The University of Chicago Evolutionary Importance of Overspecialization: Insect Parasitoids as an Example Author(s): Armand M. Kuris and Stephen F. Norton Source: The American Naturalist, Vol. 126, No. 3 (Sep., 1985), pp. 387-391 Published by: The University of Chicago Press for The American Society of Naturalists Stable URL: http://www.jstor.org/stable/2461362 Accessed: 10-06-2015 23:10 UTC Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at http://www.jstor.org/page/ info/about/policies/terms.jsp JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. The University of Chicago Press, The American Society of Naturalists and The University of Chicago are collaborating with JSTOR to digitize, preserve and extend access to The American Naturalist. http://www.jstor.org This content downloaded from 128.111.90.61 on Wed, 10 Jun 2015 23:10:37 UTC All use subject to JSTOR Terms and Conditions Vol. 126, No. 3 The AmericanNaturalist September 1985 EVOLUTIONARY IMPORTANCE OF OVERSPECIALIZATION: INSECT PARASITOIDS AS AN EXAMPLE ARMAND M. KURIS AND STEPHEN F. NORTON Departmentof Biological Sciences, Universityof California,Santa Barbara, California93106 SubmittedOctober 31, 1984; Accepted March 3, 1985 Gould (1982) reviewed evolutionarymechanisms that can operate at different hierarchicallevels: gene, individual,deme, population,and species. He suggested thatinteractions between these levels can modulateevolutionary outcomes. One such possible interaction,overspecialization, has been describedas the evolution of highlycomplex and ecologically constrainingtraits that convey a selective advantage to individuals, but lead to a higherprobability of extinctionof the species by restrictingthe abilityof the species to withstandenvironmental change (Simpson 1953; Cifelli 1969; Valentine 1969, 1973; Bretsky and Lorenz 1970; Thompson 1976; Gould 1982). Some effectsof environmentalfluctuations on the extinctionof species of differingsensitivity to environmentalchange have been modeled by Leigh (1981). Observing that overspecialization is a process operatingbetween two levels, individualand species, Gould suggestedthat overspecialization may be "a central evolutionaryphenomenon that has failedto gain the attentionit deserves" (1982, p. 385). As he remarked,it is usually dismissedas a minorand unusual phenome- non. Here we discuss the relationshipbetween complexity and ecological special- ization, provide an operational definitionof overspecialization,and place this concept in the context of evolutionarytheory. Also, since no widespread and importantexamples of extantorganisms affected by overspecializationappear to have been identified,we suggestan example thatcould provide a systemfor the studyof this phenomenon. The presence of complex morphology(or physiology,behavior) does not pre- dict the ecological breadthof a species or its evolutionarylongevity. Complexity may lead to an evolutionarycul-de-sac or open new adaptive zones (Simpson 1953). Examples from the paleontological literaturesupport both alternatives. Evidence supportingthe firstalternative includes the observation that during periodsof mass extinctionPaleozoic bryozoangenera with complex morphologies had a higherextinction rate than simplerforms (Anstey 1978). Complex genera survived better than simple genera, however, outside these periods of mass extinction.As evidence supportingthe second alternative,the increasedcomplex- ityof limbpairs in ordersof free-livingaquatic arthropodswas not correlatedwith Am. Nat. 1985. Vol. 126, pp. 387-391. ?) 1985 by The Universityof Chicago. 0003-0147/85/2603-0002$02.00.All rightsreserved. This content downloaded from 128.111.90.61 on Wed, 10 Jun 2015 23:10:37 UTC All use subject to JSTOR Terms and Conditions 388 THE AMERICAN NATURALIST TABLE 1 RELATIONSHIP BETWEEN SELECTION ON THE INDIVIDUAL AND THE POPULATION CONSEQUENCES OF SUCH SELECTION SELECTION FOR TRAIT AT THE CONSEQUENCES FOR POPULATION INDIVIDUAL LEVEL IF TRAIT BECOMES WIDESPREAD Yes No Increase or no effecton size Individual selection, kin Group selection selection Decrease in size Overspecialization Maladaptation evolutionarylongevity (Flessa et al. 1975). We suggestthat the increased com- plexityin arthropods(with a presumed specialization of function)appeared to affectonly a few of the repetitivelimb pairs at a timeand thatthe unaffectedlimb pairs retained a simple morphology(and presumablygeneralized functions).In this case, arthropodsmay have acquired specialized limbs withoutsacrificing generalizedfunctions. ESSENCE OF OVERSPECIALIZATION Problems with determiningcomplexity, specialization, and ecological con- straintsharply limit the usefulnessof a definitionof overspecializationemploying such terms.We propose thatthe essence of overspecializationis the consequence forthe populationof an adaptation.Overspecialization occurs when the effectof a trait is selectively advantageous to an individual but disadvantageous to the populationbecause it resultsin a decrease in population. Table 1 outlines the logical relationshipbetween individual selection, group selection, overspecialization, and maladaptation. Kin selection, wherein the fitnessof an individualis increased by actions that promotethe fitnessof genet- ically related individuals,is similarto individualselection (E. 0. Wilson 1975, p. 117). Group selection may explain the evolutionof traitsthat do not necessarily benefitthe individualwhen individualsare organized into small, isolated popula- tions. In these structureddemes, selection between populations may override selectionwithin a population(Wright 1969; D. S. Wilson 1980,p. 38; Leigh 1983). We distinguishoverspecialization from other forms of individualselection on the basis of its consequences. Because the consequences of individualselection for populations have generally been ignored, overspecialization has not been examinedclosely. Since overspecialized traitsare selectivelyadvantageous to the individual,overspecialization is distinctfrom a frankmaladaptation. In the table, sexual selection would be similarto eitherindividual selection or overspecializa- tion dependingon the populationconsequences of such selection. The usual examples of overspecializationhave tendedto focus on the seemingly bizarre traitsthat characterize the peacock, saber-toothedtiger, Irish elk, and others. In these cases there is no evidence that a fancytail, big canines, or big antlers(no largerthan expected for an animal of its size; Gould 1974) would be ecologically constrainingor necessarilyresult in smallerpopulation sizes. This content downloaded from 128.111.90.61 on Wed, 10 Jun 2015 23:10:37 UTC All use subject to JSTOR Terms and Conditions OVERSPECIALIZATION 389 By focusingon environmentalchange, the traditionalscenario foroverspeciali- zation tends to reduce the concept to a truism. Ultimately,all environments change. Thus, in the long run,any traitmay sooner or later become maladaptive or appear overspecialized (R. R. Warner,in littera).Such formerlyuseful traits, now maladaptations following environmentalchange, are distinctfrom over- specialization as definedhere. The negative population consequences of over- specializationare intrinsic,at times resultingautomatically from the action of an overspecialized trait. AN EXAMPLE A parasitoid may be definedas a consumer that kills one and only one host (prey)during a lifehistory stage (Kuris 1974). Most examples are foundamong the hymenopterousinsects. Typically,an adult femalewasp locates a host insectand lays one or a few eggs on or in the host. Afterhatching, the larval parasitoid slowly consumes the host insect. Following the death of the host, the parasitoid pupates and thenemerges as an adult wasp. Physiologically,parasitoids resemble parasites; ecologically, their impact is akin to predation. The consequences of host-location behavior by parasitoid insects show that in an ecologically significantgroup of organismscomposed of manyspecies, overspecializationis an importantevolutionary mechanism. Female parasitoidinsects have evolved com- plex searching mechanisms to locate suitable hosts, traits that are obviously criticalto female reproductivesuccess. Depending on the particulartype of host, such locatingbehaviors may involve visual, olfactory,tactile, and auditorycues in various combinations(Askew 1971; Cade 1975). Parasitoids are oftenhighly efficient searchers. The abilityof many parasitoid species to drivehost populationsto low levels and thento continueto locate hosts at the subsequent low densities is well documented(DeBach and Sundby 1963; Flanders 1966; Hassell and Varley 1969; Huffakeret al. 1971; Kuris 1973; but see Murdoch et al. 1984). Because of this capability they are frequentlyused as biologicalcontrol agents for host insectsthat are agriculturalpests (Huffakeret al. 1971; Kuris 1973). But, thereinlies the rub. Ultimately,however, the selectionfor efficientsearching behavior, so necessaryfor the success of the individualinsect, causes a dramatic and often persistent depletion of the host resource. The parasitoidpopulation is therebyalso reduced. That manyhost insectsare plentiful where they have been introducedbut are rare in theirnative lands supportsthe conclusion that this is a widespread