-frequency dynamics of ocean pH: a
multi-ecosystem comparison. PLoS ONE 6, e28983
47 McElhany, P. and Shallin Busch, D. (2013) Appropriate pCO
2
treatments in ocean acidication experiments. Mar. Biol. 160,
18071812
48 Shaw, E.C. et al. (2013) Anthropogenic changes to seawater buffer
capacity combined with natural reef metabolism induce extreme
future coral reef CO
2
conditions. Global Change Biol. 19, 16321641
49 Collins, S. and de Meaux, J. (2009) Adaptation to different rates of
environmental change in Chlamydomonas. Evolution 63, 29522965
50 Harvey, B.P. et al. (2013) Meta-analysis reveals complex marine
biological responses to the interactive effects of ocean acidication
and warming. Ecol. Evol. 3, 10161030
51 Kroeker, K.J. et al. (2013) Impacts of ocean acidication on marine
organisms: quantifying sensitivities and interaction with warming.
Global Change Biol. 19, 18841896
52 Maas, A.E. et al. (2012) The metabolic response of pteropods to
acidication reects natural CO
2
-exposure in oxygen minimum
zones. Biogeosciences 9, 747757
53 Calosi, P. et al. (2013) Metabolic adaptation and acclimatisation to
ocean acidication in marine ectotherms: an in situ transplant
experiment at a shallow CO
2
vent system. Philos. Trans. R. Soc.
Lond. B: Biol. Sci. 368, 20120444
54 Crook, E.D. et al. (2013) Reduced calcication and lack of
acclimatization by coral colonies growing in areas of persistent
natural acidication. Proc. Natl. Acad. Sci. U.S.A. 110, 1104411049
55 Feely, R.A. et al. (2008) Evidence for upwelling of corrosive acidied
water onto the continental shelf. Science 320, 14901492
56 Kawecki, T.J. and Ebert, D. (2004) Conceptual issues in local
adaptation. Ecol. Lett. 7, 12251241
57 Beaufort, L. et al. (2011) Sensitivity of coccolithophores to carbonate
chemistry and ocean acidication. Nature 476, 8083
58 Hendry, A.P. and Kinnison, M.T. (1999) Perspective: the pace of
modern life: measuring rates of contemporary microevolution.
Evolution 53, 16371653
59 Dunne, J.A. et al. (2004) Integrating experimental and gradient
methods in ecological climate change research. Ecology 85, 904916
60 Iglesias-Rodriguez, M.D. et al. (2008) Phytoplankton calcication in a
high-CO
2
world. Science 320, 336340
61 Langer, G. (2013) Palaeontology: plankton in a greenhouse world.
Nat. Geosci. 6, 164165
62 Ha rnstrom, K. et al. (2011) Hundred years of genetic structure in a
sediment revived diatom population. Proc. Natl. Acad. Sci. U.S.A.
108, 42524257
63 Orsini, L. et al. (2013) The evolutionary time machine: using dormant
propagules to forecast how populations can adapt to changing
environments. Trends Ecol. Evol. 28, 274281
64 Lynch, M. and Lande, R. (1993) Evolution and extinction in response
to environmental change. In Biotic Interactions and Global Change
(Kareiva, P.M. et al., eds), pp. 234250, Sinauer Associates
65 Burger, R. and Lynch, M. (1995) Evolution and extinction in a
changing environment a quantitative-genetic analysis. Evolution
49, 151163
66 Lande, R. and Shannon, S. (1996) The role of genetic variation in
adaptation and population persistence in a changing environment.
Evolution 50, 434437
67 Munday, P.L. et al. (2012) Selective mortality associated with
variation in CO
2
tolerance in a marine sh. Ocean Acidication 1,
15
68 Rost, B. and Riebesell, U. (2004) Coccolithophores and the biological
pump: responses to environmental changes. In Coccolithophores:
From Molecular Processes to Global Impact. pp. 99125, Springer
69 Lynch, M. and Conery, J.S. (2003) The origins of genome complexity.
Science 302, 14011404
70 Radwan, J. and Babik, W. (2012) The genomics of adaptation. Proc.
Biol. Sci. 279, 50245028
71 Angilletta, M.J. (2009) Thermal Adaptation: A Theoretical and
Empirical Synthesis, Oxford University Press
72 Waddington, C.H. (1942) Canalization of development and the
inheritance of acquired characters. Nature 150, 563565
73 Bradshaw, A.D. (1965) Evolutionary signicance of phenotypic
plasticity in plants. Adv. Genet. 13, 115155
74 Somero, G.N. (2010) The physiology of climate change: howpotentials
for acclimatization and genetic adaptation will determine winners
and losers. J. Exp. Biol. 213, 912920
75 Scott, G.R. and Johnston, I.A. (2012) Temperature during embryonic
development has persistent effects on thermal acclimation capacity in
zebrash. Proc. Natl. Acad. Sci. U.S.A. 109, 1424714252
76 Bonduriansky, R. et al. (2012) The implications of nongenetic
inheritance for evolution in changing environments. Evol. Appl. 5,
192201
77 Miller, G.M. et al. (2012) Parental environment mediates impacts of
increased carbon dioxide on a coral reef sh. Nat. Clim. Change 2,
858861
78 Portner, H.O. et al. (2004) Biological impact of elevated ocean CO
2
concentrations: lessons from animal physiology and earth history. J.
Oceanogr. 60, 705718
79 Stumpp, M. et al. (2012) Acidied seawater impacts sea urchin larvae
pHregulatory systems relevant for calcication. Proc. Natl. Acad. Sci.
U.S.A. 109, 1819218197
80 Pigliucci, M. et al. (2006) Phenotypic plasticity and evolution by
genetic assimilation. J. Exp. Biol. 209, 23622367
81 Stanton, M.L. et al. (2000) Evolution in stressful environments. I.
Phenotypic variability, phenotypic selection, and response to selection
in ve distinct environmental stresses. Evolution 54, 93111
82 Blows, M.W. and Hoffmann, A.A. (2005) A reassessment of genetic
limits to evolutionary change. Ecology 86, 13711384
83 Etterson, J.R. and Shaw, R.G. (2001) Constraint to adaptive evolution
in response to global warming. Science 294, 151154
84 Coyne, J.A. and Lande, R. (1985) The genetic basis of species
differences in plants. Am. Nat. 126, 141145
85 Portner, H.O. and Farrell, A.P. (2008) Physiology and climate change.
Science 322, 690692
86 Chen, X. and Stillman, J.H. (2012) Multigenerational analysis of
temperature and salinity variability effects on metabolic rate,
generation time, and acute thermal and salinity tolerance in
Daphnia pulex. J. Therm. Biol. 37, 185194
87 Conner, J.K. (2002) Genetic mechanisms of oral trait correlations in
a natural population. Nature 420, 407410
88 Parker, L.M. et al. (2012) Adult exposure inuences offspring response
to ocean acidication in oysters. Global Change Biol. 18, 8292
89 Foo, S.A. et al. (2012) Adaptive capacity of the habitat modifying sea
urchin Centrostephanus rodgersii to ocean warming and ocean
acidication: performance of early embryos. PLoS ONE 7, e42497
90 Holcomb, M. et al. (2010) Long-term effects of nutrient and CO
2
enrichment on the temperate coral Astrangia poculata (Ellis and
Solander, 1786). J. Exp. Mar. Biol. Ecol. 386, 2733
91 Calosi, P. et al. (2013) Physiological responses to simultaneous shifts
in multiple environmental stressors: relevance in a changing world.
Integr. Comp. Biol. 53, 660670
92 Vinebrooke, R.D. et al. (2004) Impacts of multiple stressors on
biodiversity and ecosystem functioning: the role of species co-
tolerance. Oikos 104, 451457
93 Kremp, A. et al. (2012) Intraspecic variability in the response of
bloom-forming marine microalgae to changed climate conditions.
Ecol. Evol. 2, 11951207
94 DeWoody, J.A. and Avise, J.C. (2000) Microsatellite variation in
marine, freshwater and anadromous shes compared with other
animals. J. Fish Biol. 56, 461473
95 Kelly, M.W. et al. (2012) Limited potential for adaptation to climate
change in a broadly distributed marine crustacean. Proc. Biol. Sci.
279, 349356
96 Colegrave, N. (2002) Sex releases the speed limit on evolution. Nature
420, 664666
97 Kiessling, W. and Simpson, C. (2010) On the potential for ocean
acidication to be a general cause of ancient reef crises. Global
Change Biol. 17, 5667
98 Fuller, R.C. et al. (2005) How and when selection experiments might
actually be useful. Integr. Comp. Biol. 45, 391404
99 Tunnicliffe, V. et al. (2009) Survival of mussels in extremely acidic
waters on a submarine volcano. Nat. Geosci. 2, 344348
100 Rodolfo-Metalpa, R. et al. (2011) Coral and mollusc resistance to ocean
acidication adversely affected by warming. Nat. Clim. Change 1,
308312
Review Trends in Ecology & Evolution February 2014, Vol. 29, No. 2
125