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First published online December 16, 2008
Journal of Experimental Biology 212, 89-94 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.020826
Sex-specific effects of prenatal testosterone on nestling plasma antioxidant capacity in the zebra finch
Department of Animal Ecology, Lund University, Ecology Building, SE-223 62 Lund, Sweden
* Author for correspondence (e-mail: michael.tobler{at}zooekol.lu.se)
Accepted 21 October 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: maternal effects, antioxidants, hormones, early development
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). Variation in offspring phenotype can be attributed to
differences in genetic as well as non-genetic influences. One important
non-genetic factor affecting the formation of the offspring phenotype is
trans-generational transfer of maternal resources. Maternal resources such as
nutrients, antibodies or hormones, can have a substantial impact on
morphological, physiological and behavioural traits of the offspring
(Mousseau and Fox, 1998).
Maternally derived hormones in particular, have been identified as important
mediators of offspring growth and behaviour in many vertebrate species (e.g.
Schwabl, 1993;
Clark and Galef, 1995;
McCormick, 1999;
Rhen and Crews, 2002).
Avian mothers convey significant quantities of androgens to their eggs,
which are known to positively influence embryonic development, post-natal
growth and competitive behaviour of the offspring (for a review, see
Groothuis et al., 2005a).
However, there is large inter-female variation in the amount of androgens
transferred to the eggs. Recent studies suggest that this variation may be
maintained because the positive effects on growth and behaviour are
counterbalanced by negative effects on the immune function of the offspring
(e.g. Groothuis et al.,
2005b). Both the T-cell mediated and the humoral immune system of
young birds seem to be negatively influenced by high yolk androgen levels
(Andersson et al., 2004;
Navara et al., 2005;
Groothuis et al., 2005a;
Groothuis et al., 2005b) [but
see also Tschirren et al. and Navara et al.
(Tschirren et al., 2005;
Navara et al., 2006)]. It has
been argued that there may be a trade-off between growth and immune function
because both are energetically costly
(Müller et al.,
2005).
In addition to the negative effects on immune function, it has been
hypothesized that high amounts of maternally derived egg steroids also may
involve costs in terms of increased susceptibility to oxidative stress as a
consequence of accelerated growth (Royle
et al., 2001; Groothuis et
al., 2006; Martin and Schwabl,
2008). This hypothesis assumes that enhanced offspring development
rate mediated by egg steroids is associated with increased cell metabolism and
a concomitant increase in the production of reactive oxygen species (ROS) (see
Martin and Schwabl, 2008).
ROS, which are produced during normal metabolic processes by the mitochondria,
can have severe cytotoxic effects as they can oxidize macromolecules such as
proteins or DNA (e.g. Finkel and Holbrook,
2000; Fang et al.,
2002).
Enzymatic antioxidants such as superoxide dismutase as well as dietary
antioxidants such as the vitamins E and C scavenge ROS and protect the
organism from oxidative damage (Finkel and
Holbrook, 2000; Barja,
2004). However, when there is an overproduction of ROS in relation
to the antioxidant defences available this can result in oxidative stress
(Finkel and Holbrook, 2000).
In birds, only one study has directly assessed the effect of accelerated
growth on the prooxidant–antioxidant system. Alonso-Alvarez et al.
(Alonso-Alvarez et al., 2007a)
found that high nestling growth rate in the zebra finch (Taeniopygia
guttata Vieillot 1817) was associated with increased susceptibility of
red blood cells to oxidative damage. This is consistent with the above
hypothesis that an increase in growth rate mediated by egg androgens could
potentially lead to changes in the prooxidant–antioxidant balance.
A recent study on zebra finches has further shown a positive effect of
experimentally elevated yolk testosterone levels on nestling resting metabolic
rate (Tobler et al., 2007).
Assuming a positive link between oxygen consumption and ROS production, such
as has been found in humans (Loft et al.,
1994), this would also support the idea that zebra finch young
hatching from eggs with elevated testosterone might be more susceptible to
oxidative stress. Some caution must be used, however, when relating metabolic
activity directly to ROS production. Uncoupling proteins located in the
mitochondrial membrane help reduce ROS production by altering membrane proton
gradients (e.g. Brand, 2000;
Speakman et al., 2004;
Balaban et al., 2005), which
means that the relationship between metabolism and ROS production is not a
simple linear one. Nevertheless, it is suggestive that high levels of egg
androgens may influence the prooxidant–antioxidant balance through their
effect on growth and/or metabolism.
Although logically appealing, the hypothesis that high levels of egg
androgens may influence the prooxidant–antioxidant balance has never
been tested. In this study, we therefore experimentally manipulated
testosterone levels in zebra finch (Taeniopygia guttata) eggs to
investigate the effect of prenatal testosterone on the chicks' antioxidant
defences, i.e. plasma total antioxidant capacity (TAC). The zebra finch is
well suited to investigate this aspect given the previous work on this species
(see above). Moreover, it has been shown that experimental elevation of yolk
testosterone results in enhanced growth and begging of female offspring
(von Engelhardt et al., 2006)
(but see Tobler et al., 2007).
If, as has been hypothesized, elevated levels of yolk testosterone would
represent a cost in terms of increased susceptibility to oxidative stress,
compensatory responses of the prooxidant–antioxidant system might be
expected. Recent studies suggest that animals increase plasma antioxidant
levels in response to increased ROS production to improve protection against
oxidative damage (Barja 2004;
Legatt et al., 2007;
Cohen et al., 2008a;
Cohen et al., 2008b).
Therefore, we hypothesized that chicks hatching from eggs with elevated
testosterone levels may have higher plasma levels of antioxidants compared
with chicks hatching from control eggs.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Testosterone injections
During egg-laying, nests were checked every morning and freshly laid eggs
were replaced with artificial ones. Collected eggs were kept in an incubator
at constant temperature (37°C) until day 4. This allowed us to monitor
embryo survival and to discard infertile eggs. On day 3 of incubation, eggs
were injected with either 500 pg testosterone in 5 µl of sterile sesame oil
(T eggs) or 5 µl sterile sesame oil only (control eggs) [see von Engelhardt
et al. (von Engelhardt et al.,
2006) for a detailed technical description of the injection
method]. In zebra finches, females transfer more testosterone to their clutch
when they are mated to an attractive male
(Gil et al., 1999;
von Engelhardt, 2004) and
there is a concomitant increase in all eggs. The injection dose of
testosterone used in our study corresponds approximately to the difference in
testosterone + dihydrotestosterone measured in yolks of eggs from females
paired with attractive males versus unattractive males and, thus,
mimics a natural scenario (see also von
Engelhardt et al., 2006). The hole in the egg shell was sealed
with a tiny drop of superglue (Super Attak; Loctite Sweden AB, Göteborg,
Sweden). All eggs within a clutch received the same treatment and clutches
were randomly assigned to treatment groups. After injection, eggs were
immediately placed back into the incubator. On day 4, eggs with live embryos
were placed in foster nests. Whole clutches were randomly assigned to foster
parents. The number of eggs that failed to hatch because of reasons other than
infertility was similar in both treatment groups (19 control and 16 T eggs).
Moreover, the frequency of hatching failures not due to infertility was not
significantly different between the treatment groups (
2=0.43,
d.f.=1, P=0.51). There was also no significant difference in the
number of hatched chicks between the treatment groups
[F1,33=0.74, P=0.40; T broods: 2.5±0.2
chicks (mean ± 1 s.e.m.), control broods: 2.3±0.2 chicks].
Nestling growth
Eggs within a clutch were marked individually on the day of laying. On the
day of hatching, we marked offspring dorsally with nontoxic color pens and if
possible identified from which egg a chick hatched. In cases where two or
three chicks hatched synchronously and we could not determine the exact egg
numbers, we use averages between the possible egg numbers (e.g. 1.5 for a
chick from either first or second egg). At the age of 8–11 days chicks
were banded with aluminium rings. Nestling body mass was measured to the
nearest 0.01 g on days 1 (hatching day), 10 and 34 post hatch. Day 10
represents a period of intensive growth and at this stage most nestlings have
obtained more than 50% of their final body mass. At day 34 nestlings have
almost reached their final body mass and start to become independent from the
parents. For the periods 1–10 and 11–34 days of age we computed
the growth rate as the increment in body mass (body mass 2 minus body mass
1).
Assessment of nestling antioxidant capacity
We collected a blood sample (
40µl) from the brachial vein at day10
and again from the jugular vein (90 µl) at day 34 within 3 min of
removal of the bird from the cage. All blood samples were centrifuged at 1000
g and plasma was stored at –50°C until further
analysis. Plasma TAC of zebra finch chicks was measured using a commercial
test kit (Abel®-41M2) purchased from Knight Scientific Limited (Plymouth,
UK;
http://www.knightscientific.com).
Abel®-41M2 is a chemiluminescent test that allows the assessment of the
TAC of a test sample (e.g. plasma) to prevent oxidation by peroxynitrite,
which has high oxidant potential and occurs naturally in inflammatory cells,
such as neutrophils and macrophages.
The basic principle of the test is as follows. The test uses the photoprotein Pholasin®, which emits light in the presence of free radicals, other reactive oxygen species and peroxidase enzymes. Antioxidants in the sample under test compete with Pholasin® for the reactive oxygen species peroxynitrite (ONOO–) which is produced in the assay by the reaction between superoxide and nitric oxide, released simultaneously and continually from a 2.5 mmol l–1 solution of 3-morpholino-sydnonimine HCl (C6H10N4O2 HCl; SIN-1). In the absence of other antioxidants, Pholasin® emits light with gradually increasing intensity, reaching a peak after a few minutes. If there are antioxidants in the sample, they will compete with the Pholasin® for the peroxynitrite and this will delay the time at which the peak luminescence occurs. The more peak luminescence is delayed, the higher is the TAC of the test sample.
Samples were run in duplicates on 96-well microplates provided with the test kit. 5 µl samples (zebra finch plasma) were dissolved in 95 µl assay buffer per well, then, 50 µl Pholasin® was pipetted into each well. The plates were then transferred to a BMG-labtechnologies Lumistar Galaxy microplate luminometer and incubated for 5 min at 30°C. After the incubation period, 50 µl of 2 mg ml–1 SIN-1 solution was injected into each well using an automatic dispenser. The plates were then read in the luminometer at 38-s intervals for 69.7 min (110 cycles) at 30°C. Each plate contained two blanks (Pholasin® and SIN-1 only) and five duplicates of a diluted standard using vitamin E analogue (VEA) 6-hydroxy-2,5,7,8-tetramethyl-chroman-2-carboxylic acid. The time until peak luminescence (i.e. TAC) for the test sample is then expressed in VEA equivalent units µmol l–1, which can be directly derived from the linear regression formula of the standard curve making it possible to compare samples between plates. The two samples from the same individual were run on the same plate. The mean of the duplicate values expressed in standard VEA equivalent unitsµmol l–1 was used in the statistical analyses. Intra- and inter-assay variation was 2% and 13%, respectively.
Data analysis and sample sizes
Data were analysed using mixed models in SAS System for Windows 9.1 (PROC
MIXED) (Litell et al., 2004). Nest was included in all models as a random
factor to control for non-independence of nestlings sharing the same genetic
parents as well as the same rearing environment. The original models for
growth rate analyses contained the following fixed effects: egg treatment,
nestling sex and mean brood size and all two-way interactions. Mean brood size
was calculated as the mean number of nestlings between days 1 and 10, and
between days 11 and 34. The original models for analyses with plasma TAC
further included both the growth rate during the 1–10 days of age period
as well as growth rate during the 11–34 days of age period. The effect
of egg number and respective interactions with egg treatment, nestling sex and
brood size were originally included in all models to test for effects of
laying order. However, the effect of egg number was not significant in any of
the models (P>0.21 in all cases) and it was therefore excluded
from all models. Initial full models were reduced in a stepwise backward
procedure removing non-significant terms (P>0.1) subsequently from
the models. Random factors were estimated with the likelihood ratio test as
described by Littell et al. (Littell et
al., 2004). The Sattherthwaite approximation was used to calculate
the denominator degrees of freedom in all models
(Littell et al., 2004).
Residuals were tested for normality and homoscedasticity. VEA units were
log-transformed to normalise the data. The significance level was set at
P<0.05.
The data set includes measures from 30 T (15 males and 15 females) and 36 control (21 males and 15 females) offspring. However, sample sizes varied between analyses because we could not obtain the correct hatchling masses of nine chicks (3 T males, 3 T females and 3 control males) owing to simultaneous hatching or hatching during late afternoon/evening. We further failed to measure body mass of five 10-day old chicks (1 T male, 2 control males, 2 control females). Three chicks (1 T male and 2 control females) were not blood sampled on day 10 because they were considered too small.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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1,26, P>0.21 in all cases; 6.80±0.30 g and
6.67±0.26 g for the egg treatment and control group respectively;
6.50±0.25 g and 6.96±0.28 g for males and females). Growth rate
between 10 and 34 days of age was negatively influenced by brood size
(parameter estimate ± s.e.m.: –0.72±0.29;
F1,33.3=6.04, P=0.019), but was unaffected by egg
treatment and sex (F<2.75, d.f.1,32, P>0.10 for
both factors and their interaction; 4.89±0.32 g and 4.46±0.30 g
for the egg treatment and control group, respectively; 4.87±0.25 g and
4.47±0.26 g for males and females). Early growth during the first 10
days of age was negatively correlated with growth during days 10–34
(–0.48±0.09, F1,37.7=26.5,
P<0.001). This means that nestlings with a high growth rate during
the first 10 days of their life had slower growth afterwards, whereas
nestlings with low growth rate during the first 10 days showed accelerated
growth later. Body mass at the age of 34 days did not differ between egg
treatment groups or sexes (F<2.80, d.f.1,34,
P>0.10 in both cases; 12.61±0.27 g and 11.99±0.25 g
for T and control offspring; 12.37±0.23 g and 12.22±0.24 g for
males and females).
Nestling antioxidant capacity
The effect of egg treatment on plasma TAC of 10-day-old nestlings depended
on nestling sex as shown by the significant interaction
(Fig. 1,
Table 1). Male, 10-day-old
nestlings hatched from testosterone-treated eggs had lower plasma TAC than
nestlings hatched from control eggs (F1,19.9=4.54,
P=0.046), whereas this effect was not apparent in females
(F1,15.1=0.90, P=0.36)
(Fig. 1). Also, in T offspring,
plasma TAC on day10 was significantly higher in females than in males
(F1,14.7=6.03, P=0.027), whereas no such
difference was found for control offspring (F1,28.9=1.93,
P=0.18; Fig. 1).
Growth rate for the 1–10 day period was not related to plasma TAC at day
10 (F1,45.3=0.29, P=0.60). Plasma TAC of
34-day-old nestlings was positively, albeit weakly, correlated to the growth
rate during the 10–34-day period
(Table 1). None of the other
variables included in the model (sex, egg treatment, brood size and growth
rate during the 1–10-day period) explained a significant part of the
variation in nestling plasma TAC at day 34 (F<2.02, d.f.1,28,
P>0.16 in all cases; VEA units 840.5±54.1 and
825.0±46.0 for T and control males, 786.2±53.1 and
758±51.8 for T and control females, respectively).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Effects of egg treatment
Differences in antioxidant status between the treatment groups at day 10 do
not appear to be linked to nestling growth. Zebra finch nestlings from both
treatment groups had similar growth rates. This contrasts with an earlier
study on zebra finches in which females profited from elevation of egg
testosterone (with the same dose injected) in terms of enhanced growth and
begging (von Engelhardt et al.,
2006). Differences in the effect of egg testosterone manipulation
on growth rates may be due to population differences in maternal egg
androgens, as zebra finch females from our population appear to transfer
somewhat higher amounts of testosterone to their eggs compared with the
population used by von Engelhardt et al.
(von Engelhardt et al., 2006)
(M.S., unpublished data).
The sex-specific effect of egg treatment on nestling antioxidant capacity
at day 10 seems not to be due to differential effects of elevated yolk
testosterone on nestling metabolism. The positive effect of elevated yolk
testosterone on nestling metabolism recently reported for zebra finches
(Tobler et al., 2007) was
independent of nestling sex. Thus, if plasma antioxidant levels were directly
influenced by metabolic activity, both males and females would have been
expected to show changes in plasma antioxidant levels. However, one
problematic aspect when relating metabolic activity and ROS production is that
this relationship appears not to be a simple (linear) one. Uncoupling proteins
located in the mitochondrial membrane can lower ROS production by changing
membrane proton gradients (Brand,
2000; Echtay et al.,
2002; Speakman et al.,
2004; Balaban et al.,
2005), which results in reduced ATP production and higher energy
requirements (e.g. Speakman et al.,
2004; da Silva et al.,
2008). Given this potential trade-off between ROS production and
ATP production efficiency it will depend on the current energy requirements
and the shape of the trade-off whether and how much animals will rely on
antioxidant defense systems for ROS protection. Consequently, higher metabolic
activity may not necessarily result in changes of plasma antioxidant levels.
Notably, a recent comparative study on birds investigating the association
between life-history variables and plasma antioxidants showed a relatively
weak association between basal metabolic rate and plasma antioxidants
(Cohen et al., 2008b).
A major component of circulating plasma TAC is uric acid, the main product
of nitrogen catabolism in birds. Levels of circulating uric acid can vary
depending on the amount of food ingested (e.g.
Kolmstetter and Ramsay, 2000)
and, thus, it could be argued that lower plasma TAC in male nestlings may
result from lower food intake of these males. However, if this was the case,
we would expect it to be translated into different growth rates which we did
not observe.
It is probable that egg testosterone manipulation influenced the
prooxidant–antioxidant balance more directly through other mechanisms
than growth and metabolism. Egg treatment may have induced permanent
physiological changes in male zebra finch chicks, which in turn negatively
affected their antioxidant defences at the age of 10 days. Such changes may,
for example, include differences in the ability to secret hormones. If egg
hormone treatment were to result in consistently higher nestling blood levels
of testosterone or related steroids this would probably affect plasma total
antioxidant capacity. It has been shown that high levels of circulating
testosterone impair antioxidant enzymes in rat and rabbit testicular tissues
(Chainy et al., 1997;
Aydilek et al., 2004) [but see
Peltola et al. (Peltola et al.,
1996)]. Moreover, high testosterone blood levels have recently
been shown also to negatively influence red blood cell resistance to a free
radical attack in adult zebra finch males
(Alonso-Alvarez et al., 2007b).
However, high levels of blood testosterone are also known to positively affect
the levels of dietary antioxidants, i.e. carotenoids
(Blas et al., 2006), possibly
through direct effects of testosterone on lipoproteins or digestive enzymes,
which regulate carotenoid availability (e.g.
Woo et al., 1993;
McGraw et al., 2006).
Unfortunately, we did not measure circulating testosterone levels in the
blood. It must also be noted that the link between yolk androgens and
circulating, endogenous androgens in nestlings is not well established.
Exposure to high levels of prenatal testosterone may also involve changes in
availability and affinity of steroid hormone receptors on proteins regulating
the prooxidant–antioxidant system and, thus, may not necessarily involve
elevated levels of circulating testosterone.
How should the difference in plasma TAC of male nestlings at the age of 10
days be interpreted? It has been hypothesized that elevated levels of yolk
testosterone could represent a cost for the offspring in terms of increased
susceptibility to oxidative stress (see Introduction). Recent studies suggest
that animals increase antioxidant levels as a compensatory response to
increased ROS production (Barja
2004; Legatt et al.,
2007; Cohen et al.,
2008a; Cohen et al.,
2008b). Therefore, if T offspring were exposed to higher levels of
ROS, a concomitant increase in plasma antioxidant levels would be expected.
However, we found that plasma TAC in male T nestlings was lower than in
control male nestlings, which does not match with this expectation. We can
only speculate about the potential causes and consequences of the difference
in plasma TAC between testosterone and control male nestlings. One possibility
is that lowered antioxidant status in T males reflects depletion of
antioxidant defences as a consequence of increased ROS production (see
Alonso-Alvarez et al., 2007a).
Alternatively, lowered antioxidant levels could also be a response to lowered
ROS production, for example as a result of enhanced bioavailability of dietary
carotenoids (see above). Thus, it is premature to conclude that reduced
antioxidant capacity during the early nestling phase represents a viability
cost to male offspring. Further studies are needed to establish the fitness
consequences resulting from the differences in antioxidant status.
Differences between the sexes
The finding of a sex-specific effect of egg treatment on antioxidant status
in 10-day-old zebra finch nestlings is not surprising given that previous work
has demonstrated that prenatal androgens affect growth and begging sex
specifically in this species (von
Engelhardt et al., 2006) [but see Tobler et al.
(Tobler et al., 2007)].
Moreover, other studies have shown male and female zebra finch chicks have
different nutritional requirements during early development
(Martins 2004;
Arnold et al., 2007) and cope
differently with sibling competition (De
Kogel and Prijs, 1996; Bradbury
and Blakey, 1998; Kilner,
1998). Thus, the sex-specific differences in plasma TAC due to egg
testosterone treatment probably have different consequences in male and female
offspring. Variation in egg testosterone levels may therefore be an important
factor for sex allocation in this species (see
von Engelhardt et al.,
2006).
Interestingly, female zebra finches have been shown to transfer higher
amounts of androgens to their eggs when paired with a more attractive male
(Gil et al., 1999;
von Engelhardt, 2004).
Moreover, yolk antioxidants are also known to vary with male attractiveness.
When paired to an attractive male, females transfer less antioxidants in
first-laid eggs than females paired with an unattractive male, but more in
later-laid eggs (Williamson et al.,
2006). More attractive males may be more likely to sire offspring
of high genetic quality or provide more benefits in terms of territory quality
or parental care and, thus, father offspring of higher viability. Hence, it
has been hypothesised that female zebra finches may fine tune development of
individual offspring and sex ratio depending on the offspring's survival
prospects by adjusting the relative amount of yolk androgens to the amount of
yolk antioxidants (e.g. Royle et al.,
2001; Groothuis et al.,
2006; Williamson et al.,
2006). Given the results from our study it is probable that
maternal antioxidants play an important role in the modulation of egg steroid
effects.
In conclusion, we provide evidence that prenatal exposure to high levels of testosterone influences the antioxidant defence system of the offspring, at least during the early developmental period. The finding of a sex-specific effect may have implications for avian sex allocation.
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Footnotes |
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