Testosterone has opposite effects on male growth in lizards (Sceloporus spp.) with opposite patterns of sexual size dimorphism
1 Graduate Program in Ecology and Evolution
2 Department of Animal Sciences, Rutgers University, New Brunswick, NJ
08901, USA
* Author for correspondence at present address: The Ohio State University, Department of Evolution, Ecology and Organismal Biology, Columbus, OH 43210, USA (e-mail: cox.541{at}osu.edu)
Accepted 20 October 2005
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Summary |
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Key words: body size, growth, hormone manipulation, proximate mechanism, reproductive investment, sexual size dimorphism, Sceloporus jarrovii, Sceloporus virgatus, testosterone
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Introduction |
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Life history ecologists have long recognized that growth may be constrained
by the preferential allocation of available energy to reproduction
(Fisher, 1930;
Reznick, 1985
;
Williams, 1966
). More
recently, behavioral endocrinologists have begun to explore the role of
hormones as proximate mediators of such trade-offs
(Ketterson et al., 1992
;
Ricklefs and Wikelski, 2002
).
For example, in male lizards, T increases activity, endurance, locomotor
performance, territorial aggression and home range size
(Cox et al., 2005
;
DeNardo and Sinervo, 1994
;
John-Alder et al., 1996
;
Klukowski et al., 1998
,
2004
;
Marler and Moore, 1988
;
Moore, 1988
;
Moore and Marler, 1987
). These
behavioral and physiological effects of T presumably enhance male reproductive
success, but they also incur costs in the form of decreased energy
acquisition, increased energy expenditure and increased parasitism
(Cox et al., 2005
;
Klukowski et al., 2001
; Marler
and Moore, 1989
,
1991
;
Marler et al., 1995
;
Olsson et al., 2000
;
Salvador et al., 1996
;
Uller and Olsson, 2003
). These
associated costs may explain why T often inhibits growth in lizards
(Abell, 1998a
;
Cox et al., 2005
;
Hews et al., 1994
;
Hews and Moore, 1995
;
Salvador and Veiga, 2000
).
However, the implications of such trade-offs with regard to SSD remain largely
unexplored.
In a previous study (Cox et al.,
2005), we showed that T inhibits growth while increasing daily
activity, movement and home-range size in males of Sceloporus
undulatus, a lizard with female-larger SSD. We interpreted these results
as evidence for a T-mediated energy allocation trade-off between male growth
and reproductive investment, and proposed this energetic growth constraint as
an explanation for SSD in this species. In the present study, we show that T
also inhibits male growth in S. virgatus, a closely related species
in which female-larger SSD develops because yearling females grow more quickly
than males during the mating season. In contrast, we show that T promotes male
growth in S. jarrovii, a sympatric congener in which male-larger SSD
develops because yearling males grow more quickly than females. Our results
provide the first direct evidence for opposite effects of T on male growth in
closely related species with opposite patterns of SSD. Further, our study is
the first to demonstrate a stimulatory effect of T on skeletal growth in any
squamate reptile. Despite this potential for growth promotion by T in
Sceloporus, we speculate that energetic costs of elevated T may
indirectly constrain male growth in S. virgatus. These T-mediated
costs of male reproductive investment may help explain the evolution of
female-larger SSD in Sceloporus.
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Materials and methods |
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We studied both S. virgatus and S. jarrovii along a
single 2 km section of streambed in Cave Creek Canyon (North Fork), located
13 km northwest of the American Museum of Natural History's
Southwestern Research Station in the Coronado National Forest, Cochise Co.,
Arizona, USA (31°5354'N, 109°13'W, elevation
16601760 m). We obtained collecting permits from the Arizona Game and
Fish Department (SP 696192, 751920 and 553889) and land use permits from the
United States Forest Service. The Rutgers University Animal Care and
Facilities Committee approved our procedures (protocol 01-019). Over three
consecutive years (20022004), we used standard mark-recapture
techniques to describe the ontogeny of sex differences in growth rate and body
size. These data, which are reported elsewhere
(Cox, 2005; R. M. Cox and H.
B. John-Alder, manuscript submitted), are summarized here because they provide
a detailed natural history framework for the design and interpretation of this
study.
In both S. virgatus and S. jarrovii, SSD is slight over
the first few months of life, but develops rapidly thereafter, reaching a
magnitude of about 10% within a year of birth. In both species, this rapid
development of SSD begins after only 23 months of postnatal activity
and growth (excluding ca. 4 months winter dormancy in S. virgatus),
roughly coincident with the onset of their respective mating seasons. On our
study plot, most males and some females of each species attain sexual maturity
as yearlings (Ballinger, 1973,
1979
;
Ballinger and Ketels, 1983
;
Smith et al., 1995
). However,
while yearling males of S. virgatus grow only half as fast as females
during their spring mating season, yearling males of S. jarrovii grow
more quickly than females during their fall mating season
(Cox, 2005
; R. M. Cox and H.
B. John-Alder, manuscript submitted). These observations raise a question of
central importance with regard to the proximate causation of SSD: during their
respective mating seasons, why do yearling males of S. virgatus grow
more slowly than females, yet yearling males of S. jarrovii grow more
quickly than females? We hypothesized that elevated T inhibits growth in
yearling males of S. virgatus, but promotes growth in yearling males
of S. jarrovii. Thus, we predicted that castration would promote and
exogenous T would inhibit male growth in S. virgatus, while
predicting opposite growth effects of castration and T replacement in S.
jarrovii.
Experimental design
We collected yearling males by hand-held noose in late April (S.
virgatus, N=71) and late August (S. jarrovii, N=67) of 2004,
near the onset of the mating season for each species. We measured SVL
to the nearest 1 mm with a ruler, body mass to the nearest 0.1 g with a
Pesola® spring scale (Pesola AG, Baar, Switzerland), and gave
each animal a unique toe clip for permanent identification. We then assigned
males to one of three size-matched treatment groups: castrated males receiving
a placebo implant (CAST), castrated males receiving a T implant (TEST), and
intact control males receiving a placebo implant (CON). Following surgical
treatments (see below), we released animals at their location of capture and
left them undisturbed until recapture in June (S. virgatus) or
October (S. jarrovii). Upon recapture, we recorded SVL and
mass for each experimental animal and calculated individual growth rates (mm
day1) by assuming linear growth and dividing change in
SVL by elapsed time.
Testosterone implants
We constructed tonic-release T implants from 5 mm lengths of
Silastic® tubing (Dow Corning, Midland, MI, USA;
0.058''i.d., 0.077''o.d.). After sealing one end of
each tubule with silicone adhesive gel (Dow Corning), we used a
Hamilton® syringe to inject 3 µl of a solution of T (T-1500,
Sigma-Aldrich Inc., St Louis, MO, USA) dissolved in dimethyl sulfoxide (DMSO;
100 µg T µl1 DMSO) into the open end of each implant.
We then sealed each tubule with silicone adhesive and waited several days for
the DMSO to evaporate and diffuse through the tubing, leaving 300 µg of
crystalline T within the lumen (ca. 1.5 mm length) of each implant. We
constructed placebo implants in identical fashion, but injected them with pure
DMSO, which left an empty tubule after evaporation and diffusion.
Surgical treatments
We anaesthetized animals with an intramuscular injection of ketamine (Vetus
Animal Health, MFA Inc., Columbia, MO, USA; 130 mg kg1 body
mass). We then exposed the testes with a single ventral incision and
bilaterally castrated (orchiectomized) CAST and TEST males by ligating each
spermatic cord with surgical silk, ablating each testis, and cauterizing each
ligated spermatic cord after removal of the testes. For CON males, we
performed `sham' surgeries in which we made identical incisions to expose and
manipulate the testes while leaving them intact. We then inserted either a T
implant (TEST) or a placebo implant (CAST and CON) into the coelomic cavity
and closed the incision with Nexaband® surgical glue
(Veterinary Products Laboratories, Phoenix, AZ, USA). We performed surgeries
within 2 days of capture, and released animals at their site of capture within
3 days of surgery. All animals appeared healthy and vigorous upon release, and
survival from surgery to release was high for both Sceloporus
virgatus (68 of 71, 96% survival) and S. jarrovii (65 of 67,
97%).
Plasma testosterone levels
To document natural seasonal and sexual variation in circulating T levels,
we periodically collected blood samples from unmanipulated yearling males and
females captured on or adjacent to our experimental plot. For each species, we
sampled 1015 individuals of each sex at approximately monthly intervals
spanning the entire first year of life (excluding winter). Animals were
permanently marked so that no individual lizard was bled more than once. To
validate the efficacy of our T manipulations, we obtained blood samples from
experimental males upon recapture. Hereafter, we distinguish between `natural'
vs `experimental' animals when discussing plasma T levels.
We collected blood samples from the postorbital sinus within 2 min of
capture using heparinized microhematocrit capillary tubes (Fisher Scientific,
Pittsburgh, PA, USA). We held samples on ice until they could be centrifuged
(within 6 h of collection), and stored the separated plasma at 20°C
until subsequent assays. We performed radioimmunoassays (RIAs) for plasma T
concentration following methods reported elsewhere
(Cox et al., 2005;
Smith and John-Alder, 1999
).
Samples were extracted twice in diethyl ether (mean 81% extraction
efficiency), dried under a stream of ultra-filtered air, and reconstituted in
phosphate buffered saline with gelatin (PBSG). Reconstituted samples were
assayed with 3H-T as a radiolabel (PerkinElmer Life Sciences Inc.,
Boston, MA, USA) and T antiserum (1:18000 initial dilution) developed in
rabbits by A. L. Johnson (The University of Notre Dame, IN, USA). We did not
separate T from other androgens prior to RIA, so our `plasma testosterone'
values should be interpreted with the caveat that they reflect any additional
binding of the T antibody to 5
-dihydrotestosterone (DHT, 50%
cross-reactivity). However, plasma DHT levels are typically only 24% of
plasma T levels in these species (Abell,
1998c
; Woodley and Moore,
1999
), so our values primarily reflect plasma T. Within each
species, we randomized samples across assays to avoid confounding sex or
sampling date with any inherent interassay variation (typically 6%;
Smith and John-Alder, 1999
).
Limits of detection were 15 pg T per assay tube.
Statistical analyses
We compared seasonal and sex differences in natural plasma T using analysis
of variance (ANOVA) with sex and sampling month as class effects with
interaction. Within each sex, we tested for seasonal patterns in natural
plasma T levels using ANOVA with sampling month as the main effect, and
determined post hoc differences among months using the
RyanEinotGabrielWelsch test (REGWQ; SAS Institute 1989).
Within males sampled during the breeding season, we assessed the allometry of
plasma T levels using analysis of covariance (ANCOVA) with sampling month as a
class effect and SVL as a covariate (i.e. based on covariance with
SVL after accounting for variance due to sampling month). We used
log10-transformed plasma T levels and SVL values for these
analyses and verified homogeneity of allometric slopes among months before
employing ANCOVA.
For experimental males, we compared plasma T levels using ANOVA with treatment as the main effect and determined post hoc separation among treatments using the REGWQ test. Growth typically decreases with size, so we compared growth rate among treatment groups using ANCOVA with treatment as the main effect and initial SVL as a covariate. We tested for homogeneity of slopes among treatment groups with a treatment-by-SVL interaction term, which we retained in our final model when significant (separate slopes model, S. virgatus), and omitted when non-significant (ANCOVA, S. jarrovii). We determined post hoc separation by comparing least-square mean growth rate based on these models. To facilitate direct inferences regarding the effect of exogenous T on growth in each species, we performed additional ANCOVA analyses excluding CON males. This allowed us to directly compare castrated males that differed in discrete fashion with regard to the presence (TEST) or virtual absence (CAST) of circulating T. All statistical analyses were conducted using SAS (version 8.2, SAS Institute, Inc.).
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Results |
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Plasma testosterone levels
Across all sampling points, mean plasma T concentration was higher in
natural yearling males than in females for both S. virgatus
(F12,141=32.91; P<0.001;
Fig. 1A) and S.
jarrovii (F12,198=100.25; P<0.001;
Fig. 1B). Female plasma T
concentration was uniformly low across sampling points for both S.
virgatus (F5,60=1,56; P=0.186;
Fig. 1A) and S.
jarrovii (F5,91=1.24; P=0.297;
Fig. 1B). However, we observed
striking seasonal differences in mean plasma T concentration within yearling
males of S. virgatus (F5,74=2.67;
P=0.028) and S. jarrovii (F6,100=17.08;
P<0.001), with peak levels attained during the mating season in
both species (Fig. 1). After
controlling for variance attributable to sampling month within the mating
season, we observed a positive relationship between plasma T concentration and
SVL (both variables log10-transformed) in yearling males
of both species (Fig. 2). While
this allometry is robust in S. virgatus
(F1,48=35.87; P<0.001), it is weak and driven
primarily by several small males in S. jarrovii
(F1,40=6.71; P=0.012). Thus, even during the
mating season, many small males of S. virgatus exhibited low plasma T
levels similar to yearling females (Fig.
2A). In contrast, only a few of the smallest males of S.
jarrovii exhibited such low plasma T levels during the mating season
(Fig. 2B).
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Growth rate
Growth rate (mm day1) decreased with body size across
experimental S. virgatus treatment groups, but the slope of this
relationship was particularly steep for CON
(Fig. 3A), yielding a
significant SVL-by-treatment interaction
(F2,39=8.72; P<0.001). Our separate slopes
regression model retaining this interaction term revealed significant effects
of both treatment (F2,39=9.36; P<0.002) and
initial SVL (F1,39=30.59; P<0.001) on
growth rate. Overall, least-square mean growth rate was significantly lower in
TEST than in CAST and CON. However, the heterogeneity of slopes among
treatment groups renders this comparison strongly size-dependent. Small
yearling CON tended to grow at high rates comparable to CAST, while large
yearling CON tended to grow at low rates characteristic of TEST
(Fig. 3A). These growth
patterns are intriguing in light of our plasma T data: CAST and small CON had
low plasma T concentrations and high growth rates, while TEST and large CON
had high plasma T concentrations and low growth rates. Although our
comparisons involving all three groups were confounded by allometry in plasma
T levels and growth rates within CON, our direct ANCOVA comparison of CAST
vs TEST unequivocally demonstrated that exogenous T inhibits growth
in castrated males of S. virgatus (F1,23=27.67;
P<0.001).
|
In S. jarrovii, growth rate of experimental males decreased with SVL (F1,34=5.14; P=0.031), and the slope of this relationship was similar across treatment groups (F2,34=1.24; P=0.304). ANCOVA revealed a strong effect of treatment on growth rate (F2,34=18.08; P<0.001), such that least-square mean growth rate was lower in CAST than in CON or TEST (Fig. 3B). Our ANCOVA comparison of CAST vs TEST reinforced the conclusion that exogenous T promotes growth in castrated males of S. jarrovii (F1,24=27.47; P<0.001), directly opposite our findings for S. virgatus. Treatment effects on mass gain (data not shown) were nearly identical to those that we observed for growth rate in SVL.
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Discussion |
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During the mating season, many small yearling males of S. virgatus
had low plasma T levels similar to females, but only a few of the smallest
males of S. jarrovii had such low plasma T levels
(Fig. 2). This may reflect
size-dependent variation in the attainment of physiological maturity among
yearling males of S. virgatus
(Ballinger and Ketels, 1983).
Despite this difference, yearling males of both species exhibited a seasonal
peak in plasma T during the mating season, and sex differences in plasma T
levels were maximal at this time. These similarities between species stand in
contrast to the observation that yearling males of S. jarrovii grow
more quickly than females during the mating season, whereas yearling males of
S. virgatus grow more slowly than females during the mating season
(Cox, 2005
; R. M. Cox and H.
B. John-Alder, manuscript submitted). Our experimental data are consistent
with the interpretation that these opposite growth patterns between species
reflect underlying differences in the effect of T on male growth
(Fig. 3).
Our results provide the first direct evidence for opposite effects of T on
male growth in two closely related species with opposite patterns of SSD. Even
within entire vertebrate classes, opposite effects of androgens on growth are
virtually unknown, regardless of patterns in SSD. In the only other comparable
study, Fennell and Scanes
(1992a,b
)
found that androgens inhibit growth in male-larger domesticated chickens but
promote growth in male-larger domesticated turkeys. Among mammals, androgens
stimulate the somatotrophic axis and promote growth in numerous male-larger
primates, ruminants and rodents (Borski et
al., 1996
; Ford and Klindt,
1989
; Gatford et al.,
1998
; Wehrenberg and Giustina,
1992
). Similar studies of female-larger mammals are generally
lacking, although castration promotes male growth in the female-larger golden
hamster (Swanson, 1967
).
Androgens stimulate the somatotrophic axis and promote growth in several
male-larger fishes (Holloway and
Leatherland, 1998
; Huggard et
al., 1996
; Kuwaye et al.,
1993
; Larsen et al.,
2004
), but we are not aware of any analogous studies of
female-larger species. Castration has no effect on male growth in the only
amphibian studied to date, the bullfrog Rana catesbeiana
(Hayes and Licht, 1992
).
However, the direction of SSD varies in this species and is probably the
result of sex differences in survival to large size, rather than sex
differences in age-specific growth rate
(Howard, 1981
). Unfortunately,
the ecological and evolutionary relevance of many of the above studies is
uncertain, since most were conducted in artificial laboratory or feedlot
environments on laboratory strains or domesticated varieties produced by
artificial selection (often for desired growth and body composition
phenotypes).
Our results for S. jarrovii provide the first unambiguous
experimental evidence for promotion of skeletal growth (i.e. elongation) by T
in any squamate reptile. Although prenatal exposure to T stimulates postnatal
mass gain in the lizard Lacerta vivipara
(Uller and Olsson, 2003),
every other study involving lizards and snakes has found either no effect or
an inhibitory effect of T on skeletal growth or mass gain
(Abell, 1998a
;
Cox et al., 2005
;
Crews et al., 1985
;
Hews et al., 1994
;
Hews and Moore, 1995
;
Klukowski et al., 1998
;
Lerner and Mason, 2001
; Marler
and Moore, 1989
,
1991
;
Salvador and Veiga, 2000
).
While these studies collectively suggest that growth inhibition by T may be
prevalent in this group, several caveats beg mention. First, several of the
above studies reported severe mass loss and/or reduced survival among
T-implanted animals (Abell,
1998a
; Hews et al.,
1994
; Hews and Moore,
1995
; Lerner and Mason,
2001
), prompting some authors to acknowledge concerns over
pharmacological T levels (Hews et al.,
1994
, pp. 110112; Hews
and Moore, 1995
, p. 99; Lerner
and Mason, 2001
, p.223). Our experiments did not have this
problem, since our induced plasma T levels were well within normal
physiological limits (Fig. 1)
and our measures of recapture success (an index of survival) were similar for
CON and TEST groups. Second, many of these previous studies were conducted in
captivity (Abell, 1998a
;
Crews et al., 1985
;
Hews et al., 1994
;
Hews and Moore, 1995
;
Lerner and Mason, 2001
). In
our own experience, laboratory conditions can ameliorate sexual growth
differences in both S. undulatus
(Haenel and John-Alder, 2002
)
and S. jarrovii, and we have repeatedly failed to detect any
difference in growth among CAST, CON, and TEST males of S. jarrovii
in captivity (R. M. Cox, M. M. Barrett, K. L. Facente, V. Zilberman, and H. B.
John-Alder, unpublished observations). Thus, while T may stimulate growth
under natural conditions, other factors (e.g., ad libitum food) are
presumably sufficient to promote rapid growth in the absence of T. Finally,
treatment with exogenous T alone may be misleading in the absence of a
complementary manipulation to remove the source of endogenous hormone. For
example, neither our study nor a previous experiment
(Marler and Moore, 1989
) found
a difference in skeletal growth between T-implanted and control males of
S. jarrovii. However, our inclusion of a CAST treatment enabled us to
demonstrate that T promotes growth in yearling males of this species. This
discrepancy may also reflect the fact that Marler and Moore
(1989
) manipulated T levels in
older males, in which growth is slow and sex differences in growth are
minor.
Our results clearly show that T inhibits growth in S. virgatus and
promotes growth in S. jarrovii, but we cannot definitively say how or
why T elicits these opposite growth responses. One possibility is that both
growth inhibition and growth promotion by T represent proximate mechanistic
targets of selection for adaptive male body size. For example, intrasexual
selection should favor large male body size in S. jarrovii because
larger males win agonistic encounters and have greater reproductive success
than small males (Ruby, 1978,
1981
;
Ruby and Baird, 1993
). On a
proximate level, this may result in the evolutionary coupling of a
male-specific mediator such as T to some existing physiological mechanism(s)
for growth promotion (Badyaev,
2002
). For example, in many mammals and fishes with male-larger
SSD, androgens promote growth by stimulating the transcription, synthesis and
secretion of mitogens such as growth hormone (GH) and insulin-like growth
factor-I (IGF-I; e.g. Borski et al.,
1996
; Holloway and
Leatherland, 1998
; Larsen et
al., 2004
; Riley et al.,
2002
; Wehrenberg and Giustina,
1992
). By analogy, the evolution of growth inhibition by T may
reflect intrasexual selection for small male size, resulting in inhibitory
effects of T on these components of the endocrine growth axis. However, males
of S. virgatus also exhibit intense intrasexual aggression in
competition for breeding females (Smith,
1985
; Vinegar,
1975a
), and mating success is greater in large than small males
(Abell, 1997
,
1998b
). This mating advantage
of large size is particularly strong within yearling males (Abell,
1997
,
1998b
), for which we have shown
that T inhibits growth. Thus, it seems unlikely that intrasexual selection for
small male size has driven the evolution of either female-larger SSD or growth
inhibition by T in S. virgatus.
One alternative explanation is that growth inhibition by T reflects an
energetic trade-off resulting from increased activity or territorial defense.
Although we did not measure daily activity period, movement, or home range
area of experimental S. virgatus males, we have previously shown that
exogenous T increases each in males of a closely related species, S.
undulatus (Cox et al.,
2005). Our manipulations in S. virgatus may have shifted
energy allocation towards either growth (CAST) or these components of male
reproductive investment (TEST). Natural peaks in plasma T levels during the
breeding season (Fig. 1) may
mediate similar energetic trade-offs, leading to reduced male growth and the
development of female-larger SSD (Cox,
2005
; R. M. Cox and H. B. John-Alder, manuscript submitted).
Patterns of size-dependent variation within yearling males of S.
virgatus are consistent with this T-mediated energetic trade-off
hypothesis; growth rate decreases with body size
(Fig. 3), while plasma T levels
(Fig. 2), reproductive maturity
(Ballinger and Ketels, 1983
)
and mating success (Abell,
1997
,
1998b
) are positively related
to size.
If energetic costs of T inhibit growth in S. virgatus, why do they
not also inhibit growth in S. jarrovii? Previous studies have shown
that T increases activity and territorial aggression in adult males of S.
jarrovii, resulting in increased metabolic expenditure and decreased
energy acquisition (Klukowski et al.,
2004,
2001
; Marler and Moore,
1988
,
1989
,
1991
;
Marler et al., 1995
;
Moore, 1988
;
Moore and Marler, 1987
).
However, although yearling males of S. jarrovii have elevated plasma
T levels during the mating season (Fig.
1), they devote a considerably smaller fraction of their annual
energy budget to reproduction than do older males
(Congdon, 1977
). Additionally,
the environmental potential for an energetic trade-off with growth may be
greater for S. virgatus in the spring than for S. jarrovii
in the fall. Sceloporus virgatus breeds during the driest months of
the year (AprilJune), when arthropod (prey) densities are relatively
low, while S. jarrovii can presumably take advantage of seasonal
peaks in arthropod abundance during the monsoon rains that precede the fall
mating season (Smith, 1996
;
Smith and Ballinger, 1994
).
Further, S. virgatus breeds upon emergence from hibernation, before
depleted energy reserves can be replenished
(Smith, 1996
), while S.
jarrovii yearlings have several months of activity to store energy before
breeding. These mechanisms are only conjectural, but it is clear that, if the
energetic cost of male reproductive investment is to provide a parsimonious
explanation for T-mediated growth inhibition in S. virgatus, then
S. jarrovii must somehow differ such that these costs are
reduced.
Given the nature of our experiments, we have focused our discussion on
growth and body size of males, but any complete explanation for SSD must also
consider female body size. Thus, opposite patterns of SSD in S.
virgatus and S. jarrovii may be related primarily to differences
in factors acting on female size. For example, Abell
(1998b) argues that fecundity
selection for large female size may be stronger in S. virgatus than
S. jarrovii because the slope of the regression line relating clutch
or litter size to female SVL is steeper in S. virgatus.
Alternatively, energetic costs of reproductive investment may differentially
constrain female growth in S. virgatus vs S. jarrovii. For example,
we have found that ovariectomized yearlings of S. jarrovii grow
faster than pregnant yearling females
(Cox, 2005
), providing strong
experimental evidence for an energetic trade-off between female growth and
reproduction in this species. However, comparisons of reproductive vs
naturally non-reproductive females suggest that reproduction constrains growth
in S. virgatus as well as S. jarrovii (R. M. Cox and H. B.
John-Alder, submitted manuscript; Vinegar,
1975b
; but see Smith, 1997). Ultimately, while factors influencing
female size may be important with regard to SSD, the fact remains that we
observed opposite effects of T on male growth in S. virgatus and
S. jarrovii.
Given the inherent limitations of two-species comparative studies
(Garland and Adolph, 1994), we
cannot definitively conclude that the opposite growth responses to T that we
observed are directly related to differences in SSD between S.
virgatus and S. jarrovii. However, our results clearly raise
interesting questions about the role of T in mediating sex differences in
growth and body size. The diversity of SSD in Sceloporus makes this
group an ideal comparative system for further study. We hypothesize that
growth promotion by T represents a proximate physiological target of sexual
selection for large male body size, and predict that T promotes (or castration
inhibits) male growth in other male-larger Sceloporus species. A test
of this prediction would greatly strengthen our understanding of growth and
SSD in Sceloporus, as would future studies of the effects of T on
components of the endocrine growth axis (e.g. GH, IGF-I, IGF binding
proteins). Such studies would be particularly informative in a comparative
context involving both male- and female-larger species. For example, we
propose that sexual selection favors large male size in both male- and
female-larger Sceloporus species, but that energetic costs of
elevated T may indirectly constrain growth in some species (e.g. S.
undulatus and S. virgatus). Thus, at a proximate level, one
might predict that T stimulates the endocrine growth axis in all
Sceloporus species, despite growth inhibition by T at the organismal
level in female-larger species. Alternatively, the opposite growth responses
that we observed in S. virgatus vs S. jarrovii may reflect
fundamental differences in the effect of T on the endocrine growth axis. This
possibility is particularly interesting in light of other apparent exceptions
(Fennel and Scanes, 1992b; Swanson,
1967
) to the established role of androgens as growth promoters in
vertebrates (e.g. Borski et al.,
1996
; Holloway and
Leatherland, 1998
; Larsen et
al., 2004
; Riley et al.,
2002
; Wehrenberg and Giustina,
1992
).
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Abbreviations |
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Acknowledgments |
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References |
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