Erolution, 46(3), 1992, pp. 828-833
RELATIVE CLUTCH MASS AND BODY SHAPE IN LIZARDS AND SNAKES:
IS REPRODUCTIVE INVESTMENT CONSTRAINED OR OPTIMIZED?
Rrcnlno SnrNe
Zoology A08, The Universityof Sydney,N.S.W. 2006' AUSTRALIA
Key words.-Adaptation, constraints, lizard, relative clutch mass, reproductive effort, snake.
ReceivedSeptember24, 1990. AcceptedNovember 18, 1991.
In its simplest form, Darwinian theory suggeststhat
natural selectionshould favor characteristicsthat maximize rates of reproduction: any mutant that leaves
more copies ofits own genesin the next generationis
(by definition) favored by natural selection.Why, then,
do so many speciesof animals reproduceat relatively
low rates? Life-history theory identifies two reasons
why reproductive output might be low: (l) tradeoffs
between current reproductive expenditure and future
probable reproductive output ("costs of reproduction,"
in terms ofenergy, time, or risk of mortality), suchthat
lifetime production of progeny is maximized by a reduction in current reproductive expenditure(Williams,
1966); or (2) constraints ofenvironment, genetics,behavior, physiology,or morphology that prevent organisms from reproducing at higher rates. Whether reproductive rates are limited by tradeoffs or by constraints
dependsupon which of these factors imposes a lower
ceiling on reproductive expenditure.For example,con"costs" mean
straints are irrelevant ifhigh reproductive
that the optimal reproductive rate in terms of maxi-
mizing individual fitness is below the maximum permitted by constraints. Similarly, tradeoffsare likely to
be irrelevant if physical constraints restrict reproduc"optimal" levels.
tive rates below
Evolutionary determinants of reproductive rates in
squamatereptileshave attractedconsiderablescientific
attention, especiallyin terms ofthe relative clutch mass
(RCM) (ratio of clutch mass to maternal mass: e.g.,
Vitt and Congdon, 1978; Vitt, l98l; Vitt and Price,
1982;Seigeland Fitch, 1984;Shine,1988;Dunham e1
a1., 1988; Anderson and Karasov, 1988; Shine and
Schwarzkopf, 1992). Several broad patterns in RCM
variation among squamateshave been identified. For
example, "wide-foraging" cnemidophorine lizards tend
"ambush predators" of
to have lower RCMs than do
the genusSceloporzs(Yitt and Congdon, 1978),RCMs
are low in anoline and gekkonid lizards with fixed clutch
sizes (Andrews and Rand, 19741'Vitt and Congdon,
1978).RCMs are lower in lizards than in snakes(Seigel
and Fitch, 1984),and aquatic snakeshave lower RCMs
than do terrestrial species(Shine, 1988). Nonetheless,
NOTES AND COMMENTS
the relative importance oftradeoffs and constraintsin
producing such patterns remains problematical. Some
authors have attributed interspecific variance in RCMs
to life-history tradeoffsfavoring different optimal levels of reproductive investment (e.g.,Tinkle, 1969;Tinkle and Hadley, 1975; Shine, 1988). Orher workers
have suggestedthat clutch massis limited by the al.nount
of space available in the maternal abdominal cavity,
and hence that body shape is a primary determinant
ofRCM (e.g.,Pianka and Parker,19751'Vitt and Congdon, 1978). The latter hypothesis attributes interspecific variance in RCM to interspecificvariance in body
shape(or more precisely, the relationship between body
mass and abdominal volume). For example,taxa with
relatively small limbs, tails, and headswill have larger
volumes available in the body cavity to carry eggsin
relation to maternal mass, and thus will have higher
RCMs. This relationship betweenbody shapeand RCM
could be interpretedin at leasttwo ways:( l) body shape
constrains reproductive expenditure below "optimal"
levels; or (2) body shape,although acting as a proximate constraint on clutch mass, has itself evolved to
allow optimal levels of reproductive expenditure.
Is body shapea significant influence on RCM? The
only evidence presented for such a relationship has
been a broad comparison among different lineagesof
lizards, with no quantification ofbody shape(Vitt and
Congdon, 1978).A more detailed examination should
be worthwhile, becausethe two main types of explanations for interspecific variance in RCMs (tradeoffs
versus body-shapeconstraints) predict different relationships betweenbody shapeand RCM. Models that
do not involve body shape simply posit that females
of somespeciesare more "full" ofeggsthan are females
of other species.In contrast, the body-shape models
begin with the premise that females of all speciesare
equally "full" ofeggs. In the presentpaper, I provide
data on body shapes of squamates,to examine the
degreeto which observeddifferencesin RCM may simply be due to interspecificvariance in the relationship
betweenbody mass and the volume potentially available to carry the clutch.
I measuredsomepreservedlizards and snakesin the
collectionsofthe CarnegieMuseum ofNatural History
(Pittsburgh, PA USA), the U.S. National Museum of
Natural History (Washington,D.C.) and the Australian
Museum (Sydney,N.S.W.).Wherepossible,specieswith
averageadult body massesofless than 50 g werechosen
to ensure overlap in body sizes among the groups to
be compared. This was not possible with the aquatic
snakesstudied, most of which were large. Hence, all
analyses were performed twice, with and without the
aquatic snakes.Exclusion ofthis group did not affect
conclusionsfrom any ofthe analyses,so only the analyses with the complete data set are reported in this
paper. Data were taken on snout-vent length (henceforth, SVL), length ofbody betweenfore and hind limbs,
mean diameter of posterior half of the body (all + I
mm), and body mass after draining of preservative
(+0.2 g, with Pesola spring balances).In speciesin
which abdomens were dorsoventrally flattened rather
than cylindrical, I gently squeezedthe abdomen to force
it into a cylindrical form before measuringthe diameter. Diameters were measuredat three evenly spaced
intervals along the abdomen, and a mean value used
in subsequentcalculations. Sex was determined from
829
external morphology in some taxa (e.g.,enlargedpostanal scalesin Sceloporus, tail shape in snakes)but was
confirmed by dissectionin doubtful cases.I attempted
to use only adult specimens,and avoided animals that
were kinked, poorly preserved,eviscerated,or gravid.
Six males and six females of each specieswere measured, and data were gathered on six specieswithin
eachofsix categoriesusedin previous analysesofRCM
in squamates(Table l).
Data on RCMs were gathered from published literature, especiallythe reviews ofVitt and Price (1982)
for lizards, and Seigel and Fitch (1984) for snakes.
These authors define RCM as the ratio ofthe clutch
mass to total maternal (clutch plus body) mass. This
method of calculation resultsin the inclusion of clutch
mass in both the numerator and denominator, and
hencemay introduce statistical artifacts (Shine, 1980).
An alternative method for calculating RCM-clutch
mass divided by the female postoviposition massavoids this problem, but may be lessdirectly comparable to my measureof abdominal volume relative to
body mass. I calculated RCMs using both methods,
converting mathematically from the "conventional,' to
the alternative system {: [("convenlional" RCU;-I ll-t]. All analyseswere performed twice, using both
methods, and no significant differenceswere apparent
between any of the major results. For specieswhere
more than one estimate of RCM was available, I calculated a mean value. For specieswith invariant clutch
sizes for which no RCM data were available. I used
publishedinformation on the relationship betweenmaternal body size and egg mass (Andrew\ and Rand,
1974; Yitt, 1986). This procedure should introduce
relatively little error, becausethe correlationsreported
betweenmaternal body sizeand eggmassare very high
(=0.97) in both groups.
The volume of the abdominal cavity of each specimen wascalculatedby applying the formula for volume
of a cylinder: V: rr2h, where r : radius and & : length
between fore and hind limbs. Becausethe abdominal
cavity must hold various internal organsaswell aseggs,
my volume estimate offers an index of available space
rather than an absolute measure.Use of this formula
as an index of spaceavailable for the clutch also assumeslittle interspecificvariance in (l) the proportion
of the total abdominal volume available to hold the
clutch, and (2) the degee of distension of the body in
gravid females. The distance between fore and hind
limbs cannot be measuredin limbless animals such as
snakes,so for these speciesI assumedthat the equivalent length was three-quartersof SVL. This estimate
was derived from measurementsof body shapesof l0
lizard speciesshowing various degreesof limb reduction (Anguis fragilis, Chalcides chalcides, C. ocellatus,
Lialis burtonis,Lygosomapunctata, L. sundevalli, Nes'
sia monodactyla, Ophisaurus attenuatus, 0. ventralis,
Typhlosaunn lineatus\. The interlimb distance as a
proportion of SVL averaged<50o/oin most lizard species with normally sized limbs, but was much higher
in lizards showing limb reduction (up to 80o/oin Chalcides chalcides and Nessia monodactyla). The fully
limbless taxa studied are much more elongatethan any
of the limbed forms (the ratio of body diameter to SVL
was 2 to 7oloin the limbless taxa studied, versus 7 to
160loin reducedJimb forms, 19 to 29o/oin normally
limbed lizards), so that the useof0.75.SVL to estimate
830
NOTES AND COMMENTS
Tesle l. Mean female body mass (g), ratio of calculated abdominal volume index (mm3) to mass (g), and
relative clutch mass (RCM) measured in preserved lizards and snakes. Each data point for mass and volume/
mass is a mean based on six specimens.RCM estimates include clutch mass in both the numerator and the
denominator, and are based on published literature. Seetext for references,definitions, and methods of calculation.
Taa
Mm
female mass (g)
Fenale volume/mass
Cnemidophorines
18.6
5.6
13.6
12.4
t4.5
8.7
Male volume/mass
RCM
io.o
0.14
0 . 15
0.16
o.12
0.17
0.16
0.15
5 75 . 5
608.5
653.4
566.1
643.4
61t.7
609.8
549.8
539.7
600.7
556.7
622.7
566.4
572.7
0.30
0.23
0.27
0.19
0.25
o.32
0.26
325.2
426.6
678.0
592.2
530.3
394.9
491.2
337.7
463.4
541.3
564.9
410.6
420.3
456.4
0.09
0.06
0.04
0 .1 8
0.06
0.07
0.08
592.2
551.4
405.9
4t4.1
451.8
5l 1.1
487.8
475.3
450.2
339.3
395.8
425.7
396.8
413.9
o.22
0.08
0.08
0.13
0.06
0.09
0 . 1I
Agki st r odon contort rix
Nerodia kirtlandi
Regina septemvittata
Sistrurus miliarius
Storeria dekayi
T r opidocIonio n li neatum
Means:
Viviparous terrestrial snakes
r 19.8
900.7
32.0
967.6
r,026.4
69.4
1,O29.8
56.7
12.8
842.6
10.9
951.0
953.0
50.3
734.5
959.r
757.r
r,034.2
739.2
748.6
828.8
0.30
0.39
0.32
0.30
o.37
0.43
0.35
Diadophis punctatus
Heterodon nasicus
H ypsiglena ochr or hynchrc
Liophis poecilogyrus
Micrurus fulvius
Opheodrys aestivus
Means:
Oviparous terrestrial snakes
I 1.6
846.7
796.4
55.0
23.4
902.6
4t.7
833.s
42.3
1,013.8
932.4
32.9
887.6
34.5
945.0
7 t3.l
710.0
731.1
780.7
844.5
787.4
0.34
0.41
0.43
0.18
0.55
0.37
0.38
Aquatic snakes
r,034.2
I,018.5
252.8
|,042.1
351.2
1,220.2
1,088.3
t,o84.2
r,146.l
0.35
0.19
Cnemidop horus exsanguis
C. inornatus
C. sonorae
C. tesselatus
C. tigris
C. uniparens
Means:
r2.2
496.4
576.8
548.8
414.7
443.3
569.6
508.3
Sceloporusclarki
S. graciosus
S. jarrovi
S. magister
S. undulatrc
S. virgatus
Means:
Sceloporines
34.9
5.9
r4.9
36.2
13.6
7.4
18.8
Anolis allisoni
A. baleatrc
A. biporcatus
A. carolinensis
A. chrysolepis
A. coelestinus
Means:
Anolines
4.5
27.9
28.0
1.6
5.6
5.2
12.l
o*.s
403.1
Gekkonids
Coleonyx variegatus
Cosymbotesplatyurus
Gecko gecko
H emidactylus fas ciatus
H. frenatw
H. mabouia
Means:
Acrochordus arafurae
A. granulattn
Aipysurus duboisii
4 1
+-J
36.9
7.9
3.3
5.5
10.3
831
NOTES AND COMMENTS
Tnnn l.
Te
A. eydouxii
H. fasciatus
Lapemis hardwickii
Means:
Continued.
Mem female mass G)
509.5
190.8
r02.2
406.8
interlimb distance may underestimate the available abdominal volume in completely limbless squamates.
Mean clutch massesfor each specieswere estimated
by multiplying RCM by mean maternal mass(the latter
from my museum data). To overcome statistical problems associatedwith ratios like RCM (e.g.,Shine, 1980;
Dunham et al., 1988),I analyzedthesedata as follows.
Both variableswere log-transformedto normalizevariances, and a general regression calculated between the
two variables(e.g.,ln clutch massversusln body mass)
using the full data set. Residuals from these general
regressions were then calculated and compared. The
sameprocedure was carried out when comparing clutch
mass to abdominal volume, or body mass to abdominal volume.
Conventional statistical analyses are generally inappropriate for tests of adaptational hypotheses,because the values for related species are not truly independent if a trait shows significant phylogenetic
conservatism(e.g.,Clutton-Brock and Harvey, 1984).
To overcome this problem in correlational analyses,I
used Pageland Harvey's (1989) program to calculate
evolutionary cftangesinthe variables ofinterest through
squamate phylogeny. This method superimposes values for living taxa (the "tips" ofthe phylogenetictree)
onto a phylogenetichypothesisfor the group, and identifies sister groups that offer independentcomparisons
with respect to the variables of interest. The program
then compares changes in one variable to concurrent
changes in another. I used this program because insufficient phylogenetic data were available to fit phylogenetically based analytical methods requiring information on branch lengthsand evolutionary rates (e.g.,
Martins and Garland, l99l). Information on branching sequenceswas taken from Dowling et al. (1983)
and Estesand Pregill (1988), and referencestherein.
My data on 42 squamate speciesreveal considerable
variance in the relationship between body mass and
abdominal volurne (Table l). For example, most snakes
have almost twice as much space available to carry
eggs,pergram ofbody weight, asdo most lizards (Table
l: means of 988 versus 512 mm3/g). Abdominal volume in relation to body mass was highly correlated
between conspecific males and females @ased on residuals from regressionsof ln volume versus ln mass
for each sex: 36 df, r : 0.90, P < 0.001); but males
consistently showed lower abdominal volumes at the
same mass (mean difference: males I l.9ololower, SE
:2.3o/o,P < 0.01).
Table I shows that clutch massesof anolines, gekkonids, and cnemidophorineswere similar, relative to
body mass, and averaged lower than those of Sceloporzs. Most snakes had higher RCMs than did most
lizards. However, these patterns changedwhen clutch
masswas plotted as a function of maternal abdominal
Female volume/ross
953.5
1,208.3
766.2
1,034.8
Male volme/mass
955.0
1,028.9
819.3
1,020.3
o.22
0.25
0.22
o.2s
volume rather than body mass. The main difference
was that the tendency for snakesto show higher RCMs
than did lizards disappeared in the latter analysis. Ratios of clutch mass to abdominal volume for the terrestrial snakes fell between those of sceloporine and
cnemidophorine lizards, and aquatic snakes were intermediate between cnemidophorines and the invariant-clutch-size Iizard taxa. The exact position of the
snakes relative to the lizards depends on the approximations used to calculate ophidian abdominal volumes. flowever, even if the "interlirnb distance" as a
proportion of SVL in snakes was estimated at 650/o
rather than 75Yoof SVL, mean values for clutch mass
relative to abdominal volurne for all three ofthe snake
groups remained below those of sceloporinelizards.
How closely linked are body shapeand RCM? Residual scoresfrom the general regression ofabdominal
volume to body mass offer an index of the amount of
space available for eggsin the body cavity, and hence
should be correlated with RCM if females ofall species
are equally "full" when carrying eggs.Residual scores
from the general regression of clutch mass to matemal
body mass were used as a nonratio measureof reproductive investment (and hence,analagousto RCM). I
used Pagel and Harvey's (1989) program to calculate
evolutionary changepin body shape (residuals.ofabdominal volume to body mass) in the phylogenetic
lineagescontaining the speciesin Table l, and compare
these to concurrent evolutionary changesin reproductive investment (residuals of clutch mass to maternal
mass). The correlation between phylogenetic changes
in my measures of body shape and reproductive investment was highly significant (r : 0.59, n: 17, P :
0.001). That is, the evolution of a larger abdominal
volume relative to masswas consistentlyaccompanied
by the evolution of a higher RCM.
I also calculated the correlation between body shape
and RCM treating the present-day mean values for
each speciesas independent data points (i.e., ignoring
phylogenetic conservatism), becausethis correlation is
easier to visualize. Again, residuals from the general
relationships between (1) clutch mass and abdominal
volume; and (2) clutch mass and body mass,were highly correlated, with body shape again accounting for
about 400/oofthe interspecific variance in relative clutch
m a s s( r : 0 . 6 7 , N : 4 2 ,
P < 0 . 0 0 1 ) .T h e r a t i o o f
abdominal volume to body masswas significantly correlated with RCM regardlessofwhether RCM was calculated with clutch mass included in both the numerator and denominator(N: 41, r : 0.68, P < 0.001),
or only in the numerator (N : 41, r : 0.64, P < 0.00 l).
These results suggestthat about 400/oofthe interspecific
variance in RCM among squamates is attributable to
body-shapedifferencesamong species.
Although my index of "available abdominal vol-
832
NOTES AND COMMENTS
ume" is undeniably imprecise,thesemeasurementsare
highly consistent:for example, the index is highly correlated between conspecific males and females (r :
0.90, df : 36, P < 0.001). Hence, random error in
measurementsis unlikely to be a problem. The ability
ofthis approximate index to explain about halfofthe
interspecific variance in RCMs in the sample (and especially, RCMs based on data from individuals and
populations other than the ones that I measured) suggestsa strongunderlying correlation betweenbody shape
and RCM. Any irnprecision in my estimates of abdominal volume should have reduced rather than increased the correlation between these variables.
My results show that the low RCMs of some squamate taxa (e.g., anoline ard gekkonid lizards, and
aquatic snakes) cannot be attributed to body shape,
becausethese animals do not differ in shapefrom related specieswith higher RCMs. Nonetheless,the high
overall correlation between body shape and RCM suggeststhat differencesin body shapemay be responsible
for many ofthe broad patterns ofRCM variance among
squamates.In some comparisons,differencesin body
shapecan accountfor somebut not all ofthe differences
in RCM (e.9.,Sceloporusversus Cnemidophorus:20o/o
differencein ratios ofabdominal volume to body mass,
versus73olodifferencein RCMs: Table l), so that taking
body shape into account decreasesthe magnitude of
the difference in RCMs, but does not eliminate it. In
contrast, the higher RCMs of snakesthan of lizards
overall (Seigeland Fitch, 1984; Dunham et al., 1988;
Table l) may be entirely attributable to differencesin
body shape.The ratio of abdominal volume to body
mass is almost twice as high in snakes as in lizards
(Table l), and hence there is little difference between
snakesand lizards in clutch mass relative to abdominal
volume. The differencein RCMs between snakesand
lizards has been attributed to the putative higher energetic efrciency of limbless locomotion, allowing a
larger burden to be carried by gravid females (Seigel
and Fitch, 1984, citing L. J. Vitt). However, recent
experiments cast doubt on the idea of energetic advantagesto limbless locomotion (Walton et al., 1990),
and my data on body shapes suggest that the high
RCMs of snakes are a simple consequenceof their
elongatemorphology.
Overall, my data show a high but not perfect correlation between body shapeand RCM. Hence, these
data support both types of hypothesesoutlined in the
introduction: those that suggesta role for body shape
in the evolution of RCM, and those that identifu other
factors independent of body shape. The finding that
evolutionary changes in body shape are significantly
correlated with concurrent shifts in RCM suggestsa
functional relationship between the two variables, in
addition to the undoubted influence of phylogenetic
conservatism. There are three alternative pathways by
which a correlation between RCM and body shape
could arise: body shape may determine RCM, RCM
may determine body shape, or some third factor may
determine both. Parsimony srrqgeststhat a simple
physical limitation of clutch mass may be the most
important factor, and hence that constraints as well as
optimizing selectionmay determine reproductive rates
among squamates.However, the consistentsexualdimorphism in body shape (with females having larger
abdominal volumes relative to mass)offerssupport for
the hypothesis that selection for increased RCM has
influenced the evolution of body shape in these animals. The correlation between RCM and body shape
is not perfect becauseof proximate variation in RCMs
causedby local environmental factors,becauseofphylogeneticconservatismin clutch size among some lineages(preventingfemalesin thesetaxa from filling their
body cavities with eggs),and becausefemalesthat are
less "full" than are other females may be favored by
natural selection under some circumstances.
The correlation between body shapeand RCM has
strong implications for evolutionary interpretations of
RCM. Kaplan and Salthe(1979) have reviewed a large
data base on amphibians, and limited data on fishes
and birds, that suggesta high correlation between abdominal volume and clutch massin theseanimals also.
Vitt and Congdon (1978) have pointed out that squamate body shapesare highly conservativephylogenetically, so that the evolution ofbroad patterns in reptilian RCM occurred in the early ancestral forms of
familial-level lineages.Hence, caution is neededin attempts to interpret differencesin RCM betweenclosely
related populations or speciesin terms oflife-history
adaptation.
In summary, the ratio of clutch mass to maternal
body mass (RCM) among lizards and snakeshas been
interpreted as (l) an adaptation for optimal reproductive expenditure, based on life-history tradeoffs; and
(2) a constraint imposed by the amount of spaceavailable for eggs in the maternal body cavity, relative to
maternal body mass.I measuredbody shapes(ratio of
body mass to abdominal volume available to hold the
clutch) in preservedspecimensof42 speciesoflizards
and snakes, to examine the relationship between body
shape and RCM. Taxa with high ratios of abdominal
volume to body massalso had high RCMs, and a phylogeneticanalysisshowedthat evolutionary changesin
body shape were accompanied by changes in RCM.
For some comparisons(e.g.,lizards versussnakes),differencesin body shape offer a simple and plausible
explanation for major differencesin RCM.
AcrNowrEpcuExrs
I thank C. J. McCoy and E. J. Censky (Carnegie
Museum), G. R. Zug (Smithsonian Museum), and H.
G. Cogger, A. E. Greer, and R. Sadlier (Australian
Museum) for allowing me to examine specimens,ano
for help in a multitude of ways. Comments on the
manuscript were provided by L. J. Vitt, R. B. Huey,
L. Schwarzkopf, R. Seigel,J. Caley, C. James, R. A,
Anderson, and two anonymous reviewers.I also thank
the Australian ResearchGrants Scheme and the Ian
Potter Foundation for financial support for the study,
and Mrs. R. Grifrth for hospitality.
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