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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

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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, ,and species. He suggested thatinteractions between these levels can modulateevolutionary outcomes. One such possible interaction,overspecialization, has been describedas the 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 ,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.

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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 )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 .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 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.

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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 (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 . 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 phenomenon (Kuris 1973; DeBach 1974). When native host populations are examined, a high prevalence of parasitoidsis oftenrecorded (Huffaker1971; DeBach 1974). Presumably, low-densityhost populations are more likely to undergo local extinctionthan high-densitypopulations (see Murdoch et al. 1984for evidence of local extinctionfrom parasitoid activity).This would result in the concomitant disappearance of the resident parasitoid population. Thus, selection for highly efficienthost-location behaviors appears to lead inevitablyto an increased likeli- hood of at least local extinctionof such parasitoids.Finally, a logical consequence of this causal chain is that the increased frequencyof an efficientsearching genotypeis accompanied by a decrease in the total abundance of this genotype.

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Some evolutionary processes may counterbalance the selection of over- specialized traits. As conditions approach local populationextinction, selection for traitsthat promote the use of alternativehost species should occur. Under these conditions founder effectsand bottlenecks may intensifyselection and providea hospitablemilieu for genetic changes enablingadaptation to a new host. To the extentthat such counteringforces operate, the overspecializationprocess does not necessarilylead to global extinction.

SUMMARY The use of parasitoidsas an example of overspecializationpermits this evolu- tionarymechanism to be studied more readily. Parasitoids are widespread, are readilycultured in laboratories,have shortgeneration times, and lend themselves to comparativestudies. Several importantquestions can be explored. Are highly host-specificparasitoids more likelyto cause local extinctionof host populations than parasitoids that exhibit low host specificity?What kinds of environmental fluctuationsendanger such specialists? What factorslimit overspecialization?

ACKNOWLEDGMENTS This paper was stimulatedby Gould's (1982) tour de force and a classroom discussion in parasitologyat the Universityof California,Santa Barbara. We thankA. E. Ebeling, R. Fraga, J. Chapman, R. Panza, S. I. Rothstein,the late J. L. King, S. S. Sweet, R. R. Warner,J. D. Shields, and E. G. Leigh for their thoughtful,stimulating, and instructivecomments.

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