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Niche Construction
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Niche Construction
Author(s): F. John Odling-Smee, Kevin N. Laland and Marcus W. Feldman
Source: The American Naturalist, Vol. 147, No. 4 (Apr., 1996), pp. 641-648
Published by: The University of Chicago Press for The American Society of Naturalists
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Vol. 147, No. 4 The AmericanNaturalist April 1996
NOTES AND COMMENTS
NICHE CONSTRUCTION
Organisms, through theirmetabolism, andtheirchoices,define,
theiractivities,
partlycreate,andpartlydestroytheirownniches.We referto thesephenomena
as "nicheconstruction." Here we arguethatnicheconstruction regularly mod-
ifiesbothbioticand abioticsourcesofnaturalselectionin environments and,in
so doing,generatesa formoffeedbackin evolutionthatis notyetfullyappreci-
ated by contemporary evolutionary theory(Lewontin1978,1983;Odling-Smee
1988,in press).
Adaptationis generallythoughtof as a processby whichnaturalselection
shapesorganisms tofitpreestablished environmental "templates."Environments
pose "problems,"and thoseorganisms bestequippedto deal withtheproblems
leave themostoffspring. Despitetherecognition thatforcesindependent of or-
ganismsoftenchangetheworldsto whichpopulationsadapt(Van Valen 1973),
thechangesthatorganisms bringaboutintheirownworldsare rarelyconsidered
in evolutionary analyses.Yet, to varyingdegrees,organismschoose theirown
habitats,mates,and resourcesand construct important components of theirlo-
cal environments suchas nests,holes,burrows, paths,webs,dams,andchemical
environments. Manyorganisms also choose,protect,and provision"nursery"
environments fortheiroffspring. Organisms notonlyadaptto environments, but
in partalso constructthem(Lewontin1983). Hence, manyof the sourcesof
naturalselectionto whichorganisms are exposedexistpartlyas a consequence
oftheniche-constructing ofpastandpresentgenerations
activities oforganisms.
Thereare numerous cases oforganisms modifying theirownselectiveenviron-
mentsin nontrivial ways,bychanging theirsurroundings or by constructing arti-
facts(Von Frisch1975;Hansell1984).One earlyexamplewas describedby Dar-
win(1881).Earthworms, through theirburrowing activities,theirdragging organic
materialintothesoil, theirmixingit withinorganicmaterial,and theircasting,
whichservesas a basis formicrobialactivity,changeboththe structure and
chemistry of soils (Lee 1985).As a resultof the accumulatedeffectsof past
generationsof earthworm nicheconstruction, presentgenerations inhabitradi-
callyalteredenvironments and are to
exposed changing sets of selection pres-
sures.
Thereis also considerable evidenceof evolutionary responsesto self-induced
For
selectionpressures. instance, socialbees,wasps,ants,andtermites construct
Am. Nat. 1996. Vol. 147, pp. 641-648.
? 1996 by The Universityof Chicago. 0003-0147/96/4704-0009$02.00.
All rightsreserved.
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642 THE AMERICANNATURALIST
elaborateneststhatthenmediateselectionformanynest regulatory, mainte-
nance,and defensebehaviors(Rothenbuhler 1964;Spradbery1973;Von Frisch
1975;MathewsandMathews1978;Hansell1984).Manyspeciesoffish,amphibi-
ans,reptiles,birds,andmammals construct nestsandburrows,whichtheninflu-
encefurther selection.Forexample,comparative evidencesuggeststhatthecom-
plexburrowsystemsexcavatedbymoles,rats,badgers,and marmots, withtheir
underground passages,interconnected chambers,and multipleentrances,have
servedas thesourceofselectionfordefense,maintenance, andregulation behav-
iorsand components ofmating rituals(Von Frisch1975;Hansell 1984).
Plants,too, changethechemicalnature,patternof nutrient cycling,tempera-
ture,humidity, and fertilityofthesoils in whichtheylive (Ricklefs1990).They
mayevenaffectlocal climates,theamountofprecipitation, and thewatercycle
(Shuklaet al. 1990).Manyplantsalso changeboththeirownand otherspecies'
local environments via allelopathy(Rice 1984),whilepine and chaparraltree
forestfiresbyaccumulating
speciesfacilitate oilsor litter(Mount1964;Allenand
Starr1982).These specieshave evolveda resistanceto fireand, in some pine
speciesthatrequirea firebeforetheirseeds willgerminate, a dependencyon it
(Allenand Starr1982).
THE EVOLUTIONARY CONSEQUENCES OF NICHE CONSTRUCTION
Theseexamples,andothers(Lewontin1982,1983),suggestthatnicheconstruc-
tionmaybe a generalphenomenon, thatit is not restrictedto a few isolated
speciesortaxa,andthatfeedbackfromphenotypically modified sourcesofselec-
tionin environments has evolutionary as well as ecologicalconsequences.Al-
thoughseveraltopicsin contemporary population biologyare alreadyconcerned
withtheevolutionary consequencesofthechangesthatorganisms bringaboutin
theirown environments (e.g., habitat,frequency- and density-dependent selec-
tion),so fartheseanalyseshave onlyfocusedon geneticloci thatinfluence the
production of the niche-constructingphenotypeitself.Whatis missingis any
exploration of thefeedbackeffectson othergeneticloci. A moregeneralbody
oftheoryis required.
In orderto encouragethe development of thistheory,in whatfollowswe
discusssomeevolutionary consequencesofnicheconstruction and detailwhyit
to thebiologicalsciences.
is likelyto be ofsignificance
EXTRAGENETIC INHERITANCE
Currently,evolutionarytheoryrestsheavilyon theassumption thatonlygenes
fromgeneration
are transmitted to generation,theprincipalexceptionbeingcul-
turalinheritance(Feldmanand Cavalli-Sforza 1976;Boyd and Richerson1985).
However, ancestralniche-constructing
organisms transmit
effectively legaciesof
modified naturalselectionpressuresin theirenvironments to theirdescendants.
Thisextragenetic inheritance
has previously beencalledan "exploitivesystem"
(Waddington 1959),an "ontogenetic inheritance"(Westetal. 1988),andan "eco-
logicalinheritance"(Odling-Smee 1988).We willintroduce it in stages.
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NOTES AND COMMENTS 643
If,ineachgeneration, eachorganism onlymodifies itsenvironment temporarily
or inconsistently, thentherewillbe no cumulative or consistent modification of
anysourceof naturalselectionin itspopulation'senvironment. If,however,in
each generation, each organism repeatedly changesitsownontogenetic environ-
mentin thesameway,because each individual inherits thesamegenescausing
itto do so, thenancestralorganisms can modify a sourceofnaturalselectionfor
theirdescendantsby repetitive nicheconstruction. The environmental conse-
quencesofsuchnicheconstruction maybe transitory andmaystillbe restricted to
singlegenerations only,butthesameinducedenvironmental changeis reimposed
sufficientlyoften,forsufficient generations, to serveas a significant sourceof
selection.
For example,individual web spidersrepeatedly makewebs in theirenviron-
ments,generation aftergeneration, because theyrepeatedlyinheritgenes in-
structing themto do so. Subsequently, theconsistent presenceofa web in each
spider'senvironment may,over manygenerations, feed back to become the
sourceofa newselectionpressurefora further phenotypic changeinthespiders,
such as the buildingby Cyclosaof dummyspidersin theirwebs to divertthe
attention ofavianpredators (Edmunds1974).Yet, thiskindoffeedbackdoes not
introducean extragenetic inheritance in evolution,because no consequenceof
nicheconstruction is transmitted through an externalenvironment fromone gen-
erationto thenext.
In morecomplexcases,inherited genesinstruct organisms tomodify repeatedly
theontogenetic environments of theiroffspring as well as, or insteadof, their
own.Heretheconsequencesofnicheconstruction are effectively"transmitted"
fromone generation to thenextvia an externalenvironment, in theformof a
parentally modified sourceofnaturalselectionfortheiroffspring. Thistransmittal
toestablishan extragenetic
is sufficient inheritance systeminevolution.Offspring
nowreceivea dualinheritance fromtheirparents,genesrelativeto theirselective
environments, and at leastsomeparentally modified sourcesofselectionin their
environments relativeto theirgenes.
Thecuckoois an example.Cuckooparentsrepeatedly selecthostnestsfortheir
offspring, generation aftergeneration, therebybequeathingmodifiedselection
pressuresas wellas genesto theiroffspring. These modified selectionpressures
have thenapparently selectedforchangedadaptationsin theoffspring, such as
a shortincubation periodor thebehavioralejectionby newlyhatchedcuckoo
chicksofhosteggsfromtheparasitized nests.Also,cuckoosthatareraisedinthe
nestsofa particular hostspeciesmaypreferentially parasitizethathostspeciesin
whoseneststheywereoriginally raisedthemselves whentheymature,possibly
learning thehostcharacteristics through imprinting(KrebsandDavies 1993).This
kindofextragenetic inheritance is currently modeledas a non-Mendelian mater-
nal inheritance (Cowlyand Atchley1992;Schluterand Gustafsson1993).Mater-
nal inheritance can generatesomecounterintuitive results,including temporarily
reversedevolutionary responsesto selection,and timelags thatmayresultin
populations continuing to evolveafterselectionhas ceased by an "evolutionary
momentum" (Feldmanand Cavalli-Sforza 1976;Kirkpatrick and Lande 1989).
Maternalinheritance is, however,a specialcase, and theeffects ofnichecon-
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644 THE AMERICAN NATURALIST
structiongeneralizeto multiple and to multipleancestors,notjust
generations
mothers.For example,supposea niche-constructing behavioris influenced by
geneticvariation at one setofloci,thatitspreadsthrough a population overmany
generations,and thatitprogressively changesthefrequency ofsomeresourcein
theenvironment as itdoes so. Supposefurther thatthefrequency oftheresource,
nowa partof an extragenetic feedsback to thepopulationto influ-
inheritance,
ence selectionat a secondset ofloci. In thesecircumstances, a timelag should
developbetweenthechangeinfrequency ofallelesat thenicheconstruction loci
and the responseto a frequency-dependent modifiedselectionpressureat the
recipientloci, the onlydifference beingthatherethe timelag is likelyto take
manymoregenerations to buildup.
Darwin'searthworms are an example.Supposea first geneticlocus influences
someniche-constructing behavior,suchas soilprocessing orburrowlining, which
subsequently affects theamountoftopsoilorthesoilnutrients intheearthworms'
environment. Another locusexpressesa phenotype thatis affected by soilcondi-
tions,suchas the structure of theepidermisor theamountof mucussecreted.
In thiscase, ancestralnicheconstruction by manygenerations of earthworms,
due to thefirstlocus,willeventually feedback to thesecondlocus and change
itsselection,butonlyaftermanygenerations ofnicheconstruction. Here again,
theeffectofthetimelag shouldbe to createan evolutionary "momentum," such
thatifthe selectionpressuresat thefirstlocus are relaxedor reversed,there-
sponseat thesecondlocus shouldcontinuein theoriginaldirection fora number
ofadditionalgenerations. Moreover,assumingmanygenerations are requiredto
modifynaturalselectionon a population,it mightnot be able to evolve fast
enoughto preventthe geneticvariationon whichits eventualresponserelies
frombeingprematurely lost. Thispossibility
also meansthatonce a population
reachesa stableequilibrium, it maytake a greaterperiodof time,or stronger
selection,forthepopulation to moveawayfromit.
INDIRECT GENE INTERACTIONS
Nicheconstruction providesa wayinwhichthedifferential phenotypic expres-
sion of genotypesat one locus can be influenced by the genotypeat another
via theexternalenvironment.
locus,indirectly For instance,thepinkcoloration
characteristic speciesis extracted
of flamingo fromthecarotenoidpigmentation
ofthecrustaceatheydigest(Fox 1979).Herethegenesinfluencing flamingo prey
choiceinteractwiththoseunderlying pigmentextraction and utilization,via the
foodresourcesintheirenvironment. In severalrespects,thegeneticbasis ofthis
feedbackis reminiscentof epistasis.In contrastto conventionalepistasis,how-
ever, nicheconstructioncan generateinteractions betweengenes in different
populations,even differentspecies.For example,thegenesthatunderliethose
ofearthworms
activities thatmodify soilstructure,thereby enhancing plantyields
(Lee 1985),haveinfluencedtheexpression ofgenesintheplantpopulationaffect-
inggrowth.Thus,theniche-constructing outputsof individualsnotonlychange
selectiveenvironments,whichfeedback to alterthefitnesses of allelesat other
loci,butmayalso influence thephenotypic expressionofthoseallelesin ontoge-
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NOTES AND COMMENTS 645
neticenvironments (Westet al. 1988).The effectof theseinteractions,
which
influenceboththenatureofthevariantssubjectedto selectionand thepattern
of
selectionactingon thosevariants,is to introducethe kindof feedbackloops
betweenpopulations and theirenvironments thatRobertson(1991)suggestsmay
makea considerable differencein evolution.
SYNTHESIZING EVOLUTIONARY BIOLOGY AND ECOLOGY
Because nicheconstruction mayapplyto interactions betweengenes in the
samepopulation, or in differentpopulations, itprovidesa mechanism fordriving
populationsto coevolvein ecosystems.Populationsmayaffecteach othernot
onlydirectly in thewaysthatare alreadymodeledby coevolutionary theory,as,
forinstance,in host-parasite coevolution(Futuymaand Slatkin1983),but also
indirectlyvia theirimpacton someintermediate abioticcomponentin a shared
ecosystem,as in competition fora chemicalor waterresource.For example,if
nicheconstruction resulting froma gene in a plantpopulationcauses the soil
chemistry to changein such a way thatthe selectionof a gene in a second
population, of plantsor microorganisms, is changed,thenthefirstpopulation's
nicheconstruction willdrivetheevolutionof the secondpopulationsimplyby
changing thephysicalstateof thisabioticecosystemcomponent.Since thedy-
namicsoftheintermediate abioticcomponent maybe qualitatively
quitedifferent
fromeitherthefrequency changesin thegenesthatunderliethenicheconstruc-
tionor thenumberof niche-constructing organisms in thefirstpopulation,this
indirectfeedback between species maygeneratesome interesting-andas yet
unexplored-behavior in coevolutionary systems.
Accounting forthe evolutionand prevalenceof mutualistic interactionsis a
stubborn problemfortheoretical populationbiologists,who usuallyassumethat
thereis somecostto thedonor(Roughgarden 1975;Mesterton-Gibbons and Du-
gatkin1992).Recentyears,however,have seena changeinthinking aboutmutu-
alism,withincreasing emphasisplacedon thefactthatmanymutualisms involve
the transferof incidental by-products, at no cost to the donor(West-Eberhard
1975;Brown1983;Janzen1985;Connor1986;Mesterton-Gibbons and Dugatkin
1992).For example,seed predators oftenbenefit thehostplantthrough thedis-
persalof its seeds at no cost to themselves(Janzen1985).These by-products,
whichare clearlya component ofa population'snicheconstruction, oftenserve
as thesourceofselectionforinterspecific investment intheirproduction (Connor
1986).For instance,fruitrepresents investment in seed dispersers(Thompson
1982).A thorough understanding ofthesecoevolutionary dynamicsmayinvolve
formalrecognition thattheniche-constructing activitiesoforganismscan change
selectionpressuresand thereby initiatemutualisticinteractions.
A SECOND ROLE FOR PHENOTYPES IN EVOLUTION
Whenphenotypes nicheconstruct, theycan no longerbe thought
ofas simply
"vehiclesforgenes," sincetheyare nowalso responsibleformodifyingsomeof
thesourcesof selectionin theirenvironmentsthatmaysubsequently feedback
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646 THE AMERICAN NATURALIST
to selecttheirgenes.Moreover,thereis no requirement fornicheconstruction
to resultdirectly fromgeneticvariationbeforeit can influencethe selectionof
geneticvariation.For instance,nicheconstruction can dependon learning, as is
thecase fortheBritishtitsthatmayhave changedtheirown selectionpressures
by openingfoilmilk-bottle tops,therebygainingaccess to a newresource.The
evolutionaryconsequencesofthislearnedinnovation areunknown, butitis possi-
ble thatthisnewresourcemaynowbe selecting forsomefurther changeinthese
tits-forinstance, fordifferent enzymes-orforimproved
digestive learning abil-
ity(FisherandHinde1949;SherryandGalef1984).Similarly, nicheconstruction
can also dependon culture,as happenswhenhumansincreasethefrequency of
thesickle-cellalleleintheirownpopulations byunwittingly increasingthepreva-
lenceof malariain theirenvironments through theiragricultural
practices(Dur-
ham 1991).The consequencesfora geneat thesecondlocus are thesame,pro-
videdtheeffectof the nicheconstruction on the environmental resourcesthat
constitutethe sourceof selectionis unchanged.The netresultis an additional
role forphenotypes in evolution.Phenotypesnot only surviveand reproduce
in theface of naturalselectionand chancebut also modifysome
differentially
sourcesof selectionin theirenvironments by nicheconstruction.
RELATIVIZATION OF EVOLUTIONARY BIOLOGY
On thebasis of empiricalevidence,Lewontin(1978, 1982,1983)has argued
thatthe "metaphorof adaptation"shouldbe replacedby a "metaphorof con-
However,theacceptanceofLewontin'spositiondemandsmorethan
struction."
just semanticadjustments to evolutionarytheory.Niche construction changes
thedynamic oftheevolutionary processinfundamental waysbecauseitprecludes
a descriptionofevolutionary changerelativeonlyto autonomousenvironments.
Instead,evolutionnowconsistsofendlesscyclesof naturalselectionand niche
construction.Equally,itis no longertenableto assumethattheonlywayorgan-
ismscan contribute to evolutionarydescentis by passingon fitor unfit
genesto
theirdescendants relativeto theirenvironments, because theycan also pass on
modificationsinthoseenvironments thatarebetterorworsesuitedto theirgenes.
Adaptation becomesa two-waystreet.
ACKNOWLEDGMENTS
to R. C. Lewontinforhisinspiration,
We are grateful support,and advice.
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F. JOHN ODLING-SMEE
INSTITUTE OF BIOLOGICAL ANTHROPOLOGY
UNIVERSITY OF OXFORD
58 BANBURY ROAD
OXFORD OX2 6QS
UNITED KINGDOM
KEVIN N. LALAND
SUB-DEPARTMENT OF ANIMAL BEHAVIOUR
UNIVERSITY OF CAMBRIDGE
MADINGLEY
CAMBRIDGE CB3 8AA
UNITED KINGDOM
MARCUS W. FELDMAN
DEPARTMENT OF BIOLOGICAL SCIENCES
STANFORD UNIVERSITY
STANFORD, CALIFORNIA 94305
SubmittedFebruary21, 1995; Revised August 7, 1995; Accepted August 16, 1995
Associate Editor: J. Bruce Walsh
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