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Proximate Determinants of Sexual Differences in Adult Body Size

Article  in  The American Naturalist · February 1990

DOI: 10.1086/285043

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Vo!. 135, No. 2 The American Naturalist February 1990

PROXIMATE DETERMINANTS OF SEXUAL DIFFERENCES

IN ADULT BODY SIZE

In many animal species, males and females attain different adult body sizes.
The processes underlying such sexual differences are undoubtedly complex and
may involve an interplay between adaptive, exaptive, and nonadaptive genetic
influences on the one hand and environmental variables on the other. For ex-
ample, large body size may be shown by males because genes for that character
confer a selective advantage in that sex (see, e.g., Darwin 1871; Trivers 1972),
because such genes have been inherited from an ancestral form (see, e.g.,
Cheverud et al. 1985), or because local environmental conditions happen to be
particularly favorable for the survival and growth of males (see, e.g., Howard
1981; Woolbright 1983, 1989; Halliday and VerrellI986). The relative importance
of such alternative factors is difficult to assess but may be clarified by considering
the proximate determinants of sexual differences in body size (hereafter, "sexual
size dimorphism," or SSD).
Alternative hypotheses about the causation of SSD make different assumptions
and predictions about the stage in ontogeny at which sexual dimorphism in mean
adult body size is determined. There are two main possibilities for ontogenetic
determination of sexual differences in mean adult body size. (1) This dimorphism
is determined mainly by the direction and degree of SSD present at the attainment
of sexual maturity. Under this hypothesis, sexual differences in mean adult size
are determined by processes operating on juveniles: sex differences either in
growth rate or in the age at maturation. (2) Mean adult SSD is determined mainly
by sex differences in growth or survival rates during adult life. Under this hy-
pothesis, differences in adult size between the sexes result because adults of one
sex grow faster or survive better than adults of the other sex.
The first of these alternatives-SSD at maturation is the prime determinant of
dimorphism in mean adult body size-is consistent with a wide range of hypoth-
eses that explain SSD as an adaptation or as a result of phylogenetic conserva-
tism. Even if mean adult SSD is the actual target of selection, this may well be
achieved evolutionarily by a modification of the genes that control SSD at matura-
tion. Local environmental conditions as well as genotypic factors may influence
the SSD at maturity (Gibbons et al. 1981; Stearns and Koella 1986).
The hypothesis that processes operating during adult life (i.e., after maturation)
are the primary determinants of mean adult SSD is also consistent with a wide
variety of evolutionary and ecological ideas. For example, such differences in
growth or survival rates between the sexes could be influenced by sex-specific
adaptations of physiology, morphology, or behavior, in which case the resulting

Am. Nat. 1990. Vol. 135, pp. 278-283.

@ 1990 by The University of Chicago. 0003-0147/90/3502-0013$02.00. All rights reserved.
 NOTES AND COMMENTS 279

SSD could be interpreted in terms of adaptation. However, these adaptationist

interpretations do not rely on the determination of SSD by processes operating
during adult life; they are equally compatible with the determination of SSD
earlier in ontogeny, as suggested above. The most interesting case concerns
hypotheses that are inconsistent with the determination of mean adult SSD at
maturity and that rely instead on processes during adult life as the prime determi-
nants of mean adult SSD. For example, if the reason that adult males are smaller
than females is that adult males allocate energy to reproduction rather than to
growth (Woolbright 1983, 1989), sexual differences in mean adult SSD must be
due primarily to sex differences in growth rate during adult life. Similarly, if the
relative mean adult body sizes of males and females are strongly influenced by
differential survival rates (as shown by Howard [1981] for Rana catesbeiana, and
suggested to be of general importance by Halliday and Verrell [1986]), sexual
differences in mean adult body sizes must be due mainly to processes operating on
adult animals. .
Clearly, this hypothesis is not applicable to animal species in which little growth
occurs after maturation. Presumably for this reason, the hypothesis that processes
acting during adult life determine SSD seems not to have been invoked in regard
to birds and mammals, which typically show determinate growth. Nonetheless,
growth continues after maturity in many mammals and may differ between the
sexes (see, e.g., Jarman 1983; Georgiadis 1985), suggesting that processes operat-
ing during adult life might affect SSD in this group as well. Growth also continues
after maturity in many invertebrates, although usually not in insects. The rele-
vance of the hypothesis to ectothermic vertebrates is clear, since growth typically
continues after maturity in these animals (in reptiles, maturity occurs at about
80% of maximum body length; Andrews 1982). In such a group, sex differences in
gfowth or mortality during adult life could greatly influence observed SSD. There
is no doubt that sexual differences in adult growth rates and survival rates do
occur (see, e.g., Tinkle 1967; Dunham 1981; Howard 1981) and, hence, that mean
adult SSD is affected by these factors. The question is whether these processes
acting during adult life are sufficiently widespread, and of sufficient magnitude, to
modify significantly any general patterns of SSD established earlier in ontogeny.
This question may be answered by examining the extent of correlation evident
between the direction and degree of SSD measured at these two stages of the life
history: at maturation and at mean adult body size. If SSD at mean adult body size
is highly correlated with SSD at maturity, then nothing that happens after maturity
(including sex differences in growth or survival rates during adult life) can have a
major influence on broad patterns in mean adult SSD. Alternatively, if proximate
effects during adult life are important determinants of mean adult SSD, then little
correlation would be expected between SSD at maturity and SSD at mean adult
body size. Comparative analyses of this type are best made among related taxa,
rather than combining higher taxonomic categories (see, e.g., Clutton-Brock and
Harvey 1984; Dunham and Miles 1985). Species can be used as independent units
in the analysis because phylogenetic conservatism is irrelevant to the hypothesis.
I examined eight data sets: five from reptiles, two from amphibians, and one from
fishes (see table 1). Maturity was defined according to morphological rather than
280 THE AMERICAN NATURALIST

TABLE I
THE RELATIONSHIP BETWEEN SEXUAL SIZE DIMORPHISM (SSD) AT THE TIME OF SEXUAL MATURATION
AND AT MEAN ADULT BODY SIZE

Proportion with Correlation

SSD in Same Coefficient
No. of Direction at between SSD
Lineage Species Each Stage at Two Stages Source

Lizards
Ano/is 65 0.95** 0.93** Fitch 1981
Sceloporus 47 0.77** 0.82** Fitch 1981
Gekkonidae 41 0.88** 0.63** Fitch 1981
Snakes
Natricinae 36 0.89** 0.63** Fitch 1981
Turtles 31 0.94** 0.90** Fitch 1981
Frogs
Chinese spp. 17 0.88** 0.93** Liu 1950
Neotropical hylids 19 0.95** 0.92** Duellman 1970
Fishes
Mugilids 10 0.60 0.83** Grant et al. 1977

** P < 0.01.

behavioral criteria in each case. All eight lineages included some species in which
females grow larger than males and others in which the reverse is true. In 89% of
all species within these lineages (n = 266), the sex that matured at a larger size
also attained a larger average adult size. The relationship between the direction of
SSD at maturity and mean adult SSD was much stronger than would be expected
by chance (X2, df = 1, P < 0.01) in seven of the eight comparisons, with the
exception being the small data set for mugilid fishes (see the table).
-Analyses of these data in terms of the degree (rather than just the direction) of
SSD yielded similar results. I calculated Fitch's (1981) measure of dimorphism
(the ratio offemale body length to male body length) for each species in the above
lineages. In each case, strong correlations were evident between SSD at maturity
and SSD at mean adult size. The proportion of the inter specific variance of mean
adult SSD that could be explained by SSD at sexual maturity ranged from 40% to
88% and was significantly greater than expected from the null hypothesis of no
relationship between these variables (P < 0.01 in each case). The correlation
between SSD's at these two stages of the life cycle tended to be highest for
comparisons among congeneric species and slightly lower for comparisons incor-
porating less closely related taxa (table 1). Stamps (1983) reported a similarly high
correlation between SSD at maturity and SSD at mean adult size in 33 lizard
species (r = 0.87). Using ratios in such analyses may sometimes introduce
statistical artifacts (see, e.g., Packard and Boardman 1988), but an alternative
analysis of these data using residuals from general regressions gave results essen-
tially identical to those based on ratios (r = 0.61 to 0.95). Visual inspection of
these regressions revealed no obvious departures from linearity. Intercepts of the
regression equations were generally close to zero: the difference between SSD's
at these two stages of the life history averaged less than 3% (range of means, 0% to
8%). Slopes of the reduced major-axis regressions were not significantly different
 NOTES AND COMMENTS 281

from 1.0 in six of these eight data sets, suggesting that dimorphism in body size
tends to be similar at maturity and at mean adult size. Overall, it is clear that the
direction of adult SSD in these animals is determined primarily by SSD at matu-
rity. This result should also apply to endothermic vertebrates, which typically
show relatively little growth after maturity. Correlations between the degree of
SSD at these two stages of the life cycle are less than 1.0 (table), possibly because
of error in the data or because of post-maturational sex differences in growth rates
or survival rates affecting adult SSD.
The hypothesis that SSD is primarily determined by sex differences in growth
rate or survival rate during adult life (in species in which growth continues after
maturation) also makes at least one prediction that can be readily evaluated.
Because fighting is risky and energetically expensive, sex differences in growth or
survival rate during adult life in species with male combat should tend to reduce
mean adult body size in males relative to that in females, compared with the SSD
expected if combat did not occur. Hence, all else being equal, one might expect a
decrease in the ratio of male size to female size in taxa with male combat
compared with taxa without this behavior. This prediction relies on a lack of
systematic shifts in other factors (such as maternal investment) concurrent with
the evolution of male combat, and such potential confounding factors deserve
further investigation. Nonetheless, it is interesting to note that the prediction
derived from the hypothesis of post-maturational determination of adult SSD is
directly contrary to that from Darwin's (1871) adaptationist hypothesis that male-
male combat favors the evolution oflarge body size in males. Darwin's hypothesis
does not specify at what point in ontogeny this SSD should be established; it
simply predicts that males should be large in species with male combat. The
success of the Darwinian prediction among both ectotherms and endotherms (see,
e.g:', Darwin 1871; Trivers 1972; Wiley 1974; Clutton-Brock et al. 1977; Shine
1978, 1979; Wells 1978; Berry and Shine 1980; Veuille and Rouault 1980; Crespi
1986) is consistent with the notion that broad patterns of SSD among animal
species are set at maturity, with only minor modification by differential growth or
survival rates of adult males and females.
Overall, the patterns documented in this study suggest that differences in pre-
maturational growth, age at maturity, or both are the primary determinants of
sexual dimorphism in adult body size. Post-maturational differences in growth or
survival rates between the sexes are not totally irrelevant but probably influence
the direction (as opposed to the degree) of adult SSD only rarely. Influences on
SSD at maturity thus deserve further investigation. A clarification of the extent of
phenotypic flexibility in SSD at maturity (as in Gibbons et al. 1981) would be
particularly valuable: if proximate environmental factors are important determi-
nants of SSD at maturity, interpretations of mean adult SSD in terms of adaptation
may be in error (RaIls and Harvey 1985).

ACKNOWLEDGMENTS

I thank R. Lambeck for assistance with data analysis, R. Lambeck, J. Caley, C.

James, and L. Schwarzkopf for comments on the manuscript, and B. Thresher
282 THE AMERICAN NATURALIST

and C. Shine for typing. This work was supported by the Australian Research
Committee.

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RICHARD SHINE
DEPARTMENT OF ZOOLOGY Ao8
UNIVERSITY OF SYDNEY
NEW SOUTH WALES 2006
AUSTRALIA
Submitted May 4, 1988; Revised October 11, 1988, and February 6, 1989; Accepted June
12, 1989
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