The Evolution of Body Size, What Keeps Organisms Small

The Evolution of Body Size: What Keeps Organisms Small?
Author(s): Wolf U. Blanckenhorn

Source: The Quarterly Review of Biology, Vol. 75, No. 4 (Dec., 2000), pp. 385-407
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VOLUME
75, No. 4
DECEMBER
THE QUARTERLY
of
2000
REVIEW
B JOLOGY
THE EVOLUTION
OF BODY SIZE:
WHAT KEEPS ORGANISMS SMALL?
WOLF U. BLANCKENHORN
ZoologischesMuseum, UniversitdtZurich
Winterthurerstrasse
190, CH-8057 Zurich, Switzerland
ABSTRACT
It is widely
agreedthatfecundity
selection
and sexualselection
arethemajorevolutionaryforces
thatselect
forlargerbodysizein mostorganisms.Thegeneral,equilibrium
viewis thatselection
forlargebodysizeis eventually
counterbalanced
byopposingselective
forces.MVhile
theevidence
forselection
favoringlargerbodysizeis overwhelming,
counterbalancing
selection
favoringsmall
lessobvious.
bodysizeis oftenmaskedbythegoodcondition
ofthelargerorganismand is therefore
Thesuggested
costsoflargesizeare: (1) viability
costsinjuvenilesdue tolongdevelopment
and/or
costsin adultsandjuvenilesdue topredation,
fastgrowth;(2) viability
parasitism,orstarvation
becauseofreducedagility,increaseddetectability,
higherenergy
heatstress,and/or
requirements,
intrinsic
costsofreproduction;
(3) decreased
matingsuccessoflargemalesdue toreducedagility
and/orhighenergy
successoflargefemalesand
and (4) decreasedreproductive
requirements;
malesdue tolatereproduction.
A reviewoftheliterature
indicatesa substantiallackofempirical
evidencefor thesevarious mechanisms
and highlights
theneedfor experimental
studiesthat
addressthefitnesscostsof beinglargeat theecological,physiological,
specifically
and genetic
levels.Specifzcally,
and comprehensive
theoretical
investigations
casestudiesofparticularmodel
in timeand spaceis sufficient
speciesareneededtoelucidatewhether
tocountersporadicselection
balanceperpetualand strongselection
forlargebodysize.
sizes over evolutionarytime (Cope's rule: Bonner 1988; McLain 1993; Jablonski 1997), and
most importantquantitativetraitsunder sexual size dimorphism (SSD) increases with
evolutionaryscrutiny.This is because body size whenmales are thelargersex but decreases
size is stronglycorrelated with many physio- with size when females are the larger sex
logical and fitness characters (Peters 1983; (Rensch's rule: Rensch 1959; Fairbairn1997).
It is widelyagreed that fecundityselection
Reiss 1989; Roff1992; Stearns1992). Body size
also exhibitsprominentgeneral evolutionary in females and sexual selection in males are
trends.Taxa are believed to evolvelargerbody the major evolutionaryforces that select for
INTRODUCTION
BODY SIZE continuesto be one of the
The Quarterly
ReviewofBiology,
December 2000, Vol. 75, No. 4
Copyright? 2000 byThe University
of Chicago. All rightsreserved.
0033-5770/2000/7504-0001$02.00
385

THE QUARTERLY REVIEW OF BIOLOGY
386
genetic
correlations
FS
SexS
constraints
4-
constraints
females
males
BodySize
FIGuRE 1.
MAJOR SELECTIVE PRESSURESTHAT

AFFECT THE EVOLUTION OF BODY SIZE
AND SEXUAL SIZE
DIMORPHISM (SSD).
forthecase wheremales are

Bodysize distributions
larger than females are depicted. Fecundity selection
(FS) tends to select for increased body size in females,
and sexual selection (SexS) for increased body size
in males;adultandjuvenileviability
selection(VS) is
assumedtoselectforsmallerbodysizeinbothsexes.
Thesethreemajorselective
pressures
arethought
to
in the sexes,resultingin the
equilibratedifferentially
SSD observed
inanyparticular
species.Somegeneral
constraints
aswellas geneticcorrelations
betweenthe
limittheevolution
sexesthatpotentially
ofSSD areindicated.
largerbodysize in manyorganisms(Figure 1).

In most ectotherms,the number of eggs a female produces increases stronglywith body
size (Wootton 1979; Shine 1988,1989; Honek
1993- Andersson 1994:252). Even in endotherms,where female reproductivesuccess is
oftennot limitedbypropagule number,larger
femalesoftenproduce offspring
of betterquality(Clutton-Brocket al. 1982, 1988). There is
also ample empiricalevidence in manyspecies
for greater mating and reproductivesuccess
of large males, be it mediated by male-male
competition or female choice (Shine 1989;
Andersson 1994). The general, equilibrium
viewis thatselectionforlarge bodysize is eventuallycounterbalanced by opposing selective
forces, primarilyviabilityselection (Endler
1986; Arak 1988; Travis 1989; Schluter et al.
1991;Andersson1994; Figure1). Such counterbalancing selection may be sufficientif it oc-
VOLUME
75
curs in only one sex, because body size is typicallyhighlygeneticallycorrelatedbetweenthe

sexes (Lande 1980; Reeve and Fairbairn1996).
Withinsome limitsset by genetic (Reeve and
Fairbairn 1996), phylogenetic (Cheverud et
al. 1985), and developmental and physiological (Peters 1983; Reiss 1989) constraints,the
threemajorselectivepressuresare thusthought
to equilibrate differentially
in the sexes, resultingin the SSD observedin a particularspecies (Fairbaim 1997; Figure 1). However,while
the evidence for fecundityand sexual selectionfavoringlargerbodysize is overwhelming,
or anyotherformof selecevidenceforviability
tionfavoringsmallbodysize is relatively
scant.
This article outlines the mechanisms proposed in theliteraturethatare believedto limit
body size in multicellularorganisms(Table 1).
The argumentscan be subdivided into three
classes according to the level of biological organization at which theyare expressed: ecological,evolutionary,and physiological.I comprehensivelyreviewand discuss the evidence
forthese mechanismsin an attemptto understand why demonstrations of the disadvantages of large body size are relativelyuncommon in the literature,even though theyare
crucial for explaining why we are not surrounded bygiganticorganisms.Studies (up to
1998) in the literaturethat demonstrate the
disadvantages of any morphological traitindicativeof large body size were compiled. The
studies are of varyingquality,but no restrictionswere placed on the findings;finaljudgement is leftto the reader. The vastmajorityof
studieswere on animals,but studies on plants
were included wheneveravailable.
ECOLOGICAL
VIABILITY
MECHANISMS
DISADVANTAGES
OF
LARGE BODY SIZE
Viabilityselectionagainstlarge body size can

occur at the preadult (uvenile) and/or the
adult lifestages.Juvenilemortality
ratesfeature
centrallyin mostlife-history
optimalitymodels
that tryto predict optimal growth,development,age, and size at maturity
(Roff1980,1992;
Stearns and Koella 1986; Kozlowski 1992;
Stearns 1992). These are the viabilitycosts of
becoming large.
There are two distinctsources of mortality
thatrelateto thebodysize eventuallyachieved

DECEMBER
2000
EVOLUTION
387
OF BODY SIZE
TABLE 1
withassociated
costsofbeinglarge
againstlargebodysizetogether
AMechanisms
thatselect
Cost of largesize
Selectionmechanism
1. Larvalor adultviability
selectionagainstlarge d Y
(a) Viability
costoflong development(predation,
or starvation)
parasitism,
costoffastgrowth(predation,parasitism,
(b) Viability
or starvation)
or increased
costof reducedagility
(c) Viability
detectability
(size-selective
predationor parasitism)
largesize
(d) Tirneand energycostof supporting
(size-selective
starvation)
(due to pleiotropy)
costof reproduction
(e) Viability
mortality)
costofbleatstress(size-selective
(f) Viability
(g) Mutationalload
2. Sexual (and reproductive)

selectionagainstlarged
costof reducedagility
(a) Matingor reproductive
costof energy(and time)
(b) Matingor reproductive
limitation
3. Selectionforearlierreproduction
at smallsizein 9
(reproductive
selection)
at largesize
Energeticcostof reproducing
in d
4. Selectionforearlierreproduction
(protandry)
laterat largesize
Matingcostwhenreprodtucing
5. Selectionforefficient
matefindingthatproduces
dwarfd
costwhenreproducing
Mating,search,and viability
laterat largesize
at reproduction (Table 1): (la) To achieve a

largersize, it is oftenassumed thatorganisms
have to growforlonger time; and (lb) If individuals want to achieve a large body size without extending their prereproductiveperiod
(i.e., development time), they have to grow
faster.In the firstcase, the longer prereproductiveperiod increases cumulativemortality
before reproduction due to predation, parasitism,and/or starvation,given nonzero mortalityratesat all times (Roff1980; Stearnsand
Koella 1986). In the second case, mortalityis
likelyto increase because of higherpredation
associated withthe riskierforagingnecessary
to achieve fastergrowth (Fraser and Gilliam
1992; Werner and Anholt 1993; Abrams et al.
1996), or higher metabolic demands necessaryfor fastergrowthunder resource limitation (Clutton-Brocket al. 1985; Gotthardet al.
1994; Blanckenhorn 1998). It is obvious that
these sources of mortalitystronglydepend on
a varietyof environmentalvariables,particularlytemperature,which is known to strongly
affectpatternsof growth,development, and
body size (Atkinson1994). While thereis substantial (and even genetic) evidence forthese
two trade-offs
between development rate and
mortalityand between growthrate and mortality (Partridge and Fowler 1993; Arendt
1997), the centralproblem withrelatingthese
viabilitycosts to body size is that individuals
which died duringjuvenile development cannot later be measured (Reznick 1985; Blanckenhorn et al. 1998). It is possible to use propagule, larval,or juvenile size as an estimateof
finalbody size, as all these measures are often
et al. 1988;
correlated(Clutton-Brock
positively
Roff 1992: Chapter 10; Sinervo et al. 1992),
but this disregards phenotypic plasticityin
growthand development,whichcan oftencompensate forinitialdisadvantagesin propagule
size (Arendt 1997; Nylinand Gotthard1998).
selection
viability
Detection of prereproductive
against large body size based on mechanisms
(la) and (lb) is thereforedifficult-perhaps
impossible,ifdue to selectiveabortion (Trivers
et al. 1985)and Willard1973; Clutton-Brock
except via selection experiments(e.g., Millar
and Hickling1991; Partridgeand Fowler1993;
Miyatake1995).
Greater mortalitydue to being large is expected, based on four furthermechanisms
(Table 1); these pertain to both adults and juveniles. (ic) Large individualsare more visible

388
VOLUME
75
TABLE 2
Viability
selectionagainst largejuvenilesize
Species
Environmental
variability
Mechanism
Method of demonstration
References
MAMMALS
Humans
(Homo sapiens)
Stabilizing selection analysis
BIRDS
Great tit
(Parus major)
Blue tit
(Parus caeruleus)
Analysisof field survival
Collared flycatcher
(Ficedula albicollis)
Stabilizing and directional

selection analysis
Garter snake
sirtalisfitchi)
(TThamnophis
(1c) ?
Predation
Side-blotched lizard
(Uta stansburiana)
Smooth newt
(Triturusvulgaris)
Fire-bellied toad
(Bombinaoriantalis)
(1c) ?
Predation
Silverside
(Menidia beryllina)
(1c)
Predation
Predation experiment
Capelin
(Mallotus villosus)
(1c)
Predation
10
Trout
(Salmo trutta)
(id) ?
11
(1c)
Predation
12
REPTILES
AMPHIBIANS
FISH
White sucker
(Catostomuscommersoni)
False pilchard
(Harengula clupeola)
(1c)
Predation
13
Spot
(Leiostomusxanthurus)
(1c)
Predation
14
(Continued)
and less agile and maneuverable. This is expected to resultin disproportionatepredation

(Ghiselin 1974; Andersson 1994), and perhaps parasitism(Solbreck et al. 1989; Zuk and
Kolluru 1998), on large individuals, despite
theirgreaterstrength.(1 d) Largerindividuals
require more food to supportthemselves(and
theiroffspring),whichincreases mortalityrisk
under resource limitation (Clutton-Brocket
al. 1985, 1988; Reiss 1989; Blanckenhorn et al.
1995; but see Millar and Hickling 1990). This
reflectsthe global argument that,because of
competition,thereis not enough food in most
natural environmentsto allow individuals to

DECEMBER
EVOLUTION OF BODY SIZE
2000
389
TABLE 2
Continued
Species
Environmental
variability
Mechanism
References
INSECTS
Melon fly
(Bactroceracurcubitae)
+
Fruit fly
(Drosophilamelanogaster)
Mosquito
(Aedesspp.)
(la), (le) ?
Selection experiment
15
(lb), (le) ?
16
(1c)
Predation
17
Caddisfly
(Chironomustentans)
(1c)
Predation
18
Various aquatic insect larvae
(1c)
Predation
Stomach content analysis
19
(le) ?
Genetic trade-off
20
(id) ?
Light and
moisture
Selection analysis
21
OTHER INVERTEBRATES
Polychaete
(Streblospio
benedicti)
PLANTS
Impatienspallida
1) Van Valen and Mellin 1967. 2) Gebhardt-Henrich and van Noordwijk 1991; Linden et al. 1992. 3) Julliard et al.
1996. 4) Linden et al. 1992; Merila et al. 1997. 5) Jayneand Bennett 1990. 6) Sinervo et al. 1992. 7) Bell 1974, 1978.
8) Kaplan 1992. 9) Gleason and Bengtson 1996. 10) Litvak and Legett 1992; Elliott and Leggett 1997. 11) Elliot
1990a,b. 12) Kelly 1996. 13) Shealer 1998. 14) Rice et al. 1993. 15) Miyatake 1995. 16) Wilkinson 1987; Bierbaum
et al. 1989; Partridge and Fowler 1993. 17) Fincke et al. 1997. 18) Macchiusi and Baker 1991. 19) Parker 1993.
20) Levin et al. 1991. 21) Stewartand Schoen 1987.
grow bigger. (le) Larger individualsin good

condition may reproduce earlier in life (because theyhave grownfasterasjuveniles) and
showgreaterreproductiveeffort(Reznick1985;
Madsen and Shine 1994). They are consequentlyexpected to suffera greatercost of reproduction,which ultimatelyshould become
manifestedintrinsicallyas a negative genetic
correlationbetween longevityand early (and
high) reproductiveeffort(Eklund and Bradford 1977; Hillesheim and Stearns 1992; Westendorp and Kirkwood 1998). This is best investigatedusingselectionexperiments(Reznick
1985, 1992). (if) Largerindividualsmaysuffer
greaterheat stress(discussedunder physiological mechanismsbelow). Mechanisms (1c) and
(1d) have been invoked in particularwithregard to flyingorganisms(Anderssonand Norberg 1981; Koenig and Albano 1987; M0ller et
al. 1998), and there is some comparativeevidence in birds (Anderssonand Norberg 1981;
Balmford et al. 1993; but see below). Some

additional (but presumablyrare) mechanisms
of adult viabilityselection against large body
size are size limitationby the overwintering
site (a plant) in a beetle (Ott and Lampo 1991),
and the limited availabilityof large shells in
hermitcrabs (Vance 1972; Harvey 1990).
Tables 2 and 3 listempiricalstudies thatreport (occasional) viability costs associated
withlargejuvenile and adult size, respectively.
In some species withcontinuous growth(particularlyfish),size-selectivepredation is often
reported without reference to whether the
preywasjuvenile or adult, so most studies appear in Table 2 (compare Sogard's (1997) reviewon size-selective
mortality
ofjuvenilefish).
The method of demonstrationand the (presumed) mechanism are given. Except for
some special cases, four classes of studies can
be identified.First,experimentalstudies (e.g.,
ofsize-selectivepredation) are clearlythebest,

390
as theydirectlyinvestigatea particularmechanism.Second, studiesthatemployquantitative

selection analysis(Arnold and Wade 1984) or
some precursor thereof (e.g., Mason 1964)
are primarilyphenomenological, so the selection mechanism is oftenunknown or unclear
(indicated by question marksin Tables 2-4).
Third, studiesthatanalyze survivalin the field
correlausinga varietyofmethodsare typically
tional, unless manipulations were used. The
fourthclass is selectionor othergeneticexperiments necessarilyrestrictedto the lab. The
environmentalvariabilitycolumn in Tables 2
and 3 featuresa plus sign ifthe phenomenon
has been observed in some environmentsbut
not others (i.e., for some traits,with regard
to some predators,at some temperatures,in
some seasons or habitats),no sign ifonly one
environmentor data set was assessed, and a
minus sign ifthe phenomenon was consistent
in more than one environment.Juvenilemortalityis generallynot assessed with regard to
sex (Table 2), whereas sex-specificselection
foradults is indicated ifknown (Table 3).
There are fewspecies forwhichviabilityselection against large juvenile size has been
demonstrated (Table 2), and there are more,
but stillnot many,species forwhichanalogous
viabilitycosts of (some aspect of) adult body
size have been demonstrated(Table 3). Some
patternswith regard to taxonomic group or
method emerged. Manystudiesapplied selection analysisand are thusmerelyphenomenological. Environmentalvariationis ubiquitous;
in a givenspecies,viability
selectionagainstlarge
size seems to occur only occasionally. Sizeselective predation is common, whereas sizespecificparasitismmay occur but is rarely(if
ever) documented (mechanism (1c): Solbreck
etal. 1989;Nishida1994;Zuk and Kolluru1998).
Energeticcostsof supportinglarge body sizes,
mechanism (ld), are ofteninvoked but rarely
(if ever) demonstrated (compare physiological mechanisms below). Viabilitycosts of reproduction, mechanism (le), have been revealed byselection experimentsin some taxa,
primarilywell-studiedand common laboratoryanimals like mice (Eklund and Bradford
1977; Millar and Hickling 1991) or Drosophila
melanogaster
(Wilkinson1987; Bierbaum et al.
1989; Partridge and Fowler 1993), and it
would be desirable to add some more species
VOLUME
75
to this list (e.g., Miyatake 1995). Few studies

of plants were found, but most animal taxa,
except the verysmall bodied and uncommon,
are represented. Large-bodied species have
the advantage thattheirmortalitycan be better observed in the field. On the other hand,
experimental(e.g., predation) studiesare naturally rare in birds and mammals and more
easilyconducted withsmall-bodiedspecies. Interestingly,
theyare most common in aquatic
habitats (Tables 2 and 3).
Research biases, possiblymotivatedby theory, practical, and/or economic considerations,have certainlycontributedto the lack of
studies that investigateviabilitycosts of large
size.For example,size-selective
predationseems
to be an issue in aquatic but not terrestrialorganisms (Tables 2 and 3). This point is clearly
illustrated by the literatureof the past ten
years (1988-98), which I compiled using the
research database OVID. Of 94 studies found
on thissubject,only4 involvednonaquatic prey
and only 11 nonaquatic predators;38 studies
merelydiscussed the subjectbut contained no
data, and 9 studies were models. This shows
that size-selectivepredation features prominentlyin theory.Moreover, in the 47 studies
which presented data, predators preferred
large individualsof a particularpreyspeciesin
27 cases, smallindividualsin 24 cases, and had
no preferencein 7 cases; in 11 studies,environmentally-mediatedvariabilityin preferences
of the predatorwere reported.This illustrates
an additional point. Studies often take the
viewpointof the predator,such as in optimal
foraging(e.g., Sutherland 1982; Stephens and
Krebs 1986), whereas here we are interested
in the viewpointof the prey. It is likelythat
several predators prey on the same species,
some of which prefersmall and others large
individuals (e.g., Lining 1992; Rice et al.
1993; Reznick et al. 1996). Therefore,the net
resultforthe preymaybe no size-specificmortalitydifferencesoverall. Studies of interactions of single predator withsingle preyspecies are thus a good start but necessarily
incomplete. Systematiccase studiesof preyorganismsare needed.
Overall, evidence for viabilitybenefits of
large size (reviewedin Roff1992:117; Andersson 1994) is much easier to findthan evidence
for viabilitycosts. Moreover, the fact that in

DECEMBER
2000
391
TABLE 3
selection
Viability
againstlargeadultsize
Species
Environmental
variability;
sex affected
Mechanism
Methodof demonstrationReferences
MAMMALS
Reindeer
(Rangifert. tarandus)
Mouse
(MIus musculus)
Y;-
(lb), (1d), (le)
Weasel
(Mustela erminea)
Y; +
Kudu
(Tragelaphusstrepsiceros)
6; +
Humans
(Homo sapiens)
(ic), (id) ?
Y;-
Life table analysis of field

survival
(id) ?

survival
(ic), (id)?
Predation;
Energy limitation

survival
(ib), (id), (le) ?
Mortalityrecords
Analysisof field survival;

Experimental manipulation
Mortalityrecords
BIRDS
Barn swallow
(Hirudo rustica)
d; +
Sand martin
(Riparia riparia)
Y; +
(id) ?
Herring gull
(Larus argentatus)
Y; +
(id) ?
Energy limitation
(breeding or winter)
Red-winged blackbird
(Agelaiusphoeniceus)
d; +
(id) ?
Energy limitation
(breeding)

Brown-headed cowbird
(Molothrusater)
d; +
(id) ?
Energy limitation
(winter)
An-alysisof field sur-vival
10
House sparrow
Y; +
(ic); (id) ?;
Storm; Energy
limitation (winter)
Directional selection analysis
11
Y; +
(id), (le) ?
12
Y; +
(ld)
13
Y; +
Selection analysis
14
15
16
An-alysisof field survival
17
(Passerdomesticus)
Song sparrow
(ic), (id)
Parasitism?;
Foraging cost
(Melospiza
melodia)
Galapagos finch
(Geospizafortis)
REPTILES
Gecko
(Aristelliger
praesignis)
Adder
Y; +
Y; +
( Vipera
berus)
Marine Iguana
(Amblyrhynchus
cristatuts)
(ic) ?
Predation
(id) ?
Prey limitation
(id) ?
Energylimitation
AMPHIBIANS
Bullfrog
(Rana catesbeiana)
d; -
(lc)
Predation
(Continued)

392
VOLUME
75
TABLE 3
Continued
Species
Environmental
variability;
sex affected
Mechanism
Method of demonstration References
FISH
Sailfin molly
(Poecilia latipinna)
Y; +
(1c)
Predation
18
Mosquitofish
(Gambusia affinis)
(1c)
Predation
19
(1c)
Predation

using fisheriesrecords
20
21
Population and sex

comparison
22
23
Laboratory experiment
24
Pacific salmon
(Oncorhynchus
nerka)
INSECTS
Bug
(Euschistusvariolarius)
6 Y
(1c)
Storm
Bug
(Lygaeusequestris)
Y; +
(1c)
Parasitoids
Bug
(Colpula lativentris)
Spruce bud moth

(Zeirapheracanadensis)
Y; +
(if)
White-tailedskimmer
(Plathelmislydia)
d; +
(id) ?
Energy limitation
(breeding)
25
Damselfly
(Enallagma boreale)
Y; +
(1c) ?
Stabilizing selection analysis;

26
27
28
29
Simulated predation experiment
30
31
Beetle
d Y
(Acanthoscellides
alboscutellatus)
(1c) ?
Fungal Parasite
Entrapment in
overwinteringsite
(plant)
Digger wasp
(Bembixrostrata)
Y;-
Parasitoid wasp
(Goniozus nephantidis)
Y; +
Bee
(Centrispallida)
Burrowingbee
(Amegilladazvsoni)
d; -
Scorpionfly
(Harpobittacusnigriceps)
d Y; +
(ld) ?
32
Water strider
(Aquarius remigis)
d Y; +
(le) ?
Directional selection analysis;

33
Fruit fly
(Drosophilamelanogaster)
Y; +
(le)
34
d Y;-
(if)
35
Analysisof field and lab

survival
36
37
?
(1c)
Predation
(1c), (ld) ?
Predation
OTHER
INVERTEBRATES
Millipede
(Alloporusuncinatus)
Isopod
(Asellusaquaticus)
Amphipod
(Hyalella azteca)
;d Y; +
(1c)
Predation
(Continued)

DECEMBER
2000
393
TABLE 3
Continued
Species
Environmental
variability;
sex affected
Mechanism
Method of demonstration References
Waterflea
(Daphnia lumholtzi)
(Ic)
Predation
38
Waterfleas
(Daphnia pulex)
(Daphnia hyalina)
9; +
(1c)
Predation
Laboratory predation
experiment
39
Copepod
(Eudiaptomusgracilis)
(1c)
Predation
Laboratory predation
experiment
40
Various Sea urchins
Y;-
(1c)
Predation
41
Various parasitic Gnathid

Isopods
Y; +
(1c)
Predation
42
Cockles
(Cerastoderma
edule)
(1c)
Predation
Foraging experiment
43
Dog-whelk
(Nucella lapillus)
Y;
44
Littleneck clam
(Protothacastaminea)
Y; +
(1c)
Predation
45
Clam
(Anodontagrandis)
Y;-
(Ic)
Predation
Food residue analysis
46
47
MOLLUSKS
Oyster
(Agerostrea
mesenterica)
Y?
Zebra mussel
(Dreissenapolymorpha)
Y; +
(1c)
Predation
48
Marsh periwinkle
(Littorariairrorata)
(1c)
Predation
49
Snail
(Umboniumn
vestiarium)
(1c)
Predation
50
Snail
(Bittumvarium)
(Ic)
Predation
51
Snail
(Cepea hortensis)
Y; +
(if) ?

52
Various mollusks
Y; +
(1c)
Predation
53
1) Skogland 1989. 2) Eklund and Bradford 1977; Millar and Hickling 1989. 3) Powell and King 1997. 4) Owen-Smith
1993. 5) Holzenberger et al. 1991; Westendorpand Kirkwood1998. 6) M0ller et al. 1998. 7) Jones 1987; BryantandJones
1995. 8) Monaghan and Metcalfe 1986. 9) Johnson et al 1981; Searcyand Yasukawa 1981; Yasukawa 1987; Weatherhead
and Clark 1994; Rohwer et al. 1996. 10) Johnson et al. 1980. 11) Bumpus 1899; Lowther 1977; Johnstonand Fleischer
1981; Lande and Arnold 1983; Crespi and Bookstein 1989. 12) Schluterand Smith 1986. 13) Price 1984; Price et al. 1984;
Grant 1986; Gibbs and Grant 1987. 14) Hecht 1952. 15) Forsman 1991a,b, 1993. 16) Wikelskiand Trillmich1997. 17)
Howard 1981. 18) Trexler et al. 1994. 19) Brittonand Moser 1982. 20) Konovalov and Shevlyakov1978; Ricker 1981. 21)
Lande and Arnold 1983; Crespi and Bookstein 1989. 22) Solbreck et al. 1989. 23) Nishida 1994. 24) Carroll and Quiring
1993. 25) Koenig and Albano 1987. 26) Anholt 1991. 27) Ott and Lampo 1991. 28) Larsson and Tengo 1989. 29) Hardy
et al. 1992. 30) Alcock 1995. 31) Alcock 1996. 32) Thomhill 1983. 33) Blanckenhom et al. 1995; Preziosi and Fairbaim
1996, 1997, 2000. 34) Hillesheim and Stearns 1992. 35) Dangerfield and Chipfunde 1995. 36) Ridley and Thompson
1979. 37) Weilbom 1994. 38) Green 1967. 39) McArdle and Lawton 1979; Scott and Murdoch 1983; Lining 1992; Stibor
and Lflning1994. 40) Svensson 1997. 41) Estes and Duggins 1995. 42) Grutter1997. 43) Sutherland 1982. 44) Berryand
Crothers1968. 45) Peterson 1982; Kabat 1990; Peitso et al. 1994. 46) Hanson et al. 1989. 47) Sambol and Finks 1977. 48)
Prejs et al. 1990; MacIssac 1994; Thorp et al. 1998. 49) Schindler et al. 1994. 50) Berry1982. 51) Wrightet al. 1996. 52)
Bantock and Bayley1973; Knights1979. 53) Merricket al. 1992.

394
VOLUME
75
TABLE 4
Sexual selectionagainst largemalesize
Species
Mechanism
References
BIRDS
Sharp-tailed
grouse
(Tynmpanuchus
phasianellts)
(2b) ?
Courtshipenergetics
Directionalselectionon
matingsuccessand courtship
characteristics
Moorhen
(Gallinulachlioropus)
(2b) ?
Incubationenergetics
(sex role reversal)
Negativerelationship
with
matingsuccess
Dunlin
(Calid7isalpina)
(2a), (2b)
Courtshipdisplay
with
courtshipcharacteristics
Tengmalm'sowl
(Aegoluius
funereus)
(2b)
Food provisioning
energetics
with
rateand
provisioning
breedingsuccess
Kestrel
(Falcotinnunctlus)
(2b)
Food provisioning
energetics
Negativerelationlship
with
rateand mate
provisioning
choice (experiment)
Stabilizing
selectionon
matingsuccess
Pied flycatcher
(Ficedulahypoleuca)
FISH
Coho salmon
(Oncorhynchus
kisutch)
(2a)
Sneakstrategy
selectionon
Disruptive
matingsuccess
Mosquitofish
(Gambusiaholbrooki)
(2a)
Sneakstrategy
with
insemination
success
8
(Continued)
some well-studiedspecies body size is sometimesfound to confera viabilityadvantageand

sometimes a disadvantage (e.g., red-winged
blackbirds: Yasukawa 1987; Langston et al.
1990; Weatherhead and Clark 1994; Rohwer
et al. 1996) implies spatio-temporal,sex, and
life-stagespecificvariabilityin viabilityselection, and generallycalls for investigatingany
selectionmechanismin multipleenvironments.
All this is not surprising.Large body size is
highlycorrelated with (i.e., either the cause
or the consequence of) good condition, and
individuals in good condition are bound to
survivebetter (Zeh and Zeh 1988; Andersson
1994). Therefore,good conditiondue to good
nutritionoftenmasks expected viabilitycosts
oflarge size (van Noordwijkand deJong 1986;
Alatalo et al. 1990; Schluter et al. 1991). It is
thus important to account for variation in
(physiological) condition when assessing the
fitnessconsequences of body size.
SEXUAL SELECTION
AGAINST
LARGE BODY SIZE
Several other mechanisms have been proposed to selectforsmall body size in eithersex
(Table 1). Except forsexual selectionfavoring
small males, direct empirical evidence for
these mechanismsis poor.
Despite overwhelmingevidence for sexual
selection forlarge male size, sexual selection
forsmall male size also occurs in nature (Ghiselin 1974; Andersson 1994). Both processes
may actuallyoccur in the same species (e.g.,
sailfinmolly:Travis1994; waterstriders:Blanckenhornet al. 1995), resultingin stabilizingsexual selection (Mason 1964; Moore 1990). The
mechanismsinvokedare analogous to mechanisms(Ic) and (Id) givenabove foradultmortality(Table 1). (2a) Smaller males may be
more agile and maneuverable when courting,
searchingformates,defendingmatingterritories,and foragingto provisiontheiroffspring;
thisresultsin increased matingand reproduc-

DECEMBER
2000
395
TABLE 4
Continued
Species
Mechanism
References
INSECTS
Wasp
politum)
(Trylpoxylon
Stabilizing selection on
mating success
Damselfly
(Enallagma hageni)
(2a) ?
Courtship display
mating success
10
Damselfly
(Coenagrionptella)
(2a) ?
Courtship display
Negative relation-shipwith
mating rate
11
Pond dragonfly
(Libellula ltcttosa)
(2a) ?
Courtship display
12
Damselfly
(Ebnallagmaboreale)
(2a) ?
Courtship display
Stabilizing selection oIn

mating success
13
mating success
14
(2a) (2b) ?
Negative relationship with

territorialsuccess
15
(2a)

courtship success
16
Disruptive selection on
mating success
17
(2a)
Courtship display

courtship success
18
(2a) ?
Flight agility

mating success
19
mating success
20
Experimentallyinduced
negative relationship with
mating success
21
California Oak Moth

(Phlyganidiacaliforntica)
Butterfly
(Heliconiussara)
Fruitfly
(Drosophilasubobsctra)
(2a) ?
Fruitfly
(Drosophilamontana)
Fruitfly
(Drosophilasilvestris)
Midge
(Chlironomuts
pluhnostts)
Beetle
(Tetraopestetraophtalamus)
Water strider
(Aquarius remigis)
?
(2b)
Energy limitation
1) Gratson 1993. 2) Petrie 1983. 3) Blomqvist et al. 1997. 4) Hakkarainen and Korpimaki 1991, 1995. 5) Hakkarainen
et al. 1996. 6) Alatalo and Luindberg 1986. 7) Gross 1985; Fleming and Gross 1994. 8) Bisazza and Pilastro 1997;
Pilastro et al. 1997. 9) Molumby 1997. 10) Fincke 1982. 11) Banks and Thompson 1985. 12) Moore 1990. 13) Anholt
1991. 14) Mason 1969. 15) Hernandez and Benson 1998. 16) Steele and Partridge 1988. 17) Aspi and Hoikkala 1995.
18) Boake 1989. 19) Neemnset al. 1990,1992,1998. 20) Mason 1964; Scheiring 1977; McCauley 1982. 21) Blanckenhorn
et al. 1995.
tive success (Banks and Thompson 1985;

Steele and Partridge 1988; Blomqvist et al.
1997; Neems et al. 1998). (2b) Smallerindividuals require less food to support themselves,
so smaller males should have freeenergyand
timeforanyactivity
thatincreases theirmating
and reproductive success; such activitiesinclude the pursuit of mates, courtship and
brood provisioning, or investmentin their
sperm supply,particularlyin species withsexual scramble competition (Ghiselin 1974;
Schwagmeyer1988,Jonssonand Alerstam1990;
Andersson 1994; Taborsky1998; Simmons et
al. 1999). I call thisthe small male time-budget

advantage (Blanckenhorn et al. 1995). (Some
people maydebate whetherto call thissexual
selection at all, but thisis a matterofsemantics
and besides the point here.)
I found evidence in the literatureforsexual
selection favoringsmall males in 21 species,
spatio-temporalvariationin thisphenomenon
again beingcommon (e.g., Tetraopes
tetraophtalamus Mason 1964; Scheiring 1977; McCauley
1982; Drosophilamontana:Aspi and Hoikkala
1995; Table 4). Studies either showed direc-

396
tional or disruptiveselection favoringsmall

males or stabilizingselection favoringintermediate males, mating advantages of small
males, or advantages of small males in behavior ultimatelyrelatingto mate acquisition or
care. Evidence comes primarilyfrom
offspring
flyingorganisms. Interestingly,evidence for
agilitydisadvantagesof large size (2a) comes
primarilyfrominsects,particularlyodonates,
whereas evidence forenergeticdisadvantages
of large size (2b) comes primarilyfrombirds
(Table 4). This likelyhas to do with the fact
thatthe formermate on the wingwhereas the
latter do not. In selection studies, however,
mechanism (2a) is ofteninvokedbut no direct
behavioral evidence is generally presented.
Conversely,some behavioral studies demonstrateadvantages of small males in courtship
but do not investigatematingsuccess or sexual
selectionin thewild (e.g., Steele and Partridge
1988). In general, an integrativeapproach
that includes experiments in multiple environments is needed to fullyinvestigatethe
mechanisms and consequences of sexual selection against large body size. The fact that
at least three studies found support for this
mechanism only at food-limitedconditions is
reassuring(Hakkarainenand Korpimaki1991,
1995; Blanckenhorn et al. 1995; Hakkarainen
et al. 1996).
Species for which alternative (e.g., sneak)
mating strategiesor tactics have been documented, sometimesinvolvingsperm competition (e.g., Wikelski and Bauerle 1996; Simmons et al. 1999), mightbe added to Table 4
(reviewedbyTaborsky1994, 1998; Gross1996).
However,I onlyincluded those studieswhere
the smallest males have been shown to have
greater mating or reproductivesuccess than
at least medium-sized males; that is, when
there is directional or disruptiveselection on
male size (Gross 1985, 1996; Fleming and
Gross 1994; Pilastro et al. 1997). This is the
rarecase. Alternativematingsystemsare often
assumed to be maintained by negative frequency-dependentselection,implyingroughly
equal mating success of all morphs or body
sizes on average, but this is verydifficultto
show (reviewed by Austad 1984; Gross 1996;
e.g., Gross 1991; Shusterand Wade 1991; Ryan
et al. 1992). Most often,small males exhibit
best-of-a-badjob strategies or tactics which
augment theirmatingsuccess to some extent
VOLUME
75
but not quite to the level oflargermales (Dawkins 1980). In the lattertwo cases, the behavioral mechanism, but not necessarily small
body size, may be favoredby selection unless
both are geneticallycoupled. Most of the examples of alternativematingsystemsreported
in fishand some otherspecies are likelyto fall
into this category (see Dominey 1980, 1984;
Grossand Charnov 1980; Farret al. 1986; Zimmerer and Kallman 1989; Shuster and Wade
1991; Taborsky1994, 1998; Gross 1996; Wikelski and Bauerle 1996; Alcock 1997a; Bisazza
and Pilastro 1997; Simmons et al. 1999). By
the same reasoning, patterns of assortative
matingbysize do not necessarilyindicate sexual selection favoringsmall males. Loading
constraintsmaypreventsmall males fromcarryinglarge females,but not large males from
carryingsmall females (Adams and Greenwood 1987). Similarly,the requirement of a
(mechanical) size match in pairs of the fish
Xenotocaeiseni,ifanything,mayindicate equal
matingsuccess offishofvarioussizes and thus
no sexual selection on bodysize (Bisazza 1997;
Pilastroet al. 1997).
OTHER DISADVANTAGES
OF LARGE BODY SIZE
Some authorshave focused on selection for

smaller female size (rather than selection for
larger male size) when attemptingto explain
male-biased SSD in mammals and birds (reproductiveselection:Table 1, mechanism (3);
Downhower 1976; Erlinge 1979; Willner and
Martin1985; Andersson 1994). Fecunditygenerallyincreases withsize and mayreach an asymptoteat large body sizes (e.g., Madsen and
Shine 1994; Blanckenhorn et al. 1999), but fecundityselectionfavoringsmallfemalesize has
notbeen invokedor found.An alternative
argumentis again based on energetics:smallerindividualsneed lessenergyand can thusreproduce
sooner, whichsupposedlyconfersa fitnessadvantage, especially in seasonal habitats that
allow onlyone (or few) breeding attemptsper
year.This advantage is particularlygreatin females, as theyinvestmuch more in reproduction thanmales. To testthisplausible hypothesis withina species, it needs to be shown that
small females indeed breed earlier and that
this confersgreater reproductivesuccess. To
myknowledge,empiricalevidence of thissort
is absent. One studyin red-wingedblackbirds

DECEMBER
2000
that specificallytested this prediction found

the opposite: largefemalesbred earlier (Langston et al. 1990). This is not surprising,forthe
same reason as given above with regard to
mortality:small females maybe in bad condition and thereforebreed later. Furthermore,
life-history
theorysuggeststhat earlier reproduction confers a fitnessadvantage only (in
times)whenpopulationsare increasing(Charlesworth1980; Lande 1982).
Energetic comparisons between the sexes
(Erlinge1979; Sandell 1989) are but of limited
help in addressingthishypothesisbecause sexspecificmetabolic efficiencyand growthrates
maybe theconsequence, ratherthanthecause,
of particular patterns in body size dimorphism,and mayrelateto traitsotherthanbody
size (e.g., behavior). In principle this also
holds true for comparisons of mortalitypatternsbetween the sexes (Clutton-Brocket al.
1985; Promislow1992). However,the equilibriumviewof SSD indeed predictsstrongerviabilitycounterselection in males than in females (i.e., male-biased mortality)if sexual
selection is strongerthan fecundityselection
(Figure 1; Clutton-Brocket al. 1985), but this
should also be detectable as greatermortality
oflargermalejuveniles(cf.discussionofmechanisms(la) and (lb) above). Nonetheless, several authors appear to be satisfiedwithcomparative evidence and argue, particularlyfor
mammals,thatdifferential
optimizationofenergyallocation to growthand reproductionis
the primaryevolutionaryforce thatproduces
life span, mortality,and consequently body
size differencesbetween the sexes and different species (Clutton-Brocket al. 1982, 1985;
Promislow1992; Chamov 1993: Chapter5; Kozlowskiand Weiner 1997).
Bya similarmechanism,selection mayfavor
earlyreproductionin males (protandry:Table
1, mechanism (4); Wiklund and Fagerstr6m
1977; Travis1994; Zonneveld 1996). In species
where encounter rateswithmates are low and
individualsreproduceseasonallyforonlya short
period, males maygain an advantage byentering the mating pool early. To emerge early,
males are assumed to abbreviate their development at the expense of a reduction in size
(cf. mechanism (la); Roff1980). While there
is indirectevidence fromcomparativestudies
across species and comparisons between the
sexes that support this selection mechanism
397
(Wiklundand Forsberg1991), empiricalstudies within species often find that males can
emerge earlyand be large,due to bettercondition and/or adaptive increases in growthrate
(Nylin et al. 1993; Blanckenhorn 1998; Nylin
and Gotthard1998) .Justas forfemales,itthereforeneeds to be shownthatsmallmales emerge
earlierand thatthisconfershigherfitness;one
withoutthe other is insufficient(e.g., Alcock
1997b). Direct empirical support for this hypothesis is also lacking.
Lastly,there are extreme cases of species
withso-called dwarfmales thatare verymuch
smaller than the female,such as anglerfishor
spiders (Table 1, mechanism (5); Andersson
1994:255). To explain thisphenomenon, several of the previous argumentshave been invoked in conjunction. Ifthe chance fora male
to mate at all is verysmall, it does not pay to
growverylarge. Instead,a male should mature
fastto increase his chances to reach reproductionand finda mate (Vollrathand Parker1992).
To ensure fertilizationof at least one batch of
eggs, the resultingdwarfmales can then permanentlyattach to a large female (Ghiselin
1974), be extremelymobile due to theiragility
advantage ("rovingmales":Ghiselin1974; Vollrathand Parker1992), or perhaps betteravoid
sexual cannibalism by the female (Elgar
1991). Comparative evidence supports some
of these mechanisms in spiders,but such evidence is merelycorrelational(Elgar 1991; Vollrath and Parker 1992; but see Prenter et al.
1998). Direct empirical evidence that shows
that small, roving males have higher reproductivesuccess is stilllacking (to the contrary:
see e.g., Vollrath 1980).
PHYSIOLOGICAL
MECHANISMS
Several of the selection mechanismsagainst

large body size listedin Table 1 are ultimately
grounded in physiology.Physiologicalallometriesare well established and representedin
the literature (Peters 1983; Calder 1984;
Schmidt-Nielsen
1984;Reiss1989). Mechanisms
(1d), (2b), and (3) are based on the factthat
metabolicrate (i.e., energydissimilation)scales
withbody mass than processes that
differently
affectenergyassimilation,such as locomotion,
renderingit increasingly
prohibitiveto support
heavier bodies in everlimitingenvironments.
Foraging,courting,and anyotherenergetically
expensive activitythataffectindividualfitness

398
should thereforebecome ever more timeand

energyconsumingforlargerindividuals.While
thisargumentis physiologicallysound and investigatedprimarilyin small flyingorganisms
withextremeenergydemandslikemoths,hummingbirds,or bats (Voigtand Winter1999 and
referencestherein; but see Millar and Hickling 1990), thesemechanismsshould ultimately
resultin greatermortality
or reduced reproductivesuccessoflargeindividualsat theecological
level;itis thislevel ofbiological organizationat
whichevidence forthese mechanismsis scant.
Note that mechanism (1d) in Table 3 bears
a question mark in most cases as it is often
supposed but rarelyshown. Mortalitycosts relating to energylimitationmaybe difficultto
detect in the field but can be experimentally
addressed (e.g., Blanckenhorn et al. 1995).
One strong experimental test would be to
keep (or select) organisms at high density
and/or low food supply over several generations,with the appropriate low density/high
food supplycontrol.This should'resultin the
evolution of (genetically) smaller body sizes.
To separate the effectsof food on growthand
development during the juvenile stage,from
those on maintenance at the adult stage, the
treatmentshould be delivered separately to
juveniles and adults.
A second physiological argument invoked
in limitingbody size is that larger organisms
mayhave increased difficulties
dissipatingheat
at high temperatures(mechanism(if) in Table
1). Heat loss in cold climates is reduced by a
relatively
smallbody surface(Bergmann'srule:
see Atkinson1994); i.e., a large bodywithshort
itis increasedin warm
appendages. Conversely,
climatesbya relativelylarge body surface;i.e.,
a small body withrelativelylong appendages.
Comparative evidence for the latterso-called
Allen's rule is mixed at best (forsome recent
studiesin birdswithconflictingresultssee McGillivray1989; Wiedenfeld 1991; Rasmussen
1994;Whaleyand White1994;BriedandJouventin1997). For endothermicanimals like birds
and mammals, larger bodies may actuallybe
advantageous in hot climates (Weathers 1981;
Schmidt-Nielsen
1997:271). On theotherhand,
Furuyama and Ohara (1993) found a correlated reductionin bodysize when selectingfor
increased heat tolerance in rats.Larger ectothermicanimals, in contrast,typicallyfeature
VOLUME
75
higher body temperatures,so the argument

mayhold (e.g., Coelho 1991; Seebacher et al.
1999); it has even been invoked to explain the
extinctionof dinosaurs(Schmidt-Nielsen1984;
Seebacher et al. 1999). I found onlytwo studies thatshow thatlarge individuals of a given
species sufferincreased mortalitydue to heat
stress,however (Carroll and Quiring 1993;
Dangerfield and Chipfunde 1995; Table 3).
EVOLUTIONARY
MECHANISMS
In addition to the preceding ecological and

physiologicalarguments,there are evolutionary arguments about what keeps organisms
small. As shall be seen, these types of arguments do not differin principle but merely
differin the level of biological organizationat
whichtheyare expressed (process vs.pattern).
Selection forlarge body size mayeventually
be balanced not by selection but by deleterious mutationsthataccumulate in the genome
(mutation-selectionbalance; Barton and Turelli 1989;Wayneand Mackay1998). This mechanism is listed as (ig) in Table 1. Of course,
these mutations must eventuallyaffectsome
measurable fitnesscomponent at the ecological level, such as viabilityor hatchingsuccess.
But that mortalityis intrinsicratherthan extrinsic (i.e., caused by selection). The same
reasoning applies if selection for large size is
constrained (and thuscounteracted) bynegative genetic correlations among fitnesscomponents due to pleiotropyor genotype-environment interactions (Barton and Turelli
1989; Roff1997; Wayneand Mackay 1998). Intrinsicsources of mortalityare best investigated using artificialselection,but one recent
testof the mutation-selectionbalance hypothesis in Drosophilamelanogaster
found no evidence with regard to body size (Wayne and
Mackay 1998).
Cope's rules state that: (1) taxa evolve to
larger body size over evolutionarytime, and
(2) that larger organisms and taxa are more
likely to go extinct (McLain 1993). They
merelydescribe patternswithoutreferenceto
specificprocesses (and are thereforenotlisted
in Table 1). While these rules were conceived
withlarge fossilmammal species in mind,they
can be generalizedto applyto anylarge-bodied
lineages withina given taxon (McLain 1993).
Contraryto popular belief, evidence for the

DECEMBER
2000
firstrule in fossil species appears to be little

more than anecdotal (Gould 1997;Jablonski
1997). Cope's second rulecan actuallybe tested
evenwithextantspecies,particularly
as itrelates
to the currentinterestin conservationbiology
in estimatingextinctionrates of populations
of rare plants and animals (e.g., Hughes et al.
1997). Within each taxon, this rule predicts
that larger species should occur in smaller
populations thatare more likelyto go extinct.
Siemann et al.'s (1996) data on insectsmaybe
construedto supportthiscontention,but I am
not aware of anyothersuch evidence.
CONCLUSIONS
399
encompassing data setson the advantagesand

disadvantagesof large size existin any species
to date. Estimatesoflifetimereproductivesuccess are most desirable (Charlesworth 1980;
1988 forexamples). As these
see Clutton-Brock
are difficultto obtain, studiesof the same species that focus on the various fitnesscomponents (i.e., fecundity,viability,or matingsuccess) need to be integrated (e.g., Arak 1988),
simulationsifnecessary(e.g.,
usinglife-history
Madsen and Shine 1994). Theoretical studies
can furtherhelp elucidate whether sporadic
selection in time and space is sufficientto
counterbalance perpetual and strong selectionforlargebodysize. Plausible physiological
hypothesesare ofteninvestigatedmechanistically,or by comparative studies,but rarelyin
termsoffitnessconsequences at theindividual
level. This should be corrected. Genetic studies are difficult,
laborious,and largelyrestricted
to organismswhich can be easily kept in the
laboratory,but are necessaryforrevealingpossible intrinsicfitnesscosts of large size. Lastly,
research and publication biases can restrict
the scope of investigationand should therefore be overcome.
In contrast,comparisons among species or
the sexes are helpful to detect patternsand
generate hypotheses but are limited in that
theyare correlational,possiblyconfoundcause
and effect,and cannot investigatethe actual
mechanisms involved (e.g., Andersson and
Norberg 1981; Clutton-Brocket al. 1985; Sandell 1989; Promislow 1992; Balmford et al.
1993). The albeit weak empirical and experimentalevidence compiled here thatshowsthe
disadvantages of large body size testifiesthat
theycan, and should, be demonstrated,given
some effort.
Schluter et al. (1991) concluded that there

is more evidence for opposing selection on
traitsthan for its lack (see also Travis 1989).
Body size is probablythe charactermostoften
invoked as affectingindividual fitnessof organisms.Almosttenyearslater,I mustconclude
thatempiricalevidenceforselectionand other
processes thatlimitbody size in naturalpopulations lags farbehind the vastincrease in sexual selection studies thatdemonstratethe advantagesof large body size (Andersson 1994).
I have argued that difficultiesin demonstrating selectionagainstlarge bodysize at theindividual organismiclevel is one major reason for
thislack.
Research effortsshould thereforefocusspecificallyon the several costs of being large, as
outlined in Table 1. Because it is likelythat
counterbalancing selection on body size occurs onlyoccasionally in timeand space, only
at some lifestagesand not others,and perhaps
onlyin one sex and not the other (Grant 1986;
Travis 1994; Reeve and Fairbairn1996; Wikelskiand Trillmich1997), and because bodysize
is frequentlyconfounded bycondition,experACKNOWLEDGMENTS
imentalapproaches in multipleenvironments I thankvariouscolleaguesfordiscussions
and helpare necessary.We need more comprehensive ful suggestions.
This workwas supportedby the
case studiesofparticularmodel species, as few SwissNationalScienceFoundation.
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The Evolution of Body Size, What Keeps Organisms Small

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The Evolution of Body Size: What Keeps Organisms Small?

Author(s): Wolf U. Blanckenhorn

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BODY SIZE continuesto be one of the

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THE QUARTERLY REVIEW OF BIOLOGY

MAJOR SELECTIVE PRESSURESTHAT

forthecase wheremales are

and sexual selection (SexS) for increased body size

largerbodysize in manyorganisms(Figure 1).

curs in only one sex, because body size is typicallyhighlygeneticallycorrelatedbetweenthe

LARGE BODY SIZE

Viabilityselectionagainstlarge body size can

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2. Sexual (and reproductive)

at reproduction (Table 1): (la) To achieve a

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THE QUARTERLY REVIEW OF BIOLOGY

Stabilizing selection analysis

Stabilizing selection analysis

Analysisof field survival

Stabilizing and directional

Stabilizing selection analysis

Stabilizing selection analysis

Stabilizing selection analysis

Analysisof field survival

Analysisof field survival

and less agile and maneuverable. This is expected to resultin disproportionatepredation

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EVOLUTION OF BODY SIZE

Various aquatic insect larvae

Stomach content analysis

grow bigger. (le) Larger individualsin good

Balmford et al. 1993; but see below). Some

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THE QUARTERLY REVIEW OF BIOLOGY

as theydirectlyinvestigatea particularmechanism.Second, studiesthatemployquantitative

to this list (e.g., Miyatake 1995). Few studies

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EVOLUTION OF BODY SIZE

(lb), (1d), (le)

Life table analysis of field

Life table analysis of field

Life table analysis of field

(ib), (id), (le) ?

Analysisof field survival;

Stabilizing selection analysis

Analysisof field survival;

An-alysisof field sur-vival

Directional selection analysis

Directional selection analysis

Stabilizing selection analysis

Analysisof field survival

Directional selection analysis

An-alysisof field survival

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THE QUARTERLY REVIEW OF BIOLOGY

Method of demonstration References

Directional selection analysis

Directional selection analysis

Population and sex

Directional selection analysis

Spruce bud moth

Directional selection analysis