Differing Selection on Plant Physiological Traits in Response to Environmental Water
Availability: A Test of Adaptive Hypotheses
Author(s): Susan A. Dudley
Source: Evolution, Vol. 50, No. 1 (Feb., 1996), pp. 92-102
Published by: Society for the Study of Evolution
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Evolution, 50(1), 1996, pp. 92-102
DIFFERING SELECTION ON PLANT PHYSIOLOGICAL TRAITS IN RESPONSE TO
ENVIRONMENTAL WATER AVAILABILITY: A TEST OF ADAPTIVE HYPOTHESES
SUSAN
A.
DUDLEY1
Departmentof Ecology and Evolution,University
of Chicago, Chicago, Illinois 60637
Abstract.-I used phenotypic selection analysis to test the predictionfromfunctionaland comparative studies of plants
that smaller leaves and more efficientwater use are adaptive in drier environments.I measured selection gradients
on leaf size and instantaneous water-use efficiency(a measure of carbon gain per unit water loss) in experimental
in thefield.Linearand nonlinear
populationsof Cakile edentulavar.lacustrisplaced intowet and dryenvironments
as predicted.Water-useefficiency
was selectedto be
selectiondifferedsignificantly
betweenthe two environments
There was also
higher,and leaf area was selectedtowarda small intermediate
optimum,in the dryenvironment.
selectionon water-useefficiency
and leaf size, suggesting
thattheoptimumleaf size
significant
positivecorrelational
in thedryenvironment
is greaterforplantswithhigherwater-useefficiency.
In contrast,
neitherleaf size norwateruse efficiency
wereselectedin thewetenvironment,
thoughlargerleaves resultedin greatervegetativebiomass.Path
analysisof the linearselectiongradientsfoundthatwater-useefficiency
affectedplantfitnessprimarily
because it
increasedvegetativebiomass,as suggestedby thehypotheses
aboutthefunction
of physiologicaltraits.These results
in waterwerenotonlyconsistentwiththefunctional
hypothesesbut also withtheobservedgeneticdifferentiation
use efficiency
and leaf size betweenwet and drysitepopulations.
selectionanalysis,pathanalysis,water-use
Keywords.-Adaptivephenotypic
plasticity,
Cakile,leafsize, multivariate
efficiency.
ReceivedAugust30, 1994. AcceptedApril25, 1995.
The evolutionary
responseto selectioncan be predicted
bythephenotypic
selectionin one generation
andthegenetic
variancesand covariances(Lande and Arnold 1983). Phenotypicselectionstudies,whichdescribetherelationship
betweentraitsand fitness,
can be used notonlyto predictthe
evolutionof the traitsstudiedbut also as an empiricaltest
To supportthehypothesis
of adaptivehypotheses.
thata trait
is adaptivein a givenenvironment,
demonstrating
thatthe
traitis correlated
withfitnessin thatenvironment
is notsufficient.The correlation
of traitand fitnessmustalso be lessened or absentin an environment
wherethetraitis notexpectedto be adaptive(Wade and Kalisz 1990). Manystudies
have demonstrated
strongnaturalselectionin thewild (Endler 1986), butfewstudieshave attempted
to testevolutionary predictionsand adaptivehypotheses.Here I describea
testof adaptivehypotheses
forplantphysiologicaltraitsthat
affectplantcarbonuptakeand waterloss. A large body of
functionalanalyses and comparativestudiesprovideshypotheseson how selectionon thesetraitsshoulddependon
environmental
wateravailability(i.e., Ehleringer1975; Givnish1986,Cowan 1986). In thispaper,I describea fieldstudy
in wetand
of selectionon leaf size and water-useefficiency
and comparethe resultswiththe predicdryenvironments
tionsof adaptivehypotheses.
In a companionpaper(Dudley
in these traits
1996), I measurethe geneticdifferentiation
betweenpopulationsfromwetand dryenvironments
as well
as the geneticcovariancematrixand comparetheseresults
withthefieldstudiesof selection.
The adaptivehypotheses
I examinein thispaperarebased
on thephysiologyof photosynthesis.
Whenplantsopentheir
stomates(poresin theleafepidermis)to allowcarbondioxide
to diffuseintotheleafforphotosynthesis,
waterdiffusesout
waterloss is potentiallycostlyfor
rapidly.Transpirational
away morewaterthantheplantcan acplants.Transpiring
quiremaycause droughtstress,whichcan compromisethe
abilityto growand to acquirecarbon,and in theextremity
is fatal (Givnish 1986; Schulze 1982). Thus, althoughincreasednet carbonacquisitiongives plantsmoreresources
(Ehto compete,grow,and reproducein all environments
leringer1975), theevolutionof traitsthataffectcarbonacin drierhabitatsbecausecarbon
quisitionmaybe constrained
gain is accomplishedat thecost of waterloss. One waythat
is by reducingwaterloss
plantsadaptto dryenvironments
(Givnish1986). Waterloss can be reducedbyhavingsmaller
leaf surface(Givnish1979)
leaves to reducethetranspiring
and thuslower
and in some cases to reduceleaftemperature
thewaterpotentialat theleafsurface(Nobel 1991). Another
potentialadaptationis to change the relativerates of gas
exchangeto maximizethecarbonassimilationto water-loss
efficiency
(Cohen 1970,Cowan
ratio,definedas thewater-use
1986).
These adaptivehypothesesare supportedby comparative
in populations
studiesshowinghigherwater-useefficiencies
and speciesfromdrierenvironments
(Gurevitchet al. 1986;
and Cooper1988). Studies
Kalisz and Teeri1986,Ehleringer
strumarium
selectionin Xanthium
grownin a
of phenotypic
cultivatedfield(Farrisand Lechowicz 1990), Prunellavulgaris grownin the greenhousein highand low lightenvironment(Winnand Evans 1991), and Plantago lanceolata
have foundsegrownin an old field(Tonsor,manuscript)
beThe relationship
lectionforhigherwater-useefficiency.
tweenbiomassand water-use
efficiency
(measuredas carbon
isotope ratio) has been exploredin both well-wateredand
in a commongardenstudyon the
environments
water-limited
desert shrub Chrysothamnusnauseosus (Donovan and Ehler-
testof the hypothesisthat
inger1994). However,a further
and smallerleaves are selected
higherwater-useefficiency
to droughtstressis to compare
1 Presentaddress:Department
of Biology,McMasterUniversity, because theyare adaptations
and
thestrength
of naturalselectionon water-useefficiency
1280 Main St. West,Hamilton,OntarioL8S 4K1, Canada.
92
? 1996 The Society forthe Study of Evolution. All rightsreserved.
SELECTION ON PLANT PHYSIOLOGICAL
TRAITS
93
Both siteshad onlysparsely
to thebeach,facingnorthwest.
distributed
annual vegetation,and consequentlyplantsrewateravailabilitywas
ceived full sunlight.Environmental
determined
by observation.The wet site containeda permanentseep of wateralongthebase of thedune.Waterwas
thesummer,
and
fromtheseep throughout
observedtrickling
plantsneartheseep grewin a slurryof sand and water.The
drysite lacked any watersourceotherthanthe lake itself.
in
exchange traits in Cakile edentula var. lacustris (Brassica- Naturalpopulationsof plantsalso indicateddifferences
ceae), a succulentC3 beach annualfoundon sandybeaches favorableness
betweensites,withverylargeplantsfoundat
alongtheGreatLakes oftheNorthAmerica(Rodman1974). thewet site and smallplantsat thedrysite,suggestingthat
This species is consideredto be subjectto edaphicdrought the plantsdo not reach the watertable. Nutrientmeasurebecause its beach sand substratedoes not retainwater,and mentsindicatedthatlevelsweresimilarand verylow forthe
Lake Michiganpopulationsof C. edentulavar.lacustrismay twosites.The twopopulationsfromcontrasting
habitatswere
populationused in this study
experienceseveraldays or weeks withoutrainfall.Popula- pooled into the experimental
variationand ensurethat
tionsof C. edentulavar.lacustrisaroundLake Michigangrow to increasetheexpectedphenotypic
populationwas notmoreadaptedto one of
in sites thatdiffergreatlyin wateravailabilitybecause of theexperimental
rainfall,
topography,
seeps,andothersourcesofgroundwater.theexperimental
environments.
To testtheadaptivehypothesessuggestedby thephysiolog- Because the breedingsystemis believedto be predomiwere genI measuredphenotypic
progenyforexperiments
selectionon instanta- nantlyself-pollinating,
ical literature,
neous water-useefficiency
and leaf size forplantsof known eratedby allowingplantsto self-fertilize.
Maternalsibships
in wa- fromthefield-collected
plantswereraisedin thegreenhouse
ancestryplaced intonaturalenvironments
contrasting
ter availability.These measurements
allow me to ask the and allowedto selfpollinate.One plantfromeach maternal
followingquestions:(1) Does selectionfavorgreaterwater- sibshipwas randomlyselectedto be the parentof the ex10 offspring
fromeach
in thedryenvironment
Approximately
generation.
use efficiency
thanin the wet envi- perimental
ronment?(2) Does selectionfavorsmallerleaf size in the of the 23 originalfamilieswere assignedto each of two
thanin thewet environment?
treatments:
wet and dry.
dryenvironment
leafsize in environments
thatdiffer
onlyin wateravailability
(WadeandKalisz 1990). Measuresofnaturalselectioncannot
provea causal relationship
betweentraitsand fitness(Mitchell-Oldsand Shaw 1987; Rausher1992),butfinding
thatthe
associationsbetweentraitsand fitnesschange as predicted
betweenenvironments
wouldprovidestrongsupportfortheir
hypothesized
adaptivevalue (Wade and Kalisz 1990).
Here I presenta studyof naturalselectionforleafand gas
MATERIALS AND METHODS
StudySpecies and Sites
Field Environments
tookadvantageof thenaturalpatchThe fieldexperiment
iness in wateravailabilityfoundat one site. At the Mount
genusnativetothesandybeachesoftheNorthAtlanticOcean Baldy site,a naturalseep has createda narrowstrip(from
wet sand
and adjoiningbodies of water.All membersof thegenusare 1-5 m in width)parallelto thebeach of extremely
Therewas abundantavailable
thewetenvironment.
succulentherbaceousannuals.Leaves of Cakilespecieshave providing
have waterduringthe entireseason near the seep. One transect
been reportedto rangefrom0.5-1.5 mmin thickness,
stomateson bothleafsurfaces,and haveundifferentiated
pa- was laid outalongthelengthof theseep for50 m. The slope
4 m above the seep providedthe dry envirenchyma(Rodman 1974). Physiological measurements approximately
made on greenhouse-grown
Cakile maritimafromnorthern ronment.The sand on the slope was well drained,and it
Californiaindicaterelativelyhighphotosynthetic
capacities receivedwateronlyfromrainfall.The wetanddrytreatments
and bothhad soil thatwas 99.9 % coarseand finesand,0.1% silt
withmaximumphotosynthetic
ratesof 37 pwM-m-2-s-'
In the
conductancesof 12 mm-s-1(De Jong1978). Cakileedentula and clay particles,and had similar,low soil nutrients.
twoparalleltransects(each of 25 m) were
var.lacustrisis an indeterminately
annualwithcon- dryenvironment,
flowering
2 m above the otherrunning
siderablevariationin flowering
schedule.Breedingsystems laid out, one approximately
In bothenvironof Cakile species rangefrompredominantly
self-pollinatingparallelto thebeach and theothertransect.
in
areas
fromperennials
away
transects
were
placed
ments,
topredominantly
Flowers
are
on
born
outcrossing.
elongating
terminalracemes.Fruitsconsistof two segments,theupper and shrubsgrowingon the seep such thattheexperimental
to only
Limitingtheexperiment
being deciduous and the lower remainingattachedto the plantsreceivedfullsunlight.
raceme.Each segmentcontainsusuallyone seed,withupper two siteswas necessarybecause of practicalconsiderations
oftheenvironmental
water
seeds beingslightlylargerthanlowerseeds. Cakileedentula butdidresulta lack ofreplication
However,althoughthe sites differed
var. lacustrisis nativeto the GreatLakes and is the only availabilitytreatment.
theyweresimilarin nutrient
memberof thegenusfoundon freshwater
beaches.It is re- markedlyin wateravailability,
gardedas a primarily
autogamoustaxon,withsmallflowers levels and in lightavailability.
Seeds of theexperimental
populationwereinducedto gerand highratesof spontaneousfruitset (Rodman1974).
and removingtheirseed
Seeds were collectedfromthe Indiana Dunes National minateby soakingthemovernight
Lakeshorefrom23 randomlychosen naturallypollinated coats. Seeds were plantedMay 7, 1990 into50:50 promix
plants,12 froma drysite (WestBeach), and 11 froma wet Turfacein plugtraysand lightlycoveredwithsoil mix.The
site(MountBaldy) approximately
a 26-kmdistancefromone plug trayswerekepton dryheat undernaturallightingfor
in 1 wk and thenin the greenhouseforthe 2-day week. All
another.These two populationsare further
characterized
within4-8 days. The seedlingswerethen
Dudley(1996). Bothsiteslay alongthebase ofdunesparallel seeds germinated
The study plant, C. edentula var. lacustris, belongs to a
94
SUSAN A. DUDLEY
transferred
to a cold frameto acclimate.Later,theywere
labeled withbird-bandtags and transplanted
to thefieldon
June12, 1990. At thattime,theyhad twoto six trueleaves.
The seedlingswereplantedin randomizedorderin thetransects every20 cm. Ratherthanplantinga straightline of
plants,theseedlingswerealternately
offseteither5 cmabove
or 5 cm belowthetransect
to presenta slightlymorenatural
appearance.
humidity
spans.The relativehumidity
of0 was verified
using
driedair and the PPM CO2 was verifiedby measuringair
passed through
soda limeto removeCO2. Leaf temperatures
in thechamberwas estimatedfromtheenergy-balance
equation (Parkinson1984; AnalyticalDevelopmentCompany
1992). Boundary-layer
resistancesforCakileleaves in a Parkinsonleaf chamberwere estimatedon filter-paper
mimics
(Parkinson1985; AnalyticalDevelopmentCompany1992).
Because boundary-layer
resistancewas correlatedwiththe
size of the "leaf," a regressionequationestimating
boundTraits
ary-layerresistanceas a functionof leaf size was used in
Leaf size and gas-exchangerates were measuredin late subsequentcalculations.
summeron survivingplants,whichwereproducingflowers Photosynthetic
ratesand stomatalconductanceswerecaland fruits.For each plant,one recentlyproducedfullyex- culatedaccordingto von Caemmererand Farquhar(1981).
panded leaf was sampled,and measuresmade of net pho- Measuresof gas exchangewerecovariatecorrectedfordate
tosynthetic
rate (assimilationof CO2 in FM C02-m-2s-1), and time (Winn and Evans 1991; Harris 1975; Farrisand
therateat whichthe leaf surfaceacquirescarbonforpho- Lechowicz1990). Lightlevelandtemperature
werenotfound
stomatalconductance(moles H20-m-2s-1), the to explainanysignificant
tosynthesis;
variancewhendateand timewere
leafsurface'sinfluence
on therateof waterloss; andthearea includedin themodel.Plantsthatappearedto be wiltedor
and weightof thedried,pressed,leaf. Instantaneous
water- to have extremely
aberrant
water-useefficiencies
wereomituse efficiency
was thencalculatedas theratioof photosyn- ted fromsubsequentanalysis(N = 3).
theticrate to stomatalconductance.Such single-leafmeaA sensitivity
analysisconductedon thedatafoundthatthe
sures of gas exchangeand leaf size are heritable(Dudley conclusionsabouttherelativedifferences
amongindividuals
1996). Because gas-exchangeratesweremeasuredon a dry- and populationswere robustto the potentialerrorin calileaf area basis whichis extrapolatedto give wet-leafarea brationoftheequipmentor estimation
of theboundary-layer
measures(see below),theseresultsaremoreaccurateas com- conductance.
parativemeasuresamongplantsratherthanas estimatesof
I harvestedplantson September15, 1990 to avoid loss of
fieldgas-exchangerates.Because fewplantsdied aftermea- the studypopulationto burial by sand, waves fromlarge
the data were used foranalysisof fecundity
se- storms,or movementof beach sand offshoreby changesin
surement,
lection.
currents.
At thistime,mostof theplantsin thedryenvironMeasurements
ofphotosynthesis
andstomatalconductance menthad ceased flowering,
but the plantsin the wet enviweredone on August23 and 24, 1990, usingan Analytical ronment
variedfrommostlyflowering
to senescent.The meaDevelopmentCompanyLCA-2 portablephotosynthesis
sys- surements
I obtainedestimateplantfitnessesgivenan early
tem(Long and Hallgren1985; Field et al. 1989). Measure- end to thegrowingseason.For an indeterminately
flowering
mentsweremade underambientlight;bothdays wereclear annual,therankingof fitnessesin a populationmaydepend
withoccasional clouds. The mean lightlevel was 990 pLM on season lengthbecausehighearlyreproduction
maycome
photons-m-2-s'.Thoughlightlevels variedfrom330-1280 at thecost of loweredvegetativegrowthreducingresources
90% of measureswere made at light forlaterreproduction
FLMphotons-m-2-s-1,
(Geber 1990).
levels above 810 FLMphoton-m-2-s-1.
Cuvettetemperatures The collectedplantswere air driedat roomtemperature.
variedfrom25-33?C. Plantsweremeasuredbetween10:00 Sand was scrubbedofftheplantswhennecessary.The airA.M. and 3:00 P.M. in a predetermined
orderthatwas random driedplantswerepartitioned
intovegetativebiomass(stems
withrespectto environment,
positionwithinenvironment,and largeroots)and reproductive
biomass(fruits)and then
and theplant'sparentage.Gas-exchangetraitscould notbe weighed.
measuredon 50% of the survivingdry-siteplantsbecause
I used the reproductive
biomass allocatedto fruitsas a
theywere moribundor defoliated.Wet-environment
plants fitnessmeasurebecause it is the hypothesizedcausal link
thatweretemporarily
inaccessiblebecauseofsandmovement betweencarbonacquisitiontraitsand fitness(Fig. 1). Most
weremade on fruitscontaintwoseeds (Rodman1974); and because Cakile
(N = 38) werenotmeasured.Measurements
all dry-environment
plantsthatpossessed leaves (N = 62) flowersindeterminately,
higher reproductivebiomass is
and on 102 wet-environment
plants.For each plant,one re- largelytheresultofmorefruits
rather
thanlargerfruits.
Using
centlyexpandednewleafwas detachedand measuredwithin fruitbiomass for fitnessmeasuresmaternalinvestment
in
90 sec. Detached leaves of this species maintainconstant reproduction,
but ignoresthe potentialforvariancein biogas-exchangeratiosformorethan5 min(Dudley,pers.obs.). mass allocatedper fruitand per seed.
The sampleleaves were subsequently
pressedand driedto
providea measureof thesize of a recentfullyexpandedleaf
Data Analysis
and leaf drymass. Areas of dryleaves wereestimatedwith
a LI-COR leaf-areameter.Wetanddryleafareasfromleaves
Means and standarddeviationswere calculatedfor leaf
sampledfromseveralgreenhousegrownplantsprovideda size,photosynthetic
water-use
efrate,stomatalconductance,
conversionfactorforcalculatinggas-exchange
rateson a wet- ficiency,
vegetative
biomass,andfruitbiomassin thewetand
leaf area basis (wet area = 1.90 dryarea in chamber).
the dry environments
forthe subsetof plantson whichI
The LCA-2 was factory
calibratedfortheCO2 andrelative measured gas exchange (PROC MEANS, SAS Institute
SELECTION ON PLANT PHYSIOLOGICAL
Vegetative
biomass
Reproductive
biomass
95
TRAITS
- numberof
fruits
numberof
seeds
Leaf
traits
1. Path model of the hypothesized relationships between physiological traitsand fitness.Only those paths indicated by thick lines
will be measured in this study.
FIG.
in regressioncoefficients
be1989). Thedifference
inmeansbetweenthestudypopulations ease in testingfordifferences
is presentedanalogouslyto tweenenvironments.
grownin thetwo environments
high
withextremely
One datapointin thewetenvironment
thegeneticdifferences
betweenpopulations(Lande and Arlarge effect
nold 1983) as thedifference
in meansfora traitbetweenthe fitnesswas foundto have a disproportionately
dividedbythepooledphenotypic
standard on theregressionanalysisand was omittedas an outlierfoltwoenvironments,
lowingthe criterionof Sokal and Rohlf(1981). In the dry
deviationforeach environment.
which include both environment,
the nonlinearselectionanalysiswas runwith
Standardizedselectiondifferentials,
directand indirectselectionon a trait,were calculatedfor and withoutone outlyingdatapointwithverylargeleafsize,
selectiongradientsreas thecovariancebetweenthestandardized and the stabilizingand correlational
each environment
traitand fitness(PROC CORR) (Lande and Arnold1983). mainedsignificant.
wereconsideredsignificantly
different I performed
a path analysisto examinethe linearcomSelectiondifferentials
dependencybetweenthewater-use
coefficient
betweenthetrait ponentsof thefunctional
from0 ifthePearsoncorrelation
from0 (Lande and efficiency
and leaf size and fitness(Arnold1983). Path diand relativefitnessdiffered
significantly
Arnold1983). Selectiondifferentials
forthesametraitin the agramscan be used to factorlinearselectiongradientson
traitsintotheeffectof a traiton some aspectof
differentphenotypic
two environments
were consideredsignificantly
Pearsoncorrelation
co- performance
fromeach otherif thez-transformed
(e.g., leaftraitson vegetativebiomass),and the
traitson fitness(e.g., vegetativebioefficients
significantlyeffectof performance
betweenthetraitand fitnessdiffered
fromeach other(Sokal and Rohlf1981). Phenotypiccorre- mass on fruitbiomass) (Arnold1983). I used a pathmodel
to affect
lationsamongtraitswere obtainedfromthePearsoncorre- thatallowed forleaf size and water-useefficiency
fitnessthroughvegetativebiomassand thatallowedforleaf
lationmatrixof traits(PROC CORR).
to affectfitnessvia an alternate
efficiency
To testthe adaptivehypothesesaboutdirectselectionon size and water-use
I calculatedlinear and path (Fig. 1; Ehleringerand Clark 1988). Path coefficients
leaf size and water-useefficiency,
nonlinear(stabilizingand correlational)selectiongradients wereestimatedusingPROC GLM to obtaintheappropriate
variablesandrelon thestandardized
followingLande and Arnold(1983). Directionalselection regressioncoefficients
gradientswereobtainedfroma linearregressionof relative ativefitness.The sumof all pathsleadingfromtheleaftraits
fitnesson the traits,and quadraticselectiongradientswere to relativefitnessequals the directionalselectiongradients
obtainedfromthenregressing
relativefitnesson linearand obtainedabove (Li 1975; Arnold1983).
quadraticterms(PROC GLM in SAS). I estimatedselection
efficiency
and leafsize to avoid
gradientsonlyforwater-use
RESULTS
from"spuriouscorrelations"(Sokal and Rohlf
collinearity
had greaterfruit
The plantsgrownin thewetenvironment
func1981) caused by includingtraitsthatare mathematical
The plants
tionsof each other.Thus,photosynthetic
rateand stomatal biomassthandid plantsin thedryenvironment.
and had veryhigh
conductancecould notbe includedin thesameregressionas grewmuchbiggerin thewetenvironment
(Table 1). In thewetsite,21% oftheoriginal
water-use
efficiency,
andbecauseleafsizes weresmallerthan fruitproduction
thecuvettesamplingarea,thecalculationsof photosyntheticplantswerewashedaway because of shiftsin sand location
rateand stomatalconductanceincludedleafsize as a divisor. and storms.Of theremainingwet-siteplants(N = 183), an
In the
fromhumantrampling.
is estimatedindependently
of additional23% died,primarily
However,water-useefficiency
in drysite,50% oftheplantsdied,eitherfromapparentdrought
leaf size. I testedfordifferences
betweenenvironments
Although
standardizedselectiongradientsthrougha testof heteroge- stress,insectdamage,or fromhumantrampling.
neityof slopes in an analysis of covariance(ANCOVA) the sites were near each other,the presenceof insectsap(PROC GLM). Because the residualsfromthe regression pearedto varybetweenthesites.More herbivoreswereobI also calculatedthe servedin the dry site, and possible pollinatorswere more
analysiswerenotnormallydistributed,
maybe theresult
levelsofthestandardized
coefficients prevalentin thewetsite.Such differences
regression
significance
in theplantsratherthanthesitesthemselves.
fromjackknifeestimatesofthevariances(FreeStat,Mitchell- of differences
amongfamilies
in both Because mortality
did notdiffer
significantly
Olds 1989). I foundthatsignificance
changedslightly
=
directionsbutthe overalltrendwas similar,suggestingthat or betweenpopulationseitherin thedryenvironment'(P
betheparametric
(P = 0.58), differences
analysiswas robustto the lack of normality 0.22) or in thewetenvironment
in traitsindicatetheaveragephenotypic
of theresidualsin thisdata set. I therefore
presentthe sig- tweenenvironments
nificancelevels fromtheparametric
analysisbecause of the plasticityforthepopulation.
96
SUSAN A. DUDLEY
1. Mean traitvaluesin each environment
withthestandarddeviationsin parentheses.
Predicteddifferences
in traitmeansbetween
in traitmeansbetweenenvironments
environments
are fromtheselectionanalysis(Table 4). The observeddifference
was standardized
by a pooled phenotypicstandarddeviationto facilitatecomparisonsamongtraits.Observeddifferences
thatagree withthepredicted
N = 101; dryenvironment,
N
directionare indicatedin bold. Probabilitiesare takenfroman analysisof variances.Wetenvironment,
60.
TABLE
Dry
environment
Trait
Photosynthetic
rate(A)
P.mol/m2/s
Stomatalconductance(g)
mol/m2/s
Water-useefficiency
(A/g)
means
24.0
(9.75)
0.55
(0.24)
45.9
0.54
(0.41)
1.20
(0.99)
0.36
(0.46)
Leaf size
cm2
Vegetativebiomass
grams
Reproductive
biomass
grams
P < 0.10; * P < 0.05; ** P < 0.01; *
means
27.5
(8.63)
1.10
(0.40)
27.4
(11.50)
P'mol/mol
Wet
environment
(13.56)
1.89
(1.21)
55.63
(49.57)
13.48
(14.91)
Predicted
differences
Observed
differences
(ZDRY - ZWET)/IP
Dry = wet
0.37*
Dry < wet
1.77***
Dry > wet
-1.44***
Dry < wet
P < 0.001.
mearate,a short-term
of carbonuptake,and photosynthetic
sureofcarbonuptake,werepositivelyassociatedwithfitness,
hypotheses.The associa resultpredictedby thefunctional
beationsbetweenstomatalconductanceand fitnessdiffered
hypotheses:
tweenenvironments
as predictedby functional
andthushigherrates
plantswithgreaterstomatalconductance
of waterloss per unitleaf area were less fitin the dryenvironment,
and therewas no associationof stomatalcon(Table 2). The asductanceand fitnessin wet environment
and fitnessdiffered
sociationsbetweenwater-useefficiency
hypotheses:
byfunctional
as predicted
betweenenvironments
whichgainedmorecarplantswithhigherwaterefficiency,
bon forthe same waterloss, weremorefitin thedryenviand fitronment,
but no associationof water-useefficiency
larger
Unexpectedly,
ness existedin the wet environment.
leaf sizes werenotassociatedwithhigherfitnessin thewet
environment
but were associatedwithhigherfitnessin the
(Table 2). This resultwas notpredictedby
dryenvironment
the hypothesisthatreductionof waterloss throughhaving
smallerleaves is adaptivein drierenvironments.
The phenotypic
correlations
amongtraitswerestrongand
(Table 3, Fig. 2). Photosyndependedon the environment
showeda strongpositive
stomatal
conductance
thetic
rate
and
TABLE 2. Standardized
directionalselectiondifferentials
in each
in
theirrelationship
was
the
wet
environment,
but
correlation
environment.
from0 in each environment
Significancedifferences
Stomatalconductancewas
and thet-testof differences
betweenselectiondifferentials
on the weakerin the dryenvironment.
same traitin thedifferent
environments
are takenfromsignificance negativelycorrelated
withleaf size in thedryenvironment.
levelsforthecorresponding
correlation
coefficient
betweenthetrait Photosynthetic
withleaf size. Leaf
rates
were
notcorrelated
=
N 57, wet environment
N
and relativefitness.Dry environment
in
with
water-use
efficiency
correlated
size
was
positively
= 99.
bothenvironments
(Table 3).
Standardizedselection
I performed
a multivariate
fecundity
selectionanalysison
differentials
in
to
size
each
environment
efficiency
and
leaf
water-use
s/U
estimatethedirectselectionon each trait(Table 4, Fig. 3).
Wet
Dry
Because of thehighmortality
beforetraitsand fitnesswere
Trait
environment
t-value
environment
of selection
measured,thepowerto testforthesignificance
rate
0.41*
Photosynthetic
0.18*
0.666
only
signifIn
environment,
the
low.
the
wet
gradients
was
Stomatalconductance
0.10
2.24*
-0.33*
icant selectiongradientwas weak stabilizingselectionon
Water-useefficiency
0.66***
3.23**
0.01
Leaf size
0.54***
0.00
2.56*
In thedryenvironment,
therewas strong
efficiency.
water-use
0.39***
Vegetative biomass
0.89***
2.06*
stadirectionalselectionforincreasedwater-useefficiency,
* P < 0.05; ** P < 0.01; **P
< 0.001.
leaf size, and positive
bilizingselectionforan intermediate
In these results,extrapolatedfromdryleaf areas (Table 1),
and in greenhouse measures with fresh leaf areas (Dudley,
pers. obs.), C. edentula var. lacustris exhibited moderately
high photosyntheticrates and very high stomatal conductances (Korner et al. 1979). High gas-exchange rates are
thoughtto be typical for amphistomatousthick leaves found
in high light environments(Mott et al. 1982). As predicted
by functionalhypothesesforadaptive plasticity,plants grown
in the dry environmenthad smaller leaves than in the wet
environment(Table 1). Contraryto adaptive-plasticitypredictions, stomatalconductances were much higherin the dry
environment.Though photosyntheticrates were also somewhat higherin the dry environment,the water-useefficiency
was lower in the dryenvironment.Specific leaf weight (ratio
of leaf weight to leaf area) was higher in the dry site (dry
0.0123g/cm2,wet = 0.0074 g/cm2,P < 0.0001), and leaves
were noticeably thickerin the dry environment.
The fecundityselection differentials,which include direct
and indirect selection, differedsignificantlybetween environmentsfor all traitsbut photosyntheticrate (Table 2). In
both environments,vegetativebiomass, a long-termmeasure
SELECTION ON PLANT PHYSIOLOGICAL
97
TRAITS
3. Phenotypic correlations among physiological traits.Wet environmentcorrelations are in the lower diagonal, dry environment
correlations are in the upper diagonal.
TABLE
Stomatal
conductance
Photosynthetic
rate
rwet/rdry
Photosyntheticrate
Stomatal conductance
Water-use efficiency
Leaf size
0.23t
0.82***
0.08
0.11
-0.37***
-0.08
Water-use
efficiency
0.57***
-0.58**
0.22*
Leaf size
0.14
-0.48***
0.65***
t P < 0.10; * P < 0.05; ** P < 0.01; *** P < 0.001.
correlationalselection between water-useefficiencyand leaf
size (Table 4, Fig. 3). As the fitnesssurface (Fig. 3) shows,
the correlational selection caused the optimum leaf size to
increase with increased water-use efficiency.There was no
significantdirectional selection gradientin the dry environment for leaf size. The significantdirectional selection differentialfor leaf size in the dry site (Table 2) appears to be
an indirectresponse to selection on water-useefficiencyand
to the correlational selection on leaf size and water-use efficiency.
Because of the small sample size, the power to test for
differencesbetween environmentsin selection on water-use
efficiencyand leaf size was low. Nonetheless, the differences
in directional selection on water-use efficiency,stabilizing
selection for an intermediateleaf size, and positive correlational selection between water-useefficiencyand leaf size
between the wet and dry environmentswere all highly significant(Table 4, Fig. 4). These differencesare consistent
with functionalhypotheses that suggest that environmental
water availability causes the selection on leaf size and wateruse efficiency.
Path-analysis models using leaf size and water-use efficiency as carbon uptake traitswere used to analyze the di10090
0
0
O
80- o
m3
0
O
Q
>
Cc
_70-
0~~~
D 60
00
E1
W CD
q
0
*
00
go
o~
0
0
E
~~3~~30
~00
20
100
0
3
0
20-
0
o
0
eDry
(Fig.
rectionalselectiongradientsin the two environments
5). The resultsagreedwiththe expectationthatleaf traits
affectfitnessthroughtheireffecton vegetativebiomass.
Greaterleaf size increasedvegetativebiomass in the wet
higherwater-useefIn the dryenvironment,
environment.
ficiencyled to greatervegetativebiomass.The analysesdid
directeffectof water-useefshow a marginallysignificant
ficiencyon fruitbiomass in the dry site. In bothenvironments,highervegetativebiomass caused increasedfitness,
buttheincreasein fruitbiomasswithvegetativebiomasswas
greater(P < 0.05, analysisofcovariance)in the
significantly
(Fig 5).
thanin thewetenvironment
dryenvironment
DISCUSSION
selection
in fecundity
This studyexaminedthedifferences
Significant
on leaftraitsbetweenwetand dryenvironments.
were found
in selectionbetweenenvironments
differences
despitetherelativelysmallsamplesizes. The results,as predictedby physiologyof carbonacquisitionand waterloss,
the importanceof net carbonuptakeforplant
demonstrate
fecundityand show thatfecundityselectionon traitsthat
as predictedbetweenwet and dry
affectwaterloss differed
environments.
As predicted,selectionforgreaterwater-use
comparedwith
was foundin thedryenvironment
efficiency
leaf
thewetenvironment.
Selectionfavoredan intermediate
whereaslargerleaves wereassize in thedryenvironment,
sociatedwithgreatervegetativebiomassin thewetenvironment.This studycomparedselectionin two stronglyconenvironments
forone species butfoundresultsthat
trasting
Further
studiesin other
supportadaptivehypotheses.
strongly
are necenvironments,
species,replicatedacrosscontrasting
essaryto see if these resultscan be generalized.In interpretingtheseresults,I considerthreequestions:thesupport
becausal relationships
of the resultsforthe hypothesized
fortheevolutionof
tweentraitsand fitness;theimplications
and the description
thetraitsin the different
environments;
of theadaptivevalue of thetraitsin each environment.
Causal Interpretationof Selection Analyses
in selectionobservedbetweenwetand dry
The difference
environments
providesdirectevidenceforthe selectiveimpact of wateravailabilityon carbonacquisitiontraits(Wade
andKalisz 1990). The pathanalysisoftheselectiongradients
providesa testof thehypothesesaboutwhywater-useeffiLeafSize (cm2)
ciencyand leafsize are selected(Arnold1983). It supported
FIG.2. The relationship
andleafsize
efficiency
betweenwater-use
and leaf
hypothesisthatwater-useefficiency
in bothenvironments.
A nonlinearanalysisofcovariancefoundthat the functional
becausetheyaffectnetcarbonacquisition.
the regressionsof water-useefficiency
on leaf size did differbe- size affectfitness
in thedryenselectionon water-useefficiency
tweenenvironments
The stronger
(P < 0.001).
0-
o
o Wet
98
SUSAN A. DUDLEY
Significancelevels fortheselectiongradientsare
4. Linearand nonlinearstandardized
selectiongradientsin each environment.
takenfromthejackknifeestimatesof the varianceof the standardizedselectiongradients.The overallmodelforthedryenvironment
is not statistically
significant.
The F-values forthe testof
is significant
at P < 0.0002. The overall model forthe wet environment
in selectiongradientsbetweenenvironments
data.
differences
are froman analysisof covarianceson thepooled standardized
TABLE
Trait
Dry
environment
I'
Linear selection gradients
Water-useefficiency
Leaf size
tP
Wet
environment
F-value
P'
0.51**
0.20
0.01
0.00
Nonlinearselection gradients
yI
y'
Water-useefficiency*water
use efficiency
Leaf size*leafsize
Water-useefficiency*leaf
size
0.12
- 1.13***
0.71**
-0.22*
0.02
0.12
6.93**
1.04
2.20
13.88***
5.31*
< 0.10; * P < 0.05; ** P < 0.01; *** P < 0.001.
success was foundto be largely
atum,earlyreproductive
butlater
by timingof allocationto reproduction,
determined
associatedwithvegetative
successwas strongly
reproductive
then
growth(Geber1990). If Cakilefollowsa similarpattern,
in yearswitha longgrowingseason,selectionforlargerleaf
butselection
size wouldbe predictedin thewetenvironment,
on water-useefficiency
wouldstillbe expectedto be greater
shrub Chrysothamnusnauseosus, Donovan and Ehleringer in thedryenvironment
thanthewet environment.
(1994) found,contrary
to the resultsin thisstudy,thatthe
phenotypiccorrelationbetweenwater-useefficiency
(meaPredictingEvolution
suredas carbonisotoperatio) and vegetativebiomass was
siblingsfrom23 familiesfromtwo
positivein well-wateredtreatments
and 0 in water-limited In this experiment,
Thoughthe
in each treatment populationswereplantedin bothenvironments.
treatments,
thoughthegeneticcorrelation
in each environhighmortality
plantssuffered
was positive.Theysuggestthatunmeasured,
correlated
traits experimental
betweensourcepopulationsor
did notdiffer
ment,mortality
such as carbonallocationmayexplaintheirresults.
thisstudyprovidesstandardized
The pathanalysisalso providesa way of evaluatingpo- amongfamilies.Therefore,
selectiongradientson thesame populationin diftentialselectionin longerseasons. Selectionon a traitthat fecundity
and can be used to predicthow that
affectsvegetativebiomassdependson thestrength
of selec- ferentenvironments
tionon vegetativebiomass,as theresultsheredemonstrate. populationwouldevolvein responseto selection.One caveat
theresponseto selectionis thathighmortality
For one indeterminately
flowering
annual,Polygonum
arun- in predicting
vironment
was caused by greatereffectsof water-useefficiencyon vegetativebiomass,a greatereffectof vegetative
and a marginally
biomasson fitness,
significant
directeffect
on fitnesscomparedwiththewetenof water-useefficiency
vironment.
The directeffectmaybe explainedbyplantswith
higherwater-useefficiency
ratesbeing more successfulin
provisioning
fruits.In a commongardenstudyon thedesert
WetEnvironment
DryEnvironment
4
FITNESS
5
FII JESS 4
33
2
~~~~~~~~~~2
0
60
*.
8
3
3. Quadraticunstandardized
selectionsurfacefor water-useefficiency(WUE) and leaf size (LEAF) in the wet and the dry
environments.
Note thattheaxes have different
scales in thetwo figures.
FIG.
SELECTION ON PLANT PHYSIOLOGICAL
99
TRAITS
selectiongradients.However,this studydid not have the
powerto identify
smallerselectiongradientsand differences
in selectionbetweenenvironments,
whichcan haveimportant
*
evolutionary
implications.
The observedselectiongradients
indicatethatpopulations
in
each
environment
will
be
under
different
selectionregimes.
4*
The significant
difference
in directionalselectionon water,tL
*
use efficiency
suggeststhatforthe same populationwaterU23
00 0o
use
will
efficiency
be selectedto increasein thedrysiteand
0
0)
0
0
toremainnearthemeaninthewetsite.The selectiongradient
analysisshowsthatleaf size was selectedto be at an inter0
CE
C
mediateoptimumin thedrysite.The lack of significant
directional
selection
on
in
leaf
size
the
dry
environment
implies
b
1
*e
~
thattheoptimumleaf size in thedryenvironment
does not
cz
differsignificantly
fromthemeanleaf size in thedryenvi~ Wae Use Efiiec 0 (A/g
0
In contrast,
ronment.
thoughtherewas no significant
selec0
tionon leaf size in the wet environment,
the path analysis
0 ~~~~~(0
suggeststhatbecauseincreasedleafsize was associatedwith
0
20
40
60
80
100
increased
vegetative
biomass,largerleafsize maybe selected
WaterUse Efficiency
(A/g)
in some years.These resultssuggestthatforthesame pop(,umoles/mole)
ulationleaf size will be selectedto remainnearthemeanin
to increasein thewet site.
FIG. 4. The relationship
betweenrelativefitnessand water-use thedrysite and potentially
The intermediate
optimumforleaf size in the dryenviin bothenvironments.
efficiency
ronment
dependedon water-use
Plantswithlower
efficiency.
water-use
weremorefitiftheyhad smallerleaves,
efficiency
weremorefitif
occurredbeforethephysiologicaltraitsweremeasured.The and plantswithhigherwater-useefficiency
mortality,
whichmayhave been an episode of survivorship theyhad largerleaves. Such correlational
selectionmay act
selection,was greatestin thedryenvironment.
As a conse- as a forceof selectionon thegeneticvariancesand covariquence,thestatisticalpowerfortestingthehypotheseswas ances thatconstrainevolution(Phillipsand Arnold1989).
low. The extremecontrastin wateravailabilitybetweenthe These resultssuggestthatselectionwas actingat the level
environments
did increasethe abilityto finddifferences
in of the leaf on the balance betweenleaf carbonuptakeand
* Dry
o Wet
5-
Vegetative
DRY Environment
57
n=57
~~~~~~~~~~biomass
0.06fitness
0.1
leafsize
6
=0.65***
~~~~~0.36*/
/
0.74***
Relative
0.25
wateruse efficiency
WET Environment
n=98
0.20*
Vegetative
0.44**
bioassRelative
~~~~~~~~~~~~fitness
leafsize
wateruse efficiency
FIG. 5. Pathanalysisof standardizedlinearselectionon leaf size and water-useefficiency.
Significant
paths(P < 0.05) are indicated
by thicklines and bold coefficients.
*P < 0.05, **P < 0.01, ***P < 0.001.
100
SUSAN A. DUDLEY
waterloss. The correlationalselectionmay reflectthe de- in drierenvironments
(e.g., Ehleringerand Cooper 1988;
pendenceof whole-plant
carbonacquisitionon multiplein- Donovan and Ehleringer1994) thoughdecreasesin waterterdependent
leaf traits,whichhas been long recognizedby use efficiency
withseasonalincreasesin droughtstresshave
physiologists(e.g., Ehleringerand Clark 1988). Thus, this been observedin some species (DePuit and Caldwell 1975;
resultfurther
supportsthe argument
thatstudiesof natural Smedleyet al. 1991). In thisstudy,thefunctional
arguments,
selectionmustbe informedby underlyingbiology of the the field-selection
beresults,and the geneticdifferences
studytraits.
tweenpopulationsall suggestthatCakile exhibiteda malThe differences
betweenselectiongradients
in thewetand adaptiveplasticresponseto the environment.
Such an apwereconsistentwitha geneticanalysisof parently
dryenvironment
maladaptiveplasticresponsesuggestseitherthatthe
betweenthewetsiteand drysitepopulations. evolutionof adaptiveplasticityin water-useefficiency
differentiation
may
A companionstudy(Dudley 1996) foundthatthepopulation be constrained
or thattheexpression
by geneticcorrelations
fromthedrysitehad higherwater-use
efficiency
and smaller of adaptivetraitcombinationsmay be constrainedby the
leaves comparedwiththepopulationfromthewet site.The phenotypic
correlations
amongtraits(Scheiner1993).
of thetraitssuggeststhatdifferentiation One phenotypic
geneticarchitecture
theadaptive
correlation
thatmayconstrain
betweenpopulationsfoundin thediffering
is plasticityof physiologicaltraitsis thatbetweenwater-use
environments
constrained
by thelowergeneticvariationforwater-useef- efficiency
and leaf size. Water-useefficiency
was positively
ficiencyand thepositivegeneticcorrelation
betweenwater- associatedwithleaf size, because stomatalconductancewas
and leaf size (Dudley 1996).
use efficiency
negativelyassociatedwithleaf size. As Figure2 shows,the
water-useefficiencies
and leaf sizes of plantsin bothenviWhether
ronments
appeartofollowa curvilinear
relationship.
Describing Adaptation
thiscorrelation
a functional
is notknown
reflects
relationship
Measuringtheadaptivevalue of traitsrequirescomparing (Bhagsariand Brown 1986). It is plausiblethatsuch a corthefitnesssurfacesfortheunstandardized
traitsin each en- relationcould be theresultof thepositivecorrelational
sevironment,
ratherthanthe standardizedselectiongradients. lectionforwater-useefficiency
and leaf size (Philips and
However,because plasticitybetweenthe two environmentsArnold 1989; Arnold 1992). Nonetheless,fora given leaf
of all traitsbut photosynthesis
was extreme,the measured size,thedry-site
than
plantshad a lowerwater-use
efficiency
selectiongradients
areforplantsshowingverydifferent
phe- the wet-siteplants(Fig. 2), suggestingthatthiscorrelation
and leaf size (Fig. 2) and is not sufficient
notypesforwater-useefficiency
in
to explainthelowerwater-useefficiency
different
correlations
betweenthetraits(Table 3). Therefore, thedry-environment
plants.
thefitnesssurfacescannotbe statistically
comparedbecause
Anotherhypothesisforthe greaterstomatalconductance
theyare valid over different
rangesof the traits,but some andhigherphotosynthetic
ratesseenin dry-site
plantsis suginferences
maybe made.
gestedbythesignificantly
higherspecificleafweightandthe
The lack of significant
directionalselectionon leafsize in observationthatleaves were thickerand moresucculentin
thedryenvironment,
coupledwithstabilizingselection,im- the plantsgrownin the dry site. Specificleaf weighthas
did oftenbeen observedto be positivelycorrelatedwithphotoplies thattheoptimumleaf size in thedryenvironment
not differsignificantly
fromthe mean leaf size in the dry syntheticrate (Bhagsari and Brown 1986). A biophysical
environment.
Leaves ofthedryenvironment
plantsweresig- constrainton thickerleaves is thatgreaterconductanceis
smallerthanin thewetenvironment.
nificantly
Thoughleaf needed to permitCO2 diffusionto the interiorof thicker
size did not affectfitnessin the wet environment,
larger leaves (Mottet al. 1982). Greatersucculencein thedry-site
leaves led to increasedvegetativebiomass.These resultsare plantsmay permitlong-term
waterstorageand thusbe an
withthehypothesis
thata smallerleafsize is adap- adaptationto drought,but this hypothesisrequiresfurther
consistent
tivein thedrysite,and a largerleafadaptivein thewetsite, studiesof thephysiologyand ecologyof succulentleaves in
in agreement
withfunctional
predictions.
C3 species.
The finding
thatwater-use
was understrongposefficiency
A weaknessof selectionanalysesis thattheyare based
itivedirectional
selectionin thedrysiteand weakstabilizing upon correlationsamong traits(Mitchell-Oldsand Shaw
selectionin the wet site agreeswithfunctionalhypotheses 1987; Wade and Kalisz 1990). Such correlations
mayresult
thathighwater-useefficiency
is morecriticalwhenwateris froma causal relationship
but
betweenthetraitsand fitness,
in averagewater-useeffi- theymay also resultfromenvironmentally
limiting.However,the difference
inducedcovariciencybetweenenvironments
suggestsan alternatehypoth- ance betweenthetraitsand fitnessor fromindirectselection
have a commonselectioncurve on unmeasured,
esis, thatthe environments
traits(Rausher1992).
correlated
phenotypic
withthewet-siteplantshavingthe These possibilitiescannotbe analyzedfromthe selection
forwater-useefficiency,
optimumvalues and thedry-siteplantshavingvalues lower statistics
studies.
butmustbe answeredthrough
independent
thantheoptimum.Therefore
theresultsdo notconclusively The extensiveliterature
on plantwateruse suggeststhatthe
supportthe hypothesisthathigherwater-useefficiencyis resultsI observedare more consistentwitha causal relamoreadaptiveinthedrysitethaninthewetsite.A conclusive tionshipbetweentraitsand fitness
thanwithenvironmentally
testwould requireexperimental
to extendthe inducedcovariance.Variationwithinthe dry treatment
manipulation
in
in each environment.
rangeof phenotypes
environmental
wateravailabilitywouldbe expectedto cause
The lowerwater-useefficiency
exhibitedby plantsin the a positivecorrelation
betweenstomatalconductanceand fitis very ness if wettersites permitmoregrowthand greaterwater
dryenvironment
comparedwiththewetenvironment
withwater-use
Variation
puzzling.Commonly
plantsshowgreater
efficiency loss butnottheobservednegativecorrelation.
SELECTION ON PLANT PHYSIOLOGICAL
TRAITS
101
logicalecologyofNorthAmericanplantcommunities.
Chapman
inthedrytreatment
in environmental
wateravailabilitycould
and Hall, New York.
also be expectedto cause a positivecorrelation
betweenleaf
J.R., and C. Clark. 1988. Evolutionand adaptationin
size and fitnessif wettersitespermitbothlargerleaves and Ehleringer,
Encelia (Asteraceae).Pp. 221-248 in L. D. Gottlieband S. K.
moregrowthbutnottheobservedintermediate
optimumfor
Jain,eds. Plantevolutionary
biology.Chapmanand Hall, New
leaf size. The significant
pathbetweenwater-useefficiency York.
J. R., and T. A. Cooper. 1988. Correlationsbetween
and vegetativebiomassin thedryenvironment
suggeststhat, Ehleringer,
carbonisotoperatioand microhabitat
in desertplants.Oecologia
if selectionon unmeasuredcorrelatedcharactersis respon76:562-566.
sibleforthesignificant
selectionon water-use
efficiency,
then Endler,J. 1986. Naturalselectionin thewild.PrincetonUniversity
the unmeasuredcharactersmustbe associatedwithcarbon
Press,Princeton,
NJ.
uptake.
Farris,M. A., and M. J.Lechowicz. 1990. Functionalinteractions
among traitsthatdeterminereproductivesuccess in a native
The selectionstudyfoundconsiderableagreement
between
annualplant.Ecology 71:548-557.
naturalselectionin thefieldand predictions
fromfunctional Field,
C. B, J.T Ball, and J.A Berry.1989. Photosynthesis:
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M. A. 1990. The cost of meristem
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arenastrum:
Negativegeneticcorrelations
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ACKNOWLEDGMENTS
betweenleaves and roots,and themarginalcostoftranspiration.
Pp. 171-214 in T. J.Givnish,ed. On theeconomyof plantform
I would like to thankM. Newtonforexcellenttechnical
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