Notes on the evolution of unpalatability in butterflies by means of individual selection

3 Pages·2003·2.3 MB·English

by  Luka Kassarov

Journal ofResearch on Ike Lepidoptera 37: 71-73, 1998 (2003)
Opinion
«
Notes on the evolution of unpalatability in
butterflies by means of individual selection
In the following note, arguments are presented must obviously be acceptable by the predator as
which challenge: 1) theevolutionofunpalatabilityin palatableregardlessofanytoxinitcontains. Logically,
butterflies by means ofindividual selection, 2) the the chemical factor causing unpalatability must
hypothesis suggesting that Batesian mimics would possessaflavorthatthe birdpredatorisable to taste,
have a good opportunity to evolve unpalatabilityby andon thebasisofthistaste, isthenabletorejectthe
individual selection, and 3) an existing hypothesis preypromptlywithoutharmingit.
foramechanismoftransitionfromBatesianmimicry To taste a butterfly and release it unharmed
toMullerianmimicry. (without disrupting the integument), the factor(s)
rendering the butterfly distasteful (unpalatable)
R. A. Fisher (1930) recognized that natural must be located on the water-impermeable outer
selection actingon individualswas a plausible force surface ofthewingorontersurface ofthechitinous
leading to evolution of distastefulness. The bodyand mustbewater-soluble. Onlywater-solnble
argtimentsfortheevolutionofunpalatabilitybymeans substances in form offree molecules can be tasted
ofindividual selection are essentiallyas follows: An (Zweers 1982). The onter surface ofthe chitinous
individual carrying a mutation that renders it less integumentandthewings,however,doesnotcontain,
palatable,andresultsin itbeingrejectedmoreoften nor it can retain, water-soluble molecules (see
by predators, will have a selective advantage over Ktissarov 1999).
normal individuals similarly attacked if the more The only way a bird could taste a butterfly and
distasteful insect is able to escape and reproduce release it unharmed requires tasting withont
moreoften thanthe“normals” (Benson 1971;Haney disruptingthe integrityofthe integnment. Thismay
& Paxton 1981). The fundamental prerequisite for happen onlywith the minimal loss ofasmall partof
evolutionofunpalatabilityin butterflies,bymeansof thewingcaughtin thebeak-beak-marktasting,orby
individual selection, requires that the distasteful non-lethal pecking. Such precision is beyond the
mutantofapalatablespeciesmustsundve theattacks abilityofabird’sgustatoryapparatus. Theapparatus
ofpredatorsandsubsequentlyreproduce. is simply not sensitive enough in terms of the very
Because thereisnovisualdifferencebetween the small numberoftaste receptors (tastebuds) and the
distastefulmutantandthenormalpalatableform,the manner oftheir distribution on the tongue and in
onlywayforabird (the main vertebrate predatorof the beak cavity. The issue is discussed in detail in
butterflies) to perceive thatthe mutantisdistasteful Kassarov (1999, 2001)
isbytastingit. Tosundve,themutantmustberejected Bydeduction the unpalatable mutant individual
bythe predatorand released unharmed after being gains no protection from predator attack because
caught, tastedandfound distasteful. Tobe efficient there is no wayfor the birds to differentiate visually
and effective at this task, the specific chemical between the normal form and the new noxions
compound(s) that render the mutant unpalatable mutant. Toachieve protection, itisessential thatthe
cannotbeatoxin. Thisisbecauseofthemanifestation noxiousmutant advertisesitsdistasteful quality, i.e.,
ofthesymptomsoftoxicityarenotinstanttmeous. For it must acquire an aposematic color pattern as the
example, a bird vomits after consumption of a theoiy of aposematism postidates. Thus, to avoid
monarch {DanauspkxippusL.) containingatleastone being attacked, the mutant must differ from the
EDgjjcardiacglycosidesorseveralmonarchswith low palatable normalform notonlybytaste. There must
toxicitycontainingatotalofone oftheglycosides be a visible difference that the bird is able to
(Brower & Fink 1885). To be eaten, the monarch discriminate and perceive as a warning signal that
72 /. Res. Lepid.
the mutantindividual should be avoided. However, example, polymerization, that provides a hardened
the last condition further necessitates previous chitinotis integument. It seems highly improbable
encounter(s) ofthe bird predatorwith the mutant, that chemical compounds that supposedly rendera
memorizingtheencounter, recognizingthe mutant butterfly distasteful simultaneously cause the
andthendifferentiatingitfromthenormalform.The integument tobecome tough and resilient.
mutant has to sun'ive the encounter(s) to become Thus, asumvalofthe mutantmustbestochastic:
fixedasanewform. the mutant simplywas notcaughtbya predatorand
Thus, itseemsreasonable thatdevelopmentofan managedtomateandreproducebychance. Random
aposematic (advertising) colorpattern necessitatesa predation, given a very low initial frequency, may
simultaneous mutation in the color pattern of the confer relative protection of the rare mutant that
mutant. However, novel warning variants gain no might thus increase its chance for sinwival. The
protectiveadvantagefrom theircolorpattern, since mutant maysubsequentlyincreasesinfrequency,but
predators cannot have previously encountered and this will occur only as long as the frequency of the
learned theircolorpatterns. Thisleadstofrequency- mutantremainsveiylow (see Mallet & Singer 1987,
dependent disadvantage of a rare variant within a Endler 1991).
species (Mallet & Singer 1987). Also, warningly While the unpalatable mutant remainsveryrare,
coloredvariantsmaybe moreconspicuousthan non- itwillbeeffectively“hidden”. So,whatselectiveforces
aposematic prey. “At very low frequencies, a couldlead toan increaseinfrequencyofthemutant?
conspicuousmutantwillnotberememberedhowever There is no apostatic selection because the bird
memorable it is because predators nearly always predatorcannotexertaselective pressure. In order
encounteritonlyonce” (Mallet&Singer 1987). And to exert selective pressure, the bird must be able to
“So little information isretained about conspicuous recognize both the unpalatable mutant and the
mutantsbypredators thattheirconspicuonsnessisa palatable form and avoid the mutant. Since there is
constant detriment because it increases the rate at no visual difference between the distasteful mutant
which they are detected” (Servedio 2000). To and the palatable form, the frequencies ofmutants
perceive the new conspicuous color form (the and palatable normals in the population will not be
mutant) as conspicuous, the bird has to taste it subjected to selection, and the rare mutants will
without disrupting the integrity of the integument receive noadvantage.
and release it without diminishing its future Huheey (1961) stated that “it seems likely that
reproductivesuccess. Thewholestoiygetsentangled unpalatablecharacteristicsareofteneliminatedfrom
in aviciouscircle. populations when in the incipient stages simply
Anotherfactorwidelyconsidered responsiblefor because the bearers did not survive the tasting
the survival of aposematic butterflies (insects) is procedure and the characteristic was not as yet
toughness and resilience of the integument. sufficiently widespread to benefit the entire
Wikhmd and Jand (1982) suggested that because population;” and further suggested, “that Batesian
many aposematic species are tough and difficult to mimics would have a good opportunity to evolve
kill (Cott 1940; Edmunds 1974), toughness would unpalatability by individual selection. Being
reduce the risk of lethal attack and allow enough protectedfromattackbythe model, anytendencyto
distasteful individuals to escape to favor develop distasteful qualities will be enhanced since
distastefulness. But “this begs the question ofhow predators would attack and taste them cautiously.”
toughnessevolves” (Endler 1991). Thus, toughness Under this scenario, it is the palatable mimic that
oftheintegumentcannotbeconsideredasprotecting mutates to unpalatability. Since both mimic and
thedistastefulmutantofapalatablebutterflybecause distasteful mutant are protected by the model, and
the evolution of toughness must precede the because there is no visual difference between the
mutation, orboth mustappearsimultaneouslyorbe mimic and the mutant, bothwould be attackedwith
genetically linked. There are no published data equal caution. The bird perceives them as the same
concerningacausal relationshipbetween toughness varietyinthesamemannerasadistastefulmutantofa
oftheintegumentandchemicalcompoundsthatmay palatable butterfly not mimicking a distasteful one.
render the insect distasteful. Such a relationship Since themutantis,infact,amimicofthemodel,but
could exist if based on a chemical reaction as, for unpalatable (distasteful) and thebirdperceivesitas
,
.,
37 71-73 1998 2003 73
: , ( )
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Acknowledgments
Dr.ThomasC.EmmelandDr.AlbertG.Moatread
earlierdraftsofthemanuscriptandprovidedhelpful
criticalcomments.
LukaKassarov,ResearchAssociate. FloridaStateCollectionofArthropods,DPI, FDACS, P.O.Box 147100,
Gainesville, FL32614-7100, USA. Correspondingaddress: 130 Spruce Street 28 B, Philadelphia PA 19106,
USA. e-mail:[email protected]