|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
First published online October 5, 2007
Journal of Experimental Biology 210, 3571-3578 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.005496
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Environmental stress affects the expression of a carotenoid-based sexual trait in male zebra finches
1 Université de Bourgogne, UMR-CNRS 5561, BioGéoSciences,
Equipe Ecologie Evolutive, 6 Bd Gabriel, 21 000 Dijon, France
2 Université de Bourgogne, Unité Propre de Recherche de
l'Enseignement Supérieur Lipides Nutrition, EA 2422, 6 Bd Gabriel, 21
000 Dijon, France
* Author for correspondence (e-mail: cyril.eraud{at}oncfs.gouv.fr)
Accepted 7 August 2007
 |
Summary |
|---|
 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Key words: carotenoids, environmental stress, self-maintenance, sexual traits, trade-offs, Taeniopygia guttata
|
Introduction |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
), it has been
suggested that only high quality males could afford to allocate resources to
produce and maintain extravagant traits. This idea is central to the handicap
hypothesis of sexual selection, and mechanisms ensuring the honesty of
sexually selected traits have been extensively investigated (reviewed in
Ligon, 1999). Interestingly,
classic examples of sexually selected traits involve bird ornaments that are
expressed or exaggerated during the mating/breeding season only. The loss of
breeding plumage in male ducks (Andersson,
1994) and the loss of orange bill colouration in American
goldfinch (McGraw, 2004) after
the breeding season are among well known examples in the class Aves. This
widespread phenomenon reveals the phenotypic plasticity of sexual traits and
emphasizes the role of forces other than sexual selection in their expression
(Wiens, 2001). For instance,
it has been suggested that the environment might exert substantial selective
pressure on sexual traits, acting upon the balance between costs and benefits
associated with their expression (reviewed in
Wiens, 2001). In particular,
when animals restrict sexual displays to the mating/breeding season only, it
is thought that benefits associated with mate attraction or competitor
eviction during this season would be outweighed by costs from environmental
factors during other times of the year
(Andersson, 1994) (but see
McGraw, 2004). Resource
availability, predation risk and habitat characteristics acting upon a signal
are usually proposed as important environmental factors shaping the expression
of sexual traits (Andersson,
1994; Wiens,
2001). Interestingly, besides these effects, ambient temperature
was also recently shown to be a proximate factor significantly affecting
sexual traits in males (West and Packer,
2002).
Among plausible hypotheses to explain how ambient temperature may affect
the expression of an ornament, it has been suggested that a thermal stress
might constrain ornamental displays through trade-offs between sexual displays
and physiological functions related to self-maintenance and survival
(West and Packer, 2002). In
homeothermic organisms, the loss of sexual ornaments at a time when
individuals have to fuel thermoregulatory functions might suggest that the
expression of sexual traits is modulated by ambient temperature through
resource-based trade-offs. In support of this, experimentally induced food
deprivation was shown to decrease the expression of coloured sexual ornaments
in male House finches (Hill,
2000). However, while these results would intuitively suggest that
the crucial limiting resource could be energy
(Hill, 2000), other key
resources in thermal-stressed individuals might also serve as the basis for
allocation trade-offs between sexual signalling and physiological functions
related to self-maintenance.
Because, in some species, carotenoid pigments are shared between different
physiological functions and colourations on a daily basis, carotenoid-based
signals offer a relevant context for investigating the effect of environmental
stress, such as ambient temperature, on the production and maintenance of
coloured secondary sexual traits, and for exploring the proximate mechanisms
shaping their expression. Carotenoids are pigments that are widely used in
animals to colour ornamental features yellow, orange or red. Carotenoid-based
sexual traits are usually more elaborated in males and several studies have
found that females mating with more coloured males experienced direct and/or
indirect benefits (Ligon,
1999). Accordingly, it has been suggested that these traits would
signal the phenotypic/genetic quality of their bearers
(Endler, 1980;
Lozano, 1994;
Olson and Owens, 1998;
McGraw and Hill, 2000;
Hill et al., 2002;
Faivre et al., 2003a;
Faivre et al., 2003b;
Alonso-Alvarez et al., 2004a;
Hõrak et al., 2004). In
addition, carotenoid-based pigmentation is hypothesized to incur important
nutritional/energy costs, since several steps of the colouration process
(absorption, metabolic conversion and transport of pigments) are thought to be
energy demanding (Hill, 2000;
McGraw et al., 2005). In line
with this hypothesis, recent findings show that the absorption of dietary
pigments is constrained by the nutrional/energy state of individuals
(Hill, 2000;
McGraw et al., 2005).
Additionally, carotenoids have antioxidant properties
(Møller et al., 2000;
Krinsky, 2001;
Blount et al., 2002;
Stahl and Sies, 2003;
Sahin et al., 2006) (but see
Costantini et al., 2006;
Costantini et al., 2007;
Hõrak et al., 2006;
Tummeleht et al., 2006) and,
consequently, pigments invested in a sexual ornament are depleted for
antioxidant defences. Relatedly, carotenoid-based sexual traits have been
supposed to reflect the antioxidant status of an individual
(von Schantz et al., 1999).
Therefore, thermal stress might shape the expression of carotenoid-based
sexual ornaments through allocation trade-offs, the key resource being energy
and/or antioxidant pigments per se since thermal stress was shown to
elicit an increased susceptibility to oxidative stress in several bird species
(Sahin et al., 2002;
Lin et al., 2006).
To our knowledge, the sensitivity of carotenoid-based sexual ornaments to
ambient temperature has never been investigated. The aim of this study was to
partially fill this gap. We used male zebra finches (Taeniopygia
guttata) as suitable models since these birds present useful biological
traits. Firstly, males express orange/red bills whose colouration relies on
carotenoid pigments (McGraw et al.,
2002). Secondly, the bill colour has been shown to be the target
of female preference (Burley and
Coopersmith, 1987; Blount et
al., 2003) (but see Collins
and ten Cate, 1996). Thirdly, males always bear a coloured bill,
with colours ranging from orange to dark red. Finally, whatever the bill
colour expressed by males, this colouration requires the allocation of
carotenoids on a daily basis, as shown by the short term variations detected
with experiments controlling access to carotenoids
(Alonso-Alvarez et al., 2004a).
Interestingly, if this contrasts with other cartenoid-based sexual ornaments
such as feathers, which require the allocation of pigments only during the
moult, this also suggests that males may have to face continuous trade-offs.
Practically, we submitted birds to a range of temperature regimes that
individuals may experience under natural conditions. For instance, zebra
finches may breed on the New England Tableland (Australia), much of which is
above 1000 m elevation, and up to 50 days of frost are expected each year
(Zann, 1996). In addition,
this species was also recorded as breeding during the winter, when mean daily
minimum temperature is 4°C (Zann,
1996). Accordingly, one group of birds was submitted to a cold
stress (6°C) for 4 weeks. This treatment was supposed to increase
metabolic rate and concomitant energy consumption compared to that of a second
group of birds that was kept within the thermoneutral zone (26°C). In
addition, half of the individuals in each treatment were provided with
supplementary carotenoids in the drinking water. If birds facing a thermal
stress give priority to self-maintenance at the expense of the sexual signal,
we predicted that males under cold stress should develop duller bills. In
addition, if energy is the only key resource implicated in a trade-off between
bill colour and self-maintenance, we predicted that males under cold stress
should be energy but not carotenoid limited and that carotenoid
supplementation would not allow them to exhibit redder bills because energy
limitation should compromise pigment allocation to the colouration
process.
|
Materials and methods |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
;
Sedunova et al., 1998), using
data from Gavrilov and Dolnik (Gavrilov
and Dolnik, 1985) we estimated that males sustained a daily energy
expenditure of 58.8 kJ day–1 and 25.3 kJ
day–1 when cold exposed and maintained at 26°C,
respectively. After this 7 day period, two groups (one in each temperature
treatment) were provided with extra carotenoids. Lutein and zeaxanthin are the
most abundant carotenoids in the diet of captive zebra finches
(McGraw et al., 2002).
Accordingly, supplemented males received a mix of lutein and zeaxanthin
[(ratio lutein/zeaxanthin=20:1, w:w) OroGlo liquid, Kemin France SRL, Nantes,
France] in the drinking water. The concentration in water (110 mg
l–1) was defined following Alonso-Alvarez et al.
(Alonso-Alvarez et al., 2004a).
Controls received tapwater only. Overall, our experimental design consisted of
four groups: non-supplemented males at 6°C (N=23) and 26°C
(N=23), and supplemented males at 6°C (N=24) and
26°C (N=23). Water, carotenoids and food were dispensed every 2
days, and each individual was carefully checked for any signs of sickness.
Birds were maintained under these conditions for 4 weeks. Only two rooms were
available for the experiment. Consequently, to minimize the risk that
differences between temperature regimes were due to a room effect, birds were
transferred between the two rooms, at the mid-point of the experiment (2 weeks
after the start of the carotenoid supplementation), while room temperature was
quickly reversed to maintain birds at the same temperature regime. Since birds
were maintained under the same conditions after the transfer, any changes in
fast dynamic variables related to physiological and behavioural traits
(between the end of the first 2 week period and the end of the last 2 week
period) would reflect changes in environmental conditions experienced by birds
due to a room effect. To detect a potential room effect, an additional
measurement of body mass and food intake (at day 21) was included in the
protocol described below. Therefore, body mass (taken as an integrative
measure of physiological condition) and food intake (taken as a measure of
behaviour) were measured immediately before and after each period elapsed in
the two rooms, and changes observed for the two variables were compared
between the two periods. For each of the experimental groups, neither change
in body mass nor change in food intake was affected by room change (paired
t-tests; food intake: all P values 
0.16, body mass: all
P values 0.24). In addition, similar results were found when
investigating a room effect within each temperature treatment (paired
t-tests; food intake: all P values 0.29, body mass: all
P values 0.42). We are therefore confident that environmental
conditions experienced by birds in the two rooms were similar and did not
produce biased results. Before the experiment, at the end of the 2 week acclimation period at 21°C (day 0), we measured mass, food intake, bill colour and circulating carotenoids in plasma. The same variables were recorded at the end of the experiment (day 35). Birds were weighed using an electronic balance (±0.1 g). Food was dispensed in a large plastic cup (height: 12 cm, diameter: 10 cm), so that seeds that were not eaten did not spill on the floor but remained within the cup, allowing us to assess food intake by weighing (±0.1 g) the amount of seeds ingested from 09:00 h to 19:00 h. A blood sample (100–150 µl) was collected from the brachial vein on day 0 and day 35 using heparinized microcapillary tubes. Blood was centrifuged at 1800 g for 15 min and the plasma was stored at –80°C until carotenoid analysis. No birds showed any sign of sickness during the course of the experiment.
Carotenoid analysis
Total plasma carotenoids were assessed by spectrophotometry following
Alonso-Alvarez et al. (Alonso-Alvarez et
al., 2004a). Briefly, carotenoids were extracted by diluting 10
µl of plasma in 190 µl of absolute ethanol. The solution was vortexed
for 1 min and centrifuged for 10 min at 1500 g to precipitate
the flocculent proteins. 100 µl of the supernatant was then added in ELISA
plates and the optical density was read with a microplate reader device at 450
nm. Carotenoid concentration was determined from a standard curve of lutein of
known concentration (700 µg ml–1). The standard curve was
achieved by serially diluting lutein in absolute ethanol as follows: 0, 0.1,
0.31, 0.625, 1.25, 2.5, 5 and 10 µg ml–1. For a subset of
individuals (N=32) high-performance liquid chromatography (HPLC)
analyses were also performed, allowing us to test for the reliability of
colorimetric measurements. The total amount of plasma carotenoids given by
colorimetric measurements was highly correlated with the sum of the four major
carotenoids (lutein, zeaxanthin, anhydrolutein, ß-cryptoxanthin)
determined by HPLC (Pearson correlation coefficient; r=0.80,
P<0.0001, N=32).
Assessment of bill colouration
Bill colour was scored under standardized conditions by reference to a
DuluxTM Trade Colour chart (Dulux, Asnières, France) as described
previously (Blount et al.,
2003; Bertrand et al.,
2006). In accordance with Blount et al.
(Blount et al., 2003), the
following specific scale was used, with scores ranging from 1 (light orange)
to 9 (dark red): 1 (69YR 34/780), 2 (56YR 28/778), 3 (44YR 26/756), 4 (34YR
20/708), 5 (31YR 18/648), 6 (16YR 16/594), 7 (19YR 13/558), 8 (09YR 11/475), 9
(14YR 10/434); where the alphanumeric code denotes the hue, the numerator is
the brightness and the denominator indicates the saturation. Bill colour was
always scored by the same observer (B.F.) in an independent room under
constant light conditions. At each time, two males were randomly selected in
each treatment group (by G.D.) and given to the observer who was therefore
blind regarding the treatment group. Colour scores were highly repeatable both
between and within observers (intraclass correlation coefficient:
R=0.96, P<0.0001, N=39; R=0.93,
P<0.0001, N=64). We also checked the relevance of the
scores obtained using the colour chart by comparing them with the hue values
provided by image analysis software (LUCIA G 4.81 Software, Nikon,
Champigny-sur-Marne, France). To do this, we scored the bill colour of 15
males using the colour chart and took a digital photograph of their bills
under standardized light conditions. The pictures were analysed to obtain a
hue value for each of them. The colour scores and the hue values were strongly
negatively correlated (Spearman's rank correlation,
rs=0.886,P<0.001, N=15) demonstrating
that the scores used in this study provided an objective and reliable measure
of variation in hue (a decrease in hue value provided by the software
indicated an increase in red colouration). At day 0, bill score and plasma
carotenoids were positively correlated (Spearman's rank correlation,
rs=0.328, P<0.002, N=93). As
expected, males circulating higher carotenoid levels displayed redder bills
(see also Blount et al., 2003;
McGraw and Ardia, 2003).
Statistical analyses
When necessary, data were log transformed to achieve the normality of
residuals and homogeneity of variances. The effects of treatments on change in
mass and food intake over the course of the experiment (from day 0 to day 35)
were analysed using repeated measurements general linear models (GLMs) and
individual contrasts. A similar analysis was performed to investigate the
effect of experimental treatments on the change in plasma carotenoid levels.
Since bill colour was recorded on an ordinal scale ranging from 1 to 9, the
effect of treatments on bill colour was investigated using a GLM with a logit
link and an ordinal error distribution (see
Bertrand et al., 2006). The GLM
was fitted with change in bill colour as the dependent variable
[post-experimental score (day 30) minus pre-experimental score (day 0)],
treatments and their interactions as fixed effects, and initial bill score as
covariate. Analyses were carried out using Statistica 7.0 (StatSoft,
Maisons-Alfort, France) and JMP 5.1 (SAS Institute, Cary, NC, USA) software
packages. P values were two-tailed and the level of significance was
set to 0.05. Means are given ± 1 s.e.m.
|
Results |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
|
Effect of cold exposure on change in circulating carotenoids
As expected, carotenoid supplementation strongly affected the amount of
circulating carotenoids in the plasma, with supplemented males showing a
greater increase in plasma carotenoids than non-supplemented ones (repeated
GLM; supplementation: F1,89=70.30, P<0.0001,
Fig. 1C). Values for
supplemented birds were similar to those reported by Alonso-Alvarez et al.
(Alonso-Alvarez et al., 2004a).
On average, supplemented birds showed a 2.6-fold increase (s.e.m.
±0.14) in their circulating carotenoid levels between day 0 and day 35.
Furthermore, changes in plasma carotenoid level also differed between the two
temperature regimes (repeated GLM; temperature:
F1,89=5.48, P=0.021). However, while the effect
of temperature did not significantly interact with the supplementation regime
(repeated GLM; temperature x supplementation:
F1,89=1.42, P=0.236), analysis revealed that the
effect of temperature relied mainly on the contrast existing between the two
non-supplemented groups (individual contrast; F1,89=6.175,
P=0.015) rather than on the contrast existing between the
supplemented groups (individual contrast; F1,89=0.665,
P=0.417, Fig. 1C).
Interestingly, in the absence of carotenoid supplementation, cold-exposed
males showed a greater increase in circulating carotenoids than males housed
at 26°C (Fig. 1C), and this
difference persisted after including food intake in the model (individual
contrast; F1,88=5.060, P=0.027).
Effect of cold exposure on change in bill colouration
After controlling for initial bill score (Wald statistic; covariate:
2=12.06, P<0.001), the change in bill colour
throughout the experiment was found to be significantly affected by the
temperature regime (Wald statistic; temperature: 2=16.48,
P<0.001). Following the prediction that males facing a thermal
stress give priority to self-maintenance at the expense of the sexual signal,
we found that in the absence of carotenoid supplementation, cold-exposed males
developed duller bills than males housed at a warm temperature
(Fig. 1D). Similarly,
carotenoid-supplemented and cold-exposed males developed less red bills than
their conspecifics kept at a warm temperature
(Fig. 1D). In addition, we
found that carotenoid supplementation significantly affected the change in
bill colour (Wald statistic; supplementation: 2=32.77,
P<0.001). Supplemented males developed redder bills than the
non-supplemented ones, even under cold exposure (Wald statistic; temperature
x supplementation: 2=0.21, P<0.604;
Fig. 1D), suggesting that birds
facing a cold stress were also carotenoid limited.
|
Discussion |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
). For instance, a
recent study has shown that, among abiotic environmental factors, ambient
temperature may constrain the expression of sexual ornaments presumably
through trade-offs between sexual traits and physiological functions related
to self-maintenance (West and Packer,
2002). To date, few studies have experimentally investigated the
plasticity of sexually selected traits in response to abiotic environmental
stressors (West and Packer,
2002). In this study, we explored the effect of environmental
stress, such as ambient temperature, on the production and the maintenance of
carotenoid-based sexual ornaments in male zebra finches. Male zebra finches
were simultaneously exposed to variable regimes of ambient temperature and
carotenoid availability to experimentally investigate the allocation of
resources to two competing functions, sexual display (bill colour) and
self-maintenance. We found that cold-exposed males reduced the expression of
the carotenoid-based sexual trait, suggesting that ambient temperature shaped
its expression. But, interestingly, carotenoid supplementation had an additive
effect, enabling supplemented males to express redder bills than their
counterparts.
Integumentary carotenoid-based colouration, such as red bill in zebra
finches, develops via a multistep process. These steps include the
absorption of carotenoid pigments from the diet, their incorporation into and
their transport through the blood stream via lipid carriers
(lipoproteins), their metabolic conversion into red ketocarotenoids
via oxidation reactions and, finally, their deposition into
integuments (Parker, 1996).
Pigmentation is therefore hypothesized to incur important
nutritional/energetic costs since metabolic conversion of yellow carotenoids
and lipoprotein assemblages are thought to be energy demanding
(Hill, 2000;
McGraw et al., 2005).
Accordingly, one hypothesis that might explain the reduced expression of bill
colour in cold-exposed birds is that thermoregulatory functions have
sequestered energy needed for the pigmentation process. Following this
hypothesis, if absorption of carotenoids and bill colouration process were
impaired due to energetic constraints only, cold-stressed birds would have
taken up lower amounts of pigments from their diet and/or would have shown a
reduced expression of their bill colour irrespective of carotenoid
availability. At first sight, one part of our results might be consistent with
this hypothesis because non-supplemented and cold-exposed males had a
depressed bill colour but higher circulating carotenoids at the end of the
experiment compared to the pre-experimental values (which could correspond to
accumulated unconverted yellow carotenoid precursors in the plasma). However,
several other results suggest that this explanation is unlikely. Firstly,
cold-stressed birds compensated by increasing their food intake, and their
body mass slightly increased during the experiment, suggesting that
cold-stressed birds remained in energy balance. Secondly, carotenoid levels
were significantly increased in a similar fashion in the two supplemented
groups, indicating that absorption of dietary pigments was not limited by the
amount of energy used to fuel the thermoregulatory functions. Thirdly, even
under cold exposure, supplemented males developed a redder bill than
non-supplemented ones, suggesting that (i) the pigmentation process was not
suppressed for cold tolerance and importantly that (ii) cold-stressed birds
were carotenoid limited.
Carotenoid pigments invested in a sexual ornament are depleted for other
functions, and in male zebra finches there is evidence that the development
and the maintenance of a colourful bill involves the mobilization of a huge
amount of carotenoids as shown by the high carotenoid concentration required
to achieve the reddest bills
(Alonso-Alvarez et al., 2004a).
Accordingly, among alternative hypotheses to that of energy limitation is that
the down-regulation of carotenoid allocation to the sexual signal in
cold-exposed males saves carotenoids to store them or up-regulate some
physiological functions related to their self-maintenance. Our findings that
carotenoids were limiting resources under cold exposure and that
non-supplemented and cold-exposed males have depressed bill colour while
circulating more carotenoids are supportive of this hypothesis. In addition,
the fact that cold-exposed and supplemented males were unable to develop and
maintain bill colour in a similar fashion to warm-exposed and supplemented
ones, notwithstanding a similar increase in circulating carotenoids within
these two groups, also supports the view that cold-exposed, supplemented males
also had to save carotenoids and prioritize self-maintenance.
Among physiological functions related to self-maintenance that might have
benefited from carotenoid saving, one could first mention the antioxidant
barriers (but see Hõrak et al.,
2006; Tummeleht et al.,
2006; Costantini et al.,
2007). It is well known that thermal stress causes high tissue
oxygen consumption and oxidative stress
(Selman et al., 2000;
Lin et al., 2006;
Sahin et al., 2002;
Sahin et al., 2006).
Therefore, it might have been crucial for cold-exposed birds to up-regulate
their antioxidant barriers to counter the increase in free radical production
during this period of high energy turnover
(Jenkins et al., 1988;
Scandalios, 2002).
Interestingly, recent studies suggest that carotenoids might contribute to the
maintenance of redox homeostasis in birds facing a thermal stress. Indeed, in
agreement with previous studies showing that carotenoid-supplemented
black-backed gulls (Larus fuscus) elicited a higher plasma
antioxidant activity (Blount et al.,
2002), Sahin et al. (Sahin et
al., 2006) have shown that supplementation with lycopene (a member
of the carotenoid family) attenuated the increase in biomarkers of oxidative
stress such as malondialdehyde and homocysteine in thermal-stressed quails
(Coturnix c. japonica). Additionally, Alonso-Alvarez et al.
(Alonso-Alvarez et al., 2004a)
have reported that male zebra finches with the highest increase in plasma
carotenoids showed the highest resistance to a free radical attack. However,
the hypothesis that cold-stressed zebra finches have upregulated their
antioxidant barriers contrasts sharply with recent experiments showing that
antioxidant defences are compromised during other metabolic workload [i.e.
breeding (Alonso-Alvarez et al.,
2004b; Wiersma et al.,
2004)]. Nevertheless, these findings might be reconciled with the
well known versatility of the antioxidant system
(Levine and Kidd, 1996).
Indeed, antioxidant defences have been shown to respond very differently
according to the pattern of metabolic workload
(Ji et al., 1998). For
instance, while acute and strenuous physical exercise can substantially impair
the effectiveness of antioxidant defences
(Robertson et al., 1991;
Aslan et al., 1998; Leeuwenburg
and Heinecke, 2001), regular physical exercise has been shown to prevent the
accumulation of oxidative damage by up-regulating the antioxidant system
via an increase of both enzymatic
(Robertson et al., 1991;
Aslan et al., 1998;
Brites et al., 1999;
Liu et al., 2000) and
non-enzymatic components (Brites et al.,
1999; Hübner-Wo'zniak et
al., 1994; Kitamura et al.,
1997; Cooper et al.,
2002; Pincemail et al.,
2002). Interestingly, long term cold exposure was also shown to
elicit an upregulation of the antioxidant system through an increase in
antioxidant enzyme activities (Selman et
al., 2000).
Among other physiological functions related to self-maintenance that might
have also benefited from carotenoid saving, one could mention the immune
defences. Indeed, cold stress has also been shown to exert variable effects on
immune functions. Although some studies suggest a negative effect of cold
exposure on immune performance (Svensson
et al., 1998; Cicho
et
al., 2002), other studies suggest that cold stress might enhance
different components of the immune system [humoral immunity
(Subba Rao and Glick, 1977);
cell-mediated immunity (Hangalapura et
al., 2004; Van Loon et al.,
2004)]. Besides their antioxidant properties, carotenoid pigments
are also potent immunostimulants in male zebra finches
(Blount et al., 2003;
McGraw and Ardia, 2003).
Accordingly, a non-mutually exclusive hypothesis might be that cold-exposed
males have saved carotenoids to up-regulate immune functions. Nevertheless,
further work is clearly needed to tease apart these two hypotheses, as well as
to investigate how non-enzymatic antioxidants such as carotenoids react to
long term cold exposure in other species.
The expression level of an ornament is a product of the balance between the
costs and benefits associated with its development and maintenance.
Accordingly, an alternative explanation for our findings could be that by
cold-exposing males, we might have changed the benefits associated with
investment in the sexual ornament, not the costs of its development and
maintenance. More specifically, birds might have used low temperature as a cue
with regard to the probability of a successful breeding event within a short
time period (Hau, 2001). This
probability being presumably reduced under cold conditions (but see
Zann, 1996;
Alonso-Alvarez et al., 2006),
birds might have reduced their investment in bill colour. In the same way,
since our males were housed in the absence of females, they might not have
been stimulated to invest carotenoids in the sexual signal to get a mate.
According to these scenarios, we might have expected the reduction in ornament
development to occur independently of any resource limitation. However, our
results showing that cold-stressed birds, as well as males kept at a warm
temperature, developed redder bills when provided with extra carotenoids,
suggest that males were not reluctant to invest carotenoids under cold
exposure or when housed in the absence of females (see also
Alonso-Alvarez et al., 2004a).
Rather our findings suggest that thermal stress might have affected the cost
of maintenance of the sexual signal and that carotenoids are among plausible
resources that might translate this cost.
In conclusion, the present study provides new insights into the plasticity
of carotenoid-based colour displays in response to abiotic environmental
stress and the potential role of resource allocation trade-offs in shaping
their expression. In addition, our results suggest that resources other than
energy may be prioritized for self-maintenance at the expense of sexual
signalling. For instance, our findings would suggest that carotenoid pigments
might serve as the basis for a resource-based trade-off between sexual
ornaments and physiological functions related to self-maintenance under
environmental stress. Moreover, the down-regulation of bill colouration in
carotenoid-supplemented and cold-exposed males would suggest that this
mechanism would be achieved through a differential allocation pathway rather
than the mobilization of keratinized pigments from the bill to the plasma.
However, the physiological functions related to self-maintenance that might
have benefited from carotenoid saving are currently equivocal. Although the
antioxidant system is among the candidates, further studies are definitely
needed since there is evidence, at least for some species, that carotenoids do
not contribute to modulating the level of oxidative damage
(Costantini et al., 2007).
|
Acknowledgments |
|---|
|
Footnotes |
|---|
Present address: Office National de la Chasse et de la Faune Sauvage,
Direction des Etudes et de la Recherche, CNERA Avifaune migratrice, Carrefour
de la Canauderie, 79 360 Villiers-en-Bois, France 
Present address: Université de Lausanne, Département Ecologie
et Evolution, Bâtiment de Biologie, 1015 Lausanne, Switzerland
|
References |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Alonso-Alvarez, C., Bertrand, S., Devevey, G., Gaillard, M., Prost, J., Faivre, B. and Sorci, G. (2004a). An experimental test of the dose-dependent effect of carotenoids and immune activation on sexual signals and antioxidant activity. Am. Nat. 164,651 -659.[CrossRef][Medline]
Alonso-Alvarez, C., Bertrand, S., Devevey, G., Prost, J., Faivre, B. and Sorci, G. (2004b). Increased susceptibility to oxidative stress as a proximate cost of reproduction. Ecol. Lett. 7,363 -368.[CrossRef]
Alonso-Alvarez, C., Bertrand, S., Devevey, G., Prost, J., Faivre, B., Chastel, O. and Sorci, G. (2006). An experimental manipulation of life-history trajectories and resistance to oxidative stress. Evolution 60,1913 -1924.[CrossRef][Medline]
Andersson, M. (1994). Sexual Selection. Princeton: Princeton University Press.
Aslan, R., Sekeroglu, M. R., Tarakcioglu, M., Bayiroglu, F. and Meral, I. (1998). Effect of acute and regular exercise on antioxidant enzymes, tissue damage markers and membran lipid peroxidation of erythrocytes in sedentary students. Turk. J. Med. Sci. 28,411 -414.
Bertrand, S., Faivre, B. and Sorci, G. (2006).
Do carotenoid-based sexual traits signal the availability of non-pigmentary
antioxidants? J. Exp. Biol.
209,4414
-4419.
Blount, J. D., Surai, P. F., Nager, R. G., Houston, D. C., Møller, A. P., Trewby, M. L. and Kennedy, M. W. (2002). Carotenoids and egg quality in the lesser black-backed gull Larus fuscus: a supplemental feeding study of maternal effects. Proc. R. Soc. Lond. B Biol. Sci. 269, 29-36.[Medline]
Blount, J. D., Metcalfe, N. D., Birkhead, T. R. and Surai, P.
F. (2003). Carotenoid modulation of immune function and
sexual attractiveness in zebra finches. Science
300,125
-127.
Brites, F. D., Evelson, P. A., Christiansen, M. G., Nicol, M. F., Basilico, M. J., Wikinski, R. W. and Llesuy, S. F. (1999). Soccer players under regular training show oxidative stress but an improved plasma antioxidant status. Clin. Sci. 96,381 -385.[CrossRef][Medline]
Burley, N. and Coopersmith, C. B. (1987). Bill color preferences of zebra finches. Ethology 76,133 -151.
Cicho, M., Chadziska, M., Ksia
ek, A. and
Konarzweski, W. (2002). Delayed effects of cold stress on
immune response in laboratory mice. Proc. R. Soc. Lond. B Biol.
Sci. 269,1493
-1497.[Medline]
Collins, S. A. and ten Cate, C. (1996). Does beak color affect female preference in zebra finches? Anim. Behav. 52,105 -112.[CrossRef]
Cooper, C. E., Vollaard, N. B. J., Choueiri, T. and Wilson, M. T. (2002). Exercise, free radicals and oxidative stress. Biochem. Soc. Trans. 30,280 -285.[CrossRef][Medline]
Costantini, D., Casagrande, S., De Filippis, S., Brambilla, G., Fanfani, A., Tagliavini, J. and Dell'Omo, G. (2006). Correlates of oxidative stress in wild kestrel nestlings (Falco tinnunculus). J. Comp. Physiol. B 176,329 -337.[CrossRef][Medline]
Costantini, D., Fanfani, A. and Dell'Omo, G.
(2007). Carotenoid availability does not limit the capability of
nestling kestrels (Falco tinnunculus) to cope with oxidative stress.
J. Exp. Biol. 210,1238
-1244.
Endler, J. A. (1980). Natural selection on color patterns in Poecilia reticulata. Evolution 34,76 -91.[CrossRef]
Faivre, B., Grégoire, A., Préault, M.,
Cézilly, F. and Sorci, G. (2003a). Immune activation
rapidly mirrored in a secondary sexual trait. Science
300, 103.
Faivre, B., Préault, M., Salvadori, F., Théry, M., Gaillard, M. and Cézilly, F. (2003b). Bill color and immunocompetence in the European blackbird. Anim. Behav. 65,1125 -1131.[CrossRef]
Gavrilov, V. M. and Dolnik, V. R. (1985). Basal metabolic rate, thermoregulation and existence energy in birds: world data. In Acta XVIII Congressua Internationalia Ornithologici (ed. V. D. Ilychiev and V. R. Dolnik), pp. 422-466. Moscow: Academy of Sciences of USSR.
Hangalapura, B. N., Nieuwland, M. G. B., de Vries Reilingh, G.,
van der Brand, H., Kemp, B. and Parmentier, H. K. (2004).
Duration of cold stress modulates overall immunity of chicken lines
divergently selected for antibody responses. Poult.
Sci. 83,765
-775.
Hau, M. (2001). Timing of breeding in variable environments: tropical birds as a model. Horm. Behav. 40,281 -290.[CrossRef][Medline]
Hill, G. E. (2000). Energetic constraints on expression of carotenoid-based plumage coloration. J. Avian Biol. 31,559 -566.[CrossRef]
Hill, G. E., Inouye, C. Y. and Montgomerie, R. (2002). Dietary carotenoids predict plumage coloration in wild house finches. Proc. R. Soc. Lond. B Biol. Sci. 269,1119 -1124.[Medline]
Hõrak, P., Saks, L., Karu, U., Ots, I., Surai, P. F. and McGraw, K. J. (2004). How coccidian parasites affect health and appearance of greenfinches. J. Anim. Ecol. 73,935 -947.[CrossRef]
Hõrak, P., Zilmer, M., Saks, L., Ots, I., Karu, U. and
Zilmer, K. (2006). Antioxidant protection, carotenoids, and
the costs of immune challenge in greenfinches. J. Exp.
Biol. 209,4329
-4338.
Hübner-Wo'zniak, E., Panczenko-Kresowska, B., Lerczak, K. and Po'snik, J. (1994). Effects of graded treadmill exercise on the activity of blood antioxidant enzymes, lipid peroxides and nonenzymatic antioxidants in long distance skiers. Biol. Sport 11,217 -226.
Jenkins, R. R., Friedland, R. and Howald, H. (1988). Free radical chemistry: relationship to exercise. Sports Med. 5,156 -170.[Medline]
Ji, L. L., Leeuwenburgh, C., Leichtweis, S., Gore, M., Fiebig, R., Hollander, J. and Bejma, J. (1998). Oxidative stress and aging: role of exercise and its influences on antioxidant system. Ann. N. Y. Acad. Sci. 854,102 -117.[CrossRef][Medline]
Kitamura, Y., Tanaka, K., Kiyohara, C., Hirohata, T., Tomita,
Y., Ishibashi, M. and Kido, K. (1997). Relationship of
alcohol use, physical activity and dietary habits with serum carotenoids,
retinol ald alpha-tocopherol among male Japanese smokers. Int. J.
Epidemiol. 26,307
-314.
Krinsky, N. I. (2001). Carotenoids as antioxidants. Nutrition 17,815 -817.[CrossRef][Medline]
Leeuwenburgh, C. and Heinecke, J. W. (2001). Oxidative stress and antioxidants in exercise. Curr. Med. Chem. 8,829 -838.[Medline]
Levine, S. A. and Kidd, P. M. (1996). Antioxidant Adaptation. Its Role in Free Radical Pathology. San Leandro, CA: A Biocurrents Division, Allergy Research Group.
Ligon, D. J. (1999). The Evolution of Avian Breeding Systems. Oxford: Oxford University Press.
Lin, H., Decuypere, E. and Buyse, J. (2006). Acute heat stress induces oxidative stress in broiler chickens. Comp. Biochem. Physiol. 144A,11 -17.[CrossRef][Medline]
Liu, J., Yeo, H. C., Övervik-Douki, E., Hagen, T., Doniger,
S. J., Chu, D. W., Brooks, G. A. and Ames, B. N. (2000).
Chronically and acutely exercised rats: biomarkers of oxidative stress and
endogenous antioxidants. J. Appl. Physiol.
89, 21-28.
Lozano, G. A. (1994). Carotenoids, parasites, and sexual selection. Oikos 70,309 -311.[CrossRef]
McGraw, K. J. (2004). Winter plumage coloration in male American goldfinches: do reduced ornaments serve signalling functions in the non-breeding season? Ethology 110, 1-9.[CrossRef]
McGraw, K. J. and Ardia, D. R. (2003). Carotenoids, immunocompetence, and the information content of sexual colors: an experimental test. Am. Nat. 162,704 -712.[CrossRef][Medline]
McGraw, K. J. and Hill, G. E. (2000). Differential effects of endoparasitism on the expression of carotenoid- and melanin-based ornamental coloration. Proc. R. Soc. Lond. B Biol. Sci. 267,1525 -1531.[Medline]
McGraw, K. J., Adkins, E. and Parker, R. S. (2002). Anhydrolutein in the zebra finch: a new, metabolically derived carotenoid in birds. Comp. Biochem. Physiol. 132B,811 -818.[CrossRef][Medline]
McGraw, K. J., Hill, G. E. and Parker, R. S. (2005). The physiological costs of being colorful: nutritional control of carotenoid utilization in the American goldfinch, Carduelis tristis. Anim. Behav. 69,653 -660.[CrossRef]
Møller, A. P., Biard, C., Blount, J. D., Houston, D. C., Ninni, P., Saino, N. and Surain, P. F. (2000). Carotenoid-dependent signals: indicators of foraging efficiency, immunocompetence or detoxification ability? Avian Poult. Biol. Rev. 11,137 -159.
Olson, V. A. and Owens, I. P. F. (1998). Costly sexual signals: are carotenoids rare, risky or required? Trends Ecol. Evol. 13,510 -514.[CrossRef]
Parker, R. S. (1996). Absorption, metabolism, and transport of carotenoids. FASEB J. 10,542 -551.[Abstract]
Parsons, P. A. (1995). Stress and limits to adaptation: sexual ornaments. J. Evol. Biol. 8, 455-461.[CrossRef]
Pincemail, J., Bonjean, K., Cayeux, K. and Defraigne, J.-O. (2002). Physiological action of antioxidant defences. Nutr. Clin. Metab. 16,233 -239.
Robertson, J. D., Maughan, R. J., Duthie, G. G. and Morrice, P. C. (1991). Increased blood antioxidant systems of runners in response to training load. Clin. Sci. 80,611 -618.[Medline]
Sahin, K., Kucuk, O., Sahin, N. and Sari, M. (2002). Effects of vitamin C and vitamin E on lipid peroxidation status, some serum hormone, metabolite, and mineral concentrations of Japanese quails reared under heat stress (34°C). Int. J. Vitam. Nutr. Res. 72,91 -100.[CrossRef][Medline]
Sahin, K., Onderci, M., Sahin, N., Gursu, M. F., Khachik, F. and Kucuk, O. (2006). Effects of lycopene supplementation on antioxidant status, oxidative stress, performance and carcass characteristics in heat-stressed Japanese quail. J. Therm. Biol. 31,307 -312.[CrossRef]
Scandalios, J. G. (2002). The rise of ROS. Trends Biochem. Sci. 27,483 -486.[CrossRef][Medline]
Sedunova, E. V., Rashotte, M. E., Pastukhov, I., Pate, K. N. and Johnson, F. J. (1998). Circadian perspective on feeding, fasting and ambient temperature effects in Zebra finch (Taeniopygia guttata). In Symposium on Avian Thermal Physiology and Energetics (ed. E. Hohtola and S. Saarela), p.33 . Oulu, Finland: Department of Biology, University of Oulu.
Selman, C., McLaren, J. S., Himanka, M. J. and Speakman, J. R. (2000). Effect of long-term cold exposure on antioxidant enzyme activities in a small mammal. Free Radic. Biol. Med. 28,1279 -1285.[CrossRef][Medline]
Stahl, W. and Sies, H. (2003). Antioxidant activity of carotenoids. Mol. Aspects Med. 24,345 -351.[CrossRef][Medline]
Subba Rao, D. S. V. and Glick, B. (1977). Effects of cold exposure on the immune response of chickens. Poultr. Sci. 56,992 -996.
Svensson, E., Råberg, L., Koch, C. and Hasselquist, D. (1998). Energetic stress, immunosuppression and the costs of an antibody response. Funct. Ecol. 12,912 -919.[CrossRef]
Tummeleht, L., Mägi, M., Kilgas, P., Mänd, R. and Hõrak, P. (2006). Antioxidant protection and plasma carotenoids of incubating great tits (Parus major L.) in relation to health state and breeding conditions. Comp. Biochem. Physiol. 144C,166 -172.
Van Loon, D. P. R., Hangalapura, B. N., Nieuwland, M. G., de Vries Reilingh, G., Kemp, B. and Parmentier, H. K. (2004). Effect of three different housing systems on immune responses and body weight of chicken lines divergently selected for antibody responses to sheep red blood cells. Livest. Prod. Sci. 85,139 -150.[CrossRef]
von Schantz, T., Bensch, S., Grahn, M., Hasselquist, D. and Wittzell, H. (1999). Good genes, oxidative stress and condition-dependent sexual signals. Proc. R. Soc. Lond. B Biol. Sci. 266,1 -12.[Medline]
West, P. M. and Packer, C. (2002). Sexual
selection, temperature and the Lion's mane. Science
297,1339
-1343.
Wiens, J. J. (2001). Widespread loss of sexually selected traits: how the peacock lost its spots. Trends Ecol. Evol. 16,517 -523.[CrossRef]
Wiersma, P., Selman, C., Speakman, J. R. and Verhulst, S. (2004). Birds sacrifice oxidative protection for reproduction. Biol. Lett. 271,360 -363.
Zann, R. A. (1996). The Zebra Finch: A Synthesis of Field and Laboratory Studies (Oxford Ornothology Series). Oxford: Oxford University Press.
CiteULike 
Complore 
Connotea 
Del.icio.us 
Digg 
Reddit 
Technorati 
Twitter What's this?
This article has been cited by other articles:
|
|
 |
|
  T. G. Murphy, M. F. Rosenthal, R. Montgomerie, and K. A. Tarvin Female American goldfinches use carotenoid-based bill coloration to signal status Behav. Ecol., November 2, 2009; (2009) arp140v1. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
