Comments on Theoretical Biology, 7: 1133, 2002
Copyright # 2002 Taylor & Francis
0894-8550/02 $12.00 + .00
DOI: 10.1080/08948550290022033
Male and Female Growth in Sexually
Dimorphic Species: Harmony, Conflict,
or Both?
Alexander V. Badyaev
Department of Ecology and Evolutionary Biology,
University of Arizona, Tucson, Arizona, USA
In most vertebrates, males and females are nearly identical in morphology
during early development, but, as a result of highly divergent growth,
achieve often remarkably different adult morphologies. Although numerous studies have documented selection pressures that favor distinct
morphologies of adult males and females, the mechanisms that enable the
initially genetically identical sexes to end up so different in morphology
are not well understood. Of special interest are the constraints imposed on
sex-specific adaptations by a common gene pool and the ways by which
males and females overcome these constraints. Recent studies show that
the rapid evolution of sex-specific developmental regulators and modifiers
of the otherwise conserved development of the sexes can produce sexual
size dimorphism while maintaining the integrity of the developmental
program that is shared between males and females.
Keywords: Age, growth, ontogeny, phenotypic plasticity, selection, sexual dimorphism
Variation in sexual size dimorphism (SSD)—a difference in size between
males and females—is commonly attributed to the combined effects of sexspecific selection pressures, sex-biased phenotypic and genetic variation,
and genetic correlations between sexes (Darwin 1871; Ralls 1977; Lande
1980; Slatkin 1984; Shine 1989; Fairbairn 1997). There have been several
Address correspondence to the current address of Alex Badyaev, 1041 E. Lowell, Dept. of
Ecology & Evolutionary Biology, University of Arizona, Tucson, AZ 85721-0088, USA.
E-mail: [email protected]
11
12
A. V. Badyaev
general approaches to the study of SSD evolution. First, researchers have
focused on documenting sex-specific selection pressures in relation to
observed SSD (e.g., Price 1984; Rising 1987; Weatherhead et al. 1987;
Preziosi and Fairbairn 1996; Powell and King 1997; Badyaev and Martin
2000). Second, studies in quantitative and population genetics have
addressed the theoretical aspects of SSD evolution, especially focusing on
the independent evolution of the sexes under divergent selection (Lande
1980; Cheverud et al. 1985; Reeve and Fairbairn 1996, 2001; Rhen 2000).
Third, SSD has been extensively studied from a physiological standpoint,
especially in relation to its neuroendocrinological controls (Gatford et al.
1998; Varma and Meguid 2001). Finally, major advances in molecular
biology, especially in relation to the evolution of sex determination, have
significantly contributed to our understanding of the genetic regulation of
the processes leading to changes in SSD (Swain and Lovell-Badge 1999;
Capel 2000; Zarkower 2001).
Despite a large volume of research and a wealth of information, there has
been a remarkable lack of integration between each of these fields and
approaches. This has significantly slowed our understanding of the genetic
basis and evolutionary significance of SSD variation. For example, numerous
empirical studies have documented the lack of sex-biased phenotypic and
genetic variance in many morphological traits (Roff 1997), and standard
quantitative genetics theory (Lande 1980; Lande and Arnold 1985) suggests
that this will strongly constrain the short-term evolution of SSD. At the same
time, numerous empirical examples of a rapid change in SSD in response to
selection (Table 1) (Mitani et al. 1996; Wikelski and Trillmich 1997;
Badyaev et al. 2000; Butler and Schoener 2000) suggest that the constraints
imposed by a shared developmental program can be mitigated, at least
temporarily, by a variety of phenotypic mechanisms. More generally, the
combination of a conserved developmental process shared between the sexes
and the rapid evolution of sex-specific modifiers of these developmental
processes may provide a compromise between what is favored by current
selection for SSD and what is possible to achieve without destroying the
integration of essential components during an organism’s development.
What is frequently found in developmental physiology studies of SSD and
nearly universally overlooked in quantitative and population genetics models
of SSD (but see Rhen 2000) is that the sex-biased expression of size-related
traits whose genetic determination is not sex limited (most traits) is
accomplished by sex-specific regulators of development (Gatford et al.
1998; Zarkower 2001). Moreover, empirical studies, especially those of
domestic animals and primates, frequently document remarkable contrast
between the slow evolution of SSD in adults and rapid and labile evolution of
growth patterns that lead to SSD (Table 1).
Recent studies in the evolution of SSD are increasingly focusing on the
sex-specific expression of gene action and the evolution of sex-specific
modifiers of alleles shared by the developmental programs of both sexes
13
Stature
Stature
Stature
Tarsus,
mass
Mass
Mass
Human
Homo sapiens
Human
Homo sapiens
Human
Homo sapiens
Japanese quail
Coturnix c. japonica
White-tailed deer
Odocoileus virginianus
Snow goose
Anser c. caerulescens
Vervet monkey
Carcopithecus aethiops
Sex-specific
sensitivity to
conditions during
growth
Mass,
size
Trait
Species
Main mechanism
TABLE 1 Examples of rapid change in sexual size dimorphism
Population differences in SSD=
male sensitivity to proportion of
protein in the diet
30% increase in SSD over
one generation=greater male
capitalization on improving
growth conditions
Experimental reduction in SSD=
unequal response of sexes to
restricted diet during growth
Decrease in SSD over 16 years
of increasing population
density=male sensitivity
Seasonal variation in SSD=changes
in male growth
Change in SSD between sites
due to variation in tourist
lodge (food) proximity=female
sensitivity
Increase in SSD over <50 years=
greater male sensitivity
Evidence for rapid change=proposed
mechanism
Turner et al. (1997)
Cooch et al. (1996)
Leberg and
Smith (1993)
Gebhardt-Henrich and
Marks (1993)
Bielicki and
Charzewski (1977)
Stini (1969)
Tobias (1972)
Source
14
Main mechanism
TABLE 1 (Continued)
Size,
mass
Tarsus
Mass
Mass
Great tit
Parus major
Domestic pig
Sus scrofa
Bighorn sheep
Ovis canadensis
Mass
Mass
Moose
Alces alces
Feral sheep
Ovis spp.
Red deer
Cervus elaphus
Tarsus
Pied flycatcher
Ficedula hypoleuca
Alpine ibex
Capra ibex ibex
Size
Trait
Species
SSD changes with nest mite
exposure=male sensitivity
Decrease in SSD in cohorts born
after winters with higher snow
cover=male sensitivity
Seasonal variation in SSD depending
on time of birth=male sensitivity
Increase in SSD over 32 years of
warmer climate=16% increase in
male weight, 10% decrease in
females
Change in SSD due to changes
in population density=male
sensitivity
Increase in SSD under experimentally
increased competition during
growth=unequal environmental
sensitivity of sexes
Change in SSD under experimental
change in competition during
growth=male sensitivity
Decrease in SSD over 19 years of
increasing population density=lack
of compensatory growth in males
Evidence for rapid change=proposed
mechanism
LeBlanc et al.
(2001)
Dunshea (2001)
Oddie (2000)
Ferguson et al.
(2000)
Réale and
Bousses (1999)
Post et al. (1999)
Toı̈go et al. (1999)
Potti (1999)
Source
15
Size
Tarsus
Spotless starling
Sturnus unicolor
House finch
Carpodacus mexicanus
Carnivorous marsupials
Dasyuridae
Mass
Mass,
size
Size
Size
Human
Homo sapiens
Anura
Eleutherodactylus
coqui
Sifakas
Propithecus spp.
Stature
Human
Homo sapiens
Sex-biased maternal
investment during
growth
Sex-specific selection
during growth
period
Trait
Species
Main mechanism
TABLE 1 (Continued)
SSD variation among 76 populations=
changes in value and maternal care
of daughters
Variation in SSD among 7 populations=
change in value and maternal care
of sons
Seasonal variation in SSD=sex bias in
maternal transference of nutrients
to eggs
Population divergence in phenotypic
SSD over 50 years=egg-based
maternal effects
Decrease in SSD in captive vs.
free-living animals=lesser
selection on ontogeny of sexes
Population difference in SSD=diet
during growth and sex-specific
dominance patterns due to
food dispersion
Greater SSD during lactation period in
captive- versus free-living animals=
less sex-limiting maternal effects
during lactation
Evidence for rapid change=proposed
mechanism
Soderquist (1995)
Ravosa et al. (1993)
Woolbright (1989)
Badyaev et al. (2002)
Cordero et al. (2001)
Hall (1978)
Holden and
Mace (1999)
Source
16
Sex-biased genetic
variance in growth
and adult traits
Main mechanism
TABLE 1 (Continued)
Selection during growth limits SSD
in Chubut aborigines
Changes in SSD=sex difference
in growth and selection
during growth
Decrease in SSD in captive-born
vs. free-living populations=lesser
selection on ontogeny of sexes
Population difference in SSD=diet
during growth and dimorphism
in growth patterns
Changes in SSD=adaptations of
juveniles to winter severity
Change in SSD under selection
on growth rate=low between-sex
genetic correlations for growth traits
Increase in SSD (78%) over 13 years
of selection on growth=additive
genetic variance for SSD
Change in SSD over 36 generations
of selection on body weight=sex
differences in heritability of growth
and body size
Size,
mass
Size
Mass
Mass,
size
Mass
Mass
Mass
Mass
Human
Homo sapiens
Howler monkey
Alouatta palliata
Mandrill
Mandrillus sphinx
Black bear
Ursus americanus
White-tail deer
Odocoileus virginianus
Domestic chicken
Gallus domesticus
Domestic chicken
Gallus domesticus
Domestic chicken
Gallus domesticus
Selection during growth limits SSD
Size
Lemurid primates
Evidence for rapid change=proposed
mechanism
Trait
Species
Liu et al. (1994)
Toelle et al. (1990)
L’Hospitalier
et al. (1986)
Mignon-Grasteau
et al. (1999)
Lesage et al. (2001)
Mahoney et al. (2001)
Setchell et al. (2001)
Jones et al. (2000)
Leigh and
Terranova (1998)
Oyhenart et al. (2000)
Source
Ontogeny of Sexual Dimorphism
17
(Rice and Chippindale 2001). What is currently both missing and needed is
an integration of the existing knowledge of patterns of sex-specific selection
on ontogeny, sex-specific aspects of development (particularly the neuroendocrinological controls of growth of males and females), and the genetic
theory of the SSD evolution. Here I review the evidence suggesting that a
thorough understanding of the environmental and genetic interactions during
the ontogeny of dimorphism provides an excellent opportunity for the
integration of molecular, physiological, and evolutionary approaches to the
study of SSD.
I focus on recent advances in understanding of the ontogenetic basis for
rapid phenotypic change in SSD in vertebrates, especially in mammals and
birds. Recent studies suggest that microevolutionary changes in the growth of
males and females can provide a solution to an apparent paradox of rapid and
adaptive evolution of SSD. The central thesis of this approach is that the
growth of males and females is governed by partially independent hormonal
and physiological controls, and this results in a sex-specific distribution of
phenotypic and genetic variation throughout ontogeny. Such differences
between sexes in the control of growth and development can lead to
differences in the way males and females respond to environmental variation
and selection during ontogeny and can produce a rapid change in SSD even
under the constraints of a shared (genetically linked between the sexes)
developmental program. Ultimately, selection for SSD should favor the
evolution of sex-specific developmental modifiers, such as sex-limited
hormonal regulators.
SHARED DEVELOPMENTAL PROGRAM OF MALES AND
FEMALES: EVOLUTIONARY COSTS AND BENEFITS
Theory
The morphological change in each sex under selection is due to the direct
response of that sex and the correlated response of the other sex (Lande
1980). Thus, the response ðRÞ of male (m) and female (f) for each trait can be
presented as:
Rm ¼
1 2
hm Sm I m þ hm hf r g Sm I f
2
and Rf ¼
1 2
hf Sf I f þ h m hf r g Sf I m
2
where h2 is the narrow sense heritability, S is the standard phenotypic
deviation, I is the selection intensity, and rg is the between-sex genetic
correlation (after Cheverud et al. 1985). Therefore, the one-generation
response of SSD to selection (RSSD) can be defined as the difference between
male and female responses:
18
A. V. Badyaev
1
RSSD ¼ ½h2m Sm Im h2f Sf If þ hm hf rg ðSm If Sf Im Þ:
2
Sex differences in either selection parameters (I) or in phenotypic and=or
genetic variance parameters (S, h2) can lead to changes in SSD (Cheverud
2
¼ h2f and Sm ¼ Sf, but Im 6¼ I f, RSSD will be proportional
et al. 1985). When hm
to jIm If j adjusted by the between-sex genetic correlation, r g (the
differences in the expression of gene effects between the sexes):
1
RSSD ¼ h2 SðIm If Þð1 rg Þ
2
When I m ¼ I f, but Sm 6¼ Sf, RSSD will be proportional to jSm 7 Sfj, adjusted
by r g:
1
RSSD ¼ h2 IðSm Sf Þð1 rg Þ:
2
Under both scenarios, the strength of between-sex genetic correlations should
play a decisive role in determining the evolution of SSD (Cheverud et al).
However, the importance of r g in predicting response of SSD to selection
in empirical studies is a debated issue. Reeve and Fairbairn (1996; 2001) have
shown that fluctuations in genetic variance of both sexes can produce
extensive and rapid changes in genetically based SSD even in the presence of
high between-sex genetic correlations. The fluctuations can occur as a result
of variation in both the strength and targets of selection and in the distribution
of allelic effects.
Empirical Examples
The lack of sex bias in genetic variation (i.e., r g ¼ 1) in the fully grown
traits (i.e., in adult size) is frequently documented, revealing a strong
constraint on genetically based changes in SSD. For example, high betweensex genetic correlations reduced the optimum response to strong sex-specific
selection by 50% in males and by 200% in females in a flycatcher (Ficedula
albicolis) (Merilä et al. 1998). Similarly, based on the findings of r g ¼ 1 for a
number of size traits in humans, it was shown that the evolution of SSD
will be 65 times slower than the evolution of the mean size of both sexes, and
that SSD will not change over thousands of years even under strong selection
(Rogers and Mukherjee 1992). In experiments, it is frequently found that
selection on one sex results in a correlated response in the other sex and that
the mean size often changes in unpredictable ways because of correlations
between the sexes (Reeve and Fairbairn 1996; Bihan-Duval et al. 1998).
However, while the sexes can be similar in the genetic variance associated
with the full expression of a size-related trait, the ontogeny of this trait can
differ between males and females. Indeed, artificial selection capitalizing on
Ontogeny of Sexual Dimorphism
19
sex-biased genetic and environmental variation during growth can accomplish significant short-term changes in SSD (Table 1). Moreover, high
between-sex genetic correlations themselves can be produced by long-term
selection for the developmental stability of physiological processes that are
shared between the sexes. For example, when such selection for sex-biased
expression of a trait is not consistent, it may be advantageous for the
developmental program not to respond rapidly to environmental change.
Thus, although high between-sex genetic correlations may limit the speed of
adaptive morphological change in each sex in response to local selection,
these constraints may be beneficial if selection pressures fluctuate (see also
Reinhold 1999). For example, in stoats (Mustela erminea), an increase in
SSD in the years with abundant food supply during growth was opposed by
higher mortality risks of populations with greater SSD during years with poor
food supplies. Consequently, populations with the average level of SSD had
the highest fitness (Powell and King 1997).
Similarly, populations and species with greater SSD are more likely to
become extinct under novel environmental conditions compared to monomorphic species (McLain 1993), partly because of the inability to rapidly
change body size (‘‘species size’’) in response to novel conditions when male
and female morphologies are highly distinct. Given the apparently adaptive
value of high between-sex genetic correlation (i.e., shared developmental
processes), selection should favor the evolution of genetic and physiological
regulators that allow the developmental program shared between the sexes to
gradually integrate environmental demands for sex-specific and age-specific
expression without disruption of shared developmental programs.
OVERCOMING CONSTRAINTS OF SHARED
DEVELOPMENTAL PROGRAMS: RAPID EVOLUTION
OF GROWTH PATTERNS
Patterns: Selection for Sex-Specific Expression
Selection acting on developmental aspects of body size—for example on
growth rate and growth duration—can produce rapid changes in SSD of adults
(Gebhardt 1992; Reeve and Fairbairn 1996). Because most genes that underlie
SSD are not sex linked, the regulatory mechanisms specific to males and
females account for a vast majority of SSD. Correspondingly, modeling the
evolution of SSD via sex-limited effects at autosomal loci results in more
accurate predictions of the evolutionary trajectory of SSD change (Rhen 2000).
Because similar levels and patterns of adult SSD can be produced by
highly distinct growth processes, we cannot understand the evolutionary
change in SSD without knowing the ontogeny of and selection on SSD
(Jarman 1983; Shea 1986; Leigh 1995). There is a remarkable contrast
20
A. V. Badyaev
between the extremely slow evolution of genetically based SSD in adults and
the rapid evolution of differences between males and females in growth
patterns. These differences in growth are evident among related species,
subspecies, and populations (Brooks 1991; Badyaev et al. 2001a), as well as
among different size-related traits within an organism (Humphrey 1998).
The two main developmental processes that produce SSD are sex
differences in growth rate and in growth duration (Cheverud et al. 1992;
McNamara 1995). In many large terrestrial herbivorous mammals and some
primates, sexes differ in growth duration while there is no difference in
growth rates (Jarman 1983; Shea and Bailey 1996). In some species, such as
bison (Bison bison), males have indeterminate growth, whereas females stop
growing soon after reaching sexual maturity (Jarman). In other species, males
and females differ in both growth rate and duration but the contribution of
these processes to adult SSD differs even among closely related species
(Leigh 1992; German et al. 1994; Taylor 1995; Lammers et al. 2001). For
example, subspecies of lowland and mountain gorillas (Gorilla gorilla)
(Taylor 1997) as well as subspecies of pygmy (Pan paniscus) and common
chimpanzees (P. troglodytes) (Shea 1985; 1986) strongly differ in growth
duration and rate. The SSD in mountain gorillas and pygmy chimpanzees is
largely produced by sex differences in growth duration, while in the common
chimpanzee it is largely a result of sex differences in growth rate (Leigh and
Shea 1996). In other species, such as the pigtailed macaque (Macaca
nemestrina), SSD is produced by complex temporal patterns of sex-specific
growth rate and sex-specific growth duration (German et al.). Similarly, in
birds, closely related taxa often differ in the contribution of sex differences in
growth duration and growth rate to adult SSD (Teather and Weatherhead
1994; Handcock et al. 1995; Badyaev, Hill et al. 2001). In reptiles, adult SSD
in some species is produced by sex differences in growth rate only (Griffith
1991), whereas other groups show a remarkable diversity in the ontogeny of
SSD (Stamps and Krishnan 1997). Brooks (1991) showed that adult SSD is
produced by a remarkable diversity of sex-specific processes during ontogeny
in four species of Labrisomidae fish.
Patterns: Selection for Age-Specific Expression
Because of the cascading effects of growth, between-sex developmental
integration during early ontogeny can carry over to later life stages,
preventing the sexes from reaching their distinct adaptive optimum. Sex
steroids that induce sex-specific growth patterns (discussed later) often
determine the time of growth termination and thus regulate final size and
SSD. For example, a close association between the timing of sexual
maturation and patterns of secretion of growth hormone (GH) in men and
women accounts for most of the variation in SSD in adults (Charmandari et al.
2001; for similar results in fishes, amphibians, and reptiles, see Shine 1990;
Ontogeny of Sexual Dimorphism
21
Stamps and Krishnan 1997). In poultry, long-term and sex-biased selection
on growth patterns lowers the genetic correlation between the age of
maximum growth and adult SSD (Bihan-Duval et al. 1998; Mignon-Grasteau
et al. 1999), while in lineages with no history of such selection, a change in
adult SSD is genetically correlated with the time of maturity (Dunnington and
Siegel 1996).
One solution to conflicting intersexual effects is the evolution of
regulatory mechanisms that, in both sexes, would limit a trait expression to
stages in which such expression is favored by selection, that is, mechanisms
that produce a relative independence of adult and juvenile stages. An
interesting example of temporal disassociation between selection favoring
SSD and development of SSD is the evolution of sexual dimorphism in the
size and shape of the pelvis in mammals. Although SSD in the pelvis is
developed during juvenile period, selection only in adult stages favors SSD in
this trait (LaVelle 1995; Lammers et al. 2001). As a result of a conflict
between selection pressures during juvenile and adult stages, SSD in the
pelvis leads to limitations of SSD of neonates (discussed later; Guégan et al.
2000).
Mechanisms: Sex-Biased Regulation of Growth
Ontogenetic intersexual conflict can be resolved by the evolution of
regulatory processes that enable the sex-specific expression of shared genes,
while maintaining the integrity of the developmental program shared between
males and females. Such sex-specific expression of morphological variation
is accomplished by the rapid evolution of hormonal controls of development.
For example, SSD in head size in garter snakes (Thamnophis sp.) is caused
by sex-specific effects of androgens during early development: When
hormonal effects are removed, sex differences in growth and SSD of adults
disappear (Crews et al. 1985; Shine and Crews 1988). Similarly, most of
the SSD in human stature is due to sex differences in the rate and duration
of growth spurts during puberty. In both sexes, growth spurts are closely
associated with a gonadal steroid-dependent rise in GH resulting in growth
gains of up to 8.5 cm=year in girls and 9.5 cm=year for boys (Metzger et al.
1994).
More generally, across all studied vertebrates, the growth of both sexes
depends on the concentration of circulating GH and growth factors (such as
insulin-like growth factors IGF-I and IGF-II) (Gatford et al. 1998). However,
despite the consistency in response to these hormones, growth is modified
between the sexes because of the sex-specific patterns of synthesis and
secretion of GH (Gatford et al. 1996), as well as the sex-specific sensitivity of
tissues to GH. The synthesis and secretion of these factors are under the
control of gonadal steroids, but the relative importance of sex steroids
for secretion of GH, the onset of their action, and the biochemical pathways
22
A. V. Badyaev
by which their effect are accomplished is different between species
(Gatford et al. 1998; Hassan et al. 2001). Furthermore, the neuroendocrinological controls of GH synthesis and secretion are highly sex-specific (Jaffe
et al. 1998; Agrawal and Shapiro 2001). For example, continuous administration of GH to rats (Rattus norvegicus) does not achieve changes in growth
patterns, while administration of GH in sex-specific pulse patterns produces a
strong and sex-specific response (Borski et al. 2000).
There are several general pathways to accomplish the sex-specific
regulation of growth despite the shared effects of GH on growth. For
example, prenatal exposure to steroids determines the sex-specific sensitivity
of the GH-producing pituitary gland to GH-controlling hormones, and thus
establishes a long-term sex-specific sensitivity of growth to GH secretion
(Chowen et al. 1998). Subsequent exposure to a similar concentration of
steroids later in life then produces a strongly sex-specific GH release and thus
sexually dimorphic growth (Painson et al. 2000). Also, gonadal steroids can
directly influence hypothalamic secretion of GH-controlling hormones
(Kamegai et al. 1999) and thus produce sex-specific plasma concentrations
of GH. Sex-specific growth patterns then are due to temporal differences
between males and females in the secretion of gonadal steroids (Potau et al.
1999). Finally, early in development, sex steroids can produce a sex-specific
density and distribution of hormonal receptors (Brandstetter et al. 2000;
Yellayi et al. 2000) and hormone-secreting cells (Lopez et al. 1995; Zhang
et al. 1999), ultimately resulting in differential sensitivity to hormones across
tissues. Early onset of hormonal sensitivity is corroborated by experiments in
which castration of adult laboratory animals did not affect the sex-specific
GH sensitivity of their tissues (Liu et al. 2000). All of these pathways can
produce highly sex-specific patterns of growth while preserving critical
features of early development that are shared between the sexes.
Mechanisms: Age-Biased Regulation of Growth
Another solution to conflicting intersexual effects is the evolution of
regulatory mechanisms that, in both sexes, would limit trait expression to
stages in which such expression is favored by selection. The sex-specific
secretion of GH (and corresponding growth) is mediated by both the patterns
of delivery of gonadal steroids and duration of exposure to these steroids (i.e.,
age). The role of age-specific mediators of sex steroids’ effects on GH
production is illustrated by the fact that the same levels of circulating steroids
in adulthood do not produce the same response of GH secretion as they do
during the juvenile period (Metzger et al. 1994). In a few species, however,
age-specific variation in growth is accomplished by variation in GH
production and not by variation in receptor sensitivity to GH (Velasco et al.
2001). In humans, different factors contribute to age dependency in growth in
Ontogeny of Sexual Dimorphism
23
men and women—both the maintenance of GH secretion and the age-specific
regulation of this secretion differ between the sexes (Orrego et al. 2001).
Sexually dimorphic size traits that are expressed only in late ontogenetic
stages (i.e., those that do not require extensive developmental integration
with other traits) should develop with the lowest intersexual conflict. For
example, the sex-specific pattern of fat deposition (Comuzzie et al. 1993),
which is under sex-biased physiological controls (Weaver et al. 1998; Pericas
et al. 2001), is expressed only late in development and shows some of the
most sex-specific expression and sex-biased genetic determination among
size-related traits. Similarly, in many species the most sexually dimorphic
growth occurs during short periods late in development (Turner et al. 1997;
Vasil’eva 1997; O’Higgins et al. 2001).
The intensity of ontogenetic intersexual conflict depends on the duration
of growth or, more generally, on the relative duration of stages when
selection favors or opposes the similar appearance of the sexes and the
relative intensity of selection during these periods. Longer growing species
are subject to more age-specific selection and thus are likely to evolve a
greater disassociation in growth patterns between the sexes. For example,
humans have a prolonged juvenile period, and sex-specific selection during
this period has strong consequences on the ontogeny of SSD. In females, the
early onset of a growth spurt (23 years earlier than males) and its higher
intensity and shorter duration compared to males, is thought to prevent the
conflict between allocation to growth and early pregnancy (Scholl et al.
1994).
More generally, these mechanisms produce highly sex- and age-specific
growth without interfering with the major regulatory aspects of development.
Such regulatory aspects of development are shared between males and
females and may be vital for the functional integration of sexually
monomorphic and sexually dimorphic traits within an organism.
EMPIRICAL EXAMPLES OF RAPID CHANGE IN SSD
Direct Selection on Male and Female Growth
Typically, SSD is favored by selection acting during the adult stage when
differences in size contribute to the reproductive success of both sexes (Wiley
1974; Jarman 1983). However, there are many species in which sex-specific
selection during growth is the most important factor in SSD variation. For
example, limitations on duration of growth of the sexes (such as from birth
synchrony or growth season duration) result in distinct patterns of growth in
males and females and thereby generate sex-specific selection on their
morphology (Crowley 2000).
An interesting example is the sex-specific selection on different rates of
growth and development in male and female embryos in mammals. In large
24
A. V. Badyaev
mammals, including humans, the differences between male and female
growth patterns are evident as early as 6 h postfertilization at the 32-cell stage
(Mittwoch 1993; Ray et al. 1995); male embryos grow up to five times faster
than female embryos during the early prenatal period. These sex differences
in development are driven by the need of early gonadal differentiation of
males and the corresponding production of gonadal testosterone necessary to
sustain the normal sex-specific development of males despite the increase in
circulating maternal estrogens as pregnancy progresses (Ray et al. 1995). In
turn, the faster initial growth of male embryos in mammals sets the stage for
the greater sensitivity of male embryos and male growth to environmental
conditions during growth (e.g., Oyhenart et al. 1998; see below).
Correspondingly, male embryos have the highest mortality under stress
during pregnancy, but also capitalize more than female embryos on favorable
environmental conditions during growth (Table 1). Several studies of
mammals suggest that the growth of males is maximized in relation to the
physiological potential of an individual and the environmental variation
during growth. For example, injections of increasing concentrations of GH do
not achieve an increase in the growth rate of male rats, but produce a
substantial increase in the growth of females (De Lama et al. 2000).
Similarly, in bighorn sheep, the growth of males is maximized and shows
lesser potential for compensatory growth compared to females. As a result,
the adult size of males reflects conditions during growth better than the adult
size of females, which, because of their slower growth, can undergo a period
of compensatory growth following unfavorable environmental conditions
(LeBlanc et al. 2001).
An example of selection for SSD during the juvenile period is found in the
sex difference in the growth of primates. In many primates, the sexes show
significant differences in the timing and duration of growth spurts. Female
primates commonly have earlier and more prolonged growth spurts,
apparently to minimize the interference between growth and a potentially
early pregnancy. In males, a delayed and more condensed growth spurt is
favored because of the benefits of retaining small size during the prolonged
juvenile period to reduce competition and agonistic interactions with older
males (Leigh 1996). Thus, sexual dimorphism in growth patterns evolves as a
result of selection pressures during the juvenile period. For example, in
mountain gorilla, SSD in skeletal structure is due to faster and longer growth
of males compared to females and is favored by distinct selection on
locomotor behaviors of the sexes during the juvenile period (Taylor 1995).
More generally, a close correlation between the social and ecological
conditions experienced during growth and the patterns of SSD acquired
during growth illustrates that sex-specific selection during ontogeny is one of
the main determinants of SSD in primates (Leigh 1995).
Intersexual ontogenetic conflict is enhanced when selection favors the
opposite pattens of SSD during juvenile and adult stages. For example, in
birds, selection during nestling and fledgling periods is often opposite
Ontogeny of Sexual Dimorphism
25
to the pattens of SSD favored in adults (Merilä et al. 1997; Badyaev,
Whittingham et al. 2001). Of special interest is the estimation of the relative
strength and direction of selection acting on juvenile versus adult males and
females.
Maternal Selection and Maternal Effects in Growth
of Males and Females
Parents can significantly influence variation in SSD of their offspring by
modifying the environment that they provide during ontogeny of male and
female offspring and by the restrictions imposed on SSD at birth by maternal
size.
Parents commonly optimize their investment in sons and daughters by
capitalizing on the different environmental sensitivity of the sexes during
growth (Stamps 1990). Subsequently, population differences in SSD are often
attributed to population differences in sex-biased maternal effects (Table 1).
For example, preferential treatment of boys and girls varies among human
cultures and is thought to account for the population variation in SSD
(Holden and Mace 1999; Oyhenart et al. 2000). In turn, sex-specific maternal
effects can be a direct consequence of maternal condition and social rank. For
example, in many primates, growth rate and growth duration of sons and
daughters depend on age, condition, and dominance rank of the mother;
heavier and more dominant mothers produce larger sons (Setchell et al.
2001). Similarly, mothers in better condition produced structurally larger
sons in a gull, and when the maternal condition deteriorated, mothers
produced mostly females that are less sensitive to environmental variation
(Nager et al. 1999). Thus, population variation in condition and the age of
breeding females is a powerful determinant of variation in SSD.
Maternal size has strong effects on the evolution of SSD by physically
restricting the size of the neonate of the larger sex and consequently SSD at
prenatal and natal stages. For example, highly size assortative matings in
humans are frequently associated with an abnormal pregnancy outcome due
to the limitations of maternal size (Mascie-Taylor and Boldsen 1988).
Similarly, an initial mating preference for structurally larger women in early
Japanese settlers in Hawaii resulted in rapid changes in SSD over several
generations (Bennett and Hulse 1982). An example of sex-biased maternal
allocation in relation to SSD of offspring are found in bird species where
mothers lay larger eggs for the smaller sex. In the American kestrel (Falco
sparverius) (Anderson et al. 1997) and spotless starlings (Cordero et al.
2001), mothers produced larger eggs for the structurally smaller sex,
apparently to mitigate the effects of within-brood competition (Table 1).
The SSD at birth and during early growth is strongly limited by the
mother’s body size and by the costs of lactation and provisioning. Even in
species where adult males are up to four times larger than females (e.g.,
26
A. V. Badyaev
mandrills, males weigh 31 kg, females 9 kg; California sea lions [Zalophus
californianus], males 270 kg, females 90 kg; elephant seals [Mirounga
angustirostris], males 3600 kg, females 900 kg) male and female newborns
are identical in size at birth. Similarly, offspring SSD during the offspring
provisioning and lactation period is low as mothers do not preferentially
provision males and females even in the most size-dimorphic species
(Teather and Weatherhead 1988; Wilkinson and van Aarde 2001). The
consequence of these limitations on the larger sex is an increased rate and
duration of growth and the evolution of adaptations that allow greater
sensitivity to (and capitalization on) environmental variation during growth.
For example, in highly sexually dimorphic seals the maternal expenditure
during lactation is equal between the sexes because of a lower metabolic rate
of sons compared to smaller, but more active, daughters (Ono and Boness
1996; Guinet et al. 1999).
Environmental Variation in Growth of Males and Females
The sexes differ in their sensitivity to environmental conditions during
growth, and in many species this is the main cause of population differences
in SSD (Table 1). In birds and mammals, a male’s growth seems to be more
affected by nutritional and environmental stress (Lucas et al. 1996; Sheldon
et al. 1998; Varma and Meguid 2001), and male growth and adult size are
strongly affected by biased parental care during growth. For example, in
humans, preferential treatment of sons often accounts for the most variation
in SSD among populations (Table 1).
Consistent patterns of environmental variation during growth, such as
seasonal changes in food supply or parasite infestation, climatic trends, or
population management practices, lead to temporal variation in SSD in many
mammalian species (Table 1). In altricial birds, the environment during
growth is influenced by competition for food within a brood. The larger sex
may have a greater competitive ability, and studies have found that sexual
dimorphism in growth and size is exaggerated by higher within brood
competition (Oddie 2000).
CONCLUSIONS
There is a remarkable gap between the wealth of knowledge about the
neuroendocrinological controls of growth in males and females and the
poorly understood genetic basis and evolutionary significance of these
mechanisms. Driven by the contrast between the frequently documented
adaptive evolution of SSD and low predictive power of the existing
quantitative genetics models for SSD evolution, new studies are focusing on
understanding the sex-specific expression of gene action, specifically on the
evolution of sex-specific modifiers of the alleles shared by developmental
Ontogeny of Sexual Dimorphism
27
programs of both sexes. What is currently missing and needed is the
integration of the existing knowledge of patterns of sex-specific selection on
ontogeny, sex-specific aspects of development, and the theory of evolution of
sex-limitation. Recent advances in the understanding of the molecular
mechanisms behind the sex-specific expression of morphological traits and
the molecular basis of sex-specific modifiers will significantly further our
understanding of the evolution of SSD. Crucial to these advances is a
thorough understanding of the environmental and genetic interactions during
the ontogeny of sexual size dimorphism.
REFERENCES
Agrawal, A. K., and B. H. Shapiro. 2001. Intrinsic signals in the sexually dimorphic circulating
growth hormone profiles of the rat. Mol. Cell. Endocrinol. 173:167181.
Anderson, D. J., J. Reeve, and D. M. Bird. 1997. Sexually dimorphic eggs, nestling growth and
sibling competition in American kestrels Falco sparverius. Functional Ecol. 11:331335.
Badyaev, A. V., G. E. Hill, M. L. Beck, A. A. Dervan, R. A. Duckworth, K. J. McGraw, P. M.
Nolan, and L. A. Whittingham. 2002. Sex-biased hatching order and adaptive population
divergence in a passerine bird. Science 295:316318.
Badyaev, A. V., G. E. Hill, A. M. Stoehr, P. M. Nolan, and K. J. McGraw. 2000. The evolution of
sexual dimorphism in the house finch: II. Population divergence in relation to local selection.
Evolution 54:21342144.
Badyaev, A. V., G. E. Hill, and L. A. Whittingham. 2001. The evolution of sexual size
dimorphism in the house finch: IV. Population divergence in ontogeny of dimorphism.
Evolution 55:25342549.
Badyaev, A. V., and T. E. Martin. 2000. Sexual dimorphism in relation to current selection in the
house finch. Evolution 54:987997.
Badyaev, A. V., L. A. Whittingham, and G. E. Hill. 2001. The evolution of sexual size
dimorphism in the house finch: III. Developmental basis. Evolution 55:176189.
Bennett, K. A., and F. S. Hulse. 1982. Shifting patterns of sex dimorphism in three Japanese
populations. Ann. of Hum. Biol. 9:441452.
Bielicki, T., and J. Charzewski. 1977. Sex differences in the magnitude of statural gains of
offspring over parents. Hum. Biol. 49:265277.
Bihan-Duval, E. L., S. Mignon-Grasteau, N. Millet, and C. Beaumont. 1998. Genetic analysis of a
selection experiment on increased body weight and breast muscle weight as well as on limited
abdominal fat weight. Br. Poult. Sci. 39:698703.
Borski, R. J., W. Tsai, R. Demott-Friberg, and A. L. Barkan. 2000. Induction of growth hormone
(GH) mRNA by pulsatile GH-releasing hormone in rats is pattern specific. Am. J. Physiol.
Endocrinol. Metab. 278:E885E891.
Brandstetter, A. M., M. W. Pfaffl, J. F. Hocquette, D. E. Gerrard, B. Picard, Y. Geay, and H.
Sauerwein. 2000. Effects of muscle type, castration, age, and compensatory growth rate on
androgen receptor mRNA expression in bovine skeletal muscle. J. Anim. Sci. 78:629637.
Brooks, M. J. 1991. The ontogeny of sexual dimorphism: Quantitative models and a case study in
labrisomid blennies. Syst. Zool. 40:271283.
Butler, M. A., and T. W. Schoener. 2000. The relationship between sexual size dimorphism and
habitat use in greater antillean Anolis lizards. Evolution 54:259272.
Capel, N. 2000. The battle of the sexes. Mech. Dev. 92:89103.
28
A. V. Badyaev
Charmandari, E., S. M. Pincus, D. R. Matthews, E. Dennison, C. H. D. Fall, and P. C. Hindmarsh.
2001. Joint growth hormone and cortisol spontaneous secretion is more asynchronous in older
females than in their male counterparts. J. Clin. Endocrinol. Metab. 86:33933399.
Cheverud, J. M., M. M. Dow, and W. Leutenegger. 1985. The quantitative assessment of phylogenetic constraints in comparative analyses: Sexual dimorphism in body weight among
primates. Evolution 39:13351351.
Cheverud, J. M., P. Wilson, and W. P. J. Dittus. 1992. Primate population studies at Polonnaruwa
III. Somatometric growth in a natural population of toque macaques Macaca sinica. J. Hum.
Evol. 23:5177.
Chowen, J. A., S. Gonzalez-Parra, L. M. Garcia-Segura, and J. Argente. 1998. Sexually
dimorphic interaction of insulin-like growth factor (IGF)-I and sex steroids in lactotrophs.
J. Neuroendocrinol. 10:493502.
Comuzzie, A. G., J. Blangero, M. C. Mahaney, B. D. Mitchell, M. P. Stern, and J. W. Maccluer.
1993. Quantitative genetics of sexual dimorphism in body fat measures. Am. J. Hum. Biol.
5:725734.
Cooch, E. G., D. B. Lank, and F. Cooke. 1996. Intraseasonal variation in the development of
sexual size dimorphism in a precocial bird: Evidence from the lesser show goose. J. Anim.
Ecol. 65:439450.
Cordero, P. J., J. Vinuela, J. M. Aparicio, and J. P. Veiga. 2001. Seasonal variation in sex ratio
and sexual egg dimorphism favouring daughters in first clutches of the spotless starling.
J. Evol. Biol. 14:829834.
Crews, D., M. A. Diamond, J. Whittier, and R. Mason. 1985. Small body size in garter snakes
depends on testes. Am. J. Physiol. 249:6266.
Crowley, P. H. 2000. Sexual dimorphism with female demographic dominance: Age, size and sex
ratio at maturation. Evolution 81:25922605.
Darwin, C. 1871. The Descent of Man and Selection in Relation to Sex. London: John Murray.
De Lama, M. A. R., A. Perez-Romero, J. A. F. Tresguerres, M. Hermanussen, and
C. Ariznavarreta. 2000. Recombinant human growth hormone enhances tibial growth in
peripubertal female rats but not in males. Eur. J. Endocrinol. 142:517523.
Dunnington, E. A., and P. B. Siegel. 1996. Long-term divergent selection for eight-week body
weight in white plymouth rock chickens. Poul. Sci. 75:11681179.
Dunshea, F. R. 2001. Sexual dimorphism in growth of sucking and growing pigs. AsianAustralasian J. Anim. Sci. 14:16101615.
Fairbairn, D. J. 1997. Allometry for sexual size dimorphism: Pattern and process in the coevolution of body size in males and females. Ann. Rev. Ecol. Systematics 28:659687.
Ferguson, S. H., A. R. Bisset, and F. Messier. 2000. The influences of density on growth and
reproduction in moose Alces alces. Wild. Biol. 6:3139.
Gatford, K. L., A. R. Egan, I. J. Clarke, and P. C. Owens. 1998. Sexual dimorphism of the
somatotrophic axis. J. Endocrinol. 157:373389.
Gatford, K. L., T. P. Fletcher, I. J. Clarke, P. C. Owens, K. J. Quinn, P. E. Walton, P. A. Grant, B.
J. Hosking, A. R. Egan, and E. N. Ponnampalam. 1996. Sexual dimorphism of circulating
somatotropin, insulin-like growth factor I and II, insulin-like growth factor binding proteins,
and insulin: Relationships to growth rate and carcass characteristics in growing lambs.
J. Anim. Sci. 74:13141325.
Gebhardt, H. S. G. 1992. Heritability of growth curve parameters and heritability of final size:
A simulation study. Growth Dev. Aging 56:2333.
Gebhardt-Henrich, S. G., and H. L. Marks. 1993. Heritabilities of growth curve parameters and
age-specific expression of genetic variation under two different feeding regimes in Japanese
quail (Coturnix coturnix japonica). Genet. Res. 62:4555.
Ontogeny of Sexual Dimorphism
29
German, R. Z., D. W. Hertweck, J. E. Sitianni, and D. R. Swindler. 1994. Heterochrony and
sexual dimorphism in the pigtailed macaque (Macaca nemestrina). Am. J. Phys. Anthropol.
93:373380.
Griffith, H. 1991. Heterochrony and evolution of sexual dimorphism in the fasciatus group of
scincid genus Eumeces. J. Herpetol. 25:2430.
Guégan, J.-F., A. T. Teriokhin, and F. Thomas. 2000. Human fertility variation, size-related
obstetrical performance and the evolution of sexual statute dimorphism. Proc. R. Soc. Biol.
Sci. Lond. Ser. B. 267:25292535.
Guinet, C., S. D. Goldsworthy, and S. Robinson. 1999. Sex differences in mass loss rate and
growth efficiency in Antarctic fur seal (Arctocephalus gazella) pups at Macquarie Island.
Behav. Ecol. Sociobiol. 46:157163.
Hall, R. L. 1978. Sexual dimorphism for size in seven 19th century northwest coast populations.
Hum. Biol. 50:159171.
Handcock, C. E., and G. D. Bradford. 1995. The evaluation of the growth parameters of size
strains of commercial broiler chickens. Br. Poult. Sci. 36:247264.
Hassan, H. A., W. J. Enright, H. A. Tucker, and R. A. Merkel. 2001. Estrogen and androgen elicit
growth hormone release via dissimilar patterns of hypothalamic neuropeptide secretion.
Steroids 66:7180.
Holden, C., and R. Mace. 1999. Sexual dimorphism in stature and women’s work: A phylogenetic cross-cultural analysis. Am. J. Phys. Anthropol. 110:2745.
Humphrey, L. T. 1998. Growth patterns in the modern human skeleton. Am. J. Phys. Anthropol.
105:5772.
Jaffe, C. A., B. Ocampo-Lim, W. S. Guo, K. Krueger, I. Sugahara, R. DeMott-Friberg,
M. Bermann, and A. L. Barkan. 1998. Regulatory mechanisms of growth hormone secretion
are sexually dimorphic. J. Clin. Invest. 102:153164.
Jarman, P. 1983. Mating system and sexual dimorphism in large terrestrial mammalian herbivores. Biol. Rev. 58:485520.
Jones, A. L., D. Degusta, S. P. Turner, C. J. Campbell, and K. Milton. 2000. Craniometric
variation in a population of mantled howler monkeys (Alouatta palliata): Evidence of size
selection in females and growth in dentally mature males. Am. J. Phys. Anthropol.
113:411434.
Kamegai, J., I. Wakabayashi, R. D. Kineman, and L. A. Frohman. 1999. Growth hormonereleasing hormone receptor (GHRH-R) and growth hormone secretagogue receptor (GHS-R)
mRNA levels during postnatal development in male and female rats. J. Neuroendocrinol.
11:299306.
Lammers, A. R., H. A. Dziech, and R. Z. German. 2001. Ontogeny of sexual dimorphism in
Chinchilla lanigera (Rodentia: Chinchillidae). J. Mammal. 82:179189.
Lande, R. 1980. Sexual dimorphism, sexual selection and adaptation in polygenic characters.
Evolution 34:292305.
Lande, R., and S. J. Arnold. 1985. Evolution of mating preference and sexual dimorphism.
J. Theor. Biol. 117:651664.
LaVelle, M. 1995. Natural selection and developmental sexual variation in the human pelvis.
Am. J. Phys. Anthropol. 98:5972.
Leberg, P. L., and M. H. Smith. 1993. Influence of density on growth of white-tailed deer.
J. Mammal. 74:723731.
LeBlanc, M., M. Festa-Bianchet, and J. T. Jorgenson. 2001. Sexual size dimorphism in bighorn
sheep (Ovis canadensis): Effects of population density. Can. J. Zool. 79:16611670.
Leigh, S. R. 1996. Evolution of human growth spurts. Am. J. Phys. Anthropol. 101:
455474.
30
A. V. Badyaev
Leigh, S. R. 1992. Patterns of variation in the ontogeny of primate body size dimorphism.
J. Hum. Evol. 23:2750.
Leigh, S. R. 1995. Socioecology and the ontogeny of sexual size dimorphism in anthropoid
primates. Am. J. Phys. Anthropol. 97:339356.
Leigh, S. R., and B. T. Shea. 1996. Ontogeny of body size variation in African apes. Am. J. Phys.
Anthropol. 99:4365.
Leigh, S. R., and C. J. Terranova. 1998. Comparative perspectives on bimaturism, ontogeny, and
dimorphism in lemurid primates. Int. J. Primatol. 19:723749.
Lesage, L., M. Crete, J. Hout, and J. P. Ouellet. 2001. Evidence for a trade-off between growth
and body reserves in northern white-tailed deer. Oecologia 126:3041.
L’Hospitalier, R., M. Bougon, M. Le Menec, and P. Quemeneur. 1986. Evolution des performances des poules reproductrices de type chair et de leur descendance, de 1962 a 1985. Bull.
Inf. Station Exp. Avicult. Ploufragan 26:318.
Liu, G., E. A. Dunnington, and P. B. Siegel. 1994. Responses to long-term selection for eightweek body weight in chickens. Poult. Sci. 73:16421650.
Liu, J. L., S. Yakar, and D. LeRoith. 2000. Mice deficient in liver production of insulin-like
growth factor I display sexual dimorphism in growth hormone-stimulated postnatal growth.
Endocrinology 141:44364441.
Lopez, M. E., B. M. Hargis, C. E. Dean, and T. E. Porter. 1995. Uneven regional distributions
of prolactin- and growth hormone-secreting cells and sexually dimorphic proportions of
prolactin secretors in the adenohypophysis of adult chickens. Gen. Comp. Endocrinol.
100:246254.
Lucas, A., B. A. Baker, M. Desai, and C. N. Hales. 1996. Nutrition in pregnant or lactating rats
programs lipid metabolism in the offspring. Br. J. Nutr. 76:605612.
Mahoney, S. P., J. A. Virgl, and K. Mawhinney. 2001. Potential mechanisms of phenotypic
divergence in body size between Newfoundland and mainland black bear populations. Can.
J. Zool. 79:16501660.
Mascie-Taylor, C. G. N., and J. L. Boldsen. 1988. Assortative mating, differential fertility and
abnormal pregnancy outcome. Ann. Hum. Biol. 15:223228.
McLain, D. K. 1993. Cope’s rules sexual selection and the loss of ecological plasticity. Oikos
68:490500.
McNamara, K. J. 1995. Sexual dimorphism: The role of heterochrony. In Evolutionary change
and heterochrony, K. J. McNamara, ed. 6589 New York: John Wiley and Sons.
Merilä, J., B. C. Sheldon, and H. Ellegren. 1997. Antagonistic natural selection revealed by
molecular sex identification of nestling collared flycatchers. Mol. Ecol. 6:11671175.
Merilä, J., B. C. Sheldon, and H. Ellegren. 1998. Quantitative genetics of sexual size dimorphism
in the collared flycatcher, Ficedula albicollis. Evolution 52:870876.
Metzger, D. L., J. R. Kerrigan, and A. D. Rogol. 1994. Gonadal steroid hormone regulation of the
somatotropic axis during puberty in humans: Mechanisms of androgen and estrogen action.
Trends Endocrinol. Metabol. 5:290296.
Mignon-Grasteau, S., C. Beaumont, B.-D. E. Le, J. R. Poivey, H. D. Rochambeau, and F. H.
Ricard. 1999. Genetic parameters of growth curve parameters in male and female chickens.
British Poult. Sci. 40:4451.
Mitani, J. C., J. Gros-Louis, and A. F. Richards. 1996. Sexual dimorphism, the operational sex
ratio, and the intensity of male competition in polygynous primates. Am. Nat. 147:966980.
Mittwoch, U. 1993. Blastocysts prepare for the race to be male. Hum. Reprod. 8:15501555.
Nager, R. G., P. Managhan, R. Griffiths, D. C. Houston, and R. Dawson. 1999. Experimental
demonstration that offspring sex ratio varies with maternal condition. Proc. Nat. Acad. Sci.
USA 96:570573.
Ontogeny of Sexual Dimorphism
31
Oddie, K. R. 2000. Size matters: Competition between male and female great tit offspring.
J. Anim. Ecol. 69:903912.
O’Higgins, P., P. Chadfield, and N. Jones. 2001. Facial growth and the ontogeny of morphological
variation within and between the primates Cebus apella and Cercocebus torquatus. J. Zool.
(Lond.) 254:337357.
Ono, K. A., and D. J. Boness. 1996. Sexual dimorphism in sea lion pups: Differential maternal
investment, or sex-specific differences in energy allocation? Behav. Ecol. Sociobiol.
38:3141.
Orrego, J. J., M. Russell-Aulet, R. Demott-Friberg, and A. L. Barkan. 2001. Semiquantification
of hypothalamic GH-releasing hormone output in women: Evidence for sexual dimorphism in
the mechanism of the somatopause. J. Clin. Endocrinol. Metab. 86:54855490.
Oyhenart, E. E., M. C. Mune, and H. M. Pucciarelli. 1998. Influence of intrauterine blood supply
on cranial growth and sexual dimorphism at birth. Growth Dev. Aging 62:187198.
Oyhenart, E. E., M. F. Torres, H. M. Pucciarelli, S. L. Dahinten, and F. R. Carnese. 2000. Growth
and sexual dimorphism in aborigines from Chubut (Argentina) I: Body analysis. Acta Med.
Auxol. 32:105113.
Painson, J. C., J. D. Veldhuis, and G. S. Tannenbaum. 2000. Single exposure to testosterone in
adulthood rapidly induces regularity in the growth hormone release process. Am. J. Physiol.
Endocrinol. Metab. 278:E933E940.
Pericas, J., P. Oliver, R. Guitard, C. Pico, and A. Palou. 2001. Sexual dimorphism in age-related
changes in UCP2 and leptin gene expression in subcutaneous adipose tissue in humans. J.
Nutr. Biochem. 12:444449.
Post, E., R. Langvatn, M. C. Forchhammer, and N. C. Stenseth. 1999. Environmental variation
shapes sexual dimorphism in red deer. Proc. Nat. Acad. Sci. USA 96:44674471.
Potau, N., L. Ibanez, M. Sentis, and A. Carrascosa. 1999. Sexual dimorphism in the maturation
of the pituitarygonadal axis, assessed by GnRH agonist challenge. Eur. J. Endocrinol.
141:2734.
Potti, J. 1999. Environmental factors and sexual differences in mass and condition of nestling
pied flycatchers Ficedula hypoleuca. Ecoscience 6:1924.
Powell, R. A., and C. M. King. 1997. Variation in body size, sexual dimorphism and age-specific
survival in stoats, Mustela erminea (Mammalia: Carnivora), with fluctuating food supplies.
Biol. J. Linnean Soc. 62:165194.
Preziosi, R. F., and D. J. Fairbairn. 1996. Sexual size dimorphism and selection in the wild in the
waterstrider Aquarius remigis: Body size, components of body size and male mating success.
J. Evolution. Biol. 9:317336.
Price, T. 1984. Sexual selection in body size, territory and plumage variables in a population of
Darwin’s finches. Evolution 38:327341.
Ralls, K. 1977. Sexual dimorphism in mammals: Avian models and unanswered questions. Am.
Nat. 111:917938.
Ravosa, M. J., D. M. Meyers, and K. E. Glander. 1993. Relative growth of the limbs and trunk in
sifakas; heterochronic, ecological and functional considerations. Am. J. Phys. Anthropol.
92:499520.
Ray, P. F., J. Conaghan, R. M. L. Winston, and A. H. Handyside. 1995. Increased number of cells
and metabolic activity in male human preimplantation embryos following in vitro fertilization. J. Reprod. Fertil. 104:165171.
Réale, D., and P. Bousses. 1999. Effects of summer and winter birth on growth of lambs in a
population of feral sheep. J. Mammal. 80:10281037.
Reeve, J. P., and D. J. Fairbairn. 2001. Predicting the evolution of sexual size dimorphism. J.
Evolution. Biol. 14:244254.
32
A. V. Badyaev
Reeve, J. P., and D. J. Fairbairn. 1996. Sexual size dimorphism as a correlated response to
selection on body size: An empirical test of the quantitative genetic model. Evolution
50:19271938.
Reinhold, K. 1999. Evolutionary genetics of sex-limited traits under fluctuating selection.
J. Evolution. Biol. 12:897902.
Rhen, T. 2000. Sex-limited mutations and the evolution of sexual dimorphism. Evolution
54:3743.
Rice, W. R., and A. K. Chippindale. 2001. Intersexual ontogenetic conflict. J. Evol. Biol.
14:685693.
Rising, J. D. 1987. Geographical variation of sexual dimorphism in size of savannah sparrows
(Passerculus sandwichensis): A test of hypotheses. Evolution 41:514524.
Roff, D. A. 1997. Evolutionary quantitative genetics. Chapman and Hall, New York.
Rogers, A. R., and A. Mukherjee. 1992. Quantitative genetics of sexual dimorphism in human
body size. Evolution 46:226234.
Scholl, T. O., J. I. Hediger, J. I. Schall, C.-S. Khoo, and R. L. Fischer. 1994. Maternal growth
during pregnancy and the competition for nutrients. Am. J. Clin. Nutr. 60:183188.
Setchell, J. M., P. C. Lee, E. J. Wickings, and A. F. Dixson. 2001. Growth and ontogeny of sexual
size dimorphism in the mandrill (Mandrillus sphinx). Am. J. Phys. Anthropol.
115:349360.
Shea, B. T. 1986. Ontogenetic approaches to sexual dimorphism in anthropoids. Hum. Evol.
1:97110.
Shea, B. T. 1985. The ontogeny of sexual dimorphism in the African apes. Am. J. Phys.
Anthropol. 8:183188.
Shea, B. T., and R. C. Bailey. 1996. Allometry and adaptation of body proportions and stature in
African pygmies. Am. J. Phys. Anthropol. 100:311340.
Sheldon, B. C., J. Merila, G. Lindgren, and H. Ellegren. 1998. Gender and environmental sensitivity in nestling collared flycatchers. Ecology 79:19391948.
Shine, R. 1989. Ecological causes for the evolution of sexual dimorphism: A review of the
evidence. Q. Rev. Biol. 64:419461.
Shine, R. 1990. Proximate determinants of sexual differences in adult body size. Am. Nat.
135:278283.
Shine, R., and D. Crews. 1988. Why male garter snakes have small heads: The evolution and
endocrine control of sexual dimorphism. Evolution 42:11051110.
Slatkin, M. 1984. Ecological causes of sexual dimorphism. Evolution 38:622630.
Soderquist, T. R. 1995. Ontogeny of sexual dimorphism in size among polytocous mammals:
Tests of two carnivorous marsupials. J. Mammal. 76:376390.
Stamps, J. A. 1990. When should avian parents differentially provision sons and daughters? Am.
Nat. 135:671685.
Stamps, J. A., and V. V. Krishnan. 1997. Sexual bimaturation and sexual size dimorphism in
animals with asymptotic growth after maturity. Evol. Ecol. 11:2139.
Stini, W. A. 1969. Nutritional stress and growth: Sex difference in adaptive response. Am. J.
Phys. Anthropol. 31:417426.
Swain, A., and R. Lovell-Badge. 1999. Mammalian sex determination: A molecular drama.
Genes Dev. 13:755767.
Taylor, A. B. 1995. Effects of ontogeny and sexual dimorphism on scapula morphology in the
mountain gorilla. Am. J. Phys. Anthropol. 98:431445.
Taylor, A. B. 1997. Relative growth, ontogeny and sexual dimorphism in gorilla (Gorilla gorilla
gorilla, and G.g. beringei): Evolutionary and ecological considerations. Am. J. Phys.
Anthropol. 43:131.
Ontogeny of Sexual Dimorphism
33
Teather, K. J., and P. J. Weatherhead. 1994. Allometry, adaptation, and the growth and development of sexually dimorphic birds. Oikos 71:515525.
Teather, K. L., and P. J. Weatherhead. 1988. Sex-specific energy requirements of great-tailed
grackle (Quiscalus maxicanus) nestlings. J. Anim. Ecol. 57:659668.
Tobias, P. V. 1972. Growth and stature in South African populations. In Human Biology of
Environmental Change, D. Vorster, ed. 96104. London: International Biological Programe.
Toelle, V. D., G. B. Havenstein, K. E. Nestor, and W. L. Bacon. 1990. Estimates of genetic
parameters in turkeys. 3. Sexual dimorphism and its implications in selection procedures.
Poul. Sci. 69:16341643.
Togo, C., J.- M. Gaillard, and J. Michallet. 1999. Cohort effects growth of males but not females
in alpine ibex (Capra ibex ibex). J. Mammal. 80:10211027.
Turner, T. R., F. Anapol, and C. J. Jolly. 1997. Growth, development, and sexual dimorphism in
vervet monkeys (Cercopithecus aethiops) at four sites in Kenya. Am. J. Phys. Anthropol.
103:1935.
Varma, M., and M. M. Meguid. 2001. Perspectives on gender differences in food intake and
frequency of disease. Nutr. Res. 21:395423.
Vasil’eva, E. D. 1997. Size-dependent variability and sexual dimorphism of skull in teleostean
fishes: Determining factors and main trends. Vopr. Ikhtiol. 37:293306.
Velasco, B., L. Cacicedo, E. Melian, G. Fernandez-Vazquez, and F. Sanchez-Franco. 2001.
Sensitivity to exogenous GH and reversibility of the reduced IGF-I gene expression in aging
rats. Eur. J. Endocrinol. 145:7385.
Weatherhead, P. J., H. Greenwood, and R. G. Clark. 1987. Natural and sexual selection on body
size in red-winged blackbirds. Evolution 41:14011403.
Weaver, J. U., N. F. Taylor, J. P. Monson, P. J. Wood, and W. F. Kelly. 1998. Sexual dimorphism
in 11 beta hydroxysteroid dehydrogenase activity and its relation to fat distribution and
insulin sensitivity; a study in hypopituitary subjects. Clinical Endocrinology 49:1320.
Wikelski, M., and F. Trillmich. 1997. Body size and sexual size dimorphism in marine iguanas
fluctuate as a result of opposing natural and sexual selection: An island comparison. Evolution 51:922936.
Wiley, R. H. 1974. Evolution of social organization and life history patterns among grouse. Q.
Rev. Biol. 49:201227.
Wilkinson, I. S., and R. J. van Aarde. 2001. Investment in sons and daughters by southern
elephant seals, Mirounga leonine, at Marion Island. Mar. Mamm. Sci. 17:873887.
Woolbright, L. L. 1989. Sexual dimorphism in Eleutherodactylus coqui: Selection pressures and
growth rates. Herpetologica 45:6874.
Yellayi, S., C. Teuscher, J. A. Woods, T. H. Welsh, K. S. K. Tung, M. Nakai, C. S. Rosenfeld, D.
B. Lubahn, and P. S. Cooke. 2000. Normal development of thymus in male and female mice
requires estrogen=estrogen receptor-alpha signaling pathway. Endocrine 12:207213.
Zarkower, D. 2001. Establishing sexual dimorphism: Conservation amidst diversity? Nature
Rev. Genet. 2:175185.
Zhang, W. H., A. Beaudet, and G. S. Tannenbaum. 1999. Sexually dimorphic expression of sst1
and sst2 somatostatin receptor subtypes in the arcuate nucleus and anterior pituitary of adult
rats. J. Neuroendocrinol. 11:129136.