Ecoevolutionary Dynamics of Carbon Cycling in the Anthropocene

2018·2.4 MB·English

by  J. Grey Monroe

Review
Ecoevolutionary Dynamics of Carbon Cycling

in the Anthropocene

J. Grey Monroe,1,2,* David W. Markman,3 Whitney S. Beck,1,3 Andrew J. Felton,1,3
M egan L. Vahsen,1,2,4 and Ya mina Pressler1,5

Climate change is altering natural selection globally, which could shift the Highlights

evolutionary trajectories of traits central to the carbon (C) cycle. Here, we Globalclimatechangeisalteringnat-

examine the components necessary for the evolution of C cycling traits to ural selection and shifting the evolu-

tionarytrajectoriesoforganismtraits.
substantially drive changes in global C cycling and integrate these compo-

nentsintoaframeworkofecoevolutionarydynamics.Recentevidencepoints Ccyclingandotherecosystemfunc-
tothe evo lu tionofCcy cli ngtraitsduringt heAnthrop ocenea ndthepo tential tio ns are m edi ated b y organism traits,
whicharesubjecttoevolutionarypro-
to significantly affect atmospheric CO . We identify directions for further
2 cesses;however,evolutionisnotyet

collaboration between evolutionary, ecosystem, and climate scientists to explicitlyincludedincurrentglobalC
cyclingm odels.
study these ecoevolutionary feedback dynamics and determine whether this

evolution will ultimately accelerate or decelerate the current trend in rising RapidevolutionofCcyclingtraitshas

atmospheric CO . been recently observed in several
2
organisms,indicatingthatevolutionary

responses to climate change could
Evolution and C Cycling on a Changing Planet
altertheCcycleandultimatelyimpact
The Earth has e nt ered a n ew ge ological epo ch, the Anthropocene, marked by rapidly atmo sph er icCO .
2
increasing atmospheric CO concentrations and changing environments [1,2]. For many
2
TheevolutionofCcyclingtraitscould
species, these changes will impose strong selection pressures and persistence will require
generate particularly important ecoe-
adaptation,directlyorindirectlyaffectingtheevolutionoffunctionaltraits,thatis,thosethat
volutionary feedbacks, the under-
characterize the ec olo gicalrole and effec t of an organ ism on its en vironm ent [3– 5]. Un der- standingo fwhichwillre quire greater

standingtheseevolutionarytrajectoriesiscritical,giventheaccumulatingevidencethattrait integrationofevolutionary,ecosystem,

andclimatescience.
evolutioninresponsetoclimatechangecouldalterkeyecosystemprocesses,includingthe

C cycle [6–9]. Describing how the C cycle is affected by trait evolution is particularly

important because organism traits influence whether C is stored or released into the

atmosphere. In addition to asking whether species will persist via evolutionary adaptation
to changing en vironmen ts, it is al so imper ative to ask how or gan ism C cyclin g traits will 1GraduateDegreeProgramin
Ecology,C olorado StateUn iversity,
evolve as species adapt and what the consequences of C cycling trait evolution on the
FortCollins,CO80523,USA
environment will be. 2Dep artment ofB ioagric ultural

ScienceandPestManagement,

ColoradoStateUniversity,Fort
Here, we examine the potential for contemporary evolution to impact global C cycling and
Collins,CO80523,USA
storage through shifts in C cycling traits. We first examine how C cycling is mediated by 3Depart men tofBio logy,Colorado

organism traits and evolution. We then discuss natural selection pressures resulting from StateUniversity,FortCollins,CO
80523 ,USA
climate change and the extent of genetic variation for C cycling traits on which this selection can 4Depar tmentofBiologicalSciences,
act.Next,wereviewthepotentialforrapidadaptiveevolutionofthesetraitstooccurduringthe Universityof No treDame, Notre

Anthropocene.Finally,wereviewevidenceandapproachestostudythedirectionandmagni- Dame,IN46556,USA
5Natura lR esourc eEcology
tudeofcontemporaryevolutiononCcyclingtraitsandresultingimpactsontheglobalCcycle.
Laboratory,ColoradoStateUniversity,
The body of work presented here reveals progress toward a synthesis between ecosystem FortCollins ,CO8052 3,US A

science and evolutionary biology and suggests valuable directions for further research. We

proposethattheevolutionofCcyclingtraitsinresponsetoclimatechangeexhibitsimportant
*Correspondence:
ecoevolutionaryfeedbackdynamicsthatprovideausefulframeworktostudyglobalCcycling
[email protected]
and storage. (J.G.Monroe).

TrendsinEcology&Evolution,March2018,Vol.33,No.3 https://doi.org/10.1016/j.tree.2017.12.006 213

©2017ElsevierLtd.Allrightsreserved.
The Organism-Mediated C Cycle

The C cycle on Earth is dominated by organism-mediated processes [10–12] (Figure 1).

PhotosynthesisandrespirationarethelargestfluxesintheglobalCcycle[2,13],withphoto-

synthesismoving20timesmoreCthanallanthropogenicsourcescombined(Figure2D).Ifall

otherfluxeswereheldconstant,anincreaseordecreaseinglobalphotosynthesisbyjust2%

would eithercompletelyoffset ordoublethecurrentrate ofincreasingatmosphericCO [2].
2

Therefore,theglobalCcyclewouldbesignificantlyaffectedbychangesinphotosynthesisand/

or respiration, which are influenced by traits such as C use efficiency [14,15], C fixation

efficiency[16], growthrate [17],nutrient stoichiometry[18,19], andmetabolism [20].

TheconcentrationofatmosphericCO isthenetresultofsimultaneousCcyclingprocesses.If
2

photosynthesisandrespirationevolvecommensurately,thecumulativeeffectonatmospheric

CO couldbezero,butifphotosynthesisandrespirationevolveatdifferentrates,theeffects
2

could be substantial. Recently, these evolutionary rates were quantified experimentally in

Chlamydomonasreinhardtii,amemberofthegroupofaquaticautotrophicorganismsrespon-

sibleforalmosthalfofglobalphotosynthesis(i.e.,phytoplankton)[21,22].Duringadecade-long

outdoormesocosmexperimentunderincreasedtemperatures,C.reinhardtiievolveda3.5-fold

Atmospheric CO
2
C fixa(cid:415)on Stoichiometry of
efficiency nutrient demand
Autotrophic Heterotrophic
organisms organisms
Short-term
storage
Long-term
storage
Root system Decomposi(cid:415)on
architecture enzymes
Fluxes mediated by...
Example
Photosynthe(cid:415)c traits C storage traits C
C cycling
Consump(cid:415)on and pool
Respira(cid:415)on traits trait
decomposi(cid:415)on traits
Figure1.Trait-MediatedProcessesintheCarbon(C)Cycle.Organismsareresponsibleforthelargestfluxes
(arrows )of Cbetweenbiotic andabioticp ool s(bo xes)inthe glo balCcy cle[2].Thes eflu xesaretrait me diate dandc anbe
influence d by photosy nthes is,re spiratio n,C storage o rco nsump ti on,an dd ecom positio ntr aits (arrows). Trait -bas ed
ecosystem pe rspectiveshaver evealedthe int egralrela tio nshipbetween spec ificorganismtra its(cir cles)and thefluxesof

C.BystudyinghowtheseCcyclingtraitswillevolveinresponsetoclimatechange,wecanconsiderhowadaptationmight

affectCcyclingandfutureatmosphericCO concentrations.ImagesreproducedcourtesyofNOAAandUSDA.
2
214 TrendsinEcology&Evolution,March2018,Vol.33,No.3
(A) (B)
Ambient Warmed
)
1
−
r
h
1
−
ell –5
c
2
O
ol
m
μ –6
(
)
s
si
e
h
t
n
y
s –7
o
t
o
h
p
t
e
n
n( 16 34
I Assay temperature (°C)
(C) (D)
200
)
1
–
r
y150
C
g
P
(
x 100
u
fl
C
al 50
u
n
n
A
0
>01.02O.0c3e.a0n5: c. h1lor.o2p.h3yll. 5a co1n cen2t ra3(cid:2) o5n (m10g/1m5230)3050 MaxLimaunmd: normalized difference land vegeta(cid:2)on inMdineixmum AnthropogseoPnuihrcocteossynthesis
Figure2.ContributionofPhotosynthesistoGlobalCCycleandPotentialforEvolution.(A)Algaeandotherphytoplanktoncontributetoapproximately40%

ofglobalphotosynthesis[21]andprovideusefulmodelsforstudyingexperimentallytheevolutionofcarbon(C)cyclingtraitsinresponsetoclimatechange-related

selectionpressures.(B)Adecade-longmesocosmexperimentfoundthat,underincreasedtemperatures,populationsofthealgaeChlamydomonasreinhardtiievolved

3.5-foldgreaternetphotosynthesiscomparedwithpopulationsevolvedunderambienttemperatures(datafrom[22]).(C)Abundancesofaquaticandterrestrial
photosy nthetico rga nismsasobser vedfroms pace .(D)Photosy nthesis isthe largestfl uxintheglob alCc ycle, movin gm orethan20 tim esthe Cre leasedby
anthropogenic sources(da taf rom[2,21 ]).The potent ialim pactofevenm ino rch angesi nph oto syn thesiso ro thero rganism -media tedC cy clingfl uxes is substant ial.

Earth system models that parameterize genotypic differentiation in C cycling traits could improve predictions of changing atmospheric CO2 concentrations.
ReproducedcourtesyofNOAA(A)andNASA(C).

TrendsinEcology&Evolution,March2018,Vol.33,No.3 215
Anthropogenic CO Figure3.AnEcoevolutionaryFeed-
2
backLoopPerpetuatedbytheEvo-

lutionofCarbon(C)CyclingTraitsin
ology ATM. Cli Rmeatsepoc hnas neg etoc aCus liemda btey aCnhtharn ogpoeg. eCn liic-
em ec cyclin g [CO2] Climat mate s CanbaOtiou2tri aicnl cesrneevaleisrcoet nsio mnheaensxt spc eh araniend ng,c etedhd ubsbi,o ytaiclmt eaarnenddy
Ecosyst Carbo n e change cience ctosrhyragciiftatlsiinnnggims mttirghashei tt sae.ti vn Eoavl tuoug tlruilonotnibolaaenrla yods ftc rtaathojleeesc,c et hpo Caorine tce gsyne cotsilafin liClgny

C acrybctlroiannitgs Enviroonnments twnatiivotaomentuu ofelredasxe pla dimhcsbeeeparrleaibccccak ttCsti eo Ocwsnli 2itmlhpl caeraoertciesnsus cercue rwherneanhtsrntea.tg ntrTiee oth nrnaaudsnist,t ,doe w pwvahooalitlcsuredih--r
Evolu(cid:415)on - s elec(cid:415) icnecnre traastieodn sa,twmhoes rpehaes rnice g(AaTtiMv e) fCeeO d2baccokns-

wouldoccurwhentraitevolutionleadsto
Evolu(cid:415)onary bi ol o gy ienccoreeavo seludti oCn asrtyo radgy en.a mU nicdse rosft aCn d icnygc lti nhge
will require the integration of climate

science, evolutionary biology, and eco-

systemecology.

increase in net photosynthesis, the difference between photosynthesis and respiration

(Figure2)[22].Theresultsofthisexperimentsuggestthatautotrophictraitevolutionresulting

from adaptation to warming climates can increase photosynthesis relative to respiration,

potentiallyleadingtoareductionintherateofincreaseofatmosphericCO towardanegative
2

feedback (Figure 3).

In addition to directly moving C to and from the atmosphere, organism traits affect the

accumulation of C in short (months–decades) and long-term (decades–millennia) storage.

Soilsholdapproximatelytwo–threetimesmoreCthantheatmosphere,andCstocksinmany

soilsarethoughttobeunsaturated[2,23].Plantroottraits,suchasdepth,alsoinfluencethe

depositionofCindeepsoils[23–25]anditwasrecentlyestimatedthata1-mincreaseinplant

rootdepthacrossjust3.9%ofarablelandwouldcompletelyoffsetallCO producedbyannual
2

fossil fuel emissions [24], indicating the potential for the evolution of root traits to impact

atmospheric CO .
2

Similarly,depositionofbiomasstothedeepoceancanresultinlong-termCstorage.Arecent

surveyofCfluxestosubsurfaceoceanlayersobservedanaveragefluxof47.6mgparticulate
organic (P O C) and in organic(PI C) Cm (cid:1)2 d(cid:1) 1 [26]. If ro ug hly extra pola te d acr oss theocean
surface areao nEa rth((cid:3)360 millio nk m2)thisratee q ualsapp roximately6. 3Pgy(cid:1) 1,w hichis
compar able to a nnual fossil fuel em ission s (7 .8Pg y(cid:1)1) [2 ]. Traits impac ting fec al m aterial in

zooplankton andthe mineralcompositionof phytoplanktonmodify theflux of Ctothe deep

ocean [26–28]. Several studies have reported the evolution of traits (e.g., 26% increase in

calcificationrate[29]and30%increaseinPIC:POC[30])thatcouldincreasethefluxofbiomass

todeepoceansinphytoplanktonadaptedtoincreasedtemperatureoracidification[29–31].

Suchashiftcouldincreasedeep-seaCstorage.OtherexamplesofCcyclingtraitsaffectingthe

storageofCincludethoseinfluencingtheflammabilityoflandplants[32],andthetemperature

sensitivityofmicrobialdecompositionenzymes[33].Thesetraitscontributetothestorageor

releaseofCfrombioticandabioticstoragepools,andfurtherinvestigationofthedirectionof

their evolutionwill bevaluable towardpredictingpotential effects onthe globalCcycle.

216 TrendsinEcology&Evolution,March2018,Vol.33,No.3
ThereislittledoubtthattraitevolutionhasimpactedtheglobalCcyclethroughoutthehistoryof

Earth[34].Theevolutionofphotosynthetictraitslikelydrovehistoricfluctuationsinatmospheric

CO [35–37];theevolutionofcellulose-decomposingenzymesinfungiincreasedthefluxfrom
2

major terrestrial C pools to the atmosphere [38,39]; and the evolution of angiosperms and

deep-rooted trees has been linked to historic 10–20-fold reductions in atmospheric CO
2

[40,41]. Thus, it is critical to recognize that changes in atmospheric CO on Earth are not
2

simplytheproductofgeologicalorotherabioticprocesses,butrathercanbelargelydrivenby

globalevolutionary trends.To understandthe effectof evolutionon Ccycling inthe Anthro-

pocene,itisimportanttoconsiderthisphenomenoninthecontextofglobalselectionpressures

resulting fromclimatechange.

Natural Selection during the Anthropocene

IncreasingatmosphericCO ischangingenvironmentsandselectionpressuresglobally[2,4].In
2

additiontothedirecteffectsofincreasedCO ,organismsarefacedwithoceanacidification
2

[42], increased temperatures [43], precipitation changes [44,45], and shifts in ecological

communities. Although there are notable challenges in conclusively showing that natural

populations adaptively evolve in response to climate change [46], recent studies provide

experimental evidence for the evolution of C cycling traits in response to such selection.

For example, traits experiencing selection under increasing CO (atmospheric or oceanic)
2

includeCfixationratesinphytoplankton[47],nitrogenfixationandgrowthratesincyanobac-

teria[48,49],andstomatalconductanceinplants[50].Adaptationtochangesintemperature

has also been shown for microbial heterotrophs [51]. The evidence for evolution under

experimentally manipulated conditions is compelling, but not sufficient to conclude that

adaptation ofCcycling traitswill be realizedundernatural conditions[46].

Evidenceoflocaladaptationtoclimateregimens,suchastemperatureinlandplants[52–54],

phytoplankton[55],heterotrophicmicrobes[56],andotherconsumers[57],providesadditional

evidencethatglobalclimatechangewillalternaturalselection.Additionally,drought-induced

selectionasaresultofclimatechangemightaffecttheevolutionofplantroottraits,whichare

important to C storage in soils [23]. For example, altered drought regimes might select for

genotypeswithgreaterallocationtorootbiomassforincreasedwateracquisitionormayselect

for genotypes exhibiting a drought escape strategy wherein plants reproduce quickly and

produceless belowgroundbiomass.

Predicting the direction of selection for C cycling traits is complicated by the interaction

between environmental drivers of selection. Although the effect of CO , temperature, and
2

precipitationonorganismsisoftennonadditive[58],itisdifficulttosimultaneouslymanipulate

multipledrivers.However,thisisimportant,givenrecentevidencethatselectioninC.reinhardtii

populationscanbestrongerwhenrespondingtomultipledriversthanwhendriversareisolated

[59].
Genetic Variation of C Cycling Traits

Adaptive evolution of C cycling traits requires standing genetic variation on which selection

pressures can act [60]. This variation can be in the form of mean differences between

genotypes or heritable variation in plastic responses to environmental conditions [61]. For

example,themodelgrassBrachypodiumdistachyonexhibitssignificantheritablevariationinC

cyclingtraits,includingrootbiomass(0.20<H2<0.36),aswellasgeneticvariationinplastic

responses (genotype(cid:4)environment interaction) to drought in the nutrient stoichiometry of

leaves[62].Indeed,thereappearstobeheritablevariationacrossmanyplantspeciesintraits

suchasrootstructureandleaflability[63,64].Areviewofleaflabilitytraitsindicatesthatthey

TrendsinEcology&Evolution,March2018,Vol.33,No.3 217
tendtoexhibitsignificantestimatesofheritability(h2ashighas0.9),although,insomecases,

heritabilityforCcyclingtraitshasnotbeendetected(reportedmedianh2estimatesrangefrom

0.1to0.3)[65].Laboratorystudiesalsohaverevealedthat,forCcyclingtraitssuchasgrowth

rate,phytoplanktonpopulationsgenerallyhavehighgeneticandclonaldiversity[66],andthere

are significant strain-specific responses to elevated CO and temperature [67–70]. This
2

indicates there issignificant genetic variationin natural plant and phytoplankton populations

and,thus,thecapacitytorespondtoselectionofCcyclingtraitsinresponsetoclimatechange.

We know relatively less about the genetic variation of C cycling traits in nonprimary

producers. For example, heritable variation in microbial C cycling traits is rarely measured,

because most studies report interspecific rather than intraspecific variation [71]. However,

recent reports confirm the presence of genetic variation among soil microbes in the

temperature sensitivity and activity of decomposition enzymes [33,72]. Heritable variation

in such C cycling traits might be common, but quantification of this variation via traditional

quantitativegenetics,genomicprediction,orcomparisonofmicrobialisolatesisstilllacking

(Box 1). Quantifying this variation and avoiding publication bias to report positive results is

important for predicting the capacity for organisms to respond to selection. Additionally,

describing genetic correlations between C cycling and other traits can provide insight into

constraints on adaptive evolution [73].

Evolution on Ecological Timescales

There is growing appreciation for the prevalence of rapid evolution occurring on timescales

comparablewithecologicalprocesses(e.g.,[74]).However,organism-environmentfeedbacks

with atmospheric CO are often studied with respect to plastic (i.e., physiological) and
2

ecological(i.e.,speciescomposition)responsestoclimatechange(e.g.,[75]).Althoughthese

arecertainlyimportantdriversofongoingCcyclingdynamics,theywilloccurintandemwith

contemporary and now apparent rapid evolution of populations. Adaptation to increased

temperature in the keystone species zooplankton Daphnia magna occurred in as little as 2
years,resulti ng ina nincrease intherm altolerance of3.5(cid:5)C [76]and theevolu tio no fmet abo -

lism-relatedgenes[77].Similarrapidadaptationtoincreasedtemperatureinvolvingmetabolic

genesortraitshasbeendocumentedinthephytoplanktonChlorellavulgarisinaslittleas100

generations [78]. Adaptation to drought has also been observed in less than a decade in a

populationoftheannualplantBrassicarapa[79].Inresponsetoseveralyearsoflate-season

droughts,thesepopulationsevolvedearlierfloweringtime(upto8daysearlier)[79],whichis

geneticallycorrelatedwithlowerrootbiomassinthecloserelativeBrassicanapus[80].Such

rapidevolutionaryshiftsinannualplantspeciescouldresultinlowersoilCstorageinenviron-

mentspredictedtoexperiencemore-frequentsummerdroughtsasaresultofclimatechange,

contributing topositivefeedback interactions withatmospheric CO .
2

These examples illustrate the potential for evolution at speeds comparable to plastic and

ecological responses to climate change. Interestingly, adaptive evolution can occur in the

opposite direction of plastic responses [81]. For example, under ocean acidification, phyto-

plankton often decrease rates of photosynthesis plastically, but evolution across multiple

generations leads to phenotypic shifts in the opposite direction to increase photosynthetic

ratesand,potentially,thelikelihoodofCsequestrationfromtheatmosphere[66].Accordingly,

predictionsoffuturetraitvaluesshouldnotbebasedonplasticresponsesalone.However,not

all seemingly strong selection pressures will engender rapid evolutionary responses. For

example, Arabidopsisthalianaplantpopulations grownunderelevatedCO inafieldsetting
2

showedincreasedgrowthandfruitproductionbutnoevolutionaryeffect,suggestingaplastic

rather thanevolutionaryresponse [82].

218 TrendsinEcology&Evolution,March2018,Vol.33,No.3
Box1.ProgressandFutureObjectives

RecentresearchhasledtosignificantprogressinunderstandingthepotentialforecoevolutionaryfeedbacksinvolvingC

cycling.Here,weoutlinetheimportantcriteriathatmakesuchfeedbackspossible.Foreach,wehighlightastatement

thathasreceivedemergingempiricalsupport(bolded)andachallengewherefutureresearchisneeded.

OrganismTraitsMediateCFluxes

Challenge:itiscriticalthattherelationshipsbetweenspecifictraits,ecosystemCfluxes,andultimatelyatmosphericCO
2
bedescribedquantitatively.

ClimateChangeWillImpactSelectionPressures

Challenge: more research is needed to predict how different components of climate change (e.g., drought and

temperature)willinteracttoalterevolutionarytrajectoriesofCcyclingtraits.

OrganismsHarborSignificantGeneticVariationforCCyclingTraits

Challenge:geneticvariationinCcyclingtraitshasnotbeenexplicitlyquantifiedinmanyorganisms,leavingagapinour

abilitytopredictevolutionaryresponses.

EvolutionCanOccuratRapidTimescales

Challenge:morestudiesareneededtounderstandthelimitsofthisevolution(e.g.,inorganismswithlonggeneration

timesorsmallpopulations).Studiesthatgobeyonddemonstratingthatrapidevolutioncanoccurtowarddetermining

whetherrapidevolutionmostoftendoesoccurwillstrengthenourabilitytoconsiderecoevolutionaryfeedbacksinthe

AnthropoceneglobalCcycle.

OngoingEnvironmentalChangesCanLeadtoRapidEvolutionofCCyclingTraits

Challenge:moreresearchisneededtodrawgeneralizableconclusionsaboutthedirectionofthisevolutionacross

speciesandenvironments,andhowevolutionwithinnativepopulationsandcommunitiescanscaletoimpactson
ecosyst em-le velcarboncyc ling. Dispa rateevide ncesu ggests thatthefirst four criteriadescri bed above ex istinnatu re,

yetstudiesthatintegratethesecomponentsarerare.Additionally,determiningthesignandmagnitudeofevolutionon

globalCcyclingandatmosphericCO remainpressingresearchobjectivesattheintersectionofevolutionarybiology
2
andecosystemscience.

Direction of Selection on C Cycling Traits

TheevolutionofCcyclingtraitscouldincrease,decrease,orstabilizeatmosphericCO con-
2

centrations, depending on the direction of natural selection on C cycling traits. Assessing

experimental evolution in microcosms and mesocosms provides one approach to study the

directionofthisevolution.Byallowingpopulationstoadapttoenvironmentssimulatingfuture

conditions, the response to selection in C cycling traits can be measured empirically. This

approach has proven especially insightful for studying the evolution of phytoplankton. These

experimentshaveobservedevolutionaryresponsestoincreasedCO (andassociatedocean
2

acidification)[17,31,47–49,66,83,84],temperature[22,78],orcombinationsthereof[29,30]and

haveprovidedvaluableinformationtowardresolvingthedirectionofselectiononCcyclingtraits.

C. reinhardtii adapted to a decade of elevated temperature in outdoor mesocosms evolved

increasednetphotosynthesis(Figure2B)[22]and,inaseparateexperiment,C.vulgarisdown-

regulated respirationrelativetophotosynthesis[78]. Additionally,populationsofthecalcifying

phytoplanktonEmilianiahuxleyiadaptedtoelevatedtemperature,exhibitingshiftsinballasting

traits,suchasPIC:POC,indirectionspredictedtoincreasesinkingspeedand,thus,thefluxofCto

deepoceans[30].Suchstudiessuggestthatselectioncausedbyincreasedtemperatureactsin

directionsthatincreasethenetfluxofCfromtheatmospheretobioticandabioticstoragepools

andproduceanegativefeedbackloopwithatmosphericCO .
2

TrendsinEcology&Evolution,March2018,Vol.33,No.3 219
However,studiesexaminingphytoplanktonevolutioninresponsetoacidificationhighlightthat

further work is needed to draw generalizable conclusions about the direction of selection

causedbyoceanacidification.Forexample,underexperimentallyincreasedCO andacidifi-
2

cation,GephyrocapsaoceanicaevolvedhigherphotosyntheticCfixationandgrowthrates[47],

whereasPhaeodactylumtricornutumevolvedreducedphotosynthesis,respiration,andgrowth

rates[84].Towhatextentsuchdiscrepanciesarecausedbydifferencesbetweentheevolu-

tionaryresponsesofspeciesorexperimentalconditionsremainunclear.Asaresult,avaluable

directionforfutureresearchwouldbetocomparetheevolutionarytrajectoriesofCcyclingtraits

inmultiplespecies(includingheterotrophs,suchasDaphnia),ideallyinfactorialdesignswith

multipleselectionpressures.

Studyingevolutionunderecologicallyrealisticconditionsisalsoimportant.Forexample,recent

(<50years)woodyencroachmentintograsslandshasalteredcommunitycompositionandC

balances within these systems [85]. Such shifts in community composition can influence

evolution by altering interactions within and across trophic levels (Figure 1). Yet, because

mesocosm approaches will not capture the more-complex influences of community-level

change,manipulativeandobservationalstudiestoassessclimate-changedrivenevolutionary

dynamicsinrealcommunities willbe valuable.

ThereareseveralalternativestomesocosmexperimentstostudythedirectionofevolutionofC

cycling traits in natural populations. The strength of selection on C cycling traits could be

measuredwithaquantitativegeneticapproachinapedigreedpopulationgrowninacommon

environmentreflectingfutureconditions[86]. Long-termmonitoringofpopulationsinexperi-

mentally modified native habitats can also be useful. For example, a 10-year precipitation

manipulation experiment within native grassland communities found that increased intra-

annualprecipitationvariabilityselectedforgenotypesofadominantgrasswithgreaterrelative

allocationtorootbiomass[87].AlthoughsuchatraitshiftmightleadtomorebelowgroundC

storage, selection on this population was variable. As a consequence, how population evo-

lution in this particular case ultimately scaled to ecosystem-level C cycling and atmospheric

feedbacks isuncertain.

Naturally occurring CO , pH, temperature, or precipitation clines are natural ecological
2

experimentsthatsubstitutespacefortime,representingachronosequenceofenvironmen-

talchange.Geneticdifferentiationalongtheseclinescanbestudiedtoinferthedirectionof

selectioninresponsetoclimatechange.Populationsadaptedtoterrestrial[88]andaquatic

CO -emitting vents [89] have evolved in environments with higher ambient CO and/or
2 2

lower pH. A recent study of Plantago lanceolata plants adapted to such elevated CO
2

habitats found genetic evidence of an evolved increase in photosynthetic capacity and

respiration rate, although the effect on net photosynthesis is unresolved [88]. Similarly, the

direction of selection on C cycling traits in response to increased temperature and aridity

can be inferred from populations diverged along natural temperature and precipitation

clines.Populationsofakeystonesnailherbivore,Radixbalthica,adaptedtowarmersprings

have evolved higher metabolic, respiration, and consumption rates (Schaum et al. 2017,

unpublisheddata).Thisisconsistentwiththeoreticalpredictionsthatincreasedtemperature

leads to shifts in the stoichiometry of the nutrient needs (increased C:nitrogen ratio),

increasedmetabolicdemand,andhigherrespirationratesofconsumers[19].Theseresults

indicate the potential for heterotrophic evolution in response to increasing temperatures to

perpetuateapositivefeedbackonatmosphericCO .Indeed,anexcitingdirectionforfuture
2

workwillbetoassesswhether such evolutionwillcounternegativefeedbacks occurringat

lower trophic levels.

220 TrendsinEcology&Evolution,March2018,Vol.33,No.3
It is also possible to measure the recent direction of evolution in C cycling traits in situ. Outstanding Questions

‘Resurrection’ studies use seed banks or other sources of dormant organisms to measure How can we best quantify relation-
recentevolutio ninplan ts[9 0],zo oplank ton [76],a ndmicro be s[91].Re surrections tu dieshave ships betw een traitv aluesand Cfluxes

to promote inclusion of traits as
providedconvincingevidencethatrapidevolutioncanoccuracrossdifferentorganisms[92]
parameters in Earth system models
and present a promising opportunity to reconstruct the direction of recent C cycling trait ofglobalC cyc ling?

evolution.Past,ongoing,andfutureevolutionofCcyclingtraitscouldalsobestudiedusing

genomicsequencedatatopredictCcyclingphenotypesinpreservedspecimens[93]orrecent Howwilldifferentcomponentsofcli-
collection s ofnatur al po pu lations [9 4]. mate cha nge(e.g .,droughtand te m-

perature)interacttoalterevolutionary

trajectoriesofCcyclingtraits?
Evolution of C Cycling Traits as an Ecoevolutionary Feedback

TheideathatorganismsaltertheirselectiveenvironmentoriginatedwithDarwin[95]andcanbe Whatarethelimits(geneticvariation,

conceptualizedundertheframeworkofecoevolutionarydynamics[96].Ecoevolutionaryfeed- population size, and trade-offs
backs occur w hen tra it e volution m od ifies environmen tal conditi ons i n response to n atural between tr aits) of the rap id evolution
ofCcyclingtraitsanddotheselimits
selection.Thisenvironmentalmodificationthenfeedsbacktoinfluencethetrajectoryoffuture
selectionp ress uresand,thus ,evolutionary chan ge.Fo rexa mp le,aposi tive feedback pre ssure vary across taxa?

wouldariseifevolutionarychangeresultsinaneven-greaterrateofatmosphericCO2increase. Aretheresultsofrecentempiricalwork

Bycontrast,negativefeedbackpressureresultsfromevolutionarychangethatreducestherate assessing the direction of C cycling
trait evolu tion represen tat ive across
of atmospheric CO2 increase. Here, we have discussed why organisms are expected to diffe rentspecie sandenvironm ents?
experience strong natural selection as a result of climate change. We have also seen the

potential forthis selectiontoleadtotheevolutionof Ccycling traits.Yet,todate, fewifany
What is the expected direction and
studiesh ave inte gratedth ese crite ria into acompl ete e coevolu tionary feed ba ckcy cle. G iven magn itud e o f the effec t of C cy cling

the primary fluxes that interact with atmospheric CO2 are those mediated by organisms [2], trait evolution on atmospheric CO2?
evolutionary changes in C cycling traits are expected to influence the balance between
Howcanweapplyourknowledgeof
atmospheric C and other pools in the C cycle. Thus, the evolution of C cycling traits might
theevolutionofCcyclingtraitstoman-
either accelerate or decelerate the current trend toward increasing atmospheric CO and
2 agementpracticesaimedatpreparing

climate change, altering the trajectory of future selection regimes and contributing to an for,ormitigating,climatechange?

ecoevolutionaryfeedbackloop.Therefore,themodelofecoevolutionaryfeedbackdynamics

provides a useful framework to conceptualize the components underlying the evolutionary How can we create opportunities at

theinstitutionallevelthatfacilitatethe
dynamics of global C cycling (Figure 3). Integrating all of the steps of such feedbacks to
collaborationnecessarytobestunder-
characterizethecontemporaryecoevolutionarydynamicsofCcyclingwillrequireanunprec- standecoevo lutionaryfe ed back sofC

edentedyetachievablesynthesisamongmultipledisciplinesandacrossmultipletaxa(Box2). cycling?

Concluding Remarks Howcantheecoevolutionarydynam-

icsofCcyclingbeextendedtounder-
Here, we have discussed recent evidence for the components of ecoevolutionary dynamics
standecoevolutionarydynamicsmore
involvingCcyclingtraits(Box1,Figure3).Therearealsoagrowingnumberofstudiesthathave broad ly?

begun to integrate these components. For example, recent work generally suggests that C

cycling traits in phytoplankton will evolve in response to elevated temperatures in directions

predicted to have a stabilizing effect on atmospheric CO , contributing toward negative
2

feedbackdynamics.Bycontrast,theoryandrecentempiricalworkindicatesthatmetabolism

and nutrient stoichiometry in heterotrophs will evolve in directions that establish positive

feedbackdynamicswithatmosphericCO .Suchcomplexitiesspeaktotheneedforgreater
2

understandingofthepotentialtradeoffsamongdifferentorganismsandtraits(aswellasacross

ecosystems and communities) as they evolve in response to climate change. Improved

prediction of the evolutionary trajectories of C cycling traits within individual ecosystems is

neededbecausetheneteffectofevolutionataglobalscalewillbeimpactedbybothpositive

and negativefeedback pressures.

AcriticalquestioniswhetherthemagnitudeofevolutionarychangesinCcyclingtraitswillbe

largeenoughtosignificantlyaffectatmosphericCO concentrations.Itisimportanttoconsider
2

thatevolutionhasdemonstratedthecapacitytoaffectglobalCcyclingthroughoutthehistoryof

TrendsinEcology&Evolution,March2018,Vol.33,No.3 221
Box2.ToolstowardaSynthesis

UnderstandingtheecoevolutionarydynamicsofCcyclingwillrequiretheintegrationofevolutionarybiology,ecosystem

ecology,andclimatescience(seeFigure3inthemaintext).Fortunately,eachofthesedisciplinesislargelyprepared

withthetoolsneededtoachievesuchasynthesis.

EvolutionaryBiology

Evolutionarybiologyisequippedwiththetoolstoquantifythecapacityforevolutionarychangeanddirectionofselection

onCcyclingtraits.Quantitativegeneticsdeliversarobuststatisticalframeworktoaccomplishthis,whereinmeasuresof
gen e tic varia tion (i. e., Va, and h2 ) and the strengt h (S) and response (R) to selec tio n on C cyclin g tra its can b e estimate d
[90].EvolutionaryresponsesofCcyclingtraitscanalsobedirectlyobservedthroughexperimentsorbycomparisonof

populationsdivergedthroughtimeoralongchronosequences.Tools,suchaslandscapegenomicsandgenomic

prediction[98]ofCcyclingtraits,mightalsoproveusefulinpredictingevolutionaryresponsesofCcyclingtraits[99].

Estimatingthedirectionandmagnitudeofrapidevolutionaryresponsesinthesetraitsandconsequencesforecosystem

processesremainsanimportantchallengetoparameterizeCcyclingmodels.

EcosystemEcology

Ecosystemecologyprovidesmodelsthatdescribetherelationshipsbetweenorganismsandenvironmentsthrough
processes suchas thecyclin gofnut rients between po olsandfluxes ,andis well-suited fortr ait-basedapp roaches.

KeypredictionsofCcyclingmodelsincludeprocessessuchasnetecosystemproductivity(NEP),whichisfundamentally
defin edasthed iffe re ncebet weento talphot osynthesis (GPP )an de cosystemre spiration(ER )[99], twopr oc essesthatare

drivenbyasuiteoftraits.Progressintrait-basedecosystemecologyhasledtolarge-scalecommunityandecosystem
model so ft heC cyc letha tincludem o re-specific, typicallysta tic,traitv alue s.Y et ,astrait-bas edapproac hes continueto

develop,movementawayfromstatictraitvaluestothosethatcanchangeasaresultofevolutionaryprocessescanadd

realism,andevenconstrainmodelpredictionswithmore-realistictraitvalues.Additionalcommunityandecosystemmodels

includingexperimentallyderivedexpectedtraitvalueshiftscouldhelpinformlarge-scaleEarthsystemmodels,allowing

better tracking of the magnitude and direction of C ecoevolutionary feedback loops on atmospheric CO2.
ClimateScience

Climatescience,whilenotthefocusofthispaper,hasseenconsiderableadvancesinrecentyearsinourabilitytomodel

howenvironmentalconditionswillchangeasafunctionofatmosphericCO.Thesemodelshavemovedwellbeyond
2
predictedincreasesinmeantemperatures,andareabletomodelchangesinclimaticvariabilityandextremeevents(e.

g.,[44]),providingimprovedaccuracyandimportantdimensionsintermsofwhichfutureselectiveenvironmentscanbe

characterized.
Earthandthatclimatechangeisalteringselectiononorganismsglobally.Itisalsoclearthat

evensmallchangestotheglobalCcyclecanhavelargeimpacts,giventhatanthropogenicCO
2

sources (burning fossil fuels, land-use change, etc.) account for less than 1.5% of global C

fluxes, yet are driving major environmental changes across the planet [2]. It is too early to

conclude that evolution will dramatically alter contemporary atmospheric CO but there is
2

mounting evidencethatthe potentialexists.

Identifyingthefeedbackpotentialofdifferenttaxawillbeusefulformanagement.Theevolution

oftraitsthatincreaseCstoragerepresentsaparticularlyvaluable‘evosystemservice’[8]and

organisms predicted to do so may be prioritized for conservation and agricultural use. For

example,C.reinhardtiishowsevidenceofevolvinggreaternetphotosynthesisinresponseto

increasedtemperature(Figure2)andlakesitinhabitsmightbetargetedforprotection.Whilethe

C storage potential of organisms will never be the only factor influencing management,

understandingtherolesoforganismsintheecoevolutionarydynamicsofCcyclingcouldlead

to more-purposefuland informeddecision-making.

Studying the evolution of C cycling traits also presents a meaningful research objective at a

more-fundamental level, because it addresses a universal challenge in biology and ecology:

222 TrendsinEcology&Evolution,March2018,Vol.33,No.3