Beetle Horn Dimorphism: Making the Best of a Bad Lot
Author(s): William G. Eberhard
Source: The American Naturalist, Vol. 119, No. 3 (Mar., 1982), pp. 420-426
Published by: The University of Chicago Press for The American Society of Naturalists
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420
BEETLE
THE AMERICAN NATURALIST
HORN DIMORPHISM: MAKING THE BEST OF A BAD LOT
There has been interestrecentlyin the occurrencein a single species of more
than one adaptive behavior or morphology.One kind of explanationfor dimorphismsof thistypeis thattheyconstitutefrequency-dependent
evolutionarystable
strategies(Gadgil 1972; Maynard Smith 1976), withthe reproductivepayoffsfor
one typeequal to those fortheotherbecause of the balances of costs and benefits
forthe two forms,and thattheyare thus maintainedin a sortof balanced genetic
polymorphism.A second possibilityis thatpayoffsforthetwo formsare notequal
but thatthe alternativeformsrepresentfacultativealternativesdesignedto funccircumstances(different
tionin different
body size, season, etc.; see Warneret al.
1975; West-Eberhard1979; Dawkins 1980 discusses both typesof explanation).
A classic example of such a dimorphismoccurs in some species of homed
beetles in which thereare two more or less distinctforms:large individualswith
well-developed horns ("majors"), and smaller ones which lack or have only
poorly developed horns ("minors") (Arrow 1951). Evidence is accumulating
(Eberhard 1977a; Palmer 1978; Eberhard 1979and references;Eberhard 1980; M.
Peinador, in prep.) that beetle horns commonlyfunctionas weapons in intraspecificbattles. The fact that the horns of many species representsubstantial
proportionsof the beetles' body weightsargues that natural selection in these
species has stronglyfavoredincreased fighting
ability.Since beetles do not grow
aftertheirlast moult(and minorsare thuscomdemnedto remainminorsfortheir
entireadult lives), the continuedexistence of hornlessor nearlyhornlessforms
seems paradoxical since one mightthinkthat selection should eliminatethose
individualspoorly equipped to fight.
This studyof the dimorphichorneddynastinebeetle Podischnus agenor Oliver
shows that the behavior and ecology of minormales differsfromthat of major
males in ways which suggest that the minor formis a facultativeadaptation
designed to reduce directcompetitionwithmajor males, and thus to compensate
partiallyforthecompetitivedisadvantageresultingfromtheminors'smallersize.
THE
BEETLE
Larval Podischnus agenor live undergroundand feed on humus in the soil,
while adults emergeabovegroundin the rainyseason (Septemberto December in
Cali, Colombia, where this study was conducted) to burrow in thick-stemmed
grasses such as sugar cane and corn where theyfeed and mate (Guagliumi1962;
Eberhard 1977b). Laboratoryrearingdata (Guagliumi1962) indicatethatthe life
cycle lasts about a year, and field observations (Eberhard 1977b) show that
females become common in sugar cane stalks about 1-3 wk aftermales have
begun to appear abovegroundin large numbers.
Only adult males have horns, and they use them as clamps and levers in
Am. Nat. 1982. Vol. 119, pp. 420-426.
? 1982 by The Universityof Chicago. 0003-0147/82/1903-0011$02.00.
All rightsreserved.
NOTES AND COMMENTS
421
complex fightsforpossession of burrowsin cane stalks (Eberhard 1977b, 1979).
Larger males consistentlydefeatsmallerones. Large males have well-developed
hornson bothhead and prothorax,but smallones have relativelyshorthead horns
and only vestiges of thoracichorns. These differencesin horn developmentare
not simply extremes of a smooth gradient,but rather representtwo distinct
morphs,as shown by the bimodal distribution
of head hornlengthsin the population and the sigmoid relation between head horn length and elytralwidth (a
convenientmeasure of body size; fig. 1).
Behavioral Differencesbetween the Morphs
Podischnus agenor obviouslyevolved in an environmentdifferent
fromthatof
today in whichthe beetles findhuge plantationsof food plantsavailable. It is thus
not appropriateto measure the present day reproductivesuccesses of the two
formsand then make subtle interpretations
of theirevolutionaryorigins. It is,
however,valid to look forbehavioraldifferencesbetweentheforms,assume that
these differencesmust have been adaptive when they evolved, and then draw
formsmay have arisen.
inferencesabout how and why the different
By markingmales with numbersscratchedon theirelytraand thenfollowing
theiractivitiesin selected portionsof cane fieldsthroughoutthe approximately
3-mo season of maximumadult activityfortwo successive years,I foundthatthe
behavior of minorsdifferedin two importantways-fromthat of majors. First,
minorswere active earlierin the season than majors (fig.2); they constituteda
substantialpartof the male populationwhen femaleswere stilluncommon,then
later virtuallydisappeared. In 1976 but not 1977 they reappeared in reduced
numberstowardthe end of the season. It is not knownwhetherthe smallermales'
earlieremergenceswere simplythe resultof theirhaving shorterdevelopmental
times or whetherother mechanismsare involved; the latterseems more likely
since smallerfemalesdid not appear earlierthanlargerones. The importantpoint
is that earlier emergence could reduce the probabilityof direct conflictwith
majors.
In addition,as shown in table 1, minorswere less oftenrecapturedin tunnels
other than those in which they were marked (the beetles' burrowingactivities
usuallycaused the stalkto die, and burrowswere inhabitedforan average of only
4.3 days, N = 322). This was truedespitethefactthatproportionally
moreminors
were marked early in the season each year and thus were more available for
recapture.This differencein recapturerates could conceivablyresultfromminor
males having eitherlower survivorshipor greatertendencyto disperse. Direct
data on longevityin the field are not available, and of course are extremely
difficult
to obtainin mobile species such as thisone, but thereare indicationsthat
thedifferences
in recaptureratesprobablyresultedat least partlyfromdifferences
in dispersal tendencies. Most recapturesof both major and minor males were
of individuals which had been found only a short time before. In 1976, for
example, 56% of the 57 beetles which were recapturedhad firstbeen seen and
marked less than 8 days previously. Minor males kept under very unfavorable
conditions(capturedlate in the season and kept withoutfood in moistenedfrass
422
THE AMERICAN NATURALIST
A
N= 625
5
OF HE.40H00]
LENGTH
10
B
N = 625
5
Cl-
~
~
~
Cu
WIDTHOF ELYTRA
.5
.
-.6
,b
U-~~~~~~~~~~~~~~~~C:1
=
I.2.
.7
I~~~~~~~~~~
.3
MAXIMlUM
119TH1flF[LYTPA
FIG. 1.-A, Distribution
ofheadhornlengths;
ofelytrawidths(an indicator
B, distribution
ofbodysize); andC, relationship
betweenelytrawidthandheadhornlength
inPodischnus
agenor.
NOTES AND COMMENTS
423
1976
5X- lOX(N = 74)
I
Ir
I
Jik
4lK
_i_
14X-(N76)
I1o-
6XI-
l
(N
99
r.--I-,r
16X- 23X(N 94)
9X
r*71-{f{1I11
6X1 19X1(N =122)
28I
.3
II
3XI - 11XL (N = 91)
22XI- 27XII (N = 127)
.2
F
5 -IOX o (N =77)
15X- 25X(N=117)
26X -3X1
1977
15VIII- 301X(N = 132)
.4
_
14XI (N = 78)
HTF1I
1--
OF HEADHORN
LENGTH
.5
.6
Fl f
rnm4ThEm
.2
.3
.4
.5
.6
LENGTH
OF HEADHORN
during
the
headhornlengths
numbers
ofmaleswithdifferent
FIG. 2.-Changes inrelative
earlyintheseasonin
malesweremorecommon
rainyseasonsof1976and 1977.Small-horned
bothyears.
fromburrowentrances)lived on the average morethana week (8.5 days,N = 22).
Underbetterconditions(capturedearlyin theseason and keptwithabundantfood)
they lived for an average of nearly 2 mo and their longevitydid not differ
fromthatof majors (P > .4, Mann-WhitneyU test). Thus the more
significantly
than eightfolddifferencein recapturerates was probablynot due exclusivelyto
senescence differences;even under extraordinarilydifficultnutritionalcircumstances in captivity,old minorslived on the average longerthanthe medianlapse
of time between firstsightingand recapture.
It is still possible that the differencesin recapture rates could be due to
differencesin predationrates on the two forms,althoughthere is no reason to
expect this. I saw only scattered,occasional evidence of predationin the field
(small accumulationsof elytraand hardbody parts)duringseveral hundredhours
ofobservationbothat nightand duringtheday. There was no signofpredationon
beetles in theirburrowsin the cane.
424
THE AMERICAN
NATURALIST
TABLE 1
RECAPTURESOF MALES OF DIFFERENT SIZES (largermales recapturedmore often)
Major
(Head Horn > 1.17 cm)
1976 ..........
1977 ..........
Mean .........
NOTE.-N
24%(N = 289)
I O%(N = 296)
17%(N = 585)
Intermediate
(1.17 ? Head Horn ? .56 cm)
Minor
(Head Horn < .56 cm)
8%(N = 95)
9%(N = 114)
9%(N = 209)
4%(N = 75)
O%(N = 47)
2%(N = 122)
= total numbersof individualsmarked.
The probable differencesin emergencetimesand dispersalmay representways
in which minormales reduce directcompetitionwith majors, by avoidingthem
both in timeand in space. Both behaviors would minimizethe minors'disadvantages as poor fighterswhich resultfromtheirsmall size.
Maintainingthe Dimorphism
For the complex behavioraland morphologicaldimorphismof thisspecies to be
maintainedby genetic differencesbetween morphsthere would have to be (1)
linkageamong genes forhorn morphology,body size, emergencetime,and dispersal tendency,and (2) absence of environmentaleffects,especially larval nutrition, on adult size. This combinationof conditionsseems veryunlikely.A large
numberof genes must be involved in determiningthese characters,and larval
nutritionis known to influenceadult size in many insects (Wigglesworth1965).
Beetle horn developmentis rigidlyassociated withextremesof adult size; there
are no small "majors" nor large "minors" known. Furthermore,size-related
facultativepolymorphismsare well known in insects. Numerous well-studied
examples occur in the social Hymenopterain whichthe extensivebehavioraland
morphologicaldifferencesbetween workers and queens are determinedby differencesin quantityand qualityof larval food (Brian 1979). Similar size-related
behavioralpolymorphismsare also knownin solitaryaculeate Hymenoptera(Alcock 1979). Finally,experimentalmanipulationof the nutritionof nymphsof the
dimorphicearwigForficulaauricularia showed thatthe amountof food consumed
determinedthe adult morphadopted (Kuhl 1928).
There is an additional,theoreticalreason forexpectingdimorphismslike thatof
P. agenor to be facultative.If a characterdepends on or is stronglyinfluencedby
and larger
body size for its effectivefunctioning(e.g., horns serve for fighting,
theneven ifthedimorphismoriginally
males are strongerand thusbetterfighters),
arises as a geneticpolymorphismtherewill be selection forthe abilityto switch
forms on the basis of body size. This argumentapplies equally well to the
possibilitythatindividualscan choose eithermorphbut make the choice in some
probabilisticway withoutregardto theirown particularcircumstances("mixed
ESS" strategy;see Dawkins 1980). In effect,males whichcan choose the alternative behavior and morphologymost appropriatefor their body sizes will be
superiorto those condemnedto eitherof the alternativesirrespectiveofbody size
(similarargumentsare givenin West-Eberhard1979; Cade 1979a; Dawkins 1980).
NOTES AND COMMENTS
425
DISCUSSION
The followingsequence of events could lead to the evolutionof behavioraland
to body size (or otherparameterssuch
structuraldimorphismslinkedfunctionally
as age, season, etc.). (1) Under conditionsof intenseintraspecificcompetition,
natural selection could favor "alternative behavior" (e.g., early emergence).
Alleles for this behavior mightspread eitherby the kind of ESS envisioned by
Gadgil (1972) or, if theirexpression was conditionedon appropriatecues (e.g.,
body size), by the selectiondescribedabove. In thefirstcase selectionwould then
favorany allele which repressedthe alternativebehavior in appropriatecircumstances. (2) As such a "switch" became established,individualsnotcarryingboth
the switchand alternativebehavioralleles would be selected against.At thispoint
alternativeforms(e.g., small males) would have a fitnessless than that of the
others,but the differencewould be less thanit was originally.(3) Selection would
favor alleles which furtherrefinedthe effectsof both the switchand alternative
would become morepronouncedand
behavioralleles. (Phenotypicmanifestations
more consistentlyassociated withappropriatecues, e.g., body size; bothcharacters would often become multi-allelic.) It would also favor morphological
modificationsappropriateto the alternativebehavior (e.g., reductionof hornsin
small individuals).These changes would furtherreduce the differencesbetween
the fitnessesof the two alternativeformsbut stillnot necessarilymake themequal.
This scheme contrastswith several discussions of polymorphismsin insects
(Gadgil 1972; Alcock 1979; Cade 1979a, 1979b, Brockman 1979; Brockmanet al.
even thoughtheir
1979) in thatalternativemorphscould be maintainedindefinitely
reproductivesuccesses were not equal to those of the originalforms.
AlthoughP. agenor shows structuralas well as behavioral componentsof its
dimorphism,it can clearlybe added to the growinglistof species withalternative
behavioralstrategiessuch as satellitemales, etc. (e.g., Warneret al. 1975; Emlen
1976 and references;Hamilton 1979; Cade 1979b; Alcock 1979; Thornhill1979).
The acquisition of satellitemorphologyas well as satellitebehavior such as has
happened in P. agenor is probablyparticularlylikelyin holometabolousinsects
since theiradult size is fixedonce theymatureand is determinedlargelyby larval
size priorto adulthood.A switchmechanismsensitiveto larval size could thusbe
positivelyselected undera long historyof intensemale-malereproductivecompetition.
ACKNOWLEDGMENTS
I thank Mario Carpena for facilitatingwork at Ingenio Melendez, and M. J.
West-Eberhardforcommentson the manuscript.Financial supportwas provided
by the Comite de Investigaciones,Universidad del Valle, Cali, Colombia.
LITERATURE
CITED
diversityin male reproductivestrategiesin some bees
Alcock, J. 1979. The evolutionof intraspecific
and wasps. Pages 381-402 in M. Blum and N. Blum, eds. Sexual selectionand reproductive
competitionin insects. Academic Press, New York.
426
THE AMERICAN NATURALIST
Arrow, G. H. 1951. Homed beetles. Junk,The Hague.
and division of labor. Pages 121-222 in H. Hermann, ed.
Brian, M. V. 1979. Caste differentiation
Social insects. Vol. 1. Academic Press, New York.
Brockman, H. J. 1979. Diversityin the nestingbehavior of mud-daubers(Trypoxylonpolitum Say;
Sphecidae). Fla. Entomol. 63(l):53-64.
Brockman,H. J., A. Grafen,and R. Dawkins. 1979. Evolutionarilystable nestingstrategyin a digger
wasp. J. Theor. Biol. 77:473-496.
Cade, W. 1979a. Alternativemale reproductivebehaviors. Fla. Entomol. 63(1):30-45.
1979b. The evolution of alternativemale reproductivestrategiesin field crickets. Pages
343-380 in M. Blum and N. Blum, eds. Sexual selection and reproductivecompetitionin
insects. Academic Press, New York.
Dawkins, R. 1980. Good strategyor evolutionarilystrategy?Pages 231-249 in G. W. Barlow and J.
Westview, Boulder, Colo.
Silverberg,eds. Sociobiology: beyond nature/nurture?
Eberhard,W. G. 1977a. Fightingbehaviorof male Golofa porteribeetles (Scarabeidae: Dynastinae).
Psyche 83(3-4):292-298.
1977b. La ecologia y comportamientodel cucarr6n de la cafia Podischnus agenor
(Scarabeidae; Dynastinae). Rev. Col. Entomol. 3(1-2):17-21.
1979. The functionof horns in Podischnus agenor (Dynastinae) and other beetles. Pages
231-258 in M. Blum and N. Blum, eds. Sexual selection and reproductivecompetitionin
insects. Academic Press, New York.
1980. Horned beetles. Sci. Am. 242(3):166-182.
Emlen, S. T. 1976. Lek organizationand matingstrategiesin the bullfrog.Behav. Ecol. Sociobiol.
1:283-313.
Gadgil, M. 1972. Male dimorphismas a consequence of sexual selection. Am. Nat. 106:574-580.
Guagliumi,P. 1962. Las plagas de la cafia de azucar en Venezuela. Centro Invest. Agron. Maracay
Monogr. no. 2, tomo 1.
males in figwasps and otherinsects. Pages 167-220 in M.
Hamilton,W. D. 1979. Winglessand fighting
Blum and N. Blum, eds. Sexual selectionand reproductivecompetitionin insects. Academic
Press, New York.
Kuhl, W. 1928. Die Variabilitatder abdominalKorperanhangevon Forficulaauricularia, L. Z. Morph
Oekol. Tiere 12:299-532.
Maynard Smith,J. 1976. Evolution and the theoryof games. Am. Sci. 64:41-45.
Palmer, T. J. 1978. A hornedbeetle which fights.Nature 274:583-584.
Thornhill,R. 1979. Competitive,charmingmales and choosy females: was Darwin correct? Fla.
Entomol. 63(1):5-30.
Warner,R., R. Robertson,and E. G. Leigh. 1975. Sex change and sexual selection. Science 190:633638.
West-Eberhard,M. J. 1979. Sexual selection, social competition,and evolution. Proc. Am. Philos.
Soc. 123(4):222-234.
Wigglesworth,V. 1965. Insect physiology.Methuen, London.
WILLIAM
SMITHSONIAN TROPICAL RESEARCH INSTITUTE
ESCUELA DE BIOLOGIA
DE COSTA RICA
UNIVERSIDAD
CIUDAD UNIVERSITARIA, COSTA RICA
SubmittedOctober 6, 1980; Accepted June 18, 1981
G.
EBERHARD