The University of Chicago 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 Stable URL: http://www.jstor.org/stable/2463239 . Accessed: 23/02/2014 15:09 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. The University of Chicago Press, The American Society of Naturalists, The University of Chicago are collaborating with JSTOR to digitize, preserve and extend access to The American Naturalist. http://www.jstor.org This content downloaded from 129.2.19.102 on Sun, 23 Feb 2014 15:09:33 PM All use subject to JSTOR Terms and Conditions Vol. 147, No. 4 The AmericanNaturalist April 1996 NOTES AND COMMENTS NICHE CONSTRUCTION Organisms,through their metabolism, their activities, and their choices, define, partlycreate, and partlydestroy their own niches. We referto thesephenomena as "nicheconstruction." Here we arguethat niche construction regularly mod- ifiesboth biotic and abioticsources of naturalselection in environmentsand, in so doing,generates a formof feedback in evolutionthat is notyet fully appreci- ated by contemporaryevolutionary theory (Lewontin 1978, 1983; Odling-Smee 1988,in press). Adaptationis generallythought of as a process by whichnatural selection shapesorganisms to fitpreestablished environmental "templates." Environments pose "problems,"and thoseorganisms best equipped to deal withthe problems leave themost offspring. Despite the recognition that forces independent of or- ganismsoften change the worlds to whichpopulations adapt (Van Valen 1973), thechanges that organisms bring about in theirown worlds are rarelyconsidered in evolutionaryanalyses. Yet, to varyingdegrees, organisms choose theirown habitats,mates, and resourcesand constructimportant components of theirlo- cal environmentssuch as nests,holes, burrows, paths, webs, dams, and chemical environments.Many organisms also choose, protect,and provision"nursery" environmentsfor their offspring. Organisms not only adapt to environments,but in partalso constructthem (Lewontin 1983). Hence, manyof the sources of naturalselection to whichorganisms are exposedexist partly as a consequence ofthe niche-constructing activities of past and presentgenerations of organisms. Thereare numerouscases oforganisms modifying their own selective environ- mentsin nontrivialways, by changingtheir surroundings or by constructingarti- facts(Von Frisch1975; Hansell 1984). One earlyexample was describedby Dar- win(1881). Earthworms, through their burrowing activities, their dragging organic materialinto the soil, theirmixing it withinorganic material, and theircasting, whichserves as a basis formicrobial activity, change both the structureand chemistryof soils (Lee 1985). As a resultof the accumulatedeffects of past generationsof earthwormniche construction, present generations inhabit radi- cally alteredenvironments and are exposedto changingsets of selectionpres- sures. Thereis also considerableevidence of evolutionaryresponses to self-induced selectionpressures. For instance,social bees, wasps, ants, and termites construct Am. Nat. 1996. Vol. 147, pp. 641-648. ? 1996 by The Universityof Chicago. 0003-0147/96/4704-0009$02.00.All rightsreserved. This content downloaded from 129.2.19.102 on Sun, 23 Feb 2014 15:09:33 PM All use subject to JSTOR Terms and Conditions 642 THE AMERICANNATURALIST elaboratenests that then mediate selection for many nest regulatory,mainte- nance,and defensebehaviors (Rothenbuhler 1964; Spradbery 1973; Von Frisch 1975;Mathews and Mathews 1978; Hansell 1984). Many species of fish, amphibi- ans, reptiles,birds, and mammalsconstruct nests and burrows,which then influ- encefurther selection. For example,comparative evidence suggests that the com- plexburrow systems excavated by moles, rats, badgers, and marmots,with their undergroundpassages, interconnected chambers, and multipleentrances, have servedas thesource of selection for defense, maintenance, and regulationbehav- iorsand componentsof matingrituals (Von Frisch1975; Hansell 1984). Plants,too, changethe chemical nature, pattern of nutrientcycling, tempera- ture,humidity, and fertilityof thesoils in whichthey live (Ricklefs1990). They mayeven affectlocal climates,the amount of precipitation,and thewater cycle (Shuklaet al. 1990).Many plants also changeboth their own and otherspecies' local environmentsvia allelopathy(Rice 1984),while pine and chaparraltree speciesfacilitate forest fires by accumulatingoils or litter(Mount 1964; Allen and Starr1982). These specieshave evolveda resistanceto fireand, in some pine speciesthat require a firebefore their seeds willgerminate, a dependencyon it (Allenand Starr1982). THE EVOLUTIONARY CONSEQUENCES OF NICHE CONSTRUCTION Theseexamples, and others (Lewontin 1982, 1983), suggest that niche construc- tionmay be a generalphenomenon, that it is not restrictedto a few isolated speciesor taxa,and that feedback from phenotypically modified sources of selec- tionin environmentshas evolutionaryas well as ecologicalconsequences. Al- thoughseveral topics in contemporarypopulation biology are alreadyconcerned withthe evolutionary consequences of the changes that organisms bring about in theirown environments(e.g., habitat,frequency- and density-dependentselec- tion),so farthese analyses have onlyfocused on geneticloci thatinfluence the productionof the niche-constructingphenotype itself. What is missingis any explorationof thefeedback effects on othergenetic loci. A moregeneral body oftheory is required. In orderto encouragethe developmentof this theory,in whatfollows we discusssome evolutionary consequences of nicheconstruction and detailwhy it is likelyto be of significanceto thebiological sciences. EXTRAGENETIC INHERITANCE Currently,evolutionary theory rests heavily on theassumption that only genes are transmittedfrom generation to generation,the principal exception being cul- turalinheritance (Feldman and Cavalli-Sforza1976; Boyd and Richerson1985). However,ancestral niche-constructing organisms effectively transmit legacies of modifiednatural selection pressures in theirenvironments to theirdescendants. Thisextragenetic inheritance has previouslybeen calledan "exploitivesystem" (Waddington1959), an "ontogeneticinheritance" (West et al. 1988),and an "eco- logicalinheritance" (Odling-Smee 1988). We willintroduce it in stages. This content downloaded from 129.2.19.102 on Sun, 23 Feb 2014 15:09:33 PM All use subject to JSTOR Terms and Conditions NOTES AND COMMENTS 643 If,in each generation, each organismonly modifies its environment temporarily or inconsistently,then there will be no cumulativeor consistentmodification of any sourceof naturalselection in its population'senvironment. If, however,in each generation,each organismrepeatedly changes its own ontogenetic environ- mentin the same way,because each individualinherits the same genescausing it to do so, thenancestral organisms can modifya sourceof natural selection for theirdescendants by repetitiveniche construction. The environmentalconse- quencesof such niche construction may be transitoryand may still be restrictedto singlegenerations only, but the same induced environmental change is reimposed sufficientlyoften, for sufficient generations, to serveas a significantsource of selection. For example,individual web spidersrepeatedly make webs in theirenviron- ments,generation after generation, because theyrepeatedly inherit genes in- structingthem to do so. Subsequently,the consistent presence of a web in each spider'senvironment may, over manygenerations, feed back to become the sourceof a newselection pressure for a furtherphenotypic change in thespiders, such as the buildingby Cyclosa of dummyspiders in theirwebs to divertthe attentionof avian predators (Edmunds 1974). Yet, thiskind of feedback does not introducean extrageneticinheritance in evolution,because no consequenceof nicheconstruction is transmittedthrough an externalenvironment from one gen- erationto thenext. In morecomplex cases, inheritedgenes instruct organisms to modifyrepeatedly the ontogeneticenvironments of theiroffspring as well as, or insteadof, their own. Here theconsequences of niche construction are effectively"transmitted" fromone generationto the nextvia an externalenvironment, in the formof a parentallymodified source of natural selection for their offspring. This transmittal is sufficientto establishan extrageneticinheritance system in evolution. Offspring nowreceive a dualinheritance from their parents, genes relative to theirselective environments,and at leastsome parentally modified sources of selectionin their environmentsrelative to theirgenes. The cuckoois an example.Cuckoo parents repeatedly select host nests for their offspring,generation after generation, thereby bequeathing modified selection pressuresas wellas genesto theiroffspring. These modifiedselection pressures have thenapparently selected for changed adaptations in theoffspring, such as a shortincubation period or the behavioralejection