SystemsView of Devetopmenr ;T# AnApprar*ffi

Timothy D. Johnston

The work of Daniel s' Lehrman provides the behavior-was conceptualfoundation rerativeryuncontroversiar for a greatdeal of the em- in psy- ;;att Inherited behavior(rnstrnct) pirical and theoreticalwork on behavioral was under- devel- stoodi be an inherent opmentthat has beenundertaken part of the individua's in the last half r"lJrp ,rr"t resurtea century' Most of his publications iro;;. evorutionaryhis- are empirical ,o.y orirr" contributionsto speciesr, *iri"i, iiu"tong"o. Instincts the literature on behaviorat *.i"".rp"9iuityi.portunilnno.rtu-unanimars, endocrinology'and many of those are although they were the most widely cited papers .T:Lg arsothought to accountfor at in that field' His t.urirJ-. human broaderimpact on behavior.irthough the mech- our thinking about behavioral unir_, development Lf inheritance,r.".r", well and ev-olutioncomes primarily from understood two theoreticalpublications: 1*^rurui"nrchein lggT; sapp lgg3), it was gener_ his tbsr critique or iirv,lil-pricitty, Konrad assume;ihu, on. Lorenz's theory of instinct, excerpted courd speak or-ine inheritance oi u.rru"io, in the chapter that follows, and a as straightfor- hlr chapter *;;i; u, oo" courd (Lehrman1970) that reiterates speakabout the inheritance and extends-the oru -o.ptorogicar ideas presentedin or physiorogicartrait, about the pup"..--n.rr""n *hi"h;; them'those .earrier controversyexisted. two publicatioot wrratis stitt guotutionury oneof theclearest starements "ontuin ,o.it"., like charres Darwin of the system,ylry (r87rj;?e"rg. of development'modern R;;;r'?irrrl, and conwy articulatiorir or rr,i.r, iroyi'rur*gan arerepresented by (1g95) used the concept of in_ the chaptersin the presentvol- stinlt ume' Lehrman to exprainttre u"t avio, and mentar himself did not use'the termi- ab'ities nology of human and nonhuman animals, of svstemsthinking, but his an'alysis but it was of wir;;;i"*es and w';;M"Dougarl developmentillustrates many of whose the most sign- wriffi were most ofmodern a"u"rop*"niur rvr,.-, responsiblefor stimulating a ;fl::ilfird: ,gtfi:'the_explanatoryurlity of the concept Asimpriei uv , trretitre of his re53 paper,-ui9*1 :xjffl,ll:fllJil?tfl?'ff[tffxiilil Lehrman articulated his develop-.nti in reaction - force in American to Lorenz's ptesentationoilurri"ur "r;;;;ortant psychology ethological a.ound t-hl turn of the rastcentury. instinct tht?tl: which ,-.rgJ Jamesdefined in the inrtin"i ur'..th. facurty writings of Lorenz and Lis.colruuotuiir., of actingin sucha way as cially to producecertain ends,without NikolaasTinbergen, during the lg3bsand"rp"- foresight of the 1940s(see *i.,;;ithout pr*rlr, Lehrman's uiuiiogru;iv ior in the per_ Jorion, rorr*n".,,1ru.n", ig90, "a*ation to this literature)'Lorenz's tuit uor.zlt:1, emphasizing not, or"ou.r., tt. both the tereorogicar first theory of instinct to engage ;;;;ivistic aspectsof the attention of instirrci. ln "r; psvchologists,nor James,swide-ranging and rather was Lehrmin's the nrsic.iti- f;;;;y;i;"1:rr, dif- cismof theconcept instinct *i, 1ur, one among of instinct ot oiiit.","g-i., -unv ofinheritedandacquiredbehaviorutt"tri*uy. d.,..-inants of behavior.In McDouga*s system,conversery, to approachthe analysis instinctbecame the founda- of behavior tion on whicr,au uet aulo. r"u, uur"o. McDougall (1908) arguedthat all humanU.tuuioriur;;"# and stinctivecore that provides ]l}:^ll1::,"d rheAcquired in Behaviol Uotf,_oi*uti"on unO l8q)-1953 for behavior. L.u_ing may play an ,*:,t:,lmportant role in determining what particular abo.ut 1920, ..inher- objects and behaviorr use of the categories t..orZ associated with .eo,?^*tt and"acquired', to exptain theortgins or ,"#fi:j:T:T*l;:ji:f:*:TJffffi::il;

r6 Timothy D. Johnston Toward a Systems View of Development t7

tive organization of the behavioral repertoire. For that instinctive behavior exists in human or non- Carmichael(1925) bolstered Kuo's position by the physiological basis of behavior" (p. aA7). about the first two decades of the twentieth cen- human animals, and that all supposed instincts pointingout that evenanatomical structure does Other authorsused behavioral and physiological tury, the concept of instinct was repeatedly in- can in principle be explained as the outcome of not developindependently of environmentalin- data to support their claims that visual percep- voked as an explanation for behavior, most often environmental influences of one kind or another. fluences.He summarizedembryological research tual organization(Hebb 1937)and sexualbehav- not on the basis of careful experimentation and Although some of Kuo's arguments are over- showingthat many presumably"inherited" struc- ior in rats (Beachl95l; Stonel95l) are innate. theoretical analysis, but by simply postulating an blown, he made an important fundamental point: tures in fish and amphibiansrequire particular although Hebb and Beach later modified their instinct whenever a type of behavior seemed in Unless we know in detailed, mechanistic terms environmentalconditions to develop normally views(Beach 1955; Hebb 1953). need of explanation. James had legitimized this what it means to say that instinctive behavior and concluded:"Heredity and environmentare In 1951,Tinbergen published his classic and in- approach (he listed more than twenty human patterns are "inherited," the use of instinct as an not antithetical,nor can they expedientlybe sep- fluential accountof ethologicaltheory, TheStudy instincts, including instincts of shyness, fear, explanatory category produces a "finished psy- arated;for in all maturation there is learning: of Instinct. Although the ethological approach acquisitiveness, play, and modesty). Although chology," or at least a "finished" developmental in all learning there is hereditary maturation" to behaviorhad beena prominent feature of the McDougall offered a more fully developed analy- psychology. That is, it tends to block further in- (p.260). Europeanscientific scene since the 1920s,it only sis, he too provided lists of instincts that were vestigation into the ontogeny of the behavior by Debateover the utility of the instinct concept, becamewidely known to Americanpsychologists intended to explain the whole range of human purporting to explain when all it really does is to and over the related concept of maturation to starting around 1950 (Dewsbury 1984: l3ltr). behavior. Indeed, such lists were common in label.Itmay be correct to identify certain elemen- explainthe developmentof instinctivebehavior, Much of the earlier literature was written in writings about instinct of this period: One writer tary movement patterns, what Kuo called "un- continuedthroughout the next twenty-fiveyears. German or Dutch, and what was published counted nearly 850 major types of instinct pro- learned reaction units," as inherited, but more From the outset,contributors to the debatehad in English had appearedin biological journals posed in the psychological literature between complex coordinations of behavior (including recognizedthat the term might be usedin more or conferenceproceedings not usually read by 1900 and 1920 (Bernard1924). those usually identified as instincts) offer too thanone way. Indeed, Dunlap (1919)opened the American psychologists(e.g., Tinbergen 1942; This cavalier use of the concept, coupled many opportunities for the influence of experi- debateby arguing that it was important "to dis- Lorenz 1950). Nonetheless,the European lit- with the vitalistic and teleological character ence to be attributed to heredity. tinguishbetween the instinct as a group of activ- erature, and especially the work of Lorenz, of McDougall's instinct theory (which made it In his later papers, Kuo (e.g., 1924) went even ities teleologically defined, and the instinct as a described a theory of instinct that avoided anathema to the mechanistic S-R psychology of farther, arguing that "in a strictly behavioristic physiologicalgroup" (p. 307; original emphasis). McDougall's teleology,while providing an ac- Watsonian behaviorism; see Boakes 1984, chap. psychology, with its emphasis on laboratory proce- Most of the anti-instinctwriters aimedtheir crit- count that was more fully developedtheoreti- 8) soon provoked a backlash. Beginning with a dure and with its insistence on physiological expla- icismsat the former useof the term, most closely cally than any availablein the work of American paper by Dunlap (1919), the "anti-instinct move- nationofbehavior, there is practically no roomfor associatedwith McDougall's theory,although, as comparative and physiologicalpsychologists. ment" in American psychology criticized the con- the concept of heredity" at all (p.428, original ital- we have seen,others (like Kuo) wishedto reject Furthermore,the theory was basedon extensive cept of instinct on a number of grounds-that it ics). In this paper, he withdrew his earlier conces- any kind of inherited behavior at all. But some observations,and someexperiments, on a large invoked vitalistic forces, that instinct theorists sion that some simple reactions may be inherited authors,especially those trained in comparative number of speciesunder natural conditions. frequently offered no evidence for the existence of because "so long as there are inherited reactions, and physiologicalpsychology, were much more Thesefeatures of Lorenz's theory made it possi- justification the instincts they proposed, and that attributing simple as they may be, there is for the sympathetictoward Dunlap's seconduse, "in- ble for Lehrman to articulate a critique of the instinctive behavior to "inborn dispositions" use of the term instinct" (p. 439). "The traditional stinct as a physiological group," by which he concept of instinct that revealedits deficiencies leaves unanswered the question of how the be- sharp distinction between inherited and acquired meant "a certain definite group of muscularand for the analysisand understandingof behavior havior comes into being. The last of these is responses,"he wrote, "should be abolished. All glandularperformances ... resultingfrom a defi- more clearlythan did earliercriticisms. most directly relevant to understanding the im- responses must be looked upon as the direct re- nitestimulus or complexof stimuli" (p. 308).For pact of the anti-instinct movement on develop- sult of stimulation. as interactions between the example,Lashley (1938) rejected the use of in- mental thinking. animal and its environment" (p. 439). Kuo in- stinct in the teleologicalsense (which he referred Systems Thinking in Lehrmanos 1953 Critique of Lorenz's Perhaps the most persistent and unforgiving of sisted that the idea of inherited behavior was to as "a dynamicsof imaginaryforces" Ip.M7l) Instinct Theory the anti-instinct critics was Zing-Yang Kuo, who simply too vague and nonspecific to do more but acceptedits value when referring to spe- wrote five theoretical articles criticizing the con- than obscure questions about the origins of the cific, identifiable behavior and its underlying Lehrman's paper was only one of several criti- cept of instinct between l92l and 1930, in addi- behavior in question. physiology-Dunlap's "physiological"instincts. cisms of the concept of instinct that appeared tion to a series of experimental reports analyzing Kuo's arguments were based more on theo- Lashleymade no apologiesfor usingthe concept around 1953, although it was by far the most the prenatal development of behavior in chicks. retical principle than on empirical evidence, of of instinctin this sense,asserting that "the dis- comprehensive. Lehrman's fluency in German In his first two papers, Kuo (1921, 1922) argued which very little pertaining to the early develop tinction betweengenetic and environmentalin- allowed him to work with the original papers that there is no evidence supporting the claim ment of behavior was then available. However. fluences... is of real significancefor problemsof on which Lorenz's ideas were based (Silver and Timothv D. Johnston Toward a Systems View of Development l8 l9

relying on sum- rable elementof the organism,dependent on its 44) explicitly noted that he had earlier Rosenblatt 1987), rather than accepted least some ethologists in the 1950s and 1960s. accounts written in own specificphysiological substrate. For exam- the existenceof innateperceptual organization maries and secondhand in Lehrman did argue that the development of all and im- ple, he suggestedthat the gradual postnatal im- part becausehe had overlooked the English, and this enhanced the credibility significance behavior involves the influence of experience, on the earlier work provementof peckingin chicks"is very probably of someof his own data and he took issue pact of his criticism. Drawing with but, like his mentor Schneirla, he urged a much (e.g., 1949), Lehrman pro- due in part to an increasein strengthof the leg Tinbergen's(1951) proposal that we should ,,experience" of Kuo and Schneirla study broader interpretation of than the thinking about devel- musclesand to an increasein balanceand stab' the organizationof innate behaviorbefore vided a framework for study_ very narrow set of circumstances generally sub_ build into a ility of the standingchick, which results partly ing learning,an approach that Hebb ,,learning." opment that he and others could concluded sumed under the term In several pa_ Although from this strengtheningof the legs and partly would be logically impossible.All coherent alternative to instinct theory. three papers pers, ethologists attempted to counter Lehrman,s his account as a sys- from the developmentof equilibrium responses" wereinfluential in shapingsubsequent discussion Lehrman did not identify assertion that some particular behavior is not in_ it embodies some (Lehrman L953: 344\, rather than to the ma- about the conceptof instinct. tems approach to development, nate by showing that it could not be explained as , sys- of specific underlying neural circuits. As might be expected, of the most significant elements of current turation many ethologistsre_ the outcome of standard conditioning piocedures This is quitesimilar to the dynamicalsystems view jectedthe argumentsof Lehrmanand psvcho_ tems thinking. his ("trial-and-error learning,') and thus concluding features of of human locomotor developmentpresented logical colleagues,although others *.r. The most readily evident "systems" *o.. that it must, in fact, be innate. It seemed difficult of the by Thelen(e.g., Thelen, Kelso, and Fogel 1987; receptive.For example,speaking at Lehrman's critique were his repudiation a conference for these ethologists to recognize that Lehrman innate and acquired behav- Thelen 1995),which explains developmentnot that brought ethologistsand their critics together distinction between was proposing to abandon the learned_innate dis_ iors, or elements of behavior, and his recognition just in terms of increasingbehavioral coordina- soon after publication of Lehrman's critique, tinction .,Let in toto, not reclassifying purportedly in- the rest of tion, but also in terms of the growing strength Tinbergen(1955) conceded: that behavior cannot be isolated from me say righi at nate behaviors as learned (Lehrman lg57). the organism's physiological and anatomical and massof the infant's limbs. the beginning,that I admit that we must drop this The most important 'innate' _ and influential response to arguments Although the term system, in the sensein use of the word for the reasons makeup. He provided both theoretical already Lehrman's criticisms came from Lorer:z himself behavior which it is employedby modern developmental given,namely that the word can and empirical evidence to show that be appliedonly in the form of a long paper in German (Lorenz categories of systemstheorists, does not appearin Lehrman's to differencesonot to characters,and cannot be neatly divided into the alsobecause t96l),later translated into English and expanded Instead, he argued, we must paper,there is no doubt that he would havebeen tests such as ours the deprivation experi_ learned and innate. [i.e., into a book (Lorenz 1965).In this book there is every pattern of entirely sympatheticto the aims of systemsthe- mentl excludeonly part of all possible analyze the development of environ- an important shift in Lorenz's position regard_ interaction ory as it is representedin this volume.The ideas mentalinfluences 102]... instead behavior in terms of a continuing [p. of drawing ing the defining feature of instincts. Originally, (not that we should seekan explanationof develop a positiveconclusion or a pseudo-conclusion between the organism and its environment by Lorerz (e.g., 1937)had drawn the learned/innate environment, as is ment in the interactionsthat occur within the de- saying this responseis innate, I want between the genotype and the to spe- distinction on the basis of whether the devel_ proposed). Although the mechanisms velopingorganism and betweenorganism and its cify the little bit we have found out about sometimes the opment of a behavior is determined by genes or involved in this in- environment,and that the organismis more than ontogeny of this response,saying that, of learning sometimes are at the environment. (This was a very strict distinc_ less obvious contributions of just a nervoussystem that processesinformation, momentwhen we studiedit, it wasnot vet condi_ teraction, other, tion; indeed, where a behavior appeared to be a In particular, he are central to the account of developmentthat tioned" Ip. 1061.Similarly, in his influential experience play a part as well. text- blend of learning and instinct, Lorenz argued experiment Lehrman advancedagainst Lorenz and the clas- book on animal behavior,Hinde (1966) rejected the isolation (or deprivation) adopted that it would always be possible to identify purely ethologicaltheory of which he wasthe chief Lehrman'sdevelopmental approach as an adequate tool for analyzing development, sical and largely learned and purely innate elements, interlocked is still possible architectand foremostadvocate. dispensedwith any attempt to draw sharp pointing out that self-stimulation dis_ or intercalated to form the behavior pattern.) But tinctions betweenlearned for an isolated animal. Later work, especially and innate behavior. he now proposed that the real Other difference lies in that of Gottlieb (e.g., 1971,l99l) has revealed the ethologists,however, refused to acceptthe the source The Responseto L,ehrman'sCritique of the information that determines its normal behav- developmentalists'critique. importance of self-stimulation for adaptiveness. If adaptiveness is determined One of by ioral development. Lehrman did not go so far as their responseswas to read Lehrman,s information acquired Lehrman'spaper was one of three publishedat position during an individual's to consider organism and environment as part of asclaiming that all behavioris the result development, sametime that criticized the concepts then the behavior is learned; if that we about the of trial-and-errorlearning and a single system, but he clearly understood that heredityhas it is determined by information acquired of instinctand innatebehavior as useful bases for no effecton during cannot partition behavior into elements and give behavior(e.g., Eibl-Eibesfeldt 196l: the evolutionary history developmentalthinking. Both Hebb (1953)and Eibl-Eibesfeldt of the species, then the a separate account of the development of each of and Kramer l95g; Hess 1962: behavior Beach (1955) marshaled similar arguments to is innate. This information meta_ provides the core of the sys- Klinghammerand Hess1964; Lorenz 1950. them, an insight that This phor formed the core of Lorenz's long reply those presentedby Lehrman, in the processre- is manifestlynot tems view of development. what Lehrman and otherswere to Lehrman (1965) and treatingfrom earlierpositions in which they had saying, echoed points made by Lehrman also criticized the ethologists for but it seemsto have been a widely ac_ other ethologists defendedthe utility of the concept.Hebb (1953: who wished to preserve the as a neatly sepa- cepted paraphraseof their position treating each innate behavior among at learned-innate distinction (e.g., Hess 1962: .t 20 Timothy D. Johnston Toward a Systems View of Development il 2l

Thorpe 1961, 1963;see Beer 1973).It is a seri- Lorenz'sand Tinbergen'swork (especiallyin the Lorenz (1965) had claimed that the adaptive (Eds.), Comparativepsychology: A (Oyama 1985;Johnston three European journals), a few direct rebut- Modern Survey, pp. ously flawedmetaphor informationspecifying an animal'sinnate behav_ 21-77. New York: McGraw-Hill. 1987)but its attractivenessfor Lorenz helps to tals of Lehrman's criticisms of Lorenz (mainly ior is in the form of a blueprintcoded in the genes Blrnard, L. L. (1924).Instinct: A Study in psy_ a large part of the disagreementbetween in the Zeitschrift), and frequent referencesto controls Social clarify that the unfolding (,,strictly determined chology.New York: Henry Holt. him and Lehrman: WhereasLehrman's primary Lehrman's empirical studies of behavioral en- maturation")of thosepatterns that are innate. Boakes,R. (1984).From Darwin to Behaviorism: psv- interestwas in understandingthe developmentof docrinologyby thoseworking in that field. Many Lehrman wrote about the genetic blueprint in chology and the Minds of Animals. Cambridge: Carir_ behavior,Lorenz's interest was in understanding papersthat seemto fall squarelyinto the domain terms that are strikingly reminiscentof Kuo's bridge University press. its adaptiveness.The deprivationexperiment, crit- of Lehrman'sanalysis ignore his 1953paper en- (1921)when he objectedto the Carmichael, useof instinct on L. (1925).Heredity and environment:Are icized so effectivelyby Lehrman, is for Lorenz tirely, and othersmention it only in passing. rhe grounds that it tends to produce a finished they antithetie,al2Journal of Abnormaland Social psy_ only incidentally concernedwith explicatingde- After 1953, most of Lehrman's own publi- psychology:"I believethat the comfort and satis_ chology20:245-260. velopment;its primary goalis to revealthe source cations dealt with his empirical researchon the factiongained from disposingof the problemsof Darwin, C. R. (1871).The Descentof Man, and Selec_ envir- of the information that makesbehavior adaptive relationsamong hormones,behavior, and ontogeneticdevelopment by the useof suchcon_ tion in Relationto Sex.London: John Murray. (Hess1962: 223;Lorenz 1965: 83tr). onment in the ring dove, exemplifyingthe kind cepts are misleading, Dewsbury, and are based upon the D. A. (1984).Comparative psychology in the of behavioral researchthat he had advocated, evasionor dismissalof the most difficuliand in_ TwentiethCentury. Stroudsburg, pA: Hutchinson Ross but not elaboratinghis theoreticalposition very terestingproblems of development" (Lehrman Co. Lehrman's Critique The Legacy of much (seeLehrman 1962\.ln 1970,he published .,genetic Dunlap, 1970:34). Almost thirty yearslater the K. (1919).Are there any instincts?Journal of another major theoretical statementin a vol- blueprint" is an idea whoseuse has becomein_ AbnormalPsychotogy | 4: 307_31 l. In the decade or so immediately after the pub- ume preparedin memory of his mentor, T. C. creasinglywidespread and that continuesto have Eibl-Eibesfeldt,I. (1961).The interactionsof unlearned lication of Lehrman's critique, discussion of his 1968.This chapter behaviour Schneirla,who had died in a stronggrip on the imaginationsof scientists patternsand learningin mammals.In J. M. ideas appeared in various theoretical papers de- and (Lehrman 1970)both expandedon the position lay personsalike (seeNelkin and Lindee 1995). Delafresnaye (Ed.), Brain Mechanigmsand Learning, voted to the analysis and reanalysis of the con- pp. 53-7 articulatedin 1953and alsoresponded directly to The rapid growth of molecular and human 3. Oxford: Blackwell. cept of instinct and the relation between learned be_ Lorenz's (1965)defense of instinct theory. I do havioral geneticsand the advent of the Human Eibl-Eibesfeldt,I., and S. Kramer. fl95g). Ethology, and innate behavior. Many of these (cited earlier) the comparative not think that therewas any fundamentalchange GenomeProject have made it more persuasive study of animal behavior.Quarterly defended the concept of instinct, but others built position Reviewof Biology33: l8l-211. in Lehrman'stheoretical between1953 than everto speakofbehavior as beinginnate or on Lehrman's arguments and developed his posi- Gottlieb, G. (1971). and 1970,but he provided additional examples geneticallyencoded, although Lehrman's argu_ Developmentof Speciesldentifica- tion further (Hinde 1966;Jensen 1961; Lehrman points tion in Birfu. Chicago:University press. to supporthis view and emphasizedsome mentsagainst such claims are as cogentnow as of Chicago 1956;Ross and Denenberg 1960;Schneirla 1956, paper. Gottlieb, G. (1991). that were only implicit in his earlier For theywere in 1953.However, as shown by thecon_ Experientialcanalization of behav_ 1966). The debate seemed, however, to engage a ioral development: example,he discussedthe problems that arise tributions to this volume, the progresi Theory. Developmentalpsychology rather limited group of writers, and the impact of of DST 27:4-13. when questions about developmentalmecha- during the sameperiod has also beenimpressive, his ideas was slow to be felt in the mainstream questions phe- Hebb, D. O. (1937).The innate organization nismsare confused with about the and it is to be hoped that more scientistsand of visual of research on comparative psychology and be- activity: I. Perceptionoffigures nomenaof adaptationto the environment.Both educatedlaypersons will be encouraged by rats reared in total havioral development. For example, none of the to use darkness.Journal ofGenetic psychology are entirely legitimatekinds of questionsabout this perspectivefor thinking about 5l: l0l_126. psychology that the develop eight chapters on comparative behavior,but they require differentmethods for mentof behavior. Hebb, D. O. (1953).Heredity and environmentin mammalian appeared in the Annual Review of Psychology their investigation;most importantly, a particu- behaviour. British Journal of Animal Be- haviourl:43-47. from 1953 to 1963 dealt seriously with the theo- lar answerto a questionin one domain doesnot Hess, retical issues he raised. There are also few empir- imply anythingabout answersto questionsin the References E. H. (1962).Ethology: An approachtoward the completeanalysis ical papers from this period that use Lehrman's other domain. "As I hope the discussionso far of behavior. New Directionsin p.rv_ Beach,F. A. (1951).Instinctive behavior: chologyl: 157-266. ideas as a framework for designing experiments has madeclear, I have not beentrying to avoid Reproductive activities.In S. S. Stevens(Ed.), Handbook-of Hinde, (1966). and interpreting data. An examination of the phylogenetic Experi_ R. A. Animal Behavior:A Synthesisof the conceptsof survival value and mental Psychology, pp. 3g7_434.New yoik: psychology four journals that published most of the research lotrn llholoSy and Comparative (lst ed.;. New adaptation,but only to preventthem from being Wiley& Sons. York: on animal behavior between 1954 and 1964 McGraw Hill. mergedwith the conceptsof thecausal analysis of B1agh,F. A. (1955). The descentof instinct.psychologi_ W. (1890).principles of psychology. york: (Animal Behaviour, Behaviour, the Journal of cal fames, New development"(Lehrman 1970:37; original em- Review62:401-410. Henry Holt. Comparative and Physiological Psychology, and phasis).The samedistinction had alsobeen made Beer, C. G. (1973).Species-typical behavior and ethol- Jensen,D. D. (1961). Zeitschrift fiir Tierpsychologie) found almost no Operationismand the question by Tinbergen(1963), who madeit clearthat these ogy. In D. A. Dewsbury and D. A. Rethlingshaver "Is this papers that draw on Lehrman's analysis in any behavior learned or innate?,' Behaviour 17: two kinds of questionsare entirely complemen- 1-8. substantive way. There are frequent citations of tary in the study of behavior. TimothYD. Johnston Toward a Systems View of Development 23 22

Anpassungund Thelen,E. (1995).Motor development Lorenz,K. Z. (1961).Phylogenetische A new synthe- (1937)'The persistenceof dichotomtes Johnston,T. D. Modifikation des Verhaltens' Zeitschrift filr sis.American Psychologist 50:. 79-95. of behavioraldevelopment' Developmental in it. rt.OV "J"pii*Tierpsychologre 18: I 39-l 87' Thelen,E., J. A. S. Kelso, and A. Fogel.(1987). Self- 149-182. Review7: (1965)' Evolution and Modifcation of organizing systems and infant motor development. (1964)' Parental Lorenz, K. Z. Klinghammer,E., and E' H' Hess' of ChicagoPress' DevelopmentalReview 7 : 39-65. innate Behavior.Chicago: University ring doves(strept opelin roseogrrsec): i.J;; in (1987)' Heredity/developmentin the Thorpe,W. H. (1961).Comparative psychology. ln- Tierpsychologie2l 338-347' Maienschein,J. ["*taf Zf,rtschrdiftir Historyand Philosophyof the nual Reviewof Psychology12: 27-50. ". psychology' Unit"a States,circa lg00' Z. Y. (1921).Giving up instinctsin Kuo, Life Sciencesg:79-93' Thorpe,W. H. (1963).Ethology and the codingprob- 18:645-664' Journalof PhitosoPhY Introductionto SocialPsychol' lem in germ cell and brain. Zeitschrift Tierpsy- acquired? McDougall, W. (1908)' fiir Y. (1922)' How are our instincts chologie20: 529-551. Kuo, Z. ogy. London: Methuen& Co' Review29 344-365' Psychological (1895)'An Introductionto Comparative Tinbergen,N. (1942).An objectivisticstudy on the in- heredity'Psy- Morgan, C. L. (1g24).Apsychology without nate behavior of animals. BibliothecaBiotheoretica Kuo,Z.Y. PsychologY.London: Walter Scott' l: Review3l 42"1-M8' 39-98. chological S' Lindee' (1995)' The DNA o-finstinc- Nelkin, D., and M' K. A. (1933)'Experimental New York: W' Tinbergen,N. (1951).The Study Lashley, il"l{:t Mystiqtue:The Geneas a Cultural lcon' of Instinct.Oxford: . isychological Review45: 445-4?1' Oxford University Press. ,iu" l"iluulot H. Freeman. of Konrad Lorenz's Lehrman,D. S. (1953)'A critique Ontogeny of Information: Tinbergen,N. (1955). Psychologyand ethology as of Biol- Oyama, S' (1985)' The behaviot' Quarterly Review Cambridge: supplementaryparts of a science ,fr""ty D'evelopmentalSystems and Evolution' of behavior. In B. "ii*tinctive33'7-363. Durham' NC: Schaffner(Ed.), Group Processes,pp. ogy 28 C"ttUtiOg. UniversityPress' (2d rev' ed" 75-167. New the organizationof mater- York: JosiahMacy Jr. Foundation. L"hrmun, D. S. (1956)' On Duke University Press,2000') instinct' In P' P' nut i.t unio, and the problem of Evolutionin Man' Tinbergen,N. (1963).On aims and methodsof ethol- ani' Romanes,G. J. (1888)' Mental L'Instinct dansle comportementdes Grass6(Ed.), Kegan Paul & Trench' ogy.Zeitschrift filr Tierpsychologie20: 4M-433. 471520' Paris:Masson' London: maux et de l'homme,pp' Innatebehav- Ross,S., and V. H' Denenberg'(1960)' (1957)'Nurture' nature' and ethology Lehrman,D. S. in its environment'In R' H' Waters' and instinct in iot, irt.'otgunism of W' H. Thorpe, "Learning W' E' Caldw-ell(Eds')' aReJe* Contem' p. e. Reihtingshaver,and CambridgeUniversity Press'1956)' pp' 43-73' New )oi*utr," Principlesof ComparativePsychology' porurYPsYchologY 2: 103-104' and ex- York: McGraw-Hill' D. S' (1962)'Interaction of hormonal in, the field Lehrman, Sapp,J. (1983).The strugglefor authority on developmentof behavior' In E' of perientialinfluences tgbo-ts:z: N& perspectiveson- the rise Behaviir: Genetics'.Instinct'and .ii"t"aliv, L. Bliss(Ed'), Rootsof the Historvof Biologv 16 311-342' pp' 142-156' New i"""ii"i. ii"r"al of Socirtlizationin Animal Behavior' psychological Schneirla,T. C. (1949)' Levels in the York: Hoeber. Sellars'V' J' McGill' issues ."p""ititt of animals' ln R' W' D. S. (1970)'Semantic and conceptual Future' pp' Lehrman, U. Farber (Eds.), Pirilosophyfor the problem' In L' R' Aronson' E' uni in the nature-nurturc New York: Macmillan' J' S' Rosenblatt(Eds')' 243-286. 'oin- Tobach,D. S. Lehrman,and of the pp' l7-50' San Schneirla,T. C. (1956)'Interrelationships irrrtop^rr, and Evolutionof Behavior' In the "acquired" in instinctive behavior' W. H. Freeman' nate" and Francisco: p. p. (Ed.), L'Instinct dansle comportementdes Uber Bildung des Grasre Lorenz, K. Z. (1937)' 9it pp' 387-452 Paris:Masson' 25 289-300' animauxet de I'homme, instintiUegri ffes. Naturwissenschaften developmentand as Lorenz (1957)'The Schneirla,T. C. (1966)' Behavioral lOz-:f t, s:z+-lZt. [Translated of Biology (Ed')' Instinctive psychology' Quarterly Review nature of instinct' In C' H' Schiller Concept' pp' "ornputuiiu.4l 283-302. Behavior: Developmentof a Modern Press'l (1987)'The develop- s.New York: InternationalUniversities Silver,R., and J. S' Rosenblatt' l2g-.l'l Lehrman' De- method in ment of a developmentalist:Daniel S' Lorenz, K. Z. (1950)' The comparative of the Psychobiology20 563-570' innate behaviour patterns' Symp^osin velopmental and "instinctive"func- "tOyitg Experimmtal Biology4:221-268' Stone,C. P. (1951)'Maturation Societyfor Psychology(3d theory of in- tions. In C. P' Stone(Ed'), Comparative Lorenz, K. Z. (1956)' The objectivistic dans le com' ed.),pp. 3G-61.New York: Prentice-Hall' stinct. in P. P. Grass6(Ed')' L'Instinct pp' 5l-76' Paris: portement desanimqux et de l'homme' Masson' ;:' #*";# a1 a A critique of KonradLorenzos Theory of InstinctiveBehavior i J .a::

Daniel S. Lehrman

Beginningabout 1931, Konrad Lorenz, with and ecologists, and partly through the recep_ his students and collaborators (notably N. tive audience provided for Lorenz and his col_ Tinbergen),has publishednumerous behavioral l._ugu., Tinbergen, by American ornithologists. and theoreticalpapers on problems of instinct The ornithologists were interested from the start, and innate behavior which have had a wide_ especially because a great part of the material on spread influence on many groups of scientific which Lorenzbased his system came from studies workers(Lorenz 193I, 1932,1935, 1937 Loter:z ; of bird behavior, but the range of interest in & Tinbergen1938; Lorenz 1939;Tinbergen 1939; America has widened considerably. Lorenz and Lorenz 1940,l94l; Tinbergen1942,194g,1950: his theories were recently the subject of some dis- Lorenz1950; Tinbergen l95l). Lorenz,sinfluence cussion at a conference in New york at which is indicatedin the founding of the Zeitschrift fiir zoologists and comparative psychologists were Tierpsychologiein 1937and in its subsequent de_ both represented (Riess 1949), and are promi_ velopment,and also in the journal Behaviour, nently represented in the recent symposium on establishedin 1948 under the editorship of an animal behavior of the Society of Experimental internationalboard headedby Tinbergen. Biologists (Armstrong 1950; Baerends 1950; Lorenz's theory of instinctive and innate Hartley 1950; Koehler 1950; Lorenz 1950; behaviorhas attracted the interest of many in_ Tinbergen 1950), and extensively used in several vestigators,partly becauseof its diagrammatic chapters of a recent American handbook of ex_ simplicity, partly becauseof its extensive use of perimental psychology which will be a standard neurophysiologicalconcepts, and partly because sourcebook for some years to come (Beach Lorcru deals l95l; with behaviorpatterns drawn from Miller l95l; Nissen l95l). thelife cycleof the animalsdiscussed, rather than Because Lorenz's ideas have gained wide atten_ with the laboratory situationsmost often found tion, and in particular because a critical dis- in Americancomparative psychology. These fac- cussion [337-338] of these matters should bring torsgo far toward accountingfor the great atten_ usefully into review Lorenz's manner of dealing tion paid to the theory in Europe, where most with basic problems in the comparative study of studentsof animal behaviorare zoologists,phys_ behavior, a consideration of Lorenz's system and iologists,zoo curators or naturalists, unlike the school seemsvery desirable at this time. psychologistswho constitute the majority of Americanstudents (Schneirla of animal behavior [Editor's Note: ln the section 1946a). omitted here pp. 338-340) Lehrman uses egg-rolling behavior in In recentyears Lorenz,s theories have attracted the gray goose to illustrate some of the features of more and more attention in the United States a classically defined "instinctive,' behavior. When as well, partly becauseof a developing interest a goose seesan egg that has rolled out ofits nest, in animal behavior among American zoologists it stands up, reaches out with its neck so that its bill is hooked over the far side of the egg, and pulls the egg back into the Tft;.RuR". appearedin the nest, using side_to_side -o.iginally euarterlyReview movements of Biology28: 337-363(1953). page bieaks und o-ir_ of its bill to prevent the egg from sions rolling areindicated in the_textas (e.g.) [337_33g]. Only away. This example illustrates appetitive thosereferences citedin theexcerptiieirintea here are b.ehavior-stretching the neck out toward ihe egg; included in the references. The referencrs have been the instinctiye act or consummatory behavior_the reformatted in the style of other contributions to this highly stereotyped movement volume, and a few errors have been corrected. of the bill that pulls Lehrman Theory 26 Daniel S. Lorenz's of InstinctiveBehavior 27

(1942), closely following Lorenz, Pecking in the Chick the egg back toward the nest; the innate releasing Tinbergen acter from that suggested by the concept of a appearance of speaks of instinctive acts as "highly stereo- unitary, innate item of pattern (or simply releaser)-the Domestic chicks behavior. Kuo,s observa- the neuromotor characteristically begin to peck outside the nest and the hard feeling of typed, coordinated movements, tions strongly suggest several interpretations itt" .gg at objects, including food grains, soon after of elicit the apparatus of which belongs, in its complete the development the egg against the bill, which together (Shepard of pecking (which, of course, are of the ani- hatching and Breed l9l3; Bird 1925; movement by triggering an innate form, to the hereditary constitution subject to further clarification). For example, instinctive Crve 1935; and others). The pecking behavior the ot orienting mal." Lorenz (1939) speaks of characteristics of head-lunge arises from releasing mechanism; and the taxis, of at least the passive head-bending o'hereditary, individually consists three highly stereotyped com- side-to-side adjustment of the behavior which are which occurs contiguously with tactual stimula_ movement-the ponents: head lunging, bill opening and closing, the egg from fixed, and thus open to evolutionary analysis." tion of the head while position of the bill that prevents and swallowing. the nervous control of the perceptual patterns They are ordinarily coordinated Lorer:z (1935) also refers to muscles is being established. By the time of hatch- rolling away.l into a single resultant act of lunging at the grain ("releasers") which are presumed to be innate ing, head-lunging opening in response to tactual stimula_ thefirst while the bill, followed by swallowing because they elicit "instinctive" behavior tion is very well established (in fact, it plays ... [338-340] when the grain is picked up. This coordination a time they are presented to the animal. He also major role in the hatching is present to some process). patterns as innate which extent soon after hatching, refers to those motor The genesis of headlunging to visual stim- Theories and improves later (even, to a slight extent, if the Problems Raised by Instinct occur for the first time when the proper stim- ulation in the chick has chick is prevented from practicing). not been analyzed. In student Grohmann uli are presented. Lorenz's Amblystoma, however, Coghill (1929) has shown to light several This pecking is stereotyped, characteristic of Even this brief summary brings (1938), as well as Tinbergen and Kuenen (1939)' that a closely analogous the species, appears shift from tactual to which ought to be critically examined determined in isolated chicks, is present questions speak of behavior as being innately visual control is a consequence of the establish- are questions, at the time of hatching, and shows some improve- with reference to the theory. These because it matures instead of developing through ment of certain anatomical ment in the relationships between which apply to instinct theories in absence of specific practice. Obvi- furthermore, learning. the optic nerve and the brain region which earlier (1) problem of ously, it qualifies as an "innate" behavior, in the general. Among them are: the It is thus apparent that Lorenz and Tinbergen, mediated the lunging senseused by Lorenz response to tactual stim_ "innateness" and the maturation of behavior; behavior which is and Tinbergen. by "innate" behavior, mean ulation, so that visual stimuli come to elicit re- in an Kuo (1932a-d) has studied the embryonic (2) the problem of levels of organization hereditarily determined, which is part of the orig- sponses established development of during a period of purely (3) the nature of evolutionary levels of which arises quite the chick in a way which throws organism; inal constitution of the animal, ,.innate', tactual sensitivity. If a similar situation obtains the use of the com- considerable light on the origin of this behavioral organization, and independently of the animal's experience and en- in the chick, we would behavior. As early be dealing with a case of parative method in studying them; and (4) the distinct from acquired as three days of embryonic vironment, and which is intersensory equivalence, in which visual stim- concepts may be age, the neck is passively bent when the heart- manner in which physiological or learned behavior. uli, because of the anatomical beat causesthe head (which relationships be- properly used in behavior analysis' There follows or implicitly, that rests on the thorax) to It is also apparent, explicitly tween the visual and tactual regions of the brain, theory in rise and fall. The head is stimulated tactually [340-341] an evaluation of Lorenz's Lorenz and Tinbergen regard as the major crite- became equivalent by the yolk sac, to tactual stimuli, which in of these general (1) the behavior be stereo- which is moved mechanically terms Problems. na of innateness that: turn became effective through an already ana- by amnion contractions synchronized with the typed and constant in form; (2) it be characteris- lyzed process of development, heartbeats which cause which involved of Behavior (3) it appear in animals which head movement. Begin- "Innateness'o tic of the species; conditioning at a very early age (Maier and ning about one day later, the head first bends have been raised in isolation from others; and (4) Schneirla 1935). actively in response Problem in animals which have to tactual stimulation. At The it develop fully formed The originally diffuse connection between about this time, too, the bill begins to open and been prevented from practicing it. head-lunge consistently speak of and bill-opening appears to be Lorenz and Tinbergen patterns close when the bird nods-according to Kuo, Undoubtedly, there are behavior strengthened by the repeated as being "innate" or "inherited" as apparently through elicitation of lung- behavior Even so, this does not nervous excitation furnished which meet these criteria. ing and billing by tactual stimulation by the yolk though these words surely referred to a definable, by the head movements through irradiation in necessarily imply that Lorenz's interpretation of sac. The repeated delimited category of behavior' It the still-incomplete elicitation of swallowing by the definite. and "innate" offers genuine nervous system. Bill-opening these behavior patterns as pressure of amniotic fluid following bill-opening would be impossible to overestimate the heuristic and closing become independent of head-activity aid to a scientific understanding of their origin probably is important which they imply for the concepts "innate" only somewhat later. in the establishment of value underlying them. After about 8 or 9 days, and of the mechanisms the post-hatching integration of bill-opening and and "not-innate." Perhaps the most effective way fluid forced into the throat by the bill and head In order to examine the soundness of the con- swallowing. to throw light on the "instinct" problem is to movements causes swallowing. On cept of "innateness" in the analysis of behavior, it the twelfth consider carefully just what it means to say that day, bill-opening always follows head-movement. will be instructive to start with a consideration of Maternal Behavior in the Rat a mode of behavior is innate, and how much I34t-3421 one or two behavior patterns which have already insight this kind of statement gives into the origin In the light of Kuo's studies the .,innateness" Another example of behavior appearing to fulfill been analyzed to some extent. and nature of the behavior. of the chick's pecking takes on a different char- the criteria of "innateness" may be found in the maternal behavior of the rat. il-s :.J. Daniel S. Lehrman Lorenz'sTheory of InstinctiveBehavior 29 28

instead of concentrated nest-building and retrieving in the rat are not example, when he says(1942) of certain by piling up any part of the female o'learned" behavior Pregnantfemale rats build nests rats' and that behavior. They fulfil all criteria of patterns of ,,The will p"l,'J.i"tfv as with normal mother the three-spined stickleback: or other material' Mother rats "innateness," i.e., of behavior ,tip."oipuper retrievingdoes not occur' which develops releasing mechanisms of these reactions are all p.,pt to the nestby picking them "reirievei' ih.i. raisesome questions con- without opportunity for practice or imitation. innate. A male that was reared in isolation ... them back to the These-considerations l" ,n" mouth and carrying of nest-building Yet, in each case, analysis of the developmental was tested with models occur cerningnativistic interpretations before it had ever seen "p Nest-building and retrieving both the process involved shows that the nest. unJ ,J,ti"uing in the rat, and concerning behavior pat- another stickleback. The . .. [stimuli] . . . had the they occur in rats which have in all normal rats; of the criteria of "innateness'"To begin terns concerned are not unitary, autonomously same releaser functions as in the experiments and they occur with no meu.ring l."n tuit.O in isolation; that practicein carrying food developing things, but rather that they emerge with normal males." Such isolation is by no sincebothare per- *Ji, i,it apparent evidenceofprevious practice, for the development ontogenetically in complex ways from the previ- means a final or may p"ffti, is partty equivalent, complete control on possible well by primiparousrats (retnevlng in car- ously developed organization .,iso- formed if nest-buildingand retrieving,to practice of the organism in effects from experience. For example, is the foi tit" first time only a few minutes young' a given setting. iut. ptu". nesting-material,and in carrying-the lated" fish uninfluenced by its own reflection first litter of a rat raised rying after the birth of the that nest-buildingactiv- What, then is wrong with the implication of the from a water film or glass wall? Is therefore riiJ.t Qgfr)has shown the animal's isolation). Both behavior patterns environ- "isolation experiment," that behavior in iri pqZ-lqzl is inverselycorrelated with developed experience with human handlers, food objects, satisfy the criteria of "innateness" in isolation may upp.- to temperature,and that it can be stopped be considered "innate" if the ani- etc., really irrelevant? 1933)' mental (Wiesner' and Sheard temperature sufficiently' This mal did not practice it specifically? Similarly, Howells and Vine (1940) have re- raisedrats in iso- by raising the Ri"r, (pers.com.), however, experiment' sug- Lorenz repeatedly refers to behavior as being ported that chicks from finding, together with Riess's raised in mixed flocks of two at the sametime preventingthem from innate because it is displayed lation, g"tit it ihe nest-buildingactivity arises by animals raised varieties, when tested in aY-mazq learn to go to carrying any objects'The ever manipulating or ", (and other object) manipulation in isolation. The raising of rats in isolation, and chicks of their own variety more readily so that feces i.Air,uty food than floor of thi living cagewas of netting where the accu- their subsequent testing for nesting behavior, to those pow- and coliectionunder conditions of the other variety. They concluded down out of reach' All food was mate- is typical of isolation dropped -rrtu,ion of certain types of manipulated experiments. The devel- that the "learning is acceleratedor retarded ... the rats nevercarried food pellets' a.rei, so that to immediaiesatisfaction of one of the opment of the chick inside the egg might be re- because of the directive influence of innate fac- were placed in regular rial leads When mature, theserats The fact that the rat garded as the ideal isolation experiment. tors." In this case, (1946b) nor- animal's needs(warmth)' Schneirla suggeststhat cages.They bred,but did not build It must breeding generallymore active at lower temperatures be realized that an animal raised in the efect of the chick's experience with its own their young normally' They is mal neslsoi retrieve Morgan 194'l\also contributes isolation from fellow-members of his species is chirping during feeding has not been adequately the floor of the l-g;o**un 1943; scatterednesting material all over activity will not necessarily isolated the of pro- place io ,tt" probability thai nest-building from ffict considered as a source of differential learning pre- und similJrly moved the young from to cessesand events which O.".fop. In addition' the rat normally.tends contribute to the devel- vious to the experiment. This criticism may also "ugs,,o!iu". without collectingthem at a-nest-place' thus to opment of any particular behavior pattern. stay cl,oseto the walls of its cage' and The im- be made of a similar study by Schoolland (1942) do a greatdeal of licking of their iemale rats time in corners'This facilitatesthe portant question is not "Is the animal isolated?" using chicks and ducklings. during pregnancy ,p.tO much own genitalia, particularly into one corner of but "From what is the animal isolated?" The iso- Even lick- cottectionof nestingmaterial more fundamental is the question of (Wi.ri., and Sheard1933)' This increased young to lation experiment, cage,and the later retrievingof the if the conditions are well ana- what [343-344] is meant by "maturation.,,We has severalprobable bases' the ing during pregnancy and Laughlin (1934) have lyzed, provides at best a negative indication that may ask whether experiments is not yet that c'orner.Patrick based on the the relative importance of which without certain specified environmental factors probably tfto*n that rats raisedin an environment assumption of an absolute dichotomy between increasedneed of the pregnant rat known. The do not developthis "universal" ten- are not directly involved in the genesis of a par- maturation and learning ever really tell us what and Schmidt 1938) opuquawalls ior salts (Heppel to the wall' Birch's ticular behavior. However, the isolation experi- is maturing, fotu.ti"m lick- dency of rats to walk close or how it is maturing? When the probably accountsin part for the increased in ment by its very nature experimentsuggests that the rat's experience does not give a positive question is examined in terms of developmental body fluids as doesthe. increased itg th" ,alty genitaliahelps to establishretriev' indication that behavior is "innate" or indeed any processesand relationships, rather than "f themselves'Birch licking its own in terms irituUitity of the genitalorgans young' as doesits experi- information at all about what the process of of preconceived licking ing as a responseto the categories, the maturation- (pers.com.) has suggested thatthis.genital material' development of the behavior really consisted of in carryingfood and nesting of. versus-learning formulation of the problem is impo,ii"t role in the development The may ptay un "n".. example of the nest-building and retrieving more or less dissipated. For example, in the retrievingof the young' He is raising or Development? by li"kilg and Maturation'vs.'Leatrtng, rats which are isolated from other rats but not rat nest-building probably does not mature eatly agewith collars femal! rats fitted from an from their food pellets or from their own geni- autonomously-and rat is effec- ExPetiment it is not learned. It is not madeof rubberdiscs, so worn that the The Isolation talia illustrates the danger somesecond.thoughts on of assuming "innate- "nest-building" which is learned. Nest-building preventedfrom licking its genitalia'Present Thesestudies suggest ness" tively experiment'" It is merely because a particular hypothesis develops in certain situations through a develop- on limited data' are that rats the nature of the "isolation indicaiions, based and about learning seems to be disproved. This is mental process in which at each stage of their young' obvious that by the criteria usedby Lorenz there is an so raised eat a high percentage what is consistently done by Tinbergen, as, for identifiable under theorists,pecking in the chick and interaction between the environment that the young inlhe nest may be found other instinct Daniel S. Lehrman Theory of InstinctiveBehavior 30 Lorenz's 3l

only from componentto componentof formsof learningdo not influenceit, and that must underlie the notion that some and organic processes, and within the organism; differ,not ous behavior pat- pattern,but alsofrom developmentalstage to thereforedo not considerit neces- terns are "inherited" as such. this interaction is based on the preceding stage the we [344-345l stage.What is requiredis a con- saryto investigateits ontogenyfurther. The "instinct" is obviously not present of development and gives rise to the succeeding developmental in the present from the tinuation of the carefulanalysis of the character- zygote. Just as obviously, it is present in the stage. These interactions are H eredity-vs.- Environment, or Development? developmentalstage, and of the behavior of the animal after earliest (zygote) stage' Learning may emerge as istics of each the appropriate age. eachstage to the next. The problem for the investigator a factor in the animal's behavior even at early transition from Much the samekind of problem ariseswhen we who wishes to the heuristicvalue of make a causal analysis embryonic stages, as pointed out by Carmichael Our scepticismregarding considerthe questionof what is "inherited."It is of behavior is: How did (1e36). the conceptof "maturation" shouldnot be inter- characteristicof Lorenz. as of instinct theorists this behavior come about? The use of "explana- the fact that the tory" 'oinnate" Peckingin the chick is also an emergent-an pretedas ignoranceor denial of in general,that "instinctive acts" are regarded categories such as and "genically plays an im- integrationof head,bill, and throat components' physicalgrowth of varied structures by him as "inherited." Furthermore, inherited fixed" obscures the necessity of investigating de- of most of the velopmental eachof which hasits own developmentalhistory' portant role in the development behavior is regarded as sharply distinct from processes in order to gain insight discussionin into This integration is already partially established kinds of behavior patterns under behavioracquired through "experience." Lorenz the actual mechanisms of behavior and their is to the inter- by the time of hatching,providing a clear exam- the presentpaper. Our objection (1937) refers to behavior which develops "en- inter-relations. The problem of development is growth that is implied problem ple of "innate" behavior in which the statement pretationof the role of this tirely independentof all experience." the of the development of new strucrures (or a specificphys' and l'It is innate" adds nothing to an understand- in the notion that the behavior It hasbecome customary, in recentdiscussions activity patterns from the resolution of the "maturing." For ing of the developmentalprocess involved' The iological substrate for it) is of the "heredity-environment"problem, to state interaction of existing structures and patterns, improvementin peck- within the statementthat "pecking" is innate, or that it example,the post-hatching that the "hereditary" and "environmental" con- organism and its internal environment, in part o'matures,"leads us away from any attempt to ing ability of chicksis very probably due tributions are both essentialto the development and between the organism and its outer environ- leg musclesand analyzeits specificorigins. The assumptionthat to an increasein strengthof the of the organism; that the organism could not ment. At any stage of development, the new fea- of the pecking grows as a peckingpattern discourages to an increasein balance and stability developin the absenceof either; and that the tures emerge from the interactions within the partly from this Lxaminationof the embryologicalprocesses lead- standing chick, which results dichotomyis more or lessartificial. (This formu- current stage and between the current stage and partly from the ing to pecking. The elementsout of whose in- strengtheningof the legs and lation, however, frequently servesas an intro- the environment. The interaction out of which responses(Cruze the teraction pecking emergesare not originally a developmentof equilibrium duction to elaborateattempts to evaluatewhat organism develops is not one, as is so often prevention-of-practice unitary pattern; they becomerelated as a con- 1935).Now, isolation or part, or even what percentage,of behavior is said, between heredity and environment. It is conclusion that sequenceof their positions in the organization experimentswould lead to the geneticallydetermined and what part acquired between organism and environment! And the was due to "matu- of the embryonicchick. The understandingpro- this part of the improvement [Howells 1945; Beach 1947; Carmichael 1947: organism is different at each different stage of its partly to growth vided by Kuo's observationsowes nothing to the ration." Of course it is due Stone 1947].)Lorenz does not make even this development. peckingabil' "maturation-versus-learning"formulation. processes,but what is growingis not much of a concessionto the necessityof develop- Modern physiological and biochemical genet- receptors Observationssuch as thesesuggest many new ilH just as, when the skin temperature mental analysis.He simply statesthat some be- ics is fast destroying the conception of a straight- is not nest- problemsthe relevanceof which is not apparent of the rat develop,what is growing havior patternsare "inherited," others"acquired line relationship between gene and somatic with the patterns are nativistically interpreted' building activity, or anything isomorphic by individual experience."I do not know of any characteristic. For example, certain strains of when oodwarf." For example,what is the nature of the rat's it. The use of the categories"maturation-vs'- statementof either Lorerz or Tinbergenwhich mice contain a mutant gene called Mice usually gives a temperature-sensitivitywhich enablesits nest- learning" as explanatory aids would allow the reader to conclude that they homozygous for "dwarf" are smaller than nor- directednessin building to vary with temperature?How doesthe false impression of unity and haveany doubts about the correctnessof refer- mal mice. It has been shown (Smith and pattern, when actu- animal developits ability to handle food in spe- the growth of the behavior ring to behavior as simply "inherited" or "geni- MacDowell 1930; Keeler 1931) that the cause of primarily unitary, cific ways? What are the physiological condi- ally the behaviorpattern is not callycontrolled." this dwarfism is a deficiency of pituitary growth in a straight line tions which promotelicking of the genitalia,etc'? nor doesdevelopment proceed Now, what exactly is meant by the statement hormone secretion. Now what are we to regard pattern. We want to know much more about the course toward the completionof the that a behavior pattern is "inherited" or "geni- as "inherited"? Shall we change the name of the concept of *dwarf" of establishmentof the connectionsbetween the It is apparent that the use of the cally controlled"?Lorenz undoubtedlydoes not mutation from to "pituitary dysfunc- as well chick'shead-lunge and bill-opening,and between "maturation" by Lorenz and Tinbergen think that the zygotecontains the instinctiveact tion" and say that dwarfism is not inherited as as it at first bill-openingand swallowing.This doeszol mean as by many other workers is not, in miniature,or that the geneis the equivalentof such-that what is inherited is a hypoactive pitu- development that we expectto establishwhich of the compo- appears,a referenceto a procrssof an entelechywhich purposefully and continu- itary gland? This would merely push the problem of develop- nents is learned and which matured, or "how but rather to ignoring the process ouslytries to pushthe organism'sdevelopment in back to an earlier stage of development. We now developsby much" each is learnedand how much matured' ment. To say of a behavior that it a particular direction. Yet one or both of these have a better understanding of the origin of the that the obvi- The effectsof learning and of structural factors maturationis tantamountto saying preformistic assumptions,or their equivalents, dwarfism than we did when we could only say it Daniel S. Lehrman #- Lorenz'sTheory of InstinctiveBehavior 32 t aa JJ

Mayr 1945; determined."Howevbl, the pituitary fluencedby him (Delacour and object in which to deposit its eggsis actually a higher (phylogenetic) is "genically developmentof the one makes turn, in the context of the Adriaanse 1947; Baerends and Baerends-van consequenceof the fact that the fly lawa the other superfluous function developed,in wasfed and stops its development.The Roon 1950).This type of analysisderives from on the larvaeof the flour moth reaching mouseas it was when the gland was developing' while it wasdevel_ of a higherpsychic performance goes hand-in_ work on the taxonomicrelations of behav- oping. By raising Nemerites hand with The problem is: What was that context and how earlier larvae upon the lar_ a reduction of the automatisirs that take (1898,l9l9), Heinroth vae of other kinds part in the action, did the gland develoPout of it? ior patternsby Whitman of moth Thorpe and Jones leavinga behaviorpattern with the (1926),and others' them, same function as the What, then, is inherited?From a somewhat (1910,1930), Petrunkevitsch caused when adult, to choosepreponder_ one originally eiisting. (Lorenz to the taxonomic antly these te37) similar argument, Jennings (1930) and Chein Lorenz's brilliant approach other moths on which to lav their characteristicshas had wide eggs.The choice (1936)concluded that only the zygote is inher- analysisof behavior of flour-moth larvaefor oviposi_ Again: a very stimulating tion is quite ited, or that heredity is only a stage of devel- influence since it provides characteristicof Nemeritesinnature. in which to study speciesdifferences In view of Thorpe It is a peculiarity opment. There is no point here in involving framework and Jones' work, it would of many behaviorpatterns of higher of behavior' obviouslybe animals, that ourselvesin tautological argumentsover the de- and the specific characteristics improper to concludefrom this fact innate instinctiveelemenls and individualty_ follow from the that the choice acquiredelements immediately finition of heredity. It is clear, however,that to However,it doesnot necessarily is basedon innately_determined follow eachother, within patterns are species-specific stimuli. Yet, a functionally unitary chain say a behavior pattern is "inherited" thtows no fact that behavior before their paper was published, of acts . .. I have charac_ patterns.We may em- the species-specific terized this phenomenonas instinct_training light on its developmentexcept for the purely neg- that they are "innate" as character of the behavior interlace_ ment. Similar interlacementsoccur typesof learning are phasizeagain that the systematicstability of a would have beenjust as impressiveevidence betweeninstinctive ative implication that certain for acts and intelligent or characteristicdoes not indicate anything about "innateness"as species-specificity insightful behavior.. . . The not directly involved. Dwarfism in thE mouse, ever is. essen@of suchan The fact that a charac- Taxonomic interlacementis that, within a chain nest-buildingin the rat, peckingin the chick, and its mode of development. analysis,while very important, is of innate instinctive not actsthere is a definitepoint, which of the stickleback's teristic is a good taxonomic characterdoes not a substitutefor concreteanalysis oi th. point is innately the"ng-zagt345-346ldance" on,o- determined,where a learned act is in meanthat it developedautonomously' The shape genyofthe givenbehavior, inserted. This courtship (Tinbergen1942) arc all "inherited" as a sourceofinfor- learned act must be acquired by each in rodents, which is a good mationabout its individual the senseand by the criteria usedby Lorenz' But of the skull bones origin and organization. in the courseof its ontogeneticdevetopment. (Romer 1945),depends in In such a case, they are not by any meansphenomena of a com- taxonomic character the chain of innate acts has a gap, rn presenceof attached muscles Levelsof Organization which, insteadof an instinctive mon type, nor do they arise through the same part upon the act, there is a,capacity concludethat be- to acquire'.(Lorenz 1937) kinds of developmentalprocesses. To lump them (Washburn 1947).We cannot [All emphasesare Lorenz,s.] or causea behavior pattern is taxonomicallystable Levelsofulnnatenessu together under the rubric of "inherited" It is apparent that Lorenz in a unitary, independentway' regards differences "innate" characteristicsserves to block the inves- it must develop in the Animals at different evolutionary extent to which learning-occurs as repre_ just at the point where In addition it would be well to keep in mind levels show tigation of their origin characteristicdiferences senting differences in the size of (Ana- that the species-characteristicnature of many in the exient and man- the gaps in the it should leap forward in meaningfulness. ner chain of innate behavior. partly from the fact of learning.In addition, within the sameani- He consideri any giuen Foley 1948,considering data from the behaviorpatterns may result "component" .,innate,, stasi and mal'sbehavior diferent activities of behavior as havebeen that all membersof the speciesgrow in the same may be more or or not field of human differentialpsychology, Iesssusceptible "innate." This is entirely and Guthrie (1921)call such to the influenceof learning,and consistent with his led to somewhat the same formulation of the environment.Smith virtual ..innate', ,,autono_ may be affectedin different ways identification of with problem as is presented behavior elements"coenotropes." Further, it is by learning "heredity-environment" (Schneirla1948, l94g\. mously developing.', not at all necessarythat thesecommon features here.) explains However, we have already of the environmentbe thosewhich seema priori .Lorenz these facts in terms of the tried to make it richnessof the animal's clear that behavior patterns classified .,innate,, to be relevant to the behavior pattern under instinctiveequipment. As as Taxonomy and OntogenY described by any criterion assumption(e.g', 1935) above,his conceptionis that instinctive do not all fall into the same cat_ study.Lorenz's frequent egory [34G34n behavior is sharply with respect to embryonic origin, develop_ pointed out the that the effectivenessof a given stimulus on first diferent from ail Lorenz (1939) has very ably behaviorleading mental history, or level of demonstratesan innate sensoryme' up to thi performanceof the organizaTion. Lorenz potential importanceof behaviorelements as tax- presentation notes that based nstrnct.This "appetitive,,behavior more or fewer of the components of He has stressedthe fact chanism specificfor that stimulus is not is conceived ,,innate.', onomic characteristics. of as the sole evolutionary behavior may be But just on analysis of the origin of the stimulus- sourceof all learned nowhere does he that evolutionaryrelationships are expressed andintelligent recognize that one component but merelyon the fact that Loretu behavior.Thus he says: may be more or as clearly (in many casesmore clearly) by simi- effectiveness, less "innate," to the or',innate,'in one or another man_ by the more haseliminated the major alternative&e sees appetitive behavior, ,variable, laritiesand diferencesin behavioras as the sole root of all We may call attention explanation' ryer. to an important dif_ commonly used physical characteristics'Lorenz nativistic not only is physiologicattyrom"tt ingluoau_ ference between that the mentallyl1nTi:" the pecking of the chick anO the a taxonomicanalysis of a fam- Thorpe and Jones(1937) have shown different from the automatism himself has made of iristinctive nest-building of the rat, both behavior innatechoice of the larvaeof the flour behavior,but ... the two diferent patterns ily of birds in these terms (Lorenz 1941),and apparently 'substitutes' pro..r* ufp"u. which develop at (vikariierend) without specific practice of the by investigatorsin- moth by the ichneumon fly Nemerites as for each otte., in iilat tfre", others have been made patterns: A major part of 'i the learning which .:-i :! ..t r Lorenz's Theory of Instinctive Behavior 35 S. Lehrman fr Daniel !i 34 x;;,

lump- translated"without steps" or "without levels." gen as evidenceof the accumulationof reaction- of concept of "innate" behavior represents a appearsto be antecedentto the emergence This is a gratuitousand very misleadingoversim- specificenergy in the instinctive center until it of many different kinds and levels chick occurs before hatching' ing-together from its way through the inhibiting innate p."ting in the essentially pheno- plification on Lorenz's part. The transition "forces" is antecedentto oiU"ti*iot on the basis of an while much of the learningwhich pre- protozoato man is zof "stepless."There arechar' releasingmechanism and "goesoff" without any typic classification, and the imposition of the emergenceof nest-buildingin the rat occurs acteristicstructural differencesbetween phyletic detectableexternal stimulus. conceived categories upon that classiflcation' after birth. levels,and these differencesare responsiblefor Lees(1949) has cited the exampleof the cycli- Shall we call thosebehavior patterns "innate" characteristrcdifferences in the organization of cal colony activitiesof the ant Eciton hamatum which EvolutionarY Levels which developbefore birth and not those behavior.A protozoan is not like a simplerman. (Schneirla 1938) as an example of "something fruitlessin view of Jeuelopafteri This would be of It is a different kind of organism,with behavior akin to'vacuumactivity."'Colonies of this army Since Lorenz does not discuss the existence the demonstratedexistence of prenatalcondition- which dependsin different wayson its structure. ant pass regularly through statary and nomadic qualitative differences with respect to modes i"g 1932;Gos1933;Spelt 1948;Hunt 1949)' The analysisof behavior mechanismsat differ- phases, each lasting about 20 days. As Lees GuV development within his category of in view of the problem of of 1:+Z-f+Sl (Schneirla that it is fre- points out on Schneirla's(1944) descrip arid'unsatisfactory surprising that his ent levels 1946b)shows [based "maturation" of various "innate" behavior it is not the so-calledpostnatal lacks any quently misleadingto speakof behaviorpatterns tionl: (Grohmann 1938)' conception of the evolution of behavior "innate" behavior patterns at or elementsas homologouswhen they seemto notion of qualitative change. Lorenzmalntalns During the stataryphase the bivouac,to which the But we must recognizethat different behavior servesimilar (or the "same") functions and have all levels a sharp distinction between "instinctive single queen is confined, remains in situ and raiding patternsmay involvelearning at differentontoge- superficiallysimilar characteristics.Analysis of and "appititive behavior" (which includes activities are minimal. During the nomadic phase the to different extents,and in different acts" out of which the specific netic stages and variable types of structuralorganizations position of the bivouac is changed each nightfall and lessof the behaviorof all oriented, goal-directed, *uyt. eo-t example,much behavior patterns emerge shows that similar strong raiding parties emergefrom the colony. This of the specific- behavior at all levels). He saYs: the rat is directly a consequence behaviors at different phyletic levels often are activity is in no way related to the abundance or than in the caseof of cor- characteristicsof its structure If we consider the unbroken seriesof forms end-productsof evolutionaryselection leading to scarcityof food in the neighborhood. 1935)'The in a the earthworm (Maier and Schneirla responding modes of behavior, which extends the similar behavior,but deriving from different of must This cyclic behavior thus appears to Lees to involvementof learning in the development smloth progressionfrom protozoa to man' we structuresso that the underlying processesand at taxis' on in that the rat's behavioris differentfrom and occurs determinethat we cannot distinguishbetween mechanismsare not the same. have the character ofa "vacuum activity," guidedby the different developmentalstages from that of the the one hand, and, on the other,behavior Lorenz's application of the conceptof evolu- it occurs periodically without any noticeable We cannot here distin- Further, someresponses of the rat (suchas simplestintelligence (Einsicht)' not of analyzingthe change in the external stimulus-conditions. This chick. our frog' an tionary changedoes consist are very much lesssub- guish between taxis and, in the case of is very misleading, for Schneirla's (1938, 1944) licking of a painful spot) speak- differentways in which behaviorpatterns at dif- as intelligence which might (anthropomorphically analysis of this behavior has shown that the ject tJ changeby learning than others'-such 'There fly'' ferent evolutionary levels depend on the struc- ing) b-elimited to the knowledge: sits the young (Sperry1945; Uyldert These change from statary to nomadic behavior is a careof 19-46)' (Lorenz1937) ture and life of the organism.It consistsrather are nol differencesin the numberof behavioral of abstractingaspects of behavior,reifying them consequence of the growth of a great new brood in the the callow workers emerge from elementswhich are "innate," but rather This is restated in a later paper (Lorenz 1939): as specific autonomous mechanisms,and then of ants. When in the sim- cocoons, their movements stimulate the way in which the structuresare involved "No sharp line can be drawn between the citing them as demonstrationsof "evolution" in their great callows developmentof behavior at different evolution- plest orienting-reaction and the highest'insight- a purely descriptivetaxonomic sense.Taxonom- adult workers to activity. As the dependent on the adults, ary levelsand for differentbehavior patterns' ful'behavior." ically, this procedureis often extremelyvaluable, mature and cease to be levels can At this point, Lorenz doesnot fully utilize the idea of It might be pointed out that whether we but by its implicit assumptionthat "elements" their enereizing effect is lessened. because of wriggling larvae from the eggs of organizationof behavior, apparently distinguish uuriout levels of behavioral organiza' of behavior maintain their nature regardlessof the emergence result of the diminishing activating effect of his cJncept of "innateness"is not the tion dipends in part on our assiduity in attempt- change in the organization in which they are supplements it is in the adults. When the larvae analysisoi th. developmentof behavior; ing to distinguish them. Preconceptions about embedded(more properly, we should say from the callows on the behav- pupate, become inactive, the adults are no putt',tt. result of a pi""on"tption that "innate" nrimber and kind of categories into which which they emerge),it hindersrather than helps and into (Wheeler 1928) and "not-innate" are the two categories ior ought to fall naturally has an important effect analysisof the behaviorpatterns themselves. longer subject to trophallactic the colony changes to its statary which behavior logically falls' Consequently on the kind of examination we make of behavior stimulation, and classifiedbehavior as we find our- period. Lorcnzand his schoolhave patterns and the kinds of distinctions .. . [348-3s8] of crite- point is relevant to our discussion is "innate" and "not-innate" on the basis selves able to make among them' The that to be nYacuum leads to a conception ria which when carefully examinedappear In the quotation above we have translated Acrtvilies' that Schneirla's analysis category of "innate" therefore (progression) Lorenz's word that is the opposite of that implied by the notion arbitrary. Their as "smootho' The so-called'ovacuum activities" or Leerlauf- kinds of behavior' which might be more literally of "vacuum activity." The periodic recurrences includesvery different "stufenlose," which i reaktionenare regardedby Lorenz and Tinber- involvelearning in many diferent ways' Lorenz's I ! tFf, 36 Daniel s. Lehrman il Lorenz'sTheory of InstinctiveBehavior 37

the result of the building up of energyin much attention to criticism of the paper at vari- Carmichael, arenot Conclusion L. (1936).A re-evaluationof the concepts the result ous stages. of any animal'snervous system. They are maturation and learning as applied to the eaily periodic recurrencesof inter-individual The following peoplealso haveread the paper, development of behavior. psychiigical of the We havesummarized the main points of Lorenz's . Review 43: The behavior is not repre- in part and at various stages,and have 45V470. stimulating effects. instinct theory, and havesubjected it to a critical made of the animalsin the manyhelpful suggestionsand comments: Carmichael,L. (1947). sented"in advance"in any We find the following seriousflaws: Drs. H. The growth of the sensorycon- examination. G. Birch, trol ofbehavior psychological colony; it emergesin the courseof the ants' re- K. S. Lashley,D. Hebb, H. Kliiver. L. beforebirth. Review54: lationshipswith one another and with the envi- l. It is rigidly canalizedby the mergingof widely Aronson, J. E. Barmack, L. H. Hyman, L. H. 3t6-324. ronment. There is no "reaction-specificenergy" differentkinds of organizationunder inappropri- Lanier,and G. Murphy. Sincethese scientists dit Chein,I. (1936).The problemsof heredity and environ_ psychology being built up. The periodicity is a result of the ate and gratuitouscategories. fer widely in the extentof their agreementor dis- ment. Journalof 2:229_244. is nol agreementwith various points Coghill, G. E. (1929). Anatomy problem periodicityof the queen'segg-laying, which 2. It involves preconcoivedand rigid ideas of of my discussion, and the of I mustemphasize that none of them Behavior.London: CambridgeUniversity press. a "center" havingany chancteristicscorrespond- innatenessand the nature of maturation. is in any way ing to the behavior.And eventhis is not a direct responsiblefor any errors of omission or com- Cuze,W. W. (1935).Maturation and learningin chicks. 3. It habitually dependson the transferenceof p relationship.If the number of larvaein a colony missionthat may appear. Journal of Comparative sychology19 : 37l_409. conceptsfrom one level to another,solely on the Delacour, is experimentallyreduced by 50 per cent, thus J., and E. Mayr. (1945). The farnily Ana- of analogicalreasoning. stimulating effect,a normal basis tidae. WilsonBulletin 57:3_55. reducingtheir total References nomadic phase cannot occur. Recent findings 4. It is limited by preconceptionsof isomorphic Gos, E. (1933). ks reflexesconditionnels chez l,em_ resemblancesbetween neural and be- bryon d'oiseau.Bulletin du Sociiti Royal (Schneirlaand Brown 1950)have in fact con- t358-3591 Adriaanse, M. S. C. (1947). Ammophila carnpestris des Sciences de Liige 4-5: 194-199; 6-7: 246_250. firmed the hypothesisthat each of the regular havioral phenomena. Latr. und Ammophila adriaansei Wilcke. Ein Beitrag Grohman, J. (1933). large-scaleegg-delivering episodes in the queen's 5. It dependson finalistic, preformationistcon- zur vergleichendenVerhaltensforschun g. Behaviour l: Modifikation oder Funktionsrei- fung? Ein Beitrag zur function basic to the cycleis a specificoutcome of ceptionsof the developmentof behavioritself. l-34. Kliirung der wechselseitigen Beziehungenzwischen Instinkhandlung her over-feeding,due to a maximalstimulation of Anastasi,A., and J. p. Foley, Jr. (194g).A proposed und Erfahrung. 6. As indicatedby its applicationsto humanpsy- Zeitschrift fiIr Tiersychologie2: 132_144. the colony by the brood. This event, occurring reorientationin the heredity-environmentcontroversy. chologyand sociology,it leadsto, or dependson Hartley, P. H. T. (1950). inevitablyat the end of eachnomadic phase, is a Psychological Review 55: 239-249. An experimentalanalysis of (or both), a rigid, preformationist, categorical interspecific recognition. Symposia of the "feed-back"type of function, not at all relatedto Armstrong, E. A. (1950).The nature and function of Society of conceptionof developmentand organization. Experimental Biology 4: 31T336. the implicationsof "vacuum activity." displacementactivities. Symposiaof the Societyof Ex_ perimental Heinroth, O. (1910).Beitriige nature of suchcategorical theo- regards"instinct" as Biology 4: 361-394. zur Biologie, namentlich The restrictive Any instinct theory which Ethologie und Psychologie Baerends,G. P. (1950).Specializations der Anatiden. Internatiorwl ries as that of Lorer:z is very well illustrated by immanent, preformed, inherited, or based on in organs and Ornithological movementswith Congress( Berlin) 5: 5g9-702. Lees'remarks on Eciton The actualdevelopment specific neural structures is bound to divert the a releasing function. Symposia of the Societyof Experimental Heinroth, O. (1930). Ueber bestimmte to the periodic performancesof developmentfrom fun- Biology 4:337_3ffi. Bewegungs_ processleading investigationof behavior weisen bei Wirbeltieren. Gesellschaft Baerends,G. P., and J. M. Baerends-vanRoon. (1950). Naturforschender this ant are well understood,and are lanownto damentalanalysis and the study of developmen- Freundezu Berlin, An introduction to the study I 929, pp. 333_342. have no essentialrelationship to any "reaction- tal problems. Any such theory of "instinct" of the ethology of cichlid fishes.Behaviour (Supplement) l: Heppel,L. A., and C. L. A. Schmidt.(1933). Srudies in nervous system;further the scientist's l_242. on specificenergy" any inevitably tends to short-circuit the potassiummetabolism of the rat during F A. (1947).Evolutionary changesin the phys_ pregrancy, they are known not to be "innate" as such investigation of intraorganic and organism' f9ach, lactation and growth. University iological control of mating behavioi in of Catifoiia iublica- (Schneirla 1938).The processesleading to this relationshipswhich mammals. tions in Physiology environmentdevelopmental PsychologicalReview 54: 297-315. 8: 189-205. behavior surely have nothing to do with the underlie the development of "instinctive" Howells, T. R. (1945).The obsolete Be1ch,F. A. (1951).Instinctive behavior,reproductive dogmasof hered_ processesleading to "vacuumactivities" in a fish. behavior. ity. PsychologicalReview 52: 23-34. activities.In S. S. Stevens(Ed.), Handbookof Experi_ superficialsimilarity is sufficientto cause Howells, Yet the mental Psychology, pp. 397434. New yoik: T. R., and D. O. Vine. (1940).The innate dif_ of a John Leesto cite the ant's behavioras an example Mley & Sons. ferential in social learning. Journal of Abnormat and type of behaviordescribed for vertebrates.This is Acknowledgments Social Psy c ho lo gy 35: 537-549. Bird, C. (1925).The relative importanceof maturation a good exampleof the tendencyencouraged by andhabit in the development pedagog_ Hunt, E. L. (1949). Establishment of conditioned I am greatlyindebted to Dr. T. C. Schneirla(who of an instinct. suchtheories to look for casesfitting the theoret- icqlSeminar 32 68-91. responsesin chick embryos.Jourrul of Comparative of this paper)and and in many typesof behavior,rather originally suggestedthe writing Browman, Physiological Psychology42: 107_ll7 . ical categories L. G. (1943).The effect of controlled tem- in the to Dr. J. Rosenblatt for many stimulating and peratures Jennings,H. S. (1930). than analysis of the processesinvolved upon the spontaneousactivity rhythms of the The Biologicat Basisof Human helpful discussionsof the problems discussed albino Nature. New York: developmentof any one behaviorpattern. rat. Journal of Experimental iootigy 94: 47j_ Norton & Co. here. Dr. Schneirla in particular has devoted 489. Keeler, C. (1931).The l-aboratory Mouse.Cambridge, MA: Harvard University press. #* Daniel S. Lehrman li Lorenz's Theory of Instinctive Behavior 38 ::!

(1938)' Taxis und Schneirla,T. C., and R. Z. Brown. (1950).Army-ant m. merulaL., und T. e. ericetarurnTurton). activ- Lorenz, K.' and N. Tinbergen' Zeitscl, Kinder, E. F. (1927).A study of the nest-building life and behavior under dry-seasonconditions. 4. Tierpsychologie Instinkthandlungin der Eirollbewegungder Graugans' filr 3: 37-6O. ity of tile albino rat. Journal of ExperimentalZoology Further investigationof cyclic processesin behavioral l. Zeitschriftfiir Tierpsychologie2: l-29' Uyldert, I. E. (1946).A conditionedreflex as a fac 47:ll'7-161. and reproductive functions. Bulletin of the American T. C. Schnierla'(1935)' Principles influencingthe lactation of rats. Acta Brevia Neerl Analyse der Taxisanteile Maier,N. R. F., and Museumof Natural History 95:263-354. Koehler, O. (1950). Die Co' dica de Physiologia, Pharmacologia,Miuobiolosia Societyof of Animal Psychology.New York: McGraw-Hill instinktartigen Verhaltens' Symposiaof the Schooland,J. B. (1942).Are there any innate behavior 86_89. (1951).Learnable drives and rewards'In ExperimentalBiolo gY 4: 269-303' Miller, N. E. tendencies?Genetic Psychology Monographs 25: 219- (Ed.), Handbook of Experimental Psy' Washburn,S. L. (1947).The relationof the tempc of embryonicbehavior S. S. Stevens 287. Kuo, Z. Y. (1932a).Ontogeny Wiley & Sons' muscleto the form of the skull. Anatomical of the chology,pp.435472.New York: John Record in Aves. I. The chronology and generalnature Shepard,J. F., and F. S. Breed.(1913). Maturation and 239-248. (1947). The hoarding instinct' Psy- behavior of the chick embryo' Joumal of Experimental Morgan, C. T. usein the developmentof an instinct. Journalof Animal Wheeler,W. M. (1928).The Social Insects. New yo 6l:395-430. chologicalReview 54:. 335-341' 3:274-285. Zoology Behaviour Harcourt, Brace& Co. (1951).Phylogenetic comparison' In S' S' Kuo, Z. Y. (1932b).Ontogeny of embryonicbehavior Nissen,H. W. Smith,P. E., and E. C. MacDowell.(1930). An heredi- (Ed.), Handbookof ExperimentalPsychology' Whitman, C. O. (1899).Animal behavior.Biologi in Aves.II. The mechanicalfactors in the variousstages Stevens tary anterior-pituitarydeficiency in the mouse.Anatom- York: JohnWiley & Sons' Lectures,I 898,pp. 285-338. leading to hatching. Journal of ExperimentalZoology pp. 347-386.New ical Record46: 249-257. R. M. Laughlin'(1934)' Is the wall- Whitman, C. O. (1919).The behavior of pigeo 62:45489. Patrick,J. R., and Smith, S., and E. R. Guthrie. (1921). General Psy- in the white rat an instinct?Journal of Publicationsof the CarnegieInstitute 257: l-161. Kuo, Z. Y. (1932c).Ontogeny of embryonic behavior seekingtendency chologyin Termsof Behavior.New York: Appleton. and environmentalfactors GeneticP sychologY M: 378-389' Wiesner,B. P., and N. M. Sheard.(1933). Maten in Aves. III' The structure Spelt,D. K. (1948).The conditioningof the human Journal of ComparativePsy- A. (1926).The value of instinct as a Behaviourin the Rat.London: Oliver & Bovd. in embryonic behavior. Petrunkevitsch, fetus rn utero. Journal of ExperimentalPsychology 38: in spiders'Biological Bulletin 50: chology13 245 272. taxonomic character 338-346. of embryonicbehavior 427432. Kuo, Z. Y. (1932d).Ontogeny Sperry,R. W. (1945).The problem of central nervous of embryonic movements (1932).A preliminary study of fetal condi- in Aves, IV. The influence Ray, W. S. reorganization after nerve regeneration and muscle behavior after hatching' Joumal of Compa- Child Developmmt3: 173-177' upon the tioning. transposition.Qunrterly Review of Biology 20:311-369. rative PsYchologY 14: 109-122' (1949).The isolation of factors of learning Riess,B. F. Stone,C. P. (1947).Methodological resourcesfor the (1949). Modern concepts of instinctive behavior in field and laboratory studies' Lees, A. D. and native experimentalstudy of innate behavior as related to Progressin the TwentiethCentury NewYork Academyof Sciences51: 1093- behaviour. Science Annalsof the environmentalfactors. PsychologicalReview 54: 342- 37:318-321. I 102. 347. (1931). Beitriige zur Ethologie sozialer S. (1945).Vertebrate Paleontology' Chicago: Lorcrrz, K. Romer, A. Thorpe,W. H., and F. G. W. Jones.(1937). Olfactory Ornithologie79: 67-127' of ChicagoPress. Corviden.Journal fiir University conditioningin a parasiticinsect and its relation to the Erkennen army-ant behavior Lorenz, K. (1932).Betrachtungen flber das Schneirla,T. C. (1938)'A theory of problem of host selection.Proceedings of the Royat der arteigenenTriebhandlungen der Ydgel Journalfiir basedupon the analysisof activitiesin a representative Societyof London,B 124:5G81. al of ComparativePsychology 25: 51-90' Ornithologie80: 50-98. species.-"Iorrn Tinbergen,N. (1939).On the analysisof social orga- Umwelt des functionsof Lorenz, K. (1935).Der Kumpan in der Schneirla,T' C. (1944).The reproductive nization among vertebrates,with specialreference to 289- group behav- Vogels. Journal filr Ornithologie 83: 137-213' th€ army-ant queenas pacemakersof the birds. American M idland Naturalis t 2l : 210-234. pattern. iournot of the New York Entomological 313. ior Tinbergen,N. (1942). An objectivistic study of the Instink- Lorerrz. K. (1937). Ueber den Begriff der Society 52:153-192. innatebehaviour of animals.Bibliotheca Biotheoretica ani' thandlung. Folia Biotheoretica2: 17-50' Schneirla,T. C' (l9a6a). ContemporaryAmerican l: 39-98. in perspective'In P' L' Harriman (Ed')' Lorenz,K. (1939). Vergleichende Verhaltensforschung' mal psychology Tinbergen,N. (1948). PhysiologischeInstinktforsch- Psychology,pp' 30G316' New ZoologischeAnzeitung I 2 (Suppl' band): 69-102' Twentieth Cintury ung.Experimtia 4: l2l-133. verursachte York: PhilosoPhicalLibrary' Loretz, K. (1940).Durch Domestikation Tinbergen,N. (1950).The hierarchicalorganization of T. C. (1946b).Problems in the biopsychol- St

The modern theory of evolution is, as is so coming from internal factors,and causesof phy- often said, a fusion of the two great insights of logeneticvariation, as being imposed from the nineteenth-century biology: Darwin's realization external environment by way of natural selec_ that the variation among species arises from the tion. (I gloss over Darwin,s later flirtation with conversion of variation between individuals with_ Lamarckism,since the proposition that the envi_ in species,and Mendel,s discovery of the segre_ ronment specificallyengenders heritable adaptive gation of discrete factors as the basis for the variation is at total variancewith the Darwinian inheritance of differences between individuals. We mechanismof evolution.)It is from this view of are constantly reminding ourselves and others environmentas the causeof organismsthat the that the immense progress made in biology in entire corpus of modern evolutionary biology the present century rests firmly on these two arises. major discoveries of a previous time. What is not We cannot appreciatefully the nature of the always appreciated, however, is that the legacies change in biology wrought by Mendel and of Darwin and Mendel are also responsible for Darwin unlesswe understandttre historical im_ certain difficulties in biology, difficulties that pre_ portance of the objectificationof the organism. vent us from some kinds of further progress and Descartes'metaphor of the organismas machine which keep us locked into a rigid framework of had virtually no impact on biology for two hun_ thought about the development and evolution dred years. So, for example,iven Harvev,s of organisms. These difficulties arise, ironically, mechanicaldescription of the circulation of from the very source of Mendel and Darwin,s Ut^o9Owas not really accepteduntil the beginning successas biologists, their separation ofinternal of the nineteenthcentury, and CasparFriedrich from external forces acting on organisms. For Wolffs epigenetictheory and Mendel the internal o.factors,'*"r" his remarkablv tha causesof modern distinction betweengenotype the form of the and phe_ organism and were, in the end, notype had no proper ..factors.,' efect in embryology until the the objects of study. The what Entwicklungsmechanikof the latter of the we now call "genes,,' were the iart subjects and the last century.Biology lackedclear organisms the objects notions of sep_ of developmental forces. arablecauses and From effectsand, more important, a this view of gene as the cause of organism systematiccommitment to the analysisof has flowed the entire co{pus Uiotog_ of modern m-echan- ical systemsalong mechanistic ical and molecular linis. Lamarck,s genetics. For Darwin. the ex_ view that information ternal from the external world world, the environment, acting on the could becomepennanently incorporated in or_ organism was the cause of the form of oiganisms. ganismsand their progenythrough the The environment, the mediation external world with its of a. living being's needs autonomous properties, and *ill *u, quintes_ was the subject and the sentially representative organism of pre_Darwinian Uiot- was, again, the object acted upon. In ogy. Darwinism, As CharlesGillespie (1959) so cogentlyputs the organism is the interaction of it: "Lamarck's two causal theory of evolution belJngsto the sequences, autonomous in their dy_ contracting namics. and self-defeatinghistory oi subjec_ Internal forces produced the variation tive science,and Darwin,s to the exjanding among organisms, and autonomous and external conqueringhistory of objectivescience.', torces molded the species on the basis of these making organisms autonomous internally _By the objects of forces caused variations. The es_ whosesubjects were senceof Darwin's the internal heritablefactors account of evolution was the separation and the external environment,by seeingorgan_ of causes of ontogenelrc variation. as isms as the effectswhose ,orri, were internal

60 Richard C. Lewontin Gene, Organism and Environment 6l

and external autonomous agents, Mendel and lations and the new observationsof radioactiv- Mendelianview that internal factors make the genetics(and of evolution) consistentlydescribe Darwin brought biology at last into conformity ity, of light, and of astronomy.Without relativity individualorganism and the Darwinian view that organisms as "determined', by their genes.It with the epistemological meta-structure that and quantum theory, physics and theoretical externalforces determine the collectivity. In the is a short step to seeingorganisms as l.lumber_ alreadycharacterized physics since Newton and chemistrywould have ground to a halt. On the balanceof this chapter,I want to make .,body clearwhy ing robots" created by their genes and chemistrysince Lavoisier. This changein world other hand, biology, far more diverse in its sub' thesetwo metaphorsare wrong. Individual devel- mind." It is not hardto seewhy suchunbiological view was absolutelyessential if biology was to ject matter, far more looselytied togetherinto a opmentis not an unfolding, and evolution is not rubbish is taken seriously.yet, the vast majority progressby making contactwith physicalscience a seriesof solutionsto presentproblems. Rather, of morphological, behavioral, and physio_ and by becoming quantitative and predictive. evendevelopment. Some branches such as molec- genes,organisms, and environments ;!j are in recip- logical differencesamong individuals do not The mechanisticreductionism and the clearsepa- ular biology have made extraordinary pro$ess rocal interactionwith each other in such €i a way "Mendelize." It is simply not possibleto read off ration of internal and externalwere as necessary by concentrating on just those questions for J.1 that each is both cause and effect in a quite the genotypicdifferences between tall and short in the nineteenthcentury for the creation of a which the simplemechanical reductionism of the complex, although perfectly analyzable, ;i way. individuals of Rumex acetosellafrom their scientificbiology as Newton's ideal bodies and nineteenthcentury is the perfect epistemology. -:i The known facts of developmentand of natural individual phenotypesor from any number of perfect determinismwere for the physicsof the Developmentalbiology, the study of cognition history make it patently clear that genes it do controlledtest crosses involving them or their rel_ seventeenth.But we must not confusethe histor- and memory, and evolutionary biology, on the ,f; not determineindividuals nor do environments atives, not to speakof the genotypic difference ically determinednecessity of a particular episte- other hand, have profited only marginally from .'{ determinespecies. betweenfaithful spousesand philanderers.The stagein the development theserapid advances.Rather, they are stalledby mologicalstance at one i reaction of many evolutionists (encouraged, of a sciencewith a perfectmodel that will guar- their attempt to use outdated conceptsto con- ,rai again, by textbooks) to this obvious fact r-i.l Gene,Environment, and Organism in is to antee all future progress.On the contrary, the front a rich phenomenologyto which thesecon- consign .,polygenic t?E Development such charactersto control,,, very progressmade possibleby certain revolu- ceptsclearly do not apply. Evolutionary biology 't invoking the multiple factor hypothesis,and thus particularly becauseit is the nexusof all ;i tionary formulations may lead eventually to suffers saving the basic €t I will begin with the obvious. It is well model that genes determine resultsthat arein contradictionwith thoseearlier other biological sciences,so that a lack of pro- '&1i known that Mendelsolved organisms.But quantitativevariation of a char_ formulationsand which can be resolvedonly by gressin developmentalbiology, in ecology, in the basicproblem of the laws of inheritance acter is not prima facie evidence that it is reexaminations behavioralscience, all arefatal to a proper under- '!:Jn by investigatingthe heredity of their reexamination.Yet those -r, influencedby many genes. ,.4i very specialsorts of diferences,those Singlegene mutations are themselvesrooted in the past formulations. standingof evolution. :i-.1 in which 'grt therewas a determinate affecting eye shape,wing variation and bristle Newtonian mechanicsand classicaloptics were Specifically,evolutionary biology must con' correspondencebetween €i genotype number in Drosophila, or enzyme activity in the forms of organisms. :'iE:i. and phenotype. Given the genotype, in seriouscontradiction with the newerobserva- front two issuesabout =-l :g the phenotypecorresponding humans,all show quantitative variation in phe_ of physicsat the end of the nineteenthcen- One is the ontogeneticprocess by which the se- to it was unam_ tions +i notype and, unlesscare is taken to control quenceof forms that comprise an individual's biguouslydefined, at leastunder the condition of the tury, but anyonefamiliar with the development condition of development, :fI Mendel'sexperimental garden. considerableoverlap of the SpecialTheory of Relativity immediately life history come into being. The secondis the .:;t Indeed, it is the essence betweengenotypes in their phenotypic distribu- phylogeneticprocess by which speciesas collec' .r*3 of the Mendelian methodologythat one seeshow that theory, in one aspecta negation i:til tions. .+i can read off the genotypegiven The fundamental general facl of pheno_ of Newtonian principles,is built entirely on a tive entitiesform and changebased on the varia- either the indi_ _ei geneticsis that the phenotypeof organisms among the individuals that make them up. vidual'sphenotype or, in the case of complete is a Newtonian framework and could never have tions *{ consequenceof ,€t dominance,the phenotypesof the progeny non-trivial interaction between been developed in the absenceof classical Classical,post-Darwinian, post-Mendelian biol- of genotype ;** a single test cross. and environmentduring developmenr. physics. ogy has settledon two metaphorsthrough which It is not alwayi explicitly *f pointed All that genesever do is to specifya nonn tt out that all of modern biochimicai, of reac_ As in physics,so too in biology. As time has the processesare seen. The first, ontogenetic,':i molecular,and developmental tion over environments.Moreover, fitnesstoo is passed,Mendel's view of organismsas the mani- processis seenas an unfoldingof a form, already geneticsalso has dependedfor progress a phenotype and varies from environment to festation of autonomousinternal "factors" with latent in the genes,requiring only an original r? on finding genetic dif_ ferences environment,both becauseother aspects and an environment , that make clear-cut, non-Jverlapping of the their own laws, and Darwin's view of organisms triggering at fertilization phenotype develop phenotypicclasses under easilycontrolled differently in different envi_ aspassive objects molded by the externalforce of adequateto allow'onormal"development to con- . condi_ tions.It is amusing ronments,and becausea given shapeor behav_ natural selection,have becomeincreasingly in tinue. The second,phylogenetic, process is seen:i to contemplatewhere bacte- riophage iour or physiologywill confer diffeient fitnesses problemand solution The environment"poses genetics(and,, afortiin, all of molecular contradiction with the known facts of develop- as ;j in different environments. genetics)would be now if Benzer,sbacteriophage During the fifteen mentaland populationbiology. But the situation the problem"; the organismsposit "solutions,"of i years mutantshad only differed between1950 and 1965,population geneti_ in biology has developedrather differently than which the bestis finally "chosen."The organismli from eachother 6y l% in the number of progeny cists,Iargely under the influenceof plant and ani_ in physics.All of physicalscience seemed blocked proposes;the environmentdisposes. These two ,i phage they produced on restrictive mal breeders and of Schmalhausen'sseminal formu- metaphorsare simply the forms of the original '' hosts. One consequenciof this by the repeatedconflict betweenclassical work, Factorsof Evolution(lg4g), methodologicalhistory is that textbooks of devotedcon-

€',d 'fi s Richard C. Lewontin Gene, Organism and Environment 63 62

edgeis usually to attempt to assignthe.relative changefrom fertilization to death. The pheno- mental problems. What then is the motive power attention to the environmentalcontin- siderable to genotype,environmgnt' devel' typeat any instant is not simply the consequence of further evolution? The solution proposed by and to the efects ofselection weights Tq gencyofphenotype for examplein a heritability of its genotypeand current environment,but also Van Valen (1973\ is that the environment is regions (see' for ex- opriental ,ro.-ir.,ut In aiferent environmental of the analysisof vari- its phenotypeat the previousinstant. That is, constantly moving and that species are and Spassky ,tody o, someother form of sim- u-pt", Lerner 1954,Dobzhansky biologists is a first order Markov process ply but un"t Tht secondfact that evolutionary development in running to keep up. In that case, it is the tgq+,'yut"oner1960, and Robertson1960)' must copewith is that the influenceof eachfactor which the next step dependsupon the present autonomous forces of environmental change that passedout of fashion *ith the advent ihi, *ork influenceofthe other factorsso state.The temporalorder of environmentsis thus govern the rate of evolution, and we would be genetics'Indeed' except dependsupon the of moleculrarpopulation to genetic' but not a sufficient,prediction of future and that no aisignment of fixed weights a critical, well advised to study the laws of environmen- for the famous work of Clausen' Keck environment-al,and noise componentsof varia- development.lfa Drosophilaadult hatchesfrom tal rather than organismic change if we want to no study of the norns of reaction Hiesey(1958), (Lewontin 1974)'There are no the pupal caseas an unusually small fly, it does understand what has been happening. More par- heterozygousgenotypes tion is possible of naturally occurring results for evolu- not matter what the contributing causeswere to adoxical is the necessity of defining environments of^Grrpta on more important experimental appeareduntil the experiments (1967)on it small,it now hasan unusuallyhigh sur- Thus' tionary biotogy than those of Rendel making without organisms. To make the metaphor of ad- iliosophila (Gupta and Lewontin 1982)' canalization,yet the early impact of thesefind- faceto volume ratio, which will play an impor- aptation work, environments or ecological niches ifr. Uuti" daia for judging the effectsof selection ings on evolutionarytheory seemsnow to be for' tant role over the rest of its life history. Small must exist before the organisms that fill them. particular genotypesare simply The in fcking' What Rendel and others have shown is changesin ambient temperatureor in its own There must be a preferred, denumerable set of shows clearly that the de- gottttt. littie that is known geneticstate on envi- activitywill be felt by it in a way differentfrom its combinations genotypesto ihe reriprocity of effectsof of factors that make "environ- velopmentalresponses of different state sibs and will have different efects on its do not ,onrn.otul sensitivityand of environmental larger ments" and a non-denumerable infinity of combi- uuryirrgenvironments are non-linear and on geneticsensitivity of the developingorganism' reproductiverate. The way in which its genotype nations of factors that are not. The history of life itre simple ordering of genotypes along attow the genotype is itself hierarchically and its future environmentalsequence influence is then the history of the coming into being of scale of phenotype' Norms Moieover, a one-dimensional sensitivityof the fly are themselveselfects of the organismas new forms no geno- organizedso thai the environmental that fit more and more closely into of reaction cross each other so that genes u genesubstitution will dependupon cause.The organismis not simply the object of these preexistent niches. But what laws of the type gives a phenotypeunconditionally larger' luttt at-otheiloci. The consequenc€is that selection developmentalforces, but is the subjectof these physical universe can be used to pick out the pos- slower,more or lessdiferent than ,*uUJr, faster, expressionofa trait' inde- forcesas well. Organismsas entities are one of the sible environments waiting to be filled? In fact, we facts seem'however' can changethe average another.These well-known of that expressionin causesof their own development. only recognize "environment" theorists pendentl!from the variation an when we seethe to havemade no impact on evolutionary to develop a char- responsatovariable environment and organism whose environment it is. Yet so long who continueto speakabout selectionfor rn.otul noise.Thus, by selection,an organismcan as we persist in thinking of evolution as adap acter and about genesthat are selectedbecause Organism and Environment in Evolution be made developmentallyinsensitive or highly tation, we are trapped into an insistence on the they producethat character' sensitiveto perturbationsof its genotype'its envi' autonomous existence of environments indepen- A se"ond,less well-known, feature of develop Our usual description of evolution by natural developmentalaccidents, or any com- dent of living creatures. In fact, we should be phenotypeis not giveneven when the ronment, selection is framed in terms of the process of mentis that externalfacts not able to list the environments are completely bination ofthese. Internal and on Mars, being care- g."o,Vp" uoO ttt environment deter' adaptation. A species' environment exists and only play a role in development,but each ful all the while not to be influenced by our Ip."in.O. Thereis a significanteffect.of "develop- changesas a consequence of some autonomous minesthe role bY the other' knowledge of earthly life! If, on the other hand, mental noise" (Waddington 1957)in producing PlaYed forces outside the species itself. This outside have Thus far, my description of development.ts we abandon the metaphor of adaptation, how phenotype.The two sidesof a Drosophila the 'i world posesproblems for the species,problems of still in terms of the organism as the object' can we explain what seems the patent "fit" of samegenotype, and no reasonabledefinition acquiring space, consumables, light, and individ- the inlternal and external to it' { organisms and their external worlds? Fish have that the left and right effect of causesboth uals of enviroiment will allow with each of the opposite sex. Those most successful in up the sideof attt o,rgh the causesthemselves interact fins, and not only fish but whales, seals, penguins sidesof a pupa developinghalfway devel- solving the problems, because, by chance, their dif- ;ther. iht final step in the integration of and even sea snakes have some sort of flattened a glasst,itt-Uottt. in-the laboratory are in morphologies, physiologies, and behaviors make optntnt"t biology into evolutionis to incorporate body part that the animal uses for swimming. ferent environments.Yet, the number of sterno- them mechanically the best fit to do so, Ieave the id" orgu.rir- as itsetf L causeof its own develop Moles have long claws as do anteaters; birds and pt"rrral bristles and the number of eyefacets difer most offspring and thus the species adapts. This mechanismby which exter' bats have wings, and so on. The marvellous fit of of an individual fly' Small ment,-asa mediating view of evolution, tetween the two sides its future' To however, has certain paradox- acting during nal and internal factors influence organisms to their environments seems obvious. eventsat the level of thermal noise gene' ical features (Lewontin 1978). One is that all describephenotype as the consequence,of What is left, then, but some concept of a progres- cell division and differentiation have large effects extant species are said to be already adapted to environrnent,and accidentleaves out ofaccouot sive fitting of organisms to predetermined adap- on the final developmentaloutcome' their environments. A good deal of evolutionary to entirely the elementof temporalorder which-is'' tive peaks? It is only the beginning of understanding ThQ; biology is taken up with demonstrating that their of the essencein a developmentalprocess' What is left out of this adaptive description of agree that internal and external factors con- features represent optimal solutions to environ- organism'sphenotype is in a continual state organism and environment is the fact, clear to all tribute to phenotype.The reactionto that knowl- Richard C. Lewontin Gene, Organism and Environment & 65

of ganisms did not pass the law of gravity. Yet, If of or- Ecologicalsuccession is preciselythe history environmentsdo not preexist,how are we to natural historians,that the environments gravitation self-destructionof speciesby alterationsof their whether is an aspect of the environ- explain the remarkablesimilarities that evolved ganismsare made by the organismsthemselves as own environment' ment of an organism depends upon biological independentlyin different groups?Not only do i of their own life activities'How do (3) Organismstransduce the physical signals properties of the organism, for example size. animalsas unrelatedas fish, mammals,and birds I know"onr.qt.nce that stones are part of the environmentof of itre exiernal world. Changesin externaltem- Bacteria are "outside" gravity, but their very all havefin-like appendageswhen they are aquat- thrushes?Because thrushes break snails on them' peratureare not perceivedby my liver as thermal small size makes them subject to a very different ic, but a whole marsupialfauna developedwith Those samestones are not part of the environ- tocatst' alterationsin the concentrations physical phenomenon, Brownian motion of mol- "wolvesr""moles," "mice," and (although juncos who will passby them in their .hung.t but as ment of The photon en- ecules,which larger organisms do not notice. no ungulates,marine forms, to make their of certain hormonesand ions' elephants,bats, or searchfor dry grasswith which metaphor of ergy impinging on my retina and the vibrational The construction rather than ad- horses). The error is to supposethat because nests.Organisms do not adapt to their environ- ut *y ear drums when I seeand-hear a aptation leads to a different formulation of natu- organismsconstruct their environmentsthey can ments; they construct them out of the bits and "netgy are immediately changed through ral selection and evolution. On the adaptive view construct them arbitrarily in the manner of a piecesof the external world' This construction rattlesnake mediation of my central nervoussystem into evolution can be represented formally as a pair of sciencefiction writer constructingan imaginary processhas a number of features: the concentration' But this differential equations. The first, describing the world. The coupled equations of coevolution determinewhat is relevant' changes in adrenalin (l) Organisms of my biology' change in organisms, O, as a function of organ- of organism and environment environment' changeis in part a consequence are not uncon- While stonesare part of a thrush's and environment, sinceanother rattlesnake would presumablyreact ism E, dOfdr.,-f(O,E), and strained.Some pathways through the organism- tree bark is part of a woodpecker's,and the rather differentlY. a second law of the autonomous change of environment space are more probable than undersidesof leavespart of a warbler's' It is the create a statistical pattern of environment, dE/dt:g(E). A constructionist others, preciselybecause there are real physical birds that determinewhich (4) Organisms life activitiesof these in the view makes this into a pair of coupled differen- relations in to all of enviionment different from the pattern the external world that constrain parts of the world, physicallyaccessible equations in external world. Organisms,by their life activ- tial which organism and environ- change.The constructionof an environmentthat ih.rn, ur" actually parts of their environments' damp oscillations,for examplein food ment coevolve, each as a function of the other, includesliving in a fluid mediumof a certainden- as organismsevolve, their environ- ities, can Moreover, in temperatureby chang- dO/dt:f(O, E), and 491fl1:g(O, E). sity and viscosityplaces certain quite loose All animalsare covered supply by storage,or con- ments,perforce, .huttg.. can' on The parallel in population genetics is between straints moist air ing their orientation or moving' They on morphology.Either the organismwill with a thin boundary layer of warm frequency-independent the contrary, magnify differencesby using small and frequency-dependent be sessile,as many are, and wait for food, or it asa consequenceof their metabolism'Small ecto- in abundanceof food typesas a cue for selection. In the first case, one postulates a set of will be vagile and chaseit. If it is vagile it may parasitesmay be completelyimmersed in that changes images.They can also integrate adaptive peaks which may or may not change in propel itself by jet action like the squid or by which thus determinestheir envi- switchingsearch toundary laylr only when time as a consequence of external forces, and a umbrella jelly-fish But if nat- and differentiate.Plants may flower scullinglike the or by flattened ronmentaltemperature and humidity' of gene a sufficientnumber of days abovea certain tem- set frequencies that change in response to appendages.But even in the last case,there are ural selectionshould increasethe body size of ' Cladoceracan the potential field represented by the adaptive those who undulate up and down (whales),side may emergethrough the perature have been accumulated these parasites,they in peaks. In the second case, the location and exis- to side (sharks), colder drier from asexualto sexualreproduction fly in the water (rays), beat tiny layer into the stratosphereof a tence peaks "hurrg",.rpo-nr. to a large alteration in oxygensupply' of the are themselves functions of the wings rapidly (seahorses), and a variety of other wlrld. It is the genesof sealions that make the food supply, irrespectiveof the genetic composition of the evolving population. fin movements.Where there is strong conver- environmentand the genesof temperatureor sea part of theii externaloscil- The model of the first process is climbing a moun- genceas in certain part of theirs' yet absolutelevel. Even the period of marsupial-placentalpairs, this lions that make the savannah a tain peak, of the second walking on carni- lation can be modulated,as when cicades count a trampoline. should be taken as evidenceabout the nature of thosegenes are descendedfrom a common While population prime number of seasonalfluctuations' It might geneticists usually model selec- constraints on developmentand physical rela- vore ancestor. that the notion of organismscon- tion as a frequency-independent process, adding tions, rather than as evidencefor pre-existing (2) Organismsalter the external world as it te objected environments leads to absurd frequency dependence as an added complication niches. part of their environments'All organ- structing their becomes do not sit around con- of marginal interest, the actual situation is the The naggingproblem of adaptationhas by taking up minerals' results.After all, hares always isms consumeresources sense reverse. Most selective processes are frequency- been resources structinglynxes! But in the most important what oneimagines the progressionof events by eating.But they may alsocreate the dependent, they do. First, the biological propertiesof lynxes as for example are any processes in to be during the processitself, since we always for their own consumption,as when ants make part a consequenceof selection which fitness depends on relative position in an observe only the finished product. If a spreadout leavesto catch ur"ir.rrrrnubly in seal's fungus farms, or trees i'e' ordered series, or in which more for catchingprey of a certain sizeand speed' there is competition flippersare an adaptationto water, at what stage sunlight.They may createan environment for resources hares.Second, lynxes are not part ofthe environ' in short supply with diferent rela- in the evolutionary history of seals did swim- hospitable to their own species,as for example are of hares,because of tive successof diferent types. ming in water becomethe "problem" which waterlevel of a pond' but' ment of moosewhile they seals when beaversraise the A problem seemsto posed creates biological differencesbetween moose and hares' be for the construc- "solved" by losing their legs?No one imagines in contrast, white pine in New England tionist Then what about laws of physical nature? Or' view by the phenomenon of convergence. that a whole group of terrestrialcarnivores sim- a denseshade that preventsits own reseeding' Richard C. Lewontin 66 II RETHINKING HEREDITY ply plungedinto the water one day, experiencing to lean so heavilyon an impoverishedview of the and organ- a new major adaptive problem, and then pro- relation betweengene, environment, the deathof ceededto adapt to it by the usual route ofnatu- ism. If the hundredthanniversary of ral selectionfor small increasesin flipper-like Darwin is not to mark the death of Darwinism, morphology.Nor, alternatively,can we say that we needto strugglefor its transfiguration. swimminghas alwaysbeen a major problem for There is, in fact, no reasonwhy we carnivores. References should not, a priori, reversethe entire scenario' Perhaps an early pinniped ancestor acquired Clausen,J., D. D. Keck, and W. W. Hiesey.(1958). slightly flipper-like appendagesfor an entirely Experimental studies on the nature of species,Vol. 3: different reason-genetic drift or some pre- Environment responsesof climatic races of Achillea 581: adaptation. Partly aquatic life then became an Carnegie Institution of Washington Publication opportunity rather than a problem.This is not a t-t29. very satisfactorytheory, at leastas a typical one Dobzhansky,T., and B. Spassky.(1g44).Manifestation ,i in Drosophila pseudoobscarain dif- for evolution, but for preciselythe samereason of genetic variants .] ferent environmetts.Genetics 29:270-290. ti that the standard adaptive story is unaccept- Falconer,D. S. (1960).Selection of mice for growth on able. Both uncoupleorganism and environment '::: high and low planes of nutrition. GeneticalResearch, in sucha way that we must regardone as under- Cwnbridge1: 9l-l13. going significant autonomous change and the ;i Gillespie, C. C. (1959). Lamarck and Darwin in the i: other as responding. history of science.In B. Glass,O. Temkin, and W. L. Concentratingas we alwayshave on the prob- : Straus (Eds.), Forerunnersof Darwin, pp. 265-291. j} changeunder natural lem of how the organisms Baltimore:Johns Hopkins University Press. ,ii selection,we haveneglected to ask seriouslyhow Gupta, A. P., and R. C. kwontin. (1982).A study of :ii which the organismis sup the environmentto reaction norms in natural populations of D. psardo- ,i cometo be a problem in posedlyresponding has obscura.Evolution36:934-948. rl the first place. Presumablythe non-aquatic carni- Lerner,T. M. (1954).Genetic Homeostasis. Edinburgh: !l vore ancestorsof the Pinnipediaslowly incorpo- Boyd. Oliver and ;l rated the water as a more and more energetically Lewontin, R, C. (1974).The analysisof varianceand ,i of their environmentwhile their significantaspect the analysis of causes. American Journal of Hwun :i physiologieschanged to make morphologiesand Genetics26:4D4ll. & reward- ';$ that appropriation more energetically Irwontin, R. C. (1978).Adaptation. Scientifc Amer' ing. Werea completereconstruction possible, we ican 239(9):l5Gl69. at which tl"j would be unable to find the moment Rendel, J. M. (1967). Canalizationand GeneContol' to swimmingwas for the flrst time a "problem" London: AcademicPress. .l be "solved" by the animal. Robertson, F. W. (1960). The ecological geneticsof ;i Organisms,then, both make and are made by growth n Drosophila.II. Selectionfor large body size .t their environmentin the courseof phylogenetic on diferent diets. Genetical Research, Cambridge l: 1 change,just as organismsare both the causesand 305-318. ul consequencesof their own ontogeneticdevelop Schmalhausen,L I. (1949). Factorsof Evolution: The ;i ment. The alienation of internal and external Theory of Stabilizing Selection. Philadelphia: -,* causesfrom each other and of both from the Blakeston. : I organism,seen simply as passiveresult, does not Van Valen, L. (1973). A new evolutionary law' tfl stand up under even the most casualsurvey of EvolutionaryTheory l: l-30. '.'1i our knowledgeof developmentand natural his- Waddington, C. H. (1957). The Strategyof the Gmes' i ;1 It is a tribute to the power of long-held London: Allen and Unwin. tory. El that the study of evolution continues *f ideology ffi