Thermal Genetic Adaptation in the Water Flea and its Impact: An Evolving Metacommunity Approach

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SYMPOSIUM
Thermal Genetic Adaptation in the Water Flea Daphnia and its
Impact:An Evolving Metacommunity Approach
Luc De Meester,
1
Wendy Van Doorslaer,Aurora Geerts,Luisa Orsini and Robby Stoks
Laboratory of Aquatic Ecology and Evolutionary Biology,Katholieke Universiteit Leuven,Ch.Deberiotstraat 32,
3000 Leuven,Belgium
From the symposium ‘‘A Synthetic Approach to the Response of Organisms to Climate Change:The Role of Thermal
Adaptation’’ presented at the annual meeting of the Society for Integrative and Comparative Biology,January 3–7,2011,
at Salt Lake City,Utah.
1
E-mail:luc.demeester@bio.kuleuven.be
Synopsis
Genetic adaptation to temperature change can impact responses of populations and communities to global
warming.Here we integrate previously published results on experimental evolution trials with follow-up experiments
involving the water flea Daphnia as a model system.Our research shows (1) the capacity of natural populations of this
species to genetically adapt to changes in temperature in a time span of months to years,(2) the context-dependence of
these genetic changes,emphasizing the role of ecology and community composition on evolutionary responses to climatic
change,and (3) the impact of micro-evolutionary changes on immigration success of preadapted genotypes.Our study
involves (1) experimental evolution trials in the absence and presence of the community of competitors,predators,and
parasites,(2) life-table and competition experiments to assess the fitness consequences of micro-evolution,and (3)
competition experiments with putative immigrant genotypes.We use these observations as building blocks of an evolving
metacommunity to understand biological responses to climatic change.This approach integrates both local and regional
responses at both the population and community levels.Finally,we provide an outline of current gaps in knowledge and
suggest fruitful avenues for future research.
Introduction
Increasing evidence shows a profound impact of
global warming on the ecology and distribution of
a wide variety of species (Parmesan 2006;Visser
2008;Heino et al.2009).The selection pressures
associated with global warming may result in the
development of strategies for thermal resistance in
local populations,either by phenotypic plasticity
or by evolutionary responses (Parmesan 2006;
Visser 2008).Most studies on thermal adaptation
mainly focused on environmentally induced plastic
responses (Angilletta 2009).As a result,thermal
micro-evolution is often ignored when making pre-
dictions about the impact of global warming on the
survival of populations,the distribution of organisms
and/or the composition of communities (Pearson
and Dawson 2003).
Ecological and evolutionary processes were until
recently generally thought to occur on different
time-scales.However,there is strong evidence for
rapid and adaptive evolutionary responses with the
potential to alter ecological processes (e.g.,Hairston
et al.2005;Thompson 2005;Carroll et al.2007;
Fussmann et al.2007;Urban et al.2008).There is
an increasing number of reports of genetically differ-
ent lineages or populations of a given species influ-
encing ecological interactions with other species
(e.g.,Yoshida et al.2003;De Meester et al.2007;
Harmon LJ et al.2009).For instance,Jones et al.
(2009) have shown that increased evolutionary
potential affects community dynamics in a model
with multiple predator and prey genotypes.These
studies underscore that the occurrence of genetically
different strains,and thus micro-evolution,may
Integrative and Comparative Biology,pp.1–16
doi:10.1093/icb/icr027
￿ The Author 2011.Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology.All rights reserved.
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strongly impact ecological dynamics.The analysis of
rapid evolution as an ecological process has the
potential for making evolutionary ecology one of
the central topics of applied biological sciences
(Thompson 1998).This is especially important
because the evolving metacommunity framework is
very valuable for studying the impact of large-scale,
strong environmental changes,such as climatic
change,pollution,eutrophication,invasive exotic spe-
cies,and fragmentation of habitats.The evolving meta-
community framework integrates community ecology,
evolution,and regional aspects (dispersal and gene
flow,metacommunity structure;Urban et al.2008).
In an effort to evaluate in a focal species
the impact of micro-evolutionary processes on the
responses to changes in temperature at both the
population and community level,we initiated a
research program using large-bodied cladocerans,
and the water flea Daphnia magna in particular,as
a model system.Being strong competitors,large zoo-
plankters such as Daphnia can be considered key-
stone species in freshwater ecosystems (Lampert
1987).Owing to this central position in the food
web,micro-evolutionary responses within Daphnia
may potentially impact the responses of communities
to environmental change.
Starting from a representative sample of a natural
population of D.magna,our general approach
involved exposing the resulting experimental popula-
tions to different thermal regimes in experimental
evolutionary set-ups,and quantifying the resulting
micro-evolutionary responses using life-table experi-
ments as well as competition trials assessing fitness
(Fig.1).As we used different experimental settings,
both in highly simplified laboratory set-ups (Van
Doorslaer et al.2009a) as well as in semi-natural
outdoor mesocosms (Van Doorslaer et al.2010),
our data also shed light on the impact of the ecolo-
gical setting on the responses to changes in tempera-
ture.Finally,we aimed at explicitly investigating one
aspect of ecological consequences of the observed
micro-evolutionary responses by quantifying the
impact of the genetic changes on the success of
immigrant genotypes to become established (Van
Doorslaer et al.2009b).Our key observations are
that (1) a change in temperature can induce rapid
Fig.1 Overview of overall design of research on thermal adaptation in the water flea Daphnia magna.The selection experiment in
the laboratory and its associated follow-up experiments are presented by Van Doorslaer et al.(2009a).The selection experiment in
the mesocosms and the associated life-table experiment are presented by Van Doorslaer et al.(2010).The follow-up study involving
competition experiments with preadapted genotypes is presented by Van Doorslaer et al.(2009b).
2
L.De Meester et al.
evolutionary shifts,(2) the nature of these responses
is impacted by ecological conditions,and (3) the
micro-evolutionary responses impact ecological
interactions.In the following paragraphs,we provide
a short overview of these observations and put them
in a larger context,focusing on the usefulness of an
evolving metacommunity framework for our under-
standing of biological responses to climatic change.
We then highlight some important avenues for
future research in a section on perspectives,focusing
on gaps in knowledge as well as on the promises of
‘‘resurrection ecology’’ and paleogenomics.
Rapid thermal micro-evolution
Experimental set-up and main results
We carried out two experimental trials to quantify
the capacity of D.magna to genetically adapt to a
change in temperature regime (Van Doorslaer et al.
2009a,2010;Fig.1 and Table 1).In both cases,we
used the dormant egg bank of a natural D.magna
population as starting material.More specifically,we
took an extensive sample of the dormant egg bank
(3600 dormant eggs) of the D.magna population
inhabiting Brown Moss (Shropshire,UK) and
hatched them in the laboratory.Hatching dormant
egg banks yield representative samples of genetic
diversity in natural populations,as in nature
Daphnia populations are re-established after winter
by hatching from the dormant egg banks in the
superficial layers of the sediments.We thus obtained
representative samples of the resident population
inhabiting Brown Moss as starting material for our
experiments.By using animals derived from one
population,we quantified evolutionary potential of
a resident natural population to respond to changes
in temperature.
Using mixtures of clones derived from the same
population (Brown Moss),we carried out two selec-
tion experiments that were designed to quantify
Table 1 Overview of similarities and differences among the laboratory (Van Doorslaer et al.2009a) and the mesocosm experiment
(Van Doorslaer et al.2010) used to study thermal adaptation in Daphnia magna using the approach of experimental evolution
Aquarium Mesocosm
Populations
Source population Brown Moss (UK) Brown Moss (UK)
Number of clones 240 clones/unit 150 clones/unit
Selection experiment
Size of units 10 L 3000 L
Temperature regimes Constant Varying naturally (outdoor)
Culling 208C and 248C Ambient and þ48C
Yes (50% every 15 days;10% very 3 days) No
Community of competitors Absent Present
Parasites Absent Present
Predators Absent Invertebrate predators
Macrophytes Absent Present
Duration of selection 3 months 6 months
Responses
Increase in fitness (competition experiments) Yes Not quantified
Performance
a
r Yes
b
No
Age at release of 1st clutch No No
No.of 1st clutch offspring Yes
c
No
Size at maturity No Yes
d
Note.The experiments differed in several aspects that may have influenced responses to selection.This makes a direct comparison of the micro-
evolutionary responses in the two designs less straightforward.Yet,the experiments do share three important features:they start with material
from the same natural population (the number of clones is different,but in both cases high enough so that they can be representative samples of
resident genetic diversity),selection involved a near-optimal versus a þ48C temperature regime,and the experiment lasted a few months.
a
Performance is quantified as intrinsic rate of population increase but without taking mortality into account.
b
Increase in performance after selection in the 248C regime compared to after selection in the 208C regime,in the 50% culling regime only.
c
Increase in number of offspring of 1st clutch after selection in the 248C regime compared to selection in the 208C regime,in the 50% culling
regime only.
d
Reduction of phenotypic plasticity (smaller reduction in size at maturity at higher temperature) of animals exposed to the high temperature
regime.
Evolving metacommunities and thermal adaptation
3
responses to a change in temperature under two
widely differing ecological settings.In the first
experiment,carried out in 10 L aquaria in the
laboratory,we exposed the Daphnia to two constant
temperature regimes (20 and 248C) as pure cultures,
i.e.,in the absence of competitors,predators and
parasites (Van Doorslaer et al.2009a).In the
second experiment,we carried out a selection experi-
ment in 3000 L mesocosms that were inoculated with
natural communities in addition to the D.magna
clones from Brown Moss.The mesocosms contained
a rich community of a large number of interspecific
competitors,invertebrate predators,and parasites
(Feuchtmayr et al.2009;Jeppesen et al.2010).For
this study,we capitalized on a large-scale ecological
experiment designed to study the combined impact
of nutrient loading,temperature and predation on
replicate pond ecosystems (Feuchtmayr et al.2009).
The experiments (laboratory and mesocosm) differed
in several aspects (Table 1;more details on methods
in Van Doorslaer et al.2009a,2010),but shared two
important aspects:(1) the starting population,and
(2) the same large number of clones used to start the
experiment,representative of the genetic diversity in
the resident population.They also shared the same
temperature regimes in which one was near-optimal
or ambient and the other involved a rise in tempera-
ture of 48C (inspired by global-warming scenarios;
IPCC 2007);in both experiments,the selection
regimes lasted for a few months (3 months in the
aquarium;6 months in the mesocosm).
When cultured in the laboratory in the absence of
interspecific competitors,predators,and parasites,
populations of D.magna showed rapid differential
micro-evolutionary responses to different tempera-
ture regimes (208C versus 248C) in one of the culling
regimes (removal of 50% of the animals every
15 days;there was no response in the regime with
10% culling every 3 days;(Van Doorslaer et al.
2009a) (Table 1).Already after 3 months of selection,
populations selected at the highest temperature
(248C) performed better in terms of their intrinsic
population growth rate both at a test temperature of
248C as well as at the test temperature of 208C.Our
results also provide indications of adaptive evolution
of thermal plasticity under experimental warming.
In our experiments using mesocosms,in which
D.magna co-existed with a community of competi-
tors,predators and parasites under semi-natural con-
ditions,we observed significant genetic changes in
size at maturity within the short period (6 months)
during which the experiment was conducted.More
specifically,body size of the Daphnia selected at the
higher temperature regime (ambient þ48C) showed
a less strong response to temperature than did ani-
mals selected at ambient temperature.Daphnia
become smaller at higher temperatures,but the
response is less strong in animals previously kept
in the mesocosms exposed to a higher temperature
regime than in animals from the mesocosms at
ambient temperature (Van Doorslaer et al.2010).
The same response was also observed for Daphnia
pulex,another Daphnia species that occurred in
these mesocosms (Van Doorslaer et al.2010).In
another study involving the large-bodied cladoceran
Simocephalus vetulus,we observed an increased ther-
mal tolerance (Van Doorslaer et al.2007).
In each of these studies,a rapid genetic change
was observed upon exposure to a different tempera-
ture regime.In addition,these micro-evolutionary
changes were adaptive.This is clear for
Simocephalus which showed increased survival (Van
Doorslaer et al.2007) and for D.magna which
showed increased population growth in the aqua-
rium experiment (Van Doorslaer et al.2009a).The
adaptive nature of the response in size at maturity
observed in the mesocosm experiment was less
straightforward to assess (Van Doorslaer et al.
2010),but we could show in follow-up experiments
that adaptive genetic changes occurred (Van
Doorslaer et al.2009b).
Methodological considerations
We observed clear shifts in ecologically relevant traits
in response to the temperature treatments in our
selection experiments.Yet,there are methodological
limitations that may interfere with too bold an inter-
pretation of our results in the context of global
change.We here briefly discuss strengths and weak-
nesses of our approach.
Temperature regimes:timing and amplitude
We observed significant evolutionary responses to
temperature in all our selection experiments.Yet,
one may argue that our temperature regimes were
quite artificial.Although inspired by predictions of
widely supported models (IPCC 2007),we indeed
applied a sledge hammer approach by immediately
exposing the selected populations to a temperature
increase that is in reality predicted to rather gradu-
ally occur over a period of 100 years.A gradual
change in selection pressures may result in a different
evolutionary response than would a sudden change
(e.g.,Collins et al.2007;Gienapp et al.2008).
Although the comment is without doubt valid,
our experimental approach focuses on the evolution-
ary potential to respond to the predicted changes
rather than on the precise trajectory of
4
L.De Meester et al.
evolutionary change.By applying a much stronger
selection gradient than is expected to occur in
nature and monitoring genetic responses over very
short time spans,we tested the limits of the studied
populations to respond to a temperature change by
micro-evolution.Although the details of the
responses we observed should not be interpreted
too boldly,our results do indicate that local popula-
tions have the capacity to show micro-evolutionary
adjustments to changes in temperature.At the least,
this shows that there is relevant evolutionary poten-
tial,which is likely to influence the ecological
responses of local populations.Finally,the shifts in
temperature applied in our experiments are realistic
in the long run,as realistic scenarios of climatic
change predict more extreme climatic events in the
future.The amplitude of the temperature change
(þ48C) and the time frame over which we moni-
tored responses to selection (several months up to
an year) are very relevant in the context of intra-
annual or inter-annual variation,and thus predicting
responses to years with,for instance,an exceptionally
warm spring or summer.Our experimental set-up is
a simplification of what happens in wild populations
in another perspective.We did not analyze responses
to an increased variation in temperature.Indeed,not
only a step-wise versus a steady temperature increase
may affect the outcome of evolutionary responses
(e.g.,Collins et al.2007),but also constant versus
fluctuating temperature regimes potentially may be
important in driving micro-evolution (e.g.,
Kingsolver et al.2009).Both,the mean temperature
experienced by organisms in their habitat as well as
the extent of fluctuations (frequency and amplitude)
in habitat temperature may be important during the
life cycles of organisms.A study by Blanford et al.
(2003) shows that variation in environmental tem-
perature can be seen as a mediating factor in the
expression of genotypic variation on which selection
can act.There is a need for more experiments that
explicitly test for micro-evolutionary responses to
increased variation in temperature (e.g.,Leroi et al.
1994).
Artificial settings
More generally,it is clear that our experiments
represent simplifications of natural conditions,
which may interact with the evolutionary responses
we observe.This is true for any experimental study
of evolution,and cautions against an over-interpre-
tation of the results.Yet again,our experiments in
the first place show that there is important evolu-
tionary potential for responses to changes in tem-
perature.An important aspect that adds to the
relevance of our results is that we carried out differ-
ent experiments under widely different environmen-
tal conditions,and that the key observation of a
rapid evolutionary response to the temperature
change was observed under all these settings.Our
experiments thus point to the generality of the capa-
city of local populations to respond genetically to a
sudden change in temperature change over a short
interval of time.They also point to the fact that the
specifics of those responses are dependent on the
ecological settings (see below).
Genetic versus maternal effects
Our experimental procedure involved isolating indi-
viduals from selection units and culturing these as
separate clonal lineages for several generations before
carrying out life-table experiments at different tem-
peratures.As a result,our experiments did not con-
found maternal with genetic influences,and the
genetic differences among populations exposed to
different temperature regimes that we report reflect
micro-evolutionary responses.While we carefully
obviated interference from maternal effects,this
does not imply that maternal effects may not be
important in shaping responses to global warming
in nature (e.g.,see Visser 2008).Several studies
have shown that maternal effects may be of evolu-
tionary significance as they provide a mechanism for
adaptive transgenerational phenotypic plasticity (e.g.,
reviewed in Mousseau and Fox 1998) and may dra-
matically enhance rates of evolutionary responses to
selection (reviewed by Mousseau et al.2009).
Evolution as changes in relative
abundance of clones
Our experiments mimic the natural situation in two
important ways:(1) we inoculated our experimental
populations using dormant eggs from the superficial
layers of the sediments;this is exactly what happens
in nature at the beginning of the growing season,
and (2) we initially inoculated the selection units
with genetically diverse populations,and then mon-
itored the genetic changes over time during the selec-
tion experiment.This mimics what happens in
nature,where genetically diverse populations are
exposed to clonal and environmental selection after
establishment.In addition,the initial populations
used in the experiments were genetically standardized
and consisted of a given number (more than 100) of
genetically distinct clones that were replicated over
experimental units,making comparisons across
experiments possible.All,or at least most,genetic
responses observed in our experiments reflect
Evolving metacommunities and thermal adaptation
5
changes in the relative abundance of the inoculated
clones rather than the genetic variation generated by
mutations typically studied in experimental evolution
trials with bacterial communities (e.g.,Remold and
Lenski 2001;Rifkin et al.2005) or generated by
sexual recombination (e.g.,Tessier et al.1992;
Goddard et al.2005).As evolution is defined as a
change in frequencies of alleles (e.g.,Ridley 2003;
Freeman and Herron 2007),the observed changes
in the relative frequency of clones clearly reflects
micro-evolutionary responses at the population
level.Significant changes in clonal diversity and her-
itability of life-history traits have been observed
within a short time-span (months) in natural
Daphnia populations (e.g.,Lynch 1984;Tessier
et al.1992).We can exclude that such changes
were induced by sexual reproduction events,because
such events would have resulted in a different geno-
typic composition than the initial population.What
we observe is only a change in the relative abundance
of genotypes inoculated in the initial population.
Thus,by definition,the observed changes in relative
frequency of clones reflect evolution and may reflect
an essential part of the micro-evolutionary responses
of any species that combines asexual and sexual
reproduction.
It would be very useful to quantify the dynamics
of the evolutionary responses over several cycles of
reproduction,i.e.,involving both parthenogenetic
and sexual reproduction.It can be expected that
sexual reproduction will result in genetic slippage
of the mean genotypic value in a direction contrary
to that resulting from selection (Lynch and Deng
1994) and thus,temporarily lower fitness.On the
other hand,sexual reproduction generates novel
genetic variation,which may increase the response
to selection during the subsequent phase of parthe-
nogenetic reproduction (e.g.,Tessier et al.1992).
Importantly,in our design we started from sam-
ples of naturally occurring genetic variation,as we
started from dormant egg banks.Natural populations
of the species studied thus,harbor enough genetic
variation at the start of the growing season to
show these rapid genetic responses.We did not
mix genotypes from different latitudes or other tem-
perature-related gradients to artificially increase
genetic variation for temperature-associated traits.
Our results show that significant genetic changes in
ecologically relevant traits can be observed after only
a few months of thermal selection in large-bodied
cladocerans,which are considered keystone species
in standing inland waters.Evolutionary responses
thus occur at ecological time-scales and may interfere
with ecological processes (Hairston et al.2005;
Pelletier et al.2009).We discuss this in more detail
below.
Importance of ecological context
Evolutionary responses take place in an ecological
setting that typically involves interaction between
individuals and the dynamics of changing popula-
tions and communities in addition to abiotic envir-
onmental conditions.Our results underscore the
importance of the ecological context in shaping
micro-evolutionary responses.First,the results
reported by Van Doorslaer et al.(2009a) show that
the laboratory environment itself represents a selec-
tion pressure upon the populations.We indeed
observed strong differences in life-history traits
between populations cultured in the laboratory aqua-
ria and the initial populations,which were hatched
from dormant eggs and represent a random sample
of genotypes from the field.This suggests that the
selective environment in the laboratory experiment
was different than the one in the field,where the
populations face multiple selection forces including
biotic interactions such as predation,interspecific
competition and parasites.Secondly,we observed
that strong fluctuations in population size imposed
by one of our culling regimes (50% every 15 days
instead of 10% every 3 days) and thereby creating
recurrent periods during which exponential growth is
possible,enhanced the rate of micro-evolution.This
indicates that population dynamics may represent an
important ecological determinant of evolution,as
they establish the relative importance of growth
rate and competitive strength (de Roos and Persson
2003;Nelson et al.2005).Third,the micro-evolu-
tionary responses obtained in the laboratory (Van
Doorslaer et al.2009a) and mesocosms (Van
Doorslaer et al.2010) were quite different
(Table 1).This suggests that the ecological setting
(amongst others,single-species isolated cultures
versus community-embedded populations) is impor-
tant in driving micro-evolutionary change and in
determining which traits adapt to a change in tem-
perature.In their review of experimental evolution
studies,Reznick and Ghalambor (2005) similarly
stress that controled laboratory conditions yield
quite different outcomes for stress responses of
organisms compared to field studies in which species
are subjected to a wide variety of selective forces,
including trade-offs between different stressors.
Our observation that the broader ecological con-
text strongly influences the resulting micro-evolu-
tionary responses is important,as it stresses the
complexity of predicting evolutionary responses,
6
L.De Meester et al.
and cautions against too bold an extrapolation of
laboratory experiments that are carried out in an
over-simplified environment.At the same time,this
warning also applies to our own mesocosm experi-
ment,because the mesocosms,even though more
complex,can hardly be considered true replicas of
real lakes.As reviewed by Angilletta (2009),both,
laboratory and mesocosm experimental designs
have their advantages and disadvantages.Selection
experiments in the laboratory,which often only
include intraspecific interactions,directly link envir-
onmental temperatures to the evolution of pheno-
types.Any difference between the phenotypes of
experimental and control lines can be attributed to
thermal adaptation.Laboratory experiments are thus
well-suited to test the potential for evolutionary
responses to temperature changes,but they are a
weak imitation of natural conditions.Field experi-
ments or experiments under semi-natural conditions
in outdoor mesocosms may reveal novel patterns of
thermal adaptation because natural selection depends
on the interaction (including trade-offs) of tempera-
ture and other environmental and biotic factors.This
increases environmental realism to an important
degree,but clearly complicates straightforward inter-
pretations of the results.The micro-evolutionary
responses that we observe in our mesocosm experi-
ment may be caused by direct selective effects of
temperature as well as by indirect temperature-
mediated effects via changes in predation pressure,
competitive interactions,availability of food,and/or
prevalence of parasites.It is impossible to disentangle
the impact of these different potential causes of
genetic changes without performing extensive addi-
tional experiments.By carrying out both laboratory
and outdoor mesocosm experiments,however,we
did cover two important and widely different
points in the spectrum of ecological complexity in
our assessment of micro-evolutionary responses to
temperature change.
Ecological consequences of evolution
Given that the micro-evolutionary changes we
observed in our experiments occur in a short span
of time,they have the potential to influence ecolo-
gical processes (e.g.,Hairston et al.2005;Urban et al.
2008).In a follow-up study to the mesocosm experi-
ment (Van Doorslaer et al.2009b),we performed an
experiment to test this for one specific interaction.
More particularly,we quantified to what degree
genetic adaptation may increase the capacity of a
resident population to reduce success of immigrant
genotypes to establish.As we wanted to mimic a
scenario relevant under climatic change,we carried
out our experiments at increased temperature
(ambient þ48C) and used genotypes from a
warmer region (southern France) as immigrants to
compete with nonadapted and warm-adapted UK
residents (cfr.Brown Moss population).The results
were striking.First,the southern genotypes had a
very strong fitness advantage over the UK residents
in the competition trials at elevated temperature
(ambient þ48C;Van Doorslaer et al.2009b).
Second,the southern genotypes also had higher fit-
ness at elevated temperatures than did the resident
populations that were allowed to adapt genetically to
the increased temperature regime during 1.3 years.
However,their fitness advantage was strongly
reduced compared to their fitness advantage when
confronted by nonwarm-adapted populations (Van
Doorslaer et al.2009b).These observations show
that the observed micro-evolutionary responses are
relevant with respect to competitive interactions of
the local population with immigrant genotypes.
We calculated that under realistic circumstances,
the increased competitive strength of warm-adapted
residents would result in a more than doubling of
the time for the immigrant genotypes to become
dominant in the local community,and that the
number of immigrants would have to be 10
4
–10
5
times higher to result in the same speed at which
half of the population would consist of immigrants
when the immigrants have to compete with warm-
adapted rather than with nonwarm-adapted resident
populations (Van Doorslaer et al.2009b).This is a
striking difference to result from only 1.3 years of
micro-evolutionary change.Unfortunately,the
mesocosm selection experiment was terminated in
the second year (Feuchtmayr et al.2009),as it
would have been instructive to monitor further
micro-evolutionary changes and to determine
whether and when local residents and preadapted
immigrant genotypes could become equally adapted
to the high temperature regime.Two expected
impacts of genetic tracking of environmental
change on community responses to climatic change
are (1) that species composition of local commu-
nities will change less in the presence than in the
absence of micro-evolutionary adaptation,and (2)
that responses of communities to global warming
will be more localized in the presence than in the
absence of evolution.Environmental changes are
expected to impact the relative fitness of different
species in a community.However,if local popula-
tions genetically track environmental changes in a
way that their fitness relations remain unchanged,
this may translate in highly reduced changes in
Evolving metacommunities and thermal adaptation
7
species composition compared to scenarios without
evolution (Fig.2).In previous mesocosm studies
investigating temperature-mediated ecological effects
related to global warming,temperature often only
had a marginal effect on community composition
(e.g.,McKee et al.2002;Moss et al.2003).In prin-
ciple,part of this absence of a shift in species com-
position may be mediated by shifts in genotype
composition within species,i.e.,evolution.The
response of a local community to global warming
may be mediated by local and regional processes
(Fig.2),as one may expect changes both in the
relative abundance of resident species in the commu-
nity,as well as immigration of new species from the
regional species pool.Specifically in the case of
global warming,immigration may be important.In
the northern hemisphere,organisms may be success-
ful when migrating northwards from southern loca-
tions,as they are preadapted to a warmer climate.
Our results,however,show that local genetic track-
ing of temperature change in resident populations
may reduce establishment success of immigrant gen-
otypes (Van Doorslaer et al.2009b).Further experi-
ments are needed to test whether this also applies to
immigration of different species.In an earlier experi-
ment,which did not focus on temperature selection,
it was shown that differences in the genotypic com-
position of D.magna may indeed impact the success
of species of the regional species pool to become
established (De Meester et al.2007).These combined
results indicate that it is not unlikely that local adap-
tation to temperature change may impact the success
of species in immigrating from other regions.If so,
evolution would have as a net effect,a reduction of
the importance of regional processes (immigration) in
the response of local communities to global warming.
Although important life-history traits clearly
evolved during experimental warming,one should
Fig.2 A schematic representation of the evolving metacommunity approach to study biological responses to climatic change.
When a local community is exposed to climatic change,it may respond locally both by changes in species composition (species sorting)
as well as by genetic adaptation of local populations that build up the community (micro-evolutionary change).Both responses may
interact with each other:If local genetic adaptation efficiently tracks environmental change,it may reduce the impact of species sorting,
whereas rapid replacement of species may not allow time for specific species to respond by evolutionary change.In addition to
the local responses,there may also be a regional impact,through immigration of novel genotypes and/or species from other
populations.These may be preadapted to the local environmental conditions that result from environmental change.In a climate-change
scenario,this would involve immigration of genotypes or species from warmer regions inhabited by populations and species that are
preadapted to higher temperatures.Importantly,local and regional processes interact,as efficient tracking of climatic change by
local processes may reduce success of immigrants in becoming established,whereas rapid replacement of resident genotypes and
species by preadapted immigrants may not allow time for local species sorting or micro-evolution.This interplay between local
and regional processes and between micro-evolution and species sorting is the key focus of an evolving metacommunity perspective.
8
L.De Meester et al.
not conclude from our results that micro-evolution-
ary responses will ‘‘solve’’ the problems associated
with climatic change.No doubt,rapid genetic track-
ing of global warming may reduce extinction rates of
local populations and the impact of migration,but
there are several reasons why one should be careful
not to over-interpret our observations.First,there is
the observation that global warming already has had
a clear impact during the past decades,including
replacements of species,mismatches in interactions
between species,local extinctions,and invasion of
warm-adapted species (e.g.,Thomas et al.2004;
Hickling et al.2006;Durant et al.2007;van der
Wal et al.2008).Second,one should not expect
perfect genetic tracking of changes in a way that
the interactions of species with their abiotic environ-
ment or with other species would not change:(1)
species differ in their capacity to evolve because of
differences in generation time,genetic variation,and
ecological,genetic,and phylogenetic constraints.This
will change interactions among species,including
interactions with food,competitors,predators,and
parasites,and (2) genetic adaptation to novel condi-
tions may entail costs,both in terms of reduced
energy or reduced evolutionary potential to respond
to other stressors (e.g.,Eranen et al.2009).In short,
temperature is not the only environmental selective
force that organisms encounter in their habitat,and
complex biotic interactions and combined effects of
multiple abiotic stressors both are expected to com-
plicate responses to global warming.
Overall,our results suggest that genetic adaptation
may occur rapidly and is likely to have far-reaching
ecological consequences (see also Jones et al.2009;
Pelletier et al.2009).From the previous paragraph,it
is clear that micro-evolution will not necessarily
mitigate the impact of global warming,but rather
change the impact.These changes may include an
alteration in the relative importance of biotic inter-
actions and different stressors,or an increased capa-
city of resident populations to respond by internal
dynamics and thus reduce the impact of immigration
from the regional genotype and species pool.From
our results,it is clear that it is important to include
evolutionary responses in predictions of changes in
community composition in response to global warm-
ing.In most research and models predicting the
potential geographic distribution of species under
current and future climatic scenarios (so-called ‘‘bio-
climate envelopes’’),evolutionary responses are
ignored (e.g.,Pearson and Dawson 2003).This is
likely to lead to wrong predictions (e.g.,Pearson
et al.2006;Skelly et al.2007).Given the rates of
evolutionary change,we observe in our experiments,
the degree to which these predictions are wrong
could be problematic,not necessarily because the
models would overestimate the impact of climatic
change,but rather because the real impact may be
of a different nature.
Future perspectives
Our results provide evidence for rapid and adaptive
micro-evolutionary responses to increases in tem-
perature,and show that these genetic changes are
likely to impact ecological responses to global warm-
ing.In the following paragraphs,we present some
ideas for future research that are inspired by our
results as well as by the methodological limitations
of the work presented here.These future perspectives
refer to the need to broaden our knowledge of evo-
lutionary responses to climatic change by including a
wider range of organisms,systems,and conditions,
the possibilities offered by new approaches and tech-
niques,and the need to further study ecological
implications of micro-evolutionary responses to cli-
matic change.
Broadening of the scope
Beyond Daphnia of temperate shallow lakes
Our study focused on micro-evolutionary responses
to temperature change in large cladocerans such as
D.magna (Van Doorslaer et al.2009a,2009b) and
S.vetulus (Van Doorslaer et al.2007).Although these
species may dominate zooplankton communities in
shallow standing waters in temperate regions and
may play a key role in the ecology of these systems,
they are typically only important in temperate cli-
matic zones and in shallow ponds and lakes.There
is a need for studies on micro-evolutionary responses
to climatic change of zooplankton in deep lakes and
in the marine realm.The responses of deep-lake
biota to increasing temperature may be different
from those of shallow-water biota,as deep lakes
are thermally stratified and thus provide additional
opportunities for organisms to respond to changes in
thermal conditions by changing their vertical-migra-
tion behavior.There is also a need to study responses
to global warming in warm semi-arid regions and in
tropical systems.Temperature change is expected to
be of less amplitude in the tropics,but environmen-
tal temperatures are already high and may be close to
the thermal tolerance limits of several species (e.g.,
for tropical terrestrial species,see Deutsch et al.2008;
Huey et al.2009).A study by Stillman (2003) shows
that marine Porcelain crab species that have evolved
the greatest tolerance to high temperatures have
done so at the expense of their capacitiy for
Evolving metacommunities and thermal adaptation
9
acclimation,and these species will be the most sus-
ceptible to increases in microhabitat temperatures.
Also,large lakes,rivers,and marine systems differ
widely in dimensions,and north–south-oriented
rivers and marine systems (e.g.,Beaugrand et al.
2002) may provide more opportunities for migration
in response to climatic change along a habitat con-
tinuum than do the ponds and lakes inhabited by
our model species D.magna,and this may strongly
modulate the observed responses.
Realistic scenarios of change
As already mentioned,we have made some prag-
matic decisions concerning the temperature regimes
that we used in our experiments.Although our
choice to impose a sudden temperature increase of
þ48C can be viewed as an acceptable compromise
between realism and feasibility,it is clear that this
approach has intrinsic limitations.Two important
and feasible additions would be to vary both the
speed of temperature change,and to expose popula-
tions to treatments with different amplitudes of tem-
perature change.The first experiment may,for
practical reasons,not include realistic rates of tem-
perature change such as a change of 518C in a
decade,but would allow quantifying the degree to
which different rates of temperature change may
impact evolutionary responses of populations.The
second experiment would test the impact of an
important expected characteristic of future climate:
increase in extreme temperatures.
The broader community and trophic cascades
Zooplankton communities interact with both,their
prey populations and with a wide range of predators,
and these interactions are likely to be strongly
impacted by global warming (Tylianakis 2009;
Gilman et al.2010).It has been shown that increased
temperature has the potential for destabilizing plank-
tonic food webs (Beisner et al.1997;Strecker et al.
2004;Wagner and Benndorf 2007).Although our
mescocosm experiments,by providing semi-natural
conditions,took this complexity caused by trophic
interactions into account to some extent,there is a
need for studies that also quantify genetic responses
to climatic change by phytoplankton,macro-inverte-
brates and fish.It has recently been shown that dif-
ferent ecotypes of three-spine sticklebacks may have
a different impact on ecosystem characteristics
(Harmon LJ et al.2009),indicating that climate-
driven evolutionary change in predators may cascade
down along the food web (see also Harmon JP et al.
2009).In addition,there is good reason to expect
bottom–up effects of climate-driven evolutionary
responses in phytoplankton.Yoshida et al.(2003)
showed that genetic diversity in algae may strongly
impact predator–prey dynamics in a zooplankton–
alga system,and the short generation time of
phytoplankton may provide ample scope for rapid
evolutionary changes (e.g.,see Vanormelingen et al.
2009).
Multiple stressors
Global warming is not the sole stressor to which
natural populations are exposed to.It is becoming
increasingly clear that the vulnerability of freshwater
communities to global warming can be exacerbated
by other anthropogenically induced large-scale envir-
onmental stressors such as eutrophication,metal pol-
lution,habitat destruction,UV irradiance,and
introductions of species (reviewed by Bronmark
and Hansson 2002;Sokolova and Lannig 2008).In
addition,climatic change itself may exacerbate pro-
blems of eutrophication and exotic species,amongst
others (Kernan et al.2010).These different anthro-
pogenic stressors may synergistically interact,leading
to intensified negative impacts on populations,spe-
cies,and communities.Several studies reported
nonadditive effects of stressors (e.g.,Coors and De
Meester 2008),while others reported temperature-
mediated effects of predation,food concentration,
pesticides,metal pollution,and/or parasitism on
freshwater communities (e.g.,Folt et al.1999;
Giebelhausen and Lampert 2001;Mitchell et al.
2005;Bernot et al.2006;Heugens et al.2006;Vale
et al.2008).There is a need for studies that quantify
patterns and constraints of micro-evolutionary
responses to multiple stressors in the framework of
climatic change.
Novel approaches to the study of evolutionary
responses to global warming
Resurrection ecology
Assessing the impact of global warming under nat-
ural conditions generally requires long-term datasets
and monitoring.Records of freshwater zooplankton
in sediments,however,offer the possibility of
extending the timescale of observation,provided
that the environmental changes of interest also
occurred in the past.Many organisms inhabiting
inland waters produce dormant stages when environ-
mental conditions deteriorate.These dormant stages
accumulate in the sediment and form dormant egg
banks.As sediments in lakes often are layered,these
dormant egg banks can be viewed as historical
archives harboring valuable information on the his-
tory of the habitat (including selective pressures) and
10
L.De Meester et al.
the resident populations and communities (reviewed
by Jeppesen et al.2001;Brendonck and De Meester
2003;Smol and Douglas 2007;Hairston and De
Meester 2008;Fig.3).The ‘‘resurrection ecology’’
approach involves hatching of dormant eggs of dif-
ferent age to compare populations from different
time periods.The procedure for comparing these
populations can be similar to the one we used to
compare populations in our experimental evolution
trials.By comparing representative samples from dif-
ferent times,it is possible to document rates and
patterns of evolution (e.g.,Hairston et al.1999;
Cousyn et al.2001;Decaestecker et al.2007).Given
that there is a clear signal of global warming during
the course of the past decades,this approach can also
be applied to reconstruct responses to climatic
change (Angeler 2007;Franks et al.2007,2008).
Genomics
In our study,we quantified responses in ecologically
relevant traits through a quantitative genetics
approach.The promise of ecological and functional
genomics in studies of climatic change is high,as
genomic tools may allow one to directly assess selec-
tion at the gene level and link genetic variation at the
DNA level directly to traits’ values (e.g.,reviewed in
Vasemagi and Primmer 2005;Hoffmann and Daborn
2007).The genetic basis of adaptive shifts has been
identified in several studies from a combination of
candidate gene studies,genome scans,and expression
studies (e.g.,Hanski and Saccheri 2006;Pool and
Aquadro 2007;reviewed in Hoffmann and Willi
2008).Understanding the genetic underpinning of
the adaptation of organisms to changing environ-
ments is of pivotal importance in evolutionary ecol-
ogy.However,it is often a challenging task because it
is nearly impossible to unambiguously attribute
selective forces within multidimensional selection
regimes.Daphnia offers unique opportunities for
the study of adaptation and environmental genomics
for several reasons:(1) a key asset of Daphnia is the
production of dormant stages that accumulate in
layered egg banks and represent a valuable resource
for the study of evolution in natural populations
using the approaches of resurrection ecology and
paleogenetics (Hairston et al.1999;Decaestecker
et al.2007) (Fig.3).Dormant stages represent the
history of evolution during environmental changes
and can be used to reconstruct the genomics of evo-
lutionary responses over long periods of time,(2) the
rapid progress of techniques in genomics,in particu-
lar DNA sequencing,opens new perspectives for
nonmodel genetic species.More importantly,geno-
mic tools for Daphnia,including the full genome
sequence,are currently being generated at a very
fast rate,thanks to the coordinated effort of the
Fig.3 In addition to the experimental evolution approach outlined in the present work,in which one starts with a representative
sample of the recent dormant egg bank of natural zooplankton populations,one can also sample different sedimentary layers that
represent an archive of the history of the resident population to study responses to climatic change in the recent past.The layered
dormant egg banks can be used in a ‘‘resurrection ecology’’ approach,in which one hatches dormant eggs from different time periods
and compares their traits (e.g.,Cousyn et al.2001).In addition,it is also possible to apply a paleogenomics approach,using variation in
genes underlying traits to reconstruct micro-evolutionary changes through time.The main advantage of the paleogenomics approach is
that it is not dependent on the capacity to hatch dormant eggs,so that the time frame over which micro-evolutionary responses can be
studied can be extended substantially.We here,list 1565 as a date of interest as it represents a period of relatively low temperatures
(‘‘little ice age’’ in the Middle Ages).The 1960s are a decade characterized by relatively low temperatures,whereas the recent decade
is characterized by high average temperatures globally.
Evolving metacommunities and thermal adaptation
11
Daphnia Genomics Consortium (www.wfleabase
.org),and (3) the short generation time of Daphnia
allows an experimental evolution approach,pivotal
to verify the signature of adaptation in the wild
when reverse genetics is not available (this is typical
of nonmodel genetic species).The rapid progress of
genomics and the key assets of Daphnia open new
enthralling perspectives for answering questions of
central interest in ecological genetics.How many
and what genes are responsible for adaptive
responses in the wild?Does adaptation following
an environmental change arise more frequently
from standing genetic variation or from new muta-
tions?What type(s) of genetic variation (poly-
morphism in coding regions,regulatory changes,
gene duplications,inversions) is responsible for
adaptation?Is adaptation the result of many genes
of small effect or of few genes of large effect?These
questions have always intrigued evolutionary biolo-
gists and for years they have tried to answer them
through empirical and theoretical approaches.
However,these questions remain only partly
addressed because of technical and experimental lim-
itations.The availability of next-generation sequen-
cing technologies associated with a well-known
ecological context in species with a central role in
natural ecosystems has the potential to revolutionize
genomic research and enables us to focus on a large
number of outstanding questions that previously
could not be addressed effectively.
The broader framework:evolving metacommunities
The responses of biological communities to climatic
change may be profoundly impacted by the interac-
tions among responses at the population and the
community level,and among local and regional pro-
cesses (see Fig.2;evolving metacommunity
approach,Urban et al.2008).At the level of the
local community,environmental change may cause
both a shift in species composition (species sorting)
as well as a selection-mediated genetic change in trait
values of resident species (micro-evolution).These
two processes may interact with each other,as on
the one hand,genetic adaptation of resident species
may reduce their replacement by other species,
whereas at the other hand a population may be dis-
placed before it had time to genetically adapt to the
changing environmental conditions.
These local processes,however,interact with
regional processes.The response of a local commu-
nity may indeed also be modulated by immigration
of species from elsewhere (Fig.2).This may include
species from the regional species-pool at the
landscape level,but may also involve long-distance
dispersal.It has indeed been shown that regional
influences may occur at different geographic scales
from high rates of dispersal and associated genetic
exchange between habitats located only a few
meters from each other up to dispersal of organisms
over 41000 km (e.g.,Frisch et al.2007).Especially
in aquatic organisms producing dormant stages,
occasional long-distance dispersal of individuals
from other latitudes by migrating birds is possible
(Figuerola and Green 2002;Green and Figuerola
2005;Frisch et al.2007).The long-distance dispersal
of organisms from regions with a warmer climate
has the potential of being an important driver of
ecological responses to climatic change.This
regional influence may again involve both
responses at the population level (immigration of
new genotypes;gene flow) as well as responses
at the community level (immigration of new species;
dispersal).
Importantly,the local and regional processes as
outlined here may interact;a strong local response
may reduce the impact of immigration,whereas suc-
cessful immigration of warm-adapted genotypes or
species may shortcut local responses (Fig.2).
However,in addition to preventing local populations
from matching their local selective optima,gene flow
may also contribute to an increase in genetic varia-
tion,thereby increasing the adaptive potential that
allows populations to track changing thermal
optima under global warming (the swamping and
spreading effect of gene flow at the margins of the
geographic range is reviewed by Bridle and Vines
2007).It may indeed be that the genetic variance
present in a local population will not be sufficient
for repeated adaptive adjustments to continuously
increasing temperatures,and that preadapted geno-
types from warmer regions entering local popula-
tions may facilitate a sustained response to thermal
selection.Understanding how these various processes
interact and shape the responses of local commu-
nities to climatic change is of key importance for,
amongst others,adjusting the current models pre-
dicting changes in species distribution and biodiver-
sity in response to climatic change.Current models
predict that many species will expand their geo-
graphic range northward,thereby following the shift-
ing temperature zones and resulting in colonization
of new habitats (‘‘bioinvasions’’) with potential con-
flicts with native species through altered competitive
and/or predatory interactions (Rahel and Olden
2008;Rahel et al.2008).
Our results indicate that rapid micro-evolution
may enhance the capacity of native populations to
12
L.De Meester et al.
reduce immigration of southern warm-adapted
(invasive) individuals of the same species.So far,
however,we did not yet include parallel responses
at the community level and the interaction between
local genetic and community responses (e.g.,see
Dangles et al.2008;le Roux and McGeoch 2008;
Schaefer et al.2008).In general,there is a need to
quantify the impact of micro-evolutionary changes
on:(1) Species sorting in the local community;it
is conceivable that genetic adaptation reduces the
degree to which species composition changes in
response to environmental change,but so far this
has not been quantified;(2) Establishment of immi-
grant species;similar to the reduction in the success
of immigrant genotypes to become established shown
by Van Doorslaer et al.(2009b),one may expect that
genetic adaptation of local populations to environ-
mental change may reduce immigration rates of spe-
cies from the regional species-pool;(3) Trophic
interactions and structure;micro-evolutionary
responses may not only change competitive strength
of species in the local community (e.g.,Peck et al.
2009),but may also alter predator–prey (Harmon JP
et al.2009) and host–parasite dynamics.Organisms
at different trophic levels tend to differ strongly in
generation time (cf.rate of adaptation) and dispersal
rates.This may yield intriguing dynamics,which are
currently,however,very poorly understood;and (4)
Ecosystem functions and services;In general,micro-
evolutionary responses may impact ecosystem char-
acteristics and functions (e.g.,Harmon LJ et al.
2009),and thus also ecosystem services.Although
freshwater ecosystems provide a wide variety of valu-
able goods and services for human societies,aware-
ness of the need to conserve freshwater biodiversity
seems limited.Ecosystems’ goods and services repre-
sent the benefits human populations derive,directly
or indirectly,from ecosystems’ functions (Dudgeon
et al.2006).The variety of benefits provided by
freshwater ecosystems include regulation of waste
and nutrients;retention of soil;provisioning of
water and food (fish);and cultural services such as
recreation (e.g.,Farber et al.2006).If micro-evolu-
tionary responses impact the resilience of ecosystems
or their capacity to resist change,or other ecosystem
functions such as the efficiency of energy transfer
and productivity,then this may strongly impact
the various ecosystem services mentioned above.
Clearly,there is still much to learn,and in our opi-
nion the concept of evolving metacommunities
(Urban et al.2008) offers a solid framework for
structuring different processes and for designing
experiments.
General conclusions
The key message of our research is that significant
genetic adjustments to increased temperature in the
context of global warming can take place in our
model system,the waterflea Daphnia,in a short
time frame of a few months or years.We found
evidence for thermal micro-evolution in life-history
traits and competitive ability in a keystone freshwater
zooplankton species that occurs on an ecologically
relevant time scale (i.e.,within one growing
season).Given this information,we emphasize the
need to incorporate evolutionary responses in
models that aim at predicting the responses of popu-
lations and communities to global warming (see also
Peck et al.2009).We further show that evolution has
the potential to profoundly influence ecological pro-
cesses by impacting the relative importance of local
and regional dynamics,which highlights the impor-
tance of the perspective of an evolving metacommu-
nity for further research on the biological
consequences of global warming for freshwater eco-
systems (e.g.,Urban and Skelly 2006;Urban et al.
2008;Gilman et al.2010).
Funding
K.U.Leuven Research Fund projects (grants GOA/
2008/06 and PF/2010/07);Fund for Scientific
Research (FWO) (project G.0419.08);EU project
EURO-LIMPACS;IWT fellowship (to W.v.D.and
A.G.);L.O.is a postdoctoral researcher of the FWO.
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