Evolution of Feeding Preferences in Phytophagous Insects
Author(s): V. G. Dethier
Reviewed work(s):
Source: Evolution, Vol. 8, No. 1 (Mar., 1954), pp. 33-54
Published by: Society for the Study of Evolution
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EVOLUTION OF FEEDING PREFERENCES IN
PHYTOPHAGOUS INSECTS
V. G.
DETEIER
Baltimore
Department
of Biology,The JohnsHopkins University,
ReceivedMay 28. 1952
The extent to which biological races
representa transientstage in the evolution of species, especiallyamong insects,
has been the subject of extendeddiscussion ever sincetheexistenceof thesecategories was firstdemonstratedby Walsh
in 1864. It is consideredby many that
isolation,at least to some extent,by host
preferences
is a sine qua non forbiological races (Thorpe, 1930; Mayr, 1942;
Huxley, 1942). With such emphasis
placed on host preferenceit is indeed
surprisingthatonlycomparatively
meagre
attentionhas been directedtoward the
physiologyand evolutionof host habits.
A thoroughanalysis of the problemsof
host selectionwould appear to be a logical
prerequisiteto an intelligentunderstanding of the role of biologicalraces in evolution. This reviewhas been undertaken
in .the hope that it will reveal in some
measurethe lacunae as well as the matricesin our knowledgeof one well known
aspect of host selection,namely,the host
preferencesof plant feedinginsects.
I
Conceive,forthe moment,of an organism as a complicatedbiochemicalmachine surroundedby a hostile environment. It may isolate itself completely
and remainquiescentfor long periods of
timeas do seeds, animal spores,and certaindiapausinginsects. Under theseconditionsenergiesare directedtowardmaintainingthe status quo. If the organism
is to accomplishanythingbeyond static
existence,and is to reproduce,theremust
be energy transfersacross the surfaces
separatingthe internalfromthe external
environment.And this too requiresenergy. If an organismis small and contentto sit in one place takingin energv
EVOLUTION
8: 33-54. March,1954.
33
in the formin which it is to be found
there and dyingwhen the supply is exhausted, then the principal, and practicallyonly,requirementfor existenceis
a selectivelypermeable surface through
which the environmentcannot act adversely. From passivityto aggressiveness is a step which involvesfood procurementand locomotion. Execution of
these accomplishmentsin turn requires
a signalsystem,coordinating
mechanisms,
and furthercomplexities.
With the acquisitionof mobility,animals also acquired the potentialitiesfor
expanded opportunitiesfor self selection
of diet, a talentwhich is largelydenied
to sessile organismsand constitutesno
problemfor dormantones: Sessile marine-organisms,for example, can select
only from those food substanceswhich
the environmenttransports to them.
Among sessile species some, such as sea
anemones, do indeed exercise a degree
of selection (Pantin and Pantin, 1943).
Other species, notably cockles, oysters,
and mussels,are generallybelievedto ingest indiscriminately
all particleswhose
size permitshandling(Verwey, 1952).
Throughouttheanimalkingdomthe selectionof diethas becomemosthighlydevelopedamongmobilespecies. It has attained finestdiscrimination
among parasitic forms and, of free-livingspecies,
among those insects which feed upon
plants. Plant feeders account for approximatelyfifty
per cent of livinginsect
species. In no other groups of animals
are feedingpreferencesso sharplydelineated. The questionsas to the originsand
evolution of these precise relationships
existing between certain phytophagous
insects and their host plants are indeed
thornyones. Until recentlythe mecha-
34
V. G. DETHIER
nism underlyingfood preferenceand the are remarkablysimilar in their requiredirectingforces operatingin the execu- ments. All require an adequate supply
tion of the relationshipwere poorly un- of amino acids, a sterol,eight to ten of
derstood and a matter of considerable the known B vitamins,carbohydratein
speculation. Now 'witha clearer under- readilyavailable form,and a numberof
standingof these factorsit is possible to minerals(cf. Trager, 1947 and thepapers
scrutinizemore intelligently
the mass of of Fraenkel and Leclercq). Insects difrecords of insect/plant relationships fer in their quantitativeand qualitative
and do not
forcarbohydrate
which have been bequeathed to us by requirements
scores of field entomologistsand to de- as a rule require fat (Fraenkel, 1953).
rive fromthismiddenof notes some ink- The most successfulof the few attempts
formson a synthetic
ling of the directionwhich the develop- to feed leaf-feeding
mentof intimateinsect/plant
biocoenoses dietwas thatmade withcornborerlarvae
(Pyrausta nubilalis). These grow well
may have taken.
Considered solely from the point of on glucose, casein, cholesterol,corn oil,
view of energy source, organisms are minerals,yeast, choline,and lyophilized
limitedonly by their biochemicalinade- corn leaves. Growthis reduced in the
quacies, and among heterotrophs
the ca- absence of leaf preparation and with
pabilitiesof utilizingenergysources un- yeastreplacedby pure B vitamins(Beck,
der a multiplicity
of formsare such that Lilly, and Stauffer,1949).
the scantyknowledge
Notwithstanding
the majorityof heterotrophsare potentialy omnivorous. In seeking to under- at presentavailable to us it appears unstand the fact of diet selectionthe ques- reasonableto imagine that the,basic rephytophagous
tions then arise: (1) do the various quirementsof the different
species of phytophagousinsectshave dif- species are not essentialythe same, or
ferentnutritionalrequirements? (2) are. that the enzymesystemsof polyphagous
thepreferred
plantssuperiorfromthenu- forms differ radically from those of
tritivepointof view? (3) is the under- strictlymonophagousforms (cf. Brues,
lying basis of plant preferencea nutri- 1920). Perhaps there exist quantitative
degrees
whichreflectdifferent
tional one? These are extraordinarily differences
in the utilizationof availdifficultquestions to answer unequivo- of efficiency
cally because our knowledgeof the nu- able materials. It is a fact that phytotrientrequirementsof phytophagousin- phagous insectsas a group do not pracsects and of the food value of different tice economyof feeding. From one half
plantsand of the same plantundervary- to two thirdsof the food is eliminatedas
ing conditionsis patheticallyscanty. It feces. Most oftheprotein,fat,and simple
must be emphasizedthat thereis a vast carbohydratemay be utilized; but starch
betweenthe food ingestedand and cellulose are excreted mostly undifference
the nutrientsactually required and uti- changed (Fraenkel, 1953). Chlorophyll
lized. - It is an all too commonmistake is degradedbutapparentlynotused. The
to equate gross food intakeand utilizable waste is strikinglyillustratedby the recent work of Gray (1952), who has
constituents(cf. Uvarov, 1928).
Even a reasonably complete under- shown that the pineapple mealybug,
standingof the nutritionalrequirements Pseudococcus brevipes, secretes in its
of phytophagousinsects is not now en- honeydewlarge amountsof as many as
joyed (Uvarov, 1928; Trager, 1947; nine differentamino acids and amides.
Fraenkel,1953). Of those insectswhich The numberof amino acids secretedinhave been studied more or less inten- creases as feedingis increased. Excess
sively, Tribolium confusum, Tenebrio carbohydrateis not, therefore,ingested
molitor, Ephestia kuehniellac,Blatella merelyas incidentalto an attemptto ingermanica,and Drosophila melanogaster sure an adequate proteinsupply.
FEEDING PREFERENCES
IN INSECTS
35
On the otherhand,underthreatof im- tended, that insects may pupate before
pendingstarvationmany insectstend to- maximumgrowthhas been attained,with
ward widerpolyphagyand can surviveon the resultantproductionof runts, that
increasesto varyingextents,and
the altereddiet (Brues, 1939). Further- mortality
more,as Dethier (1947) and othershave thatfecundity
may declineand population
pointedout, even insectswith restricted densitydecrease (Painter, 1951; Fennah,
diets can, by various experimentalarti- 1953; Kennedy,1953). In certainspecific
fices,be induced to feed successfullyon cases the failure of insects to maintain
foreignfood plants.
themselveshas exhibiteda distinctcorAs far as can be judged from avail- relationwith the presenceor absence of
able data, leaves possess ample supplies specificcompoundsin the plant. For exof linoleicacid
oftheessentialnutrients(Fraenkel,1953), ample,a low concentration
from in somefoodplantsofthesugar beetweband thereare not great differences
one species to the next. It is not known worm (Loxostege sticticalis) has been
offemaleswhich
to what extent optimal concentrations associatedwithinfertility
vary with season, growthstage, soil, etc. fed thereonas larvae (Pepper and HastThese changes have been studied inten- ings, 1943). Deposition of lignin and
sively only in a few agriculturalcrops pentosesin alfalfaunderalteredconditions
(and mulberry). In the otherfew spe- of light and moisturehas paralleled recies investigatedthe changes have been ducedfeedingon thepartofthepea aphis,
studied exclusivelywith respectto spe- Macrosiphumpisi (Emery, 1946).
maniHow directlythe aforementioned
cializedcompoundssuch as lignin,carotenoids, and essential oils (Guenther, festationsreflectthe nutritionaladequacy
1948). Fraenkel (1953) considersthat of the plant is a matterof considerable
evidenceis lackingto the effectthat sea- doubt. They do not prove (nor can the
sonal changes in plants are of great im- possibilitybe excluded) that optimum
varycriticallyfromone
portancein the nutritionof insects. Fen- levelsof nutrients
nah (1953), on the other hand, main- species of plant to the next or withina
tains, at least insofaras Homoptera in speciesfromtimeto time. In attempting
observationssuchas theseone
the humid areas of the Neotropical re- to interpret
gion are concerned,that the qualitative must take into considerationthe possible
and toxins
repellents,
compositionof food solutes is not con- actionofattractants,
stantlyoptimal and that relative abun- in influencingthe quantityof food inand min- gested. The studyby Wagner (1944) of
dance of nitrogen,carbohydrate,
eral fractions(i.e., the overall metabolic the feedinghabits of Drosophila mulleri
rate of the host plant) is of greaterim- and D. aldrichiis a case in point. Several
portancethan such gross factorsas total species of drosophilidsfeed in the cactus
or even the C/N Opuntia lindheimeribut actually subsist
nitrogenor carbohydrate
espeupon the various microorganisms,
ratio.
The criteria customarilyaccepted in ciallyyeasts,foundin the cactus. Of the
assessing the nutritionalvalue of food yeast species present,nine supportedthe
are growth,development,longevity,fe- growthof D. mulleribut only six were
to D. aldrichi. This resultby
cundity,and populationdensity. On these satisfactory
bases there can be no doubt whatsoever itselfis not prima-facieevidenceof a difthatcertainspecies,varieties,and organs ferencein the basic nutritionalrequireof plantsserve the growthand reproduc- mentsof the two drosophilids.
tive requirementsof particular insects
Dethier (1947) and Fraenkel (1953)
more effectivelythan do others. The believe that nutritionally
tounimportant
factsare amplydocumentedthat the du- ken stimuli (attractantsand repellents)
ration of immaturestages of insectsfed are predominantly
responsiblefor reguon unfavorableplantsmay be greatlyex- lating the feeding preferencesof phy-
36
V. G. DETHIER
It is suggested (loc. cit.) that one set
tophagousinsects. Kennedyand his coworkers(1950-1953) and Fennah (1953), of compoundsmay be involvedin differon the otherhand,are of the firmopinion entiatingplantspeciesand anotherin leaf
that the relationbetweenpreferenceand age differences.This conceptwould cernutritionalrequirements,especiallyas it tainly agree with evidence from other
is of a more quarters(Dethier, 1953). It would harapplies to tissue preference,
causal nature and of considerablymore monizewiththe idea thatone set of comacknowledged. pounds subserveselaborateecologicaldifimportance
thanheretofore
and theothera moreprobably
Kennedyhas investigatedin great detail, ferentiation
suit- uniformnutritionalrequirement.A tenchieflywithrespectto thedifferential
abilityof leaves of a -singleplant,thefeed- tativealternativeexplanationmay be ofing preferencesof two species of aphids, fered,namely,that these aphids are esthe black bean aphis (Aphis fabae) and sentiallypolyphagous,attackinganyavailthe peach potatoaphis (Mysus persicae). able plantspeciesnot containingrepellent
on or toxic compounds,and that leaf age
Bothoftheseinsectsfeedpreferentially
are governedby one or more
young growingleaves and old senescing preferences
leaves, on both customaryhosts and un- compoundsacting on a contact (gustausual hosts. There is an activebehavioral tory) chemicalsense. These may or may
preferencefor these leaves quite in addi- not be directlyrelatedto nutrition. Such
would not disagreewith
tionto a speciesdiscrimination.Physical an interpretation
stimuliare notinvolved,olfactory
maybe, the observationthat A. fabae appears to
more sharplybetweenleaves
and gustatorymostcertainlyare (cf. Fife discriminate
and Frampton,1936,and Day and McKin- of the same plant than betweenleaves of
non, 1951). While fecundityis admit- two plant species (Kennedy and Booth,
tedlynot an accurateindex of the actual 1951).
Thus, while the recognitionof food by
nutrientvalue of the food ingested(since
tokenstimuliis
unimportant
thereis no controlover the quantityin- nutritionally
differences certainlywell established(Fraenkel and
gested), thefactthatfecundity
correlatedmoredirectlywithleafage with- Gunn, 1940; Dethier, 1947, 1953; Tinin a plant than with plant species differ- bergen, 1951; Thorsteinson,1953), the
good and
ence has promptedKennedy (1953) to relationbetween nutritionally
argue that the factors mediatingintra- sensoriallyattractivematerialsremainsan
dif- open question. It is clear that the four
are fundamentally
specificpreferences
ferentfromthoseoperatingin the case of relevantpropertiesof a host plant-odor,
interspecificpreferences. Both involve taste,toxins,nutrients-occurin varying
as Chin (1950) has shown
but the former combinations,
behavioraldiscrimination,
has been termeda "nutrient"discrimina- for Solanaceae (cf. also Fennah, 1953).
tionin that,it is postulated,A. fabaereacts Kennedyis of the firmopinionthat it is
behaviorallyto certainnutrientsor com- improbablethat these vary randomlyor
poundsassociatedwiththem. The actual that insectsalways react to tokenswhich
involvementof nutrientsrequires proof. mayonlyhappento be associatedwithnuIt has beennotedthatthetwoaphisspecies trients. Yet it has been amply demonin that the physiologi- stratedthatall nutrientsare not stimulatbehave differently
cal ages of the preferedleaves differ ing and that some,compoundswhichare
slightly. Also, there appear to be dif- eminentlyacceptable to insects are nuferencesin the behaviorof alatae and ap- tritionallyinadequate (Vogel, 1931; von
terae (Kennedyet al., 1950). If thepref- Frisch,1934; Trager,1947; Hassett et al.,
a questionofnutrition, 1950).
erenceis so entirely
thenthese different
species and different It is whenthe selectionof plantsby the
nutrient ovipositingfemaleof holometabolousinformsmusthave slightlydifferent
sects is consideredthat a predominantly
requirements.
FEEDING PREFERENCES
IN INSECTS
37
nutritionalapproach is most difficult
to made of birds are particularlypertinent.
invoke. The femaleselectsa plantor part Lack (1949) has observedthatcloselyrethereofwhichis to feed the larvae and is latedbirdslivingin thesame habitatdiffer
not at all the properfoodforherself. In in diet,thattwomonophagousspeciescanthe case of gall insectsand certainminers not persistif theycompetefor the same
whose presencein the planttissue stimu- diet,thatpolyphagousspecieslivingin the
lates that tissue to growthwhich is said same habitatfrequentlyshow an overlap
to be high in nutrients,it can hardlybe in diet. Amadon (1950), in speakingof
argued that the plant or tissue is chosen the Hawaiian honeycreepers,
has pointed
initiallyon a nutritionalbasis since the out thatwherespeciesa alone occupiesan
choice is made before the hypertrophy island it has generalizedfeedinghabits
commences. An outstandinginstanceis but whereit sharesan island withspecies
thatof certainsingle-tissueleaf minersin b each has a restricted
diet.
Indirect evidence of the value of rewhichovipositionon the top surfaceof a
leaf leads the larva to mine in the nutri- strictedfeedingis seen in the numerous
tionallypreferredpalisade layer,and an examplesof widespread,althoughnot inegg on the under surface presents the variable, specialized sharing of the enemerginglarva with the disadvantageof vironment(Huxley, 1942). Rather exmining in the nutritionallyinadequate tensivedata relatingto butterflies
of the
spongyparenchyma(Hering, 1926). All genus Colias have been gatheredby Hoof these lines of evidence indicate con- vanitz (1949, 1950). In NorthAmerica,
is nottheprimedi- C. philodice,feedingon Trifolium,overvincingly
thatnutrition
rectingprincipleunderlyingpreferential laps geographicallyand ecologicallywith
feeding. The failureto surviveand re- C. eurytheme,feedingon Medicago; C.
produceon various plantscannotbe con- christina,
feedingon Astragalusand other
strued ipso facto as indicativeof nutri- legumes,overlapswith C. gigantea,feedtionaldeficiency.As willbe shownbelow, ing on Salix; C. hecla,feedingon Astrabehavioral factors and toxic principles galus, with C. nastes on Astragalusand
play a considerablepart.
Trifolium;C. interioron Vaccinium,with
We must,then,seek elsewhereforpur- C. philodice on Trifolium. C. palaeno,
poses served by food plant preference. C. interior,C. pelidne,and C. behri,all
Obviously,it is ecologicallyexpedientthat feedingon Vaccinium,show some overlap
some specializationof feedinghabits ex- but also considerablegeographicreplaceist. From the point of view of species ment. In the butterfly
genus Basilarchia
competation
thereare advantagesin filling thespeciesB. archippusoverlapstherange
all ecologicalnichesso thatas manyplants ofeach ofthefourremainingspecies (Hoas possible serve as host plants. This vanitz,1950). The foodplantsare identiwould be accomplishedif all insectswere cal for four of the five species. Among
unrestrictedly
polyphagous,but viewed in copperbutterflies
ofthegenusLycaena,L.
terms of interspecificcompetitionpoly- hypophlaeas,feedingon Rumnex,
overlaps
inferiorto monophagy in theeasternUnited StateswithL. epixphagyis distinctly
or oligophagy. To just how greatan ex- anthe,feedingon Vacciniumand withL.
tentcompetition
varieswiththenumberof thoe,feedingon Rumex.
speciesrestricted
to a give foodis a probPolyphagyis a luxurywhichcan be enlem concerningwhichfew pertinentdata joyed under certain conditions only.
are available. Numerous studies have Amongits obviousadvantagesare thelack
been made of protozoa (Gause, 1934, of completedependenceupon the fluctu1937) and of predatorybirds (e.g. Cush- atingfortunesofa singleplantspeciesand,
ing, 1944) but few of insects (cf. Park, too, at least superficially,
betterpotenti1941; Wagner,1944; Crombie,1945; Sol- alities for world-widedistribution.Moomon, 1949). Some of the observations nophagyis a realisticsolutionto theprob-
38
V. G. DETHIER
lem of speciespressure. It too permitsof
world-widedistribution
if it is associated
with a cosmopolitanplant. The milkweed butterfly
(Danaus plexippus),which
in North America feeds exclusivelyon
Asclepias,is an outstandingexampleof a
restricted
feederof wide geographicaldistribution.
The very apt statementof Kennedy
(1953) that "the favouredhost plant is
not merelysomethingfed on, it is something lived on" suggests other services
renderedby preferredfood plants. The
its
plantis acceptedwithits microclimate,
shelter, its predators, its diseases. A
is selected. Comparable
wholecommunity
instances of habitat selection by vertebrates are well known (Miller, 1942).
Finally the plant is not a passive partner
to the association. It also plays a part in
preference,respondingas an organism
and developing protective mechanisms
whichinterfere
with the utilizationof its
tissuesas foodby insects. This aspect of
preferencehas been expounded at great
lengthby Painter (1951) in his book on
plant resistance. In short,the course of
indevelopmentof foodplantpreferences
volves simultaneousevolutionof resistant
mechanismsbyplantsand oftoleranceand
preference
by insectsso thatthepictureat
any time is one of dynamicequilibrium
moving toward a perfectsymbioticrelationship.
When we considertheforegoing
facts,it
is apparentthat we should not expect a
prioria close correlation
betweennutrition
and plantpreferences.The end servedby
foodplantpreferenceis neithersolelynor
primarilya nutritiveone, and in orderto
appreciatetheevolutionary
trendsin feeding preferencesit is desirableto inquire
firstinto the mechanismof the phenomenon.
II
The wholeproblemof foodplant selectionmaybe statedin theformof two primaryquestions: (1) how is thepreference
implemented? (2) what is the genetic
basis and evolutionaryhistoryof specific
plantpreferences?
As a fixedpoint of departureone can
beginwiththe observationthatinsectsas
a group exhibitall degrees of preference
fromthe polyphagousspecies which will
feed on a vast numberof plants to the
monophagousspecies whichrestricttheir
feedingto a singleplantspeciesor variety,
evento a specifictissuetherein. As Brues
(1946) has emphasized,however,there
may exist among the most polyphagous
formsmarkedpreferences
in diet (cf. also
Koyama, 1951). The innatepotentialto
choosedietsthusappearsto be commonto
mostinsectsand differswithintheclass in
degree only. Before considering the
mechanismof plant selection,however,it
is advisable to examine brieflyand to
eliminatesome of thosefactorswhichinfluence superficiallythe expression of
preference
buthave littleor no directbearing on the geneticsof the performance
or
theimmediatephysiologyofhostselection.
To indicatethata plant is preferredis
to implyin the broadestsense thatit will
supporta populationof insectsand permit their propagation. From the point
of view of an individualinsect,however,
a preferred
plantmaybe one thatis more
inacceptable even though nutritionally
adequateor highlytoxic. In thelatterinstancea preferredplant is not to be confused with a susceptibleone. Since the
insect'sdeathis hastened,theplantis protected,and such a plant is as much resistantas thatwhichis unacceptablein the
firstplace. The diversequalitiescomprising resistancehave been studied extensively by Painter,and the subject is excellentlytreatedby him (1951) (cf. also
Snelling,1941).
Preferencepatternsare moldedby geographical expediency, ecological variability,and seasonal cycles. It goes without saying that many plants might be
eminently
acceptableto a giveninsectwere
the geographicalranges of the two coextensive. This has been borne out by
laboratorytests but even more spectacularlyby the behaviorof introducedpests,
FEEDING PREFERENCES
whichin various parts of the world have
tastedand foundto theirlikingplantsnot
formerly
available. It is noteworthy
that
very little thoughtfulinvestigationhas
been directedtoward the restraintsimposedupontheecologicaland geographical
distributionof an insectby the range of
its food plants (but see Huxley, 1942, p.
185; Wulff,1943; Brues, 1946, p. 112;
and Pfadt, 1949). Similarly neglected
are considerationsof the role whichplant
ecology plays in delineatingfood plant
preferences. Of considerableimportare
the inequalitiesof microclimateswithin
the area occupied by an insect or plant
species (see, for example,Wolfe, Wareham,and Scofield,1949). Thus, thereare
manyplantswhichgrow undersuch conditionsoftemperature,
soil charhumidity,
acteristics,and lightas to place thembeyond the pale for certain insects. And
finally,unless the growing season of a
plantcoincideswiththe appearanceof the
feedingstages of an insectthe plant obviouslycannot serve as food. From the
point of view of the plant the foregoing
conditionshave been termedevasion or
pseudoresistance(Painter,1936). In certain cases thepreferences
of an individual
insectchange with the season in accordance withtheseasonalsuccessionofplants.
One very fineexample is offeredby the
swallowtailbutterfly
Papilio machaonL.,
which, in desert areas, feeds on a succession of different
host plants (Buxton,
1923).
Althoughthe phenomenonof evasion
playsa limitedrolein theobjectiveexpression of preferences,
it sheds littlelighton
the dynamicsof selection. Given a number ofavailableplants,preference
operates
by selection on the part of the insect.
But in manyformspreference,as far as
the individualis concerned,is apparent
ratherthan real. It fitsonly the broad
definitionstated previously. An insect
populationmayinitiateattackon a variety
of plants indiscriminately
and be unable
to maintainitselfbecause either (a) the
plantchosen (randomly) was deficientin
required nutrients,(b) contained toxic
IN INSECTS
39
materials,(c) was protectedby physical
whichimpededfeeding,or
characteristics
(d) containedrepellentcompoundswhich
mediated against feeding (cf. e.g. Ishii,
1951). Painter (1936) has classifieda
and b as antibiosis; c and d, as passive
resistance. In all of thesecases thepopulation retiresto a different
plant lacking
or failsto migrate
adverse characteristics
and is decimated. In the absence of migration,survivorsmightformthe cadre
whichcould developby selectionthrough
successivegenerationsa straincapable of
survivingon the resistantplant. This
end has been achieved several times experimentally(see Brues, 1924). In nature it is comparativelyinfrequentbecause insects usually desert an unfavorable plant or are completelywiped out.
In anyevent,thefinalselectionofa susceptibleplantis by defaultand maybe termed
passiveselection. Whereasthismayhave
been the evolutionary
forerunner
of active
selection (see p. 42), it is uneconomical
to thespeciesin theimmediatesense since
such passive selection is regulated by
survivaland involveshigh mortality.
Active selection,on the otherhand, as
with any self selection of diet, presupposes a means of recognition. While
adult insectsare at libertyto select their
own diets, many larval formsare never
granted this opportunitysince they are
restricted
by spatialfactorsto thefoodselected by the ovipositingfemale. Such
larvae, however,in common with those
which employa greateror lesser degree
of foraging are none-the-lessendowed
with the ability to identifya preferred
plant. Whereas thisabilitymay serve no
apparentusefulpurpose in the more sedentaryforms,it is as essential to free
foraginglarvae as to adults. This is especially true in cases where the female
mayovipositon thewrongplant,and many
instancesare recordedin whichthe range
of choice of the ovipositingadult fails to
correspondto that of the larvae (e. g.
Salt, 1935). Then too, many species
simplyovipositin the vicinityof the preferredfood (e.g. Argynnis); and others,
40
V. G. DETHIER
of the subfamily tions. For monophagousand oligophasuch as some butterflies
Hesperiinae,may eject eggs into space to gous species these are chemicallyspecific
fallby the wayside. It is imperativethat stimuli which rigidly control feeding.
larvaeofthesespeciesbe able to searchfor Polyphagousspecies, which usually feed
on any materialthat lacks repellents,are
and recognizesuitablefoodplants.
While vision,phototaxis,geotaxis,and not held undertightreinby specificcomattractiveness
play a part in di- pounds,but the differential
hygrotaxisundoubtedly
rectinginsectsto the properenvironment of various acceptablenonrepellentplants
for ovipositionand feeding,the ultimate undoubtedlyowes its being to different,
forcesworkingat close range are largely ratherlabile taste preferences(cf. Brues,
chemical(cf. Painter,1936, and Dethier, 1947,p. 120).
The remaininglink in the chain of
1947 for reviewand discussionof attracby feedinglies in the
tantsand physicalfactorsgoverningovi- eventsconsummated
position). In order to understandthe realm of plant physiologyand biochemmechanismof action of these, it is con- istry. The plant,whichis the source of
venientto break down into three basic the.chemical stimuli,is by no means a
ofspecificcompounds.
componentparts the behavior pattern standardrepository
which culminates in normal feeding, It is an extremelycomplicatedorganism
in its own right. Among its constituents
namely: (a) orientationto the food, (b)
biting response, (c) continuedfeeding. whichare of importancefromthe insects'
The entirecomplexis underthepredomi- point of view are chiefly:carbohydrates,
nant controlof the chemicalsenses, but fats,proteins,minerals,alkaloids,and eseach phase may be directedby discrete sentialoils. The last two mentionedcomthemaprisethosegroupsthatcontribute
chemicals.
and different
If theinsectis notalreadyin theproper jorityof odors and tastes. The essential
as a resultof having oils include benzene derivatives,straight
feedingenvironment
emergedfromeggs laid there,it is guided chaincompounds,and terpenes. The first
thereby vision,light,gravity,and mois- twogroupsare believedto be derivedfrom
ture. Final orientationto the plant or fat and carbohydratemetabolismrespecproperpart thereofby monophagousand tively. As forthe terpenes,availableevioligophagousspecies is effectedby odors dence suggeststhattheyare derivedfrom
emanatingfromtheplanttissues. In many a commonprecursorin a stepwisefashion
polyphagous species orientationto the (Guenther,1948, 1949).
It has been shownthattheseplantconplantor propertissueis, up to thispoint,
random. At thistime,in theusual course stituentsvary with the time of day, the
of events,a strongbitingresponseis initi- seasons,thegrowthstage of theplant,the
ated by odor,contactchemicalstimuli,or tissue,climaticconditions,and soil condiotherless specificstimuli. The chemicals tions. Consequently,the plant species or
thesetwophasesofbehaviormay variety,althougha botanicentity,is not a
initiating
or may not be identical. Many poly- chemical entity. It is not homogenous.
phagous species are regulated in their Rather is it a heterogeneousmicrochemchieflyby the presenceor ab- ical environmentchanging in time and
preferences
sence of taste substanceswhich are pre- space withchangingconditionsof growth,
sumablynon-specific.The physiologyof climate,and soil. A realizationof this
thesefactorshas been discussedin detail situationrendersunderstandablemanyof
the reactionsof insectstowardtheirhost
byDethier(1947, 1953).
mechanismof plants. It is commonknowledgethatinIn short,thephysiological
active selectiondepends largelyupon ol- sects ovipositonly on certain organs or
factoryand contactchemical (gustatory) tissues,thattrophicformswill eat certain
stimulationby compoundswhich are ef- partsto the exclusionof others,thatnew
low concentra- growthis frequentlypreferredto older
fectiveat extraordinarily
FEEDING PREFERENCES
tissue, that the plant may be relatively
immuinefrom attack at certain seasons,
that the same plantvarietygrownin differentgeographicalareas may be attacked
to different
degrees,thatindividualplants
in a standmayappear moreresistantthan
others,and that susceptibility
may vary
withsoil conditions.
Of especialimportance
is theknowledge
that the syntheticactivityof plants and
the compositionof theiroils is greatlyalteredbyhybridization
and polyploidy,
and
thatmutationscan interruptthe stepwise
productionofterpenesat anypoint(Guenther,1948). Changes of this nature,occurring in the evolution of plants, act
directlyupon the insectsand are of profound,significancein molding feeding
preferences. The consequence of these
interactionswill be realized below.
III
In attemptingto solve the riddles of
the evolutionaryhistoryof active preferenceswe are inquiringintothe,emergence
of definitivebehaviorpatternswhich develop in insects in' conjunctionwith an
evolvingstimulusfieldprovidedby plants.
Many stimuliare preceptedby the sense
organs,but onlycertainones have meaningand set offor releasean aspectoffeeding response. The action of releasingor
of token stimuliis believed to be innate
(Tinbergen,1951), thatis, the natureof
the response is instinctiveand its basis
genetic. Its survivalvalue depends,upon
the closenesswith which it fitsthe need
to be filled. How have the instinctive
responses to diverse token stimuli been
evolved?
Since the pattern of insects' feeding
habitsis by no means static,the progress
of evolutioncan be studiedprofitably
by
reconstructing
the past fromthe current
phylogeneticpicture and by examining
carefullycontemporary
changesand fluxes
in feedingpreferences.Phytophagousinsects were undoubtedlyoriginallypolyphagous (Brues, 1920, 1946; Hering,
1926; Takahashi, 1938). Certainlythe
polyphagous state is more widespread
IN INSECTS
41
amongthe oldergroupsalthoughnot confinedto them. Furthermore,under duress the majorityof species are drivento
greaterpolyphagy. Environmentalsituations which released the feedingbehaviour ofprimitive
polyphagousinsectswere
probablyvery general and non-specific.
This conceptionis certainlyin accordwith
the behavior of contemporarycounterparts. Insectsare obligedto learn which
among a greatvarietyof objects are edible. Two processes,accordingto Thorpe
(1950), may expedite the accomplishment: (1) associativelearningon a trial
and errorprincipleand (2) habituation.
The latter has been definedas "an activityofthecentralnervoussystemwhereby innate responsesto certain relatively
simple stimuli,especiallythose of potential value . . . wane as the stimulicontinuefora longperiodwithoutunfavorable
results." Habituationcould not operate
in monophagousand oligophagousinsects
but may have been influential
in the developmentof them. If, as Thorpe (loc.
cit.) states,"learninginvolvedin perception must . . . be phylogenetically
prior
to anythingwhichcould be classed as instinctand must indeed be an essential
component,on the perceptoryside at
least,ofeventhemostrigidinstinct,"
then
it is not difficult
to conceivehow the instinctivebehavior characteristicof monophagy and oligophagy might have
arisen froma more generalizedbehavior
associated with polyphagy. We can imagine the change as havingbeen brought
about throughthe agency of passive selectionaided by associativelearning,hanaturalselection,and isolation,a
bituation,
collective process culminatingeither in
well developedinnatepreferencesor perpetuated phenotypicpreferences. Five
lines of developmentfrom a primitive
polyphagousstatemay be postulated(fig.
1).
(1) Even in themostliberallypolyphagous formsas, forexample,grasshoppers
(Brunsenand Painter,1938; Pfadt,1949)
and the gipsy moth (Mosher, 1915) the
phenomenonof passive selectionis wide-
V. G. DETHIER
42
/
/ NO SELECTION
NEW MONOPHAGY
r
PASSVEP\REFERENCE
SECIE
SELECTIO0
PLANT MUTATES
|
/ PLANT MUTATES
OLFACTORY
Q
~~~~~~~~~~~~~~~~~~~~~~CONDITIONI
AND SELECTS
NEW PLANT
MUTATIONS
MUTATION,
SELECTION
\
ISOLATIONREMOVED
HYBRIDIZATION
PHENOTYPICPERPETUATION
(HOPKINSHOSTSELECTION)
l
l
MONOPHAGOUS
ISOLATON
NO ISOLATION
ETC.
(V\
/
\
NEW MONOPHAGY
/
MUTATIONS
NON-GENETIC RACES
(LABILE FEEDING PREFERENCES)
FREE HYBRIDIZATION
ISOLATION
CONTINUED
GENETIC RACES
(RIGID FEEDING HABITS)
FIG.
and oligophagy
of monophagy
1. Postulatedlines of development
state.
polyphagous
froma primitive
spread. For mnany
species of insects it survivors were then isolated by such
may be of minorimportanceonly, serv- eventsas prolongedimmaturestages,ening merelyto channelthe activitiesof the forced hibernation,reduced activity,or
species intorestrictedecologicalnichesor comparablealterationsin growthand degeographicalareas or forcingpopulation velopment which would prevent them
movementsof greateror less magnitude. spatiallyor temporallyfrommatingwith
Caution should be exercised,however,in othersof the species,the stage would be
relatingperiodic migrationscausally to set forthe developmentof a so-calledrefeeding requirements(Williams, 1930). sistantrace. It is reasonableto imagine
Where the impactof passive selectionis thegenotypeof manypolyphagousspecies
slightor transient,the action leads to no as being constitutedof large stabilized
significant
changein feedingbehavior;and gene complexesfromwhichspecial-strains
frequencyof
thepolyphagoushabitsofa speciesare re- characterizedby a different
tained. Plant-feedingorthopteroidin- genes may be selected. Spatial isolation
sects representexamplesof groups which would then prevent the mixing of the
apparentlyhave retainedpolyphagyun- genes of such strainswiththose of other
changedfora long periodof time (Brues, segments of the population. It would
1920) and are still affectedby a type of fosterinbreeding. Thus, from a single
polyphagouspopulation it ought to be
passive selection.
(2) Types of passive selectionexempli- possible to separategroups characterized
fied by antibiosisand passive resistance by dissimilar feeding habits. Indeed,
(see p. 39) can, under favorablecondi- such groups have appeared in natureas
tions,formthebasis forthe establishment resistantvarietiesof plantshave been inof new feedinghabits by introducinga troducedor developed. Resistantstrains
selective factor. Of a population of exist in polyphagousinsectsand in those
polyphagous insects which settled by of more restrictedfeedinghabits as well
chance upon an unfavorableplant, only and merely await selection. Painter
a small proportionwould survive. If the (1930, 1941) and Painter and Jones
FEEDING PREFERENCES
IN INSECTS
43
(1948) have shown,forexample,thatthe sects were reared on privet,the normal
hessianfly(Phytophagadestructor)pop- food,foreverygeneration,but samplesof
ulationof Kansas has consistedof a num- each generation were tested for their
ber of strainswhichhave been selectedin abilityto accept ivy by presentationand
the manner indicatedabove. Similarly, preferencetests. Only a poor abilityto
by selectionon a laboratoryscale it is a eat ivy was developed. Ivy-bredinsects,
strains on theotherhand,developedan increased
simplematterto produceartificially
of a polyphagousspecies whichwill feed preferencefor ivy with each successive
successfully
on a plantwhichwas, in large generation. There was no mortalityto
measure, unacceptable to the original be considered,and it wouldappearthatseruledout. The most
population. Representativeexperiments lectionwas definitely
include: transference
of the chrysomnelidsatisfactoryexplanationof these results
condibeetlePhratoravitellinaefromSalix fra- invokesthemechanismof olfactory
gilis to S. viminalis (Schroder, 1903); tioning,which will be discussed below.
thescale Lecaniumrobinarium
frompeach For furtherdiscussion of Sladden's exto locust (Marchal, 1908) ; the caterpillar perimentsthe works of Thorpe (1940)
Lasiocampa quercus from oak to pine and Huxley (1942) should be consulted.
All insectscannotbe manipulatedwith
(Pictet,1911); thesawflyPontaniasalicis
fromSalix andersonianac
to S. rubra (Har- equal facility,nor can any and everytype
rison, 1927). The shiftswere attended of food shiftbe undertaken. Such diwtih high mortalityrates, and survivors versityindicatesthat the degree of plastended at firstto be puny. Eventually, ticityvaries greatlyfromone species to
however,a normallyvigorouspopulation the next. Generallyspeaking,the more
was builtup over a periodof severalgen- restricteda species is in its feeding,the
in alteringits feeding
erations. Most of the timepioneerfeed- greaterthedifficulty
ers experiencedas great difficulty
in re- habits.
turningto theirancestralplantas theydid
(3) Olfactoryconditioningaffordsanin adapting to the new one. This fact, otheropportunity
for the developmentof
plus the initial high mortality,indicates altered feeding preferences. From the
veryclearlythata selectiveprocesswas in timeofWalsh's (1864, 1865) pioneerdisprogress,and thatit screenedout froma coveries of biologicalraces, the idea has
heterozygouspopulationthoseformswith persistedthat some sort of memoryof
changedfeedinghabits. While selection larvalfeedinghabitspredisposesadults of
seems both logical and adequate, it must a polyphagousspecies to ovipositon the
be admittedthatno geneticworkhas been same species of plantas thatupon which
to confirm
undertaken
this. Furthermore, theythemselveshad fed. This idea was
accurateinformation
regardingindividual laterenunciatedas the Hopkins Host Sevariationin host preferencesamong in- lectionPrinciple(Hopkins, 1917). Since
sects and the variabilitywithinpolypha- Hopkins' time numerous investigations
gous populations is completelylacking. aimed at testingthe hypothesishave been
Carefulstudiesof feedinghabitvariability undertaken. At firstglance the collective
among populationsof monophagous,oli- results appear contradictory. In sumgophagous,and polyphagousspeciesof in- mary,it may be statedthat the principle
is valid forsome speciesofinsectsand not
sects would be invaluable.
There are on recordseveralexperiments for others (consult Thorpe, 1930 for a
involvingfood transferencewhere selec- list of those whichdo show a preference
tion does not sufficeto explain the re- for the plant upon whichtheymatured).
sults. Most noteworthyare those con- No evidence favoringthe principlewas
ductedwith the parthenogenetic
stickin- obtained for: the pea weevil, Bruchus
sect Dixippus morosus (Sladden, 1934, quadrimaculatus(Larson, 1927) ; thecodwhich
1935; Sladden and Hewer, 1938). In- ling moth,Carpocapsa pom4onella,
44
V. G. DETHIER
feeds usually on apples but not infre- on fromgenerationto generationa feeding
quentlyon walnuts (Quayle, 1926); the "tradition." In thisway non-genetic
feedhymenopterousparasite Trichogramma, ing races are perpetuated.
groups of whichwere'raised on different The crucialproblemis whethera phehostsforas manyas 43 to 63 generations nomenonlike olfactoryconditioningcan
(Salt, 1935); the European corn borer, bringabout sympatricsplittingof a single
Pyrausta nubilalis (Thompson and populationinto two non-breedingpopuParker, 1928). Artemisiawas believed lations. Mayr (1947) has discussedthis
to have been the originalhost plant for problemcriticallyin considerabledetail.
the corn borer; yet there is no striking It is clear thatin the absence of effective
ovipositionalpreferencefor it. Maize is isolatingmechanismstherewould be free
thepreferred
plant,bothfortheArtemisia hybridizationbetween individuals with
feedingpreferencesso that the
strainand themaize strain;butArtemisia different
exertsa weak attractionforfemalesof its preferencesfosteredby olfactorycondistrainwhilefailingto attractthose of the tioning-could never become sorted out
maize strain. To thisextentthe Hopkins genetically. Instead theywould at most
Host Principleapplies. There is no rea- be perpetuated(because of the female's
races." Thus,
son a priorito expectidenticalconditions preference)as "phenotypic
of olfactory
to exist in different
species. The ermine in evaluatingthe significance
factorforthe
as an effective
moth,Hyponomeutacognatella,although conditioning
closelyrelatedto H. padella,whichshows establishmentof populations with new
a questionof fundaa pronouncedtendencyto split into bio- feedingpreferences,
logicalraces,is itselfquitestable (Thorpe, mental importancearises, i.e., whether
olfactoryconditioningby itselfcan lead
1929, 1931).
ofolfactory
and to any kindof isolationand bringabouta
Untilthedemonstration
pre-imaginalconditioning
by Thorpe and non-geneticmatingpreferenceor restricJones (1937) (see also Thorpe, 1938), tion (cf. Thorpe, 1943, 1944), or whether
there was 'no sound physiologicalbasis the isolationmustbe interjectedfromanwhich would satisfactorilyexplain the otherquarter. If, associated with olfactherewere also specific
principle. Thorpe, and later Cushing toryconditioning,
formemberssimilarly
(1941), were able to show that certain matingpreferences
insects,whilein thelarvalor pupal stages, conditioned,that behavior would supply
became conditionedto the specificodors thenecessaryisolatingfactor. This, howof theirhost or host plant. The parasite ever, is a point upon which few experiHabrobraconcan be conditionedto such mentaldata are available. Whereselective
an extentin thelarvalstageto theodor of matinghas been put to test, the results
an abnormalhostthatit will show an ovi- have been positivethoughnotalwaysconforthathost; Droso- vincinglyso (Thorpe, 1930). Of trepositionalpreference
phila can evenbe conditionedin the larval mendous import is the knowledge of
stage to the odor of peppermint(Thorpe, whetherselectivemating,when present,
1938). While these preferencesarising occursin races thatare geneticor phenofrom conditioningare in no wise so typic. Again, the geneticsof the cases
stronglyingrainedor permanentlyfixed studiedare in doubt. The apple-feeding
strains of Hypoas any germinalpreferences
thatmay ex- and hawthorn-feeding
ist,theymaypossiblybe adequateto serve nomeutapadella do exhibitselectivematin establishingnon-geneticraces charac- ing (Thorpe, 1929). Yet manygood spefeedinghabitsdo not
terizedby the possessionof specificfeed- cies withdistinctive
ing preferences. Cushing (1944) has show selectivematingand do hybridize
presentedevidence that the learning of freely,as, for example,Colias eurythemne
specificfeedinghabits by the young of and C. philodice (Hovanitz, 1948, 1949a,
certainraptorialbirds resultsin passing 1949b). Two strains of Pyrausta nu-
FEEDING
PREFERENCES
IN INSECTS
45
bilalis,the European corn borer,do ex- typicraces would never,in theabsence of
hibit-matingpreferencesfor membersof spatial isolation,lead to geneticallydetheirown strain,but hereit is knownthat terminedpreferences. With spatial isothe strainsare fixedon a germinalbasis lationit can be the firststep in evolution(Arbuthnot,1944). If it should develop ary divergencethroughthe operationof
thatthe preferencesexist only in genetic the Baldwin-LloydMorgan Principle of
races, then other isolating mechanisms organic selection. This states,in effect,
that modificationsrepeated for a numwould have to be invoked.
Olfactoryconditioningcould lead in- ber of generationsmay hold a strain
directlyto isolationthroughfactorsother withinan environmentwhere mutations
thanpreferential
mating. For example,it tending in the same directionwill be
is conceivablethat the rates of develop- selected.
(4) Passive selectionmightoperatedimenton different
plantsmightvary sufficientlyto isolate adults temporally,that rectlyas an isolatingfactorso as to aid
of specializedfeeding
changesin distribution
oftheplantsmight in the establishment
effectit, thattheremightbe selectivefac- habits. A polyphagousspecies, by virtors, quite apart fromthe plants them- tue of its catholicityof feeding,is freselves, in the respective environments. quentlyable to occupy widely divergent
Or, in thecase ofan insectwhosesphereof ecologicalnichesand geographicalranges.
activityis restrictedto the host or its Different segments of the population
immediatevicinity,therewould be some could become restrictedto special groups
degree of spatial isolation. Any of these of plantsmerelyby extendingtheirrange
factors,arisingas an indirectconsequence intoareas whereone speciesof planthapofrestricted
feeding,wouldtendto prevent pens to grow abundantlyto the virtual
hybridization.Isolationarisingfromthis exclusion of others. Or, discontinuities
or any other origin would enhance the in plantrangesarrangedso thatone segchancesof the new feedinghabitsbecom- mentof the insectpopulationfounditself
ing germinallyfixed,but it must be em- in a different
plant communityfromthe
phasizedthatthe provenexistenceof iso- other,and isolated, would assist in the
latingmechanismsotherthan spatial,es- differentiation
of distinctgene frequencies
peciallythe preferential
matingof pheno- in the two segmentsof the population.
typic races, is at the moment lacking. Plant diseases, fire,increasingxeric conFurthermore,
thereare activeforceswork- ditions,inundation,normalplant succesing againstthe establishment
of sympatric sion, glaciation,and cultivationin recent
groups isolated by feeding preference times,all may be operativeat one timeor
alone. One of these is the tendencyof another.
animalsto pass througha dispersalstage
Very few examples of direct isolation
in which they would come into contact are well documented,but two, based on
with other segmentsof the population. indirectevidence,maybe givenas illustraAnotheris the reversibility
of all condi- tive. Larvae of thegeometridmothOpotioningthat is not reenforced. The re- rabia autumnatafeedin Europe on Betula,
view of Mayr (1947) should be con- Alnus,Larix, and Pinus. The subspecies
sultedforfurtherdetails.
filigrammaria
feedsin the larval stage on
The feedinghabitsof phenotypicraces Calluna, Erica, and Vacciniun. Harriwould be expected to be rather labile. son (1920) believed that filigrammaria
Furthermore,it would be expected that evolved fromautumnatawith the assistunder stress of adverse circumstancesor ance of climax glaciationwhich isolated
changed geographic extension of either the parent species into two groups, one
the plant or the insecttherewould be a in the southeastof Europe and the other
facile reversionto other feedinghabits. to the west of Great Britain. It was preIn any event,the establishment
of pheno- sumedthatconditionsin the west favored
46
V. G. DETHIER
the growthof Calluna and relatedspecies
to an extentwhichcaused a reductionin
the ancestralplants,Betula, etc. Consequently,one groupofmothswas restricted
to feedingon Ericaceae while the other
remainedon the originalfood,plants. At
larvae prethepresenttimefiligrammaria
ferCallunaand otherericaceousplantsbut
retain the abilityto eat and develop on
birchas evidencedby successfulbreeding
for fivegenerations. Conversely,autumnata feedssuccessfully
on Calluna. Within historicaltimesa larchfeedingrace of
the Betula-Alnus-feeding
species has developed as a resultof isolationfollowing
the replacementof alders by plantingsof
testswere not conlarch. Unfortunately,
ductedto determinewhetherthe races so
developed are now genotypicor phenotypic. Nevertheless,the example illustratesone way in whicha populationmay
and vagaries
be splitby thediscontinuities
of plantdistribution.
A rather similar account is given of
race evolutionwith concomitantfeeding
preferencedevelopmentin the silkworm
mothgenusPlatysamia(Sweadner, 1937).
At the beginningof the ice age in North
America Platysamiastock was presumed
isolated in two groups,one in the southeast and theotherin thesouthwest. From
the formerthepresentspeciesP. cecropia
arose; from the latter, the species P.
euryalisand P. gloveri. The factorwhich
isolatedthe two groupswas consideredto
have been the presenceof treelessplains
since the larvae are restrictedin their
feedingto deciduoustreesand shrubs. P.
cecropia is liberallypolyphagousin its
habits; P. gloverifeeds on Salix, Ribes,
and Alnus. As the ice retreatedand the
trees followed,the mothsextendedtheir
respectiveranges north. Hybridization
of P. gloveriand P. euryalisin the region
of Nevada gave rise to the formP. kasloensis. When forms migratingup the
Rocky Mountain chain reached Canada,
there appeared a bridge to the eastern
forestsin the form of the wolf willow
Elaeagnus. Part of the genus became
adapted to this food plant and to Salix
and gave rise to the species P. nokomis.
Once establishedin the east P. nokomis
is supposedto have splitinto two groups
one of whichbecameadaptedto larchand
gave rise to P. columbia. Today theform
P. nokomisfeedsprimarilyupon Elaeagnus and Salix; thespeciesP. columbia,on
Larix americana.
feeders
(5) The evolutionof restricted
frompolyphagousformshas been postulated as arising directlyby mutations
becamereproductively
whichsubsequently
isolatedfromtheparentstock. It is difficult to imagine how this end could be
achievedin practice. In general,the importanceof genetic changes as primary
isolating mechanismsis seriously questioned (cf. Dobzhansky, 1941; Huxley,
1942; Mayr, 1942). Specifically,the
problem of isolating mutants with refroma parentpolyphstrictedpreferences
agous stock does not appear possible especiallysincethepolyphagousstockcould
by
equallywell feedon theplantpreferred
the mutant.
There remain for discussion the histories of the aphids, leaf hoppers, leaf
miners, and gall wasps, groups about
which an enormousvolume of unrelated
factsrelatingto feedinghave accumulated,
but in each case the lack of key experiinterpretamentaldata makesany detailedtionof theevolutionof theirfeedingpreferencesin termsof modernconceptshazardous. It also seems wise to hold in
abeyancenew discussionsoftheintriguing
problemof host alternation(see Mordwilko,1928; Kennedyand Booth, 1951).
The gall wasp (Cynips) story is only
slightlymoreamenableto analysis. This
genus, which is restrictedto white oaks,
is presumed to have originatedin the
southwesternNorth America duringthe
Oligoceneor Miocene. Oaks are believed
to have originatedin theidenticalarea and
era. It is assumed that Cynips was always associated with oak. The Pacific
coast populationBesbicus is restrictedto
the group of oaks centering around
Quercuslobata,Q. dumosa,and Q. garryana. It is thoughtto have reached the
FEEDING PREFERENCES
IN INSECTS
47
Sierras before the Great Basin became Pergesa elpenor& which feeds on Epiarid in the Miocene. Ancestralstocksof lobium and Celerio hippophaes ? which
Cynipsechinusand C. guadaloupensisare feeds on Hippophae rhamnoides. The
said to have perpetuateda preferencefor gravid females naturallylaid their eggs
Q. lobata-dumosaand Q. chrysolepsisre- on H. rhamnoides,but the larvae would
spectively. C. centricolais restrictedto feedonlyon Epilobium. Harrison( 1926),
Q. stellata. The C. melleagroupsh6wsa workingwith geometridmoths,crossed
preferencefor Q. stellata; the C. pezomna- males of Lycia hirtaria,which feed on
choidesgroup forthe Q. alba group; the many species of deciduous trees a-nd
C. gemmucla
groupfortheQ. prinusgroup. shrubs,and femalesof Nyssia graecaria
Kinsey (1936) believedthatspeciationin and N. zonaria, which feed on Achillea
and other low-growingherCynipsarose mostcommonlyby mutation millefolium,
and hybridization
followedby isolationin baceous plants. Hybrid larvae fed only
which stricthost preferencesplayed an upon the food of the male parent. They
important role (but cf. Dobzhansky, were sterile,so furthercrosses could not
1941). The lack of physiologicaland be made. Since hybridsof Poecilopsis
ecological experimentsdesigned specifi- pomonaria,whichfeedson manydeciduous
cally to elucidatethe mechanismof host trees and shrubs, including Crataegus,
plant selectioncoupled with the absence and P. isabellae, which feeds solely on
of pertinentbiochemicalstudies on the larch, are cross-fertile,more extensive
oaks, which are a heterogenicgroup in- studies could be undertakenwith these
cluding a great number of biotypes species. F1 larvaefromreciprocalcrosses
(Chaney, 1949), are obstaclesto further fedsolelyon larch. All othercrossesand
analysis.
back crosses up to the F4 producedonly
If geneticraces characterizedby differ- larvae which would feed exclusivelyon
entfeedingpreferences
could have become hawthorn. This reportedresult is diffiestablished,thereafterthe usual mecha- cult to explain on any genetic basis.
nisms of isolation and selection would Sweadner's (1937) experimentson hywork towardspeciation. Usually, spatial bridizationin thegenusPlatysamiayielded
isolation operates first. This goal, the no information
of pertinencehere because
origin of new species, is related to the all hybrids fed successfullyon Prunus
presentdiscussiononly insofaras the es- serotina. Two subspecies of the moth
tablishmentof a species mightsignal the Celerio,C. euphorbiaeand C. mauretanica
hchievementof a new fixed feedingbe- normallyfeed on Euphorbia and refuse
havior. The questionof the actual exist- Salix. Yet thehybridfromC. euphorbiae
ence of geneticallyestablished feeding ? x C. mauretanicae and fromthe recipraces has not been sufficiently
well in- rocalcrossfedreadilyon Salix (Goeschen,
vestigatedto indicate the frequencyof 1913; cf. also Schulze, 1913). Hybridithese groups in nature. In very many zation experimentsin the butterfly
genus
cases crucial experimentswhich would Basilarchiaby Edwards (1877) and Field
identifygenetic and phenotypic races (1910, 1914) yieldedlittleinformation
of
have never been undertaken. Some per- value, again because the feedinghabitsof
tinentdata are available foreightgroups, theseveralspeciesare ratherlabile. Two
but no clear pictureemergesfromthese. species are concerned,B. astyanax and
There is littledoubt that preferencesin B. arthem'is.The hybridof these two is
strictmonophagousand oligophagousspe- the formB. proserpina. Larvae froma
cies are germinallyfixed. The extentto crossbetweenB. astyanax? and B. arthewhich genetic and acquired preferences mis e fed only on cherry,the food plant
intergradein polyphagous species and preferred
by B. astyanax. A capturedfevarious races remains untested. Denso male B. proserpina,oviposited only on
(1909) crossed the two hawk moths, Prunus serotina the preferredplant of
48
V. G. DETHIER
B. astyanax and refused birch, poplar,
Once races have become firmlyestaband willow, the preferredplants of B. lished theywould tend to maintaintheir
arthemis. Larvae fromthe eggs laid by identityby one or more of the several
this female fed on Prunus and meta- mechanismsof isolation. Should these
morphosedintoadultsof whichninewere be discontinued,
thecourseis openforfree
B. proserpina and seven were white hybridizationwith other races to occur.
bandedB. arthemis. Larvae froma cross By such a process secondarypolyphagy
betweenB. archippus ? and B. arthemis can arise. This has undoubtedly
occurred
,3fedon willow,a foodplantacceptableto quite frequentlyin evolution. On the
bothparents. These larvaedevelopedinto otherhand, effectiveisolation,now reintypical B. proserpina. Inability to ex- forcedby associationwith special plants
tendtheexperiments
to succeedinggenera- and ecological niches would lead to the
tionsprecludeda thoroughanalysisof the developmentof species withnarrowlyregeneticsof the feedingpreference. Ho- strictedfeedinghabits. These in turnby
vanitz (1944), workingwith Colias but- directmutationmightgive rise to forms
terflies,has shown that C. eurythemeis withaberrantfeedinghabits,and, if spasterile if the larvae are reared on red tially or reproductivelyisolated, would
clover; C. philodice,sterileif the larvae representthegenesisofraceswithina speare reared on alfalfa. In neithercase, cies separated solely by feedingpreferhowever,do the adultsexhibitoviposition ences. In the last case the problemis
nor the larvae,feedingpref- again thatof separatingthe mutantsfrom
preferences,
erences. The different
diet requirements the parentstock so that geneflowis preof the two species,and phenotypicaltera- vented. Mayr (1947) has pointedoutthat
tions,as well as thepresenceor absenceof new mutantsin diploid bisexual animals
diapause, have a genetic basis which is always occur firstas heterozygotes
which
multifactorial.
will forma bridgewithindividualsin the
Two different
strainsof the European parent stock. A possible mechanism
cornborer,Pyraustanubilalis,were intro- wherebya shiftof feedinghabits might
duced into the United States. The one occurwas suggestedby Stern (see Mayr,
in New England is a multivoltine
strain; 1947) :
i.e., it producesmorethanone generation
"Let theanimalAA, whichis host speper year. The mid-westernstrain was cificon
plant1, have themutationa which
originallyunivoltine. It has been shown
in homozygousconditionproduces host
by Arbuthnot(1944) that the eastern
forplant2. Let us thenmake
specificity
strain is homozygous multivoltine;the
the followingassumptions:
Toledo strain, a mixture of univoltine
and multivoltinegenerations. A strain
"Assumption1: Let AA live only on
of homozygousunivoltinemoths could
plant 1.
be isolatedfromthe latter,but no homo"Assumption2: Let aa live only on
zygous multivoltine
mothscould be proplant2.
duced. Evidence indicatedthat the uni"Assumption3: Let the heterozygotes
voltinestateis recessive. There is a clear
Aa be exactlylike AA.
indication-of
a difference
in hostplantre4: Let therebe littleor no
"Assumption
lationshipsin the two strains (Painter,
the reproductivephase
in
dispfersal
1951). The New England multivoltine
A
so
animals
do not meet aa
that
populationfeedsupon200 different
plants;
animals.
the midwesternstrainis more rigidlyre"'Assumption5: Let A be ill adaptedto
strictedto corn and a few weedy plants
plant2.
associated with corn. Moths of the two
strains exhibit distinct mating prefer"Assumption6: Let aa be ill adaptedto
ences formembersof theirown strain.
plant 1.
FEEDING PREFERENCES
IN INSECTS
49
sequently,feedingpreferences
maychange
to accommodateplant changes,and monophagousinsectsas well as polyphagous
ones enlarge their menu to include additionalplant species as convergentplant
"Then there will be littlemixing be- evolutionprogresses (8). The scheme
tweenthe populationson 1 and 2 and the of evolutionof feedingpreferencesin the
opportunity
is providedfora gradual pil- butterfly
genusPapilio proposedby Dething up of additional genetic differences ier (1941) is a case in point. It illustrates
betweenthesepopulations."
a sequence by which an insect may be
Whether or not such a scheme can broughtinto contactwith new odors to
work remainsto be seen. All evidence which it can become conditioned,and
favoringtheoriginof new restricted
feed- thus,by incorporating
additionalbotanical
ing habits is at best indirectand poorly unitsinto its life,becomeexposed to new
documented. Food plant changes in the streamsof geneticchange.
pierid butterfliesconstitute one case.
The fourhundredor so species in the
Pierid larvae are essentiallycruciferae- genus Papilio may be grouped into four
feeders,buta fewgeneraattackthe Legu- categories: (1) species whose feeding
minosae. -Membersof the genera Catop- habits are varied; (2) Aristolochia-feedsilia and Callidryasare restrictedto the ers; (3) Umbelliferae-feeders;
and (4)
singleplant genus Cassia in widelysepa- Rutaceae-feeders. Investigationinto the
rated parts of the world. It has been -feedinghabitsof the lattertwo groupsreproposed (Brues, 1924) that the ac- veals some suggestivetrendsin the evoluquisitionof a leguminousfoodplantarose tion of feedinghabits in that section of
as theresultofa mutationor someequally thegenus.
basic change.
Only eleven species of Papilio are now
Within historicaltime a change which known to eat Umbelliferae. These are:
can best be explainedon the basis of mu- P. ajax and its races, P. bairdi and its
tationshas occurredin the feedinghabits races, P. zelicaon,P. indra, P. machaon
of the apple-maggotfly,Rhagoletis po- and its races,P. hospiton,P. alexamor,P.
monella. The apple-maggotflyappearsto demoleus,P. ophidecephalus,
P. constanibe nativeto NorthAmerica,whereit ap- nus, and P. paeon. It is curiousthatin a
parently bred originally in Crataegus. large cosmopolitangroup with more or
At the presenttimethereare two strains, less standardfeedinghabitsa few speciec
one of whichbreedsin blueberriesand the should have acquired the Umbelliferaeotherin apples. In thestateof Maine the feedinghabit. The factthatUmbelliferaestrainhas beenpresentfromear- feedersas exemplifiedby P. ajax will eat
blueberry
liesthistoricaltimes;theapple formorigi- species of Ruta suggeststhat theyprobnatedwithinveryrecenttimes. Attempts ably formerlybelongedto the Rutaceaeto transferthe apple strainsto blueberry feeders. To understandthe transition
and -viceversa have been entirelyunsuc- from Rutaceae-feedersto Umbelliferaecessful (Woods, 1915).
feeders,it is necessaryfirstto consider
Up to this point all postulatesimply thechangesthathave takenplace in Rutachangesand mutationslargelyon thepart ceae-feeders. Rutaceous plants may be
of the insectagainsta ratherstableor in- dividedon the basis of theiressentialoils
effectiveplant background. This idea, into four groups: those with lemon or
of course, hardly representsan accurate orange-likeodor containingcitral (e.g.
descriptionof events. The pla-ntunder- Citrus), thosewitha rue odor containing
goes evolutionand exerts a selectiveef- methylnonylketone
(e.g. Ruta), thoseconfecton bothpolyphagous(fig. 1, stage 2)
tainingboth oils in varyingproportions
and monophagousinsects (7-10). Con- (e.g. Zanthoxylum),and those of a mint
"Assumption 7: Let segregated aa
formedon plant1 have difficulties
in
findingplant 2, even though the
originalaa found2.
50
V. G. DETHIER
or camphortype. Most of the evidence exposed to insect attack for the longest
points toward species of Citrus as being periodsof timewould by naturalselection
the originalhost plantsof Rutaceae-feed- develop resistantfactorsto a greaterdeers. The transitionof Citrus-feeders
to gree than others (Painter, loc. cit.). In
Ruta-feedersmay have been gradual,that some species preadaptationoccurs. A
is, Citrusto Zanthoxylumto Ruta. Then wellknowninstanceofthedevelopment
of
the transitionfrom Rutaceae-feedersto resistantstrainsin the absence of insect
Umbelliferae-feeders
may have been af- attack is that characteristicof sorghum
fectedby means of the rutaceous plant (Snelling et al., 1937; Painter, 1941).
Dictamnus fraxinella, which contains Varieties broughtto the United States
methylchavicoland anethole(compounds from Africa and Asia, where neither
foundin Umbelliferae),orPelea madagas- chinch bugs nor similar sorghumpests
carica,whichcontainsanethole. It seems exist,alreadyexhibtedmarkedresistance
probable, however, that the change to to chinchbugs.
such plantsas D. frcaxinella
and P. madaAs an alternativeto the evolvingplant
gascaricaproceededby way of intermedi- actingas a selectivescreen for those inates, Zanthoxylumn
and Ruta, and not di- sects which alone can accommodateto a
rectlyfromCitrus. The proposedline of particularplant mutant,thereis the posevolution would then be Citrus (and sibility of those insects being selected
plants containingcitral) to Zanthoxylum whichwill accept all of the mutants(9).
(or other plants containingcitral and Greaterplasticityof this sort would.lead
methylnonylketone
in varying propor- to the developmentof a polyphagous
tions) to Ruta (or plants containing group. Or, if the various plant mutants
methylnonylketone)
to D. fraxinella(or were to exerciseno selectivevalue as far
similarplantscontainingmethylchavicol, as the insect is concerned, polyphagy
anethole,etc.). Or Ruta may have been wouldagain develop. A similarset ofciromittedfromthe series. P. cresphontes, cumstances,that is, no selective action,
for example,feeds,on a wide varietyof could and does workin anotherdirection
Rutaceae of differentchemical constitu- forthoseinsectspecieswhichundergooltion (Dethier, 1941). Some species such factoryconditioning(10). From a moas P. andraemon,P. cresphontes,
P. ma- nophagousspecies phenotypicraces theochaon,and P. ajax representvarioussteps reticallywould arise.
in the changefromone feedinghabitto a
SUMMARY
new and different
one. The acceptanceof
In viewing the evolution of feeding
food plants from other families (e.g.
Piper) may be explainedin part by their habits withinhistoricaltime we observe
some insectsremainingconstantfor long
chemicalcomposition.
In just whichdirectionP. hospitonand periods, some shiftinggraduallyto new
P. alexanor are progressingis difficult plants or enlargingtheirmenu,some alquite suddenly,
to determinein the face of such a paucity teringfeedingpreferences
of facts. Whether they eat any plants some polyphagousspecies formingbioother than species of Ferula and Seseli, logical ratces,others not, introducedinwhichare characterizedby thepresenceof sects attacking plants not previously
known to be acceptable,and native insulfides,is not known.
As indicatedearlier,those characteris- sects shiftingtheir attack to introduced
tics of plantswhichare operativein host plants. These kaleidoscopicpatternsof
selection,be it active or passive, have a behaviormerelyreflectthe diverse ways
insectspecies may regenetic basis. It has been shown that in whichdifferent
some are due to single genes and others spond to changes withinthe plant. The
to-multiplefactors(Painter, 1951). It is drama of changing feeding preferences
even possiblethatplantswhichhave been observedcurrentlyand in the past thus
FEEDING
PREFERENCES
resolvesitselfinto a dynamicequilibrium
betweentwo changingsystems,the plant
and the insect. The outcomeat any particulartimedependsin large measure on
the geneticpotentialities
and relativerates
of changeand stabilityin the two organisms.
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