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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
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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 evolutionarymechanismsthatcan operate at different
hierarchicallevels: gene, individual,deme, population,and species. He suggested
thatinteractionsbetween these levels can modulateevolutionaryoutcomes. One
such possible interaction,overspecialization,has been describedas the evolution
of highlycomplex and ecologically constrainingtraitsthat convey a selective
advantage to individuals, but lead to a higherprobabilityof extinctionof the
species by restricting
the abilityof the species to withstandenvironmental
change
(Simpson 1953; Cifelli 1969; Valentine 1969, 1973; Bretskyand Lorenz 1970;
Thompson 1976; Gould 1982). Some effectsof environmentalfluctuationson the
extinctionof species of differing
sensitivityto environmentalchange have been
modeled by Leigh (1981).
Observing that overspecializationis a process operatingbetween two levels,
individualand species, Gould suggestedthatoverspecializationmaybe "a central
evolutionaryphenomenonthathas failedto gain the attentionit deserves" (1982,
p. 385). As he remarked,it is usuallydismissedas a minorand unusual phenomenon. Here we discuss the relationshipbetweencomplexityand ecological specialization, provide an operational definitionof overspecialization,and place this
concept in the context of evolutionarytheory.Also, since no widespread and
importantexamples of extantorganismsaffectedby overspecializationappear to
have been identified,we suggestan example thatcould providea systemforthe
studyof this phenomenon.
The presence of complex morphology(or physiology,behavior) does not predict the ecological breadthof a species or its evolutionarylongevity.Complexity
may lead to an evolutionarycul-de-sac or open new adaptive zones (Simpson
1953). Examples fromthe paleontological literaturesupport both alternatives.
Evidence supportingthe firstalternativeincludes the observation that during
periodsof mass extinctionPaleozoic bryozoangenerawithcomplex morphologies
had a higherextinctionrate than simplerforms(Anstey 1978). Complex genera
survived better than simple genera, however, outside these periods of mass
extinction.As evidence supportingthe second alternative,theincreasedcomplexityof limbpairs in ordersoffree-living
aquatic arthropodswas notcorrelatedwith
Am. Nat. 1985. Vol. 126, pp. 387-391.
All rightsreserved.
?) 1985 by The Universityof Chicago. 0003-0147/85/2603-0002$02.00.
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THE AMERICAN NATURALIST
388
TABLE 1
RELATIONSHIP
BETWEEN SELECTION
CONSEQUENCES FOR POPULATION
IF TRAIT BECOMES
WIDESPREAD
Increase or no effecton size
Decrease in size
ON THE INDIVIDUAL AND THE POPULATION CONSEQUENCES
OF SUCH SELECTION
SELECTION FOR TRAIT AT THE
INDIVIDUAL LEVEL
Yes
No
Individual selection,kin
selection
Overspecialization
Group selection
Maladaptation
evolutionarylongevity(Flessa et al. 1975). We suggestthatthe increased complexityin arthropods(with a presumed specialization of function)appeared to
affectonlya few of the repetitivelimbpairs at a timeand thatthe unaffectedlimb
pairs retaineda simple morphology(and presumablygeneralizedfunctions).In
this case, arthropodsmay have acquired specialized limbs withoutsacrificing
generalizedfunctions.
ESSENCE OF OVERSPECIALIZATION
Problems with determiningcomplexity, specialization, and ecological constraintsharplylimitthe usefulnessof a definitionof overspecializationemploying
such terms.We propose thatthe essence of overspecializationis the consequence
forthepopulationof an adaptation.Overspecializationoccurs whentheeffectof 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 thatpromotethe fitnessof genetically relatedindividuals,is similarto individualselection(E. 0. Wilson 1975,p.
117). Group selection may explain the evolutionof traitsthatdo not necessarily
benefitthe individualwhen individualsare organizedinto small, isolated populations. In these structureddemes, selection between populations may override
selectionwithina population(Wright1969; D. S. Wilson 1980,p. 38; Leigh 1983).
We distinguishoverspecializationfromotherformsof 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 selectivelyadvantageousto the
individual,overspecializationis distinctfroma frankmaladaptation.In the table,
sexual selection would be similarto eitherindividualselectionor overspecialization dependingon the populationconsequences of such selection.
The usual examples of overspecializationhave tendedto focus on theseemingly
bizarre traitsthat characterize the peacock, saber-toothedtiger,Irish elk, and
others. In these cases thereis no evidence thata fancytail, big canines, or big
antlers(no largerthan expected foran animal of its size; Gould 1974) would be
ecologically constrainingor necessarilyresultin smallerpopulationsizes.
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OVERSPECIALIZATION
389
By focusingon environmentalchange, the traditionalscenarioforoverspecialization tends to reduce the concept to a truism. Ultimately,all environments
change. Thus, in the long run,any traitmay sooner or laterbecome maladaptive
or appear overspecialized (R. R. Warner,in littera).Such formerlyusefultraits,
now maladaptations followingenvironmentalchange, are distinctfrom overspecialization as definedhere. The negative population consequences of overspecializationare intrinsic,at timesresultingautomaticallyfromthe action of an
overspecialized trait.
AN EXAMPLE
A parasitoid may be definedas a consumer that kills one and only one host
(prey)duringa lifehistorystage (Kuris 1974). Most examples are foundamongthe
hymenopterousinsects. Typically,an adultfemalewasp 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 thenemergesas an adult wasp. Physiologically,parasitoidsresemble
parasites; ecologically, their impact is akin to predation. The consequences
of host-location behavior by parasitoid insects show that in an ecologically
significant
groupof organismscomposed of manyspecies, overspecializationis an
importantevolutionarymechanism.Female parasitoidinsectshave evolved complex searching mechanisms to locate suitable hosts, traits that are obviously
criticalto femalereproductivesuccess. Dependingon the particulartypeof host,
such locatingbehaviorsmayinvolvevisual, olfactory,tactile,and auditorycues in
various combinations(Askew 1971; Cade 1975).
Parasitoids are oftenhighlyefficientsearchers. The abilityof manyparasitoid
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
biologicalcontrolagentsforhost insectsthatare agriculturalpests (Huffakeret al.
1971; Kuris 1973). But, thereinlies the rub. Ultimately,however,the selectionfor
efficient
searchingbehavior,so necessaryforthe success of the individualinsect,
causes a dramatic and often persistentdepletion of the host resource. The
parasitoidpopulationis therebyalso reduced. That manyhostinsectsare 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 highprevalence of parasitoidsis
oftenrecorded (Huffaker1971; DeBach 1974).
Presumably, low-densityhost populations are more likely to undergo local
extinctionthanhigh-density
populations(see Murdochet al. 1984forevidence of
local extinctionfromparasitoid activity).This would resultin the concomitant
disappearance of the residentparasitoid population. Thus, selection for highly
efficienthost-locationbehaviors appears to lead inevitablyto an increased likelihood of at least local extinctionof such parasitoids.Finally,a logicalconsequence
of this causal chain is that the increased frequencyof an efficientsearching
genotypeis accompanied by a decrease in the total abundance of thisgenotype.
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390
THE AMERICAN NATURALIST
Some evolutionary processes may counterbalance the selection of overspecialized traits.As conditionsapproach local populationextinction,selection
for traitsthat promotethe use of alternativehost species should occur. Under
these conditions founder effectsand bottlenecks may intensifyselection and
providea hospitablemilieuforgeneticchanges enablingadaptationto a new host.
To the extentthatsuch counteringforcesoperate, the overspecializationprocess
does not necessarilylead to global extinction.
SUMMARY
The use of parasitoidsas an example of overspecializationpermitsthis evolutionarymechanismto be studied more readily. Parasitoids are widespread, are
readilyculturedin laboratories,have shortgenerationtimes,and lend themselves
to comparativestudies. Several importantquestions can be explored. Are highly
host-specificparasitoidsmore likelyto cause local extinctionof host populations
than parasitoids that exhibitlow host specificity?What kinds of environmental
fluctuationsendangersuch specialists? What factorslimitoverspecialization?
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 fortheir
thoughtful,
stimulating,and instructivecomments.
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