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First published online November 1, 2006
Journal of Experimental Biology 209, 4414-4419 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02540
Do carotenoid-based sexual traits signal the availability of non-pigmentary antioxidants?
1 Laboratoire de Parasitologie Evolutive, Université Pierre et Marie
Curie, CNRS UMR 7103, quai St Bernard, 75252 Paris cedex 05, France
2 Université de Bourgogne, UMR CNRS 5561 BioGéoSciences,
Equipe Ecologie Evolutive, 6 Blvd Gabriel, 21000 Dijon, France
* Author for correspondence (e-mail: sbertran{at}snv.jussieu.fr)
Accepted 12 September 2006
 |
Summary |
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 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
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Key words: carotenoids, free radicals, melatonin, oxidation, sexual advertisement, zebra finch
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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), in particular during mate choice. The honesty of
carotenoid-based signals is thought to be reinforced by two non-exclusive
mechanisms. First, since carotenoids are ultimately produced by plants and
must be absorbed by animals from their diet to produce sexual signals
(Kodric-Brown, 1985;
Kodric-Brown, 1989;
Hill, 1991;
Badayev and Hill, 2000), the
capacity to produce carotenoid-based coloration would be ultimately linked to
the individual ability to acquire, assimilate, and process carotenoids
(Endler, 1980;
Hill, 1990;
Hill, 1999). Second, because
carotenoids have important physiological functions as immunoenhancers
(Lozano, 1994;
Chew and Park, 2004) and free
radical scavengers (von Schantz et al.,
1999; Krinsky,
2001), only high quality males could afford the cost of using
carotenoids in sexual signals. This hypothesis is based on the assumption that
carotenoids are limiting, and that carotenoids allocated to the signal are no
longer available as immunoenhancers or antioxidants. The role of carotenoids
as modulators of the immune response has recently received much attention
(Chew and Park, 2004). In a
few studies, carotenoid supplementation has been shown to improve both the
expression of sexual signals and the immune response
(Blount et al., 2003;
McGraw and Ardia, 2003),
presumably because of a direct effect of these pigments on tegumentary colour
and immune functioning. Similarly, an experimental activation of the immune
system has been shown to reduce the expression of carotenoid-based signals and
to reduce the amount of carotenoids in the plasma of two bird species
(Faivre et al., 2003;
Alonso-Alvarez et al., 2004)
(see also Navara and Hill,
2003).
The other potential important function of carotenoids is as antioxidants
(Krinsky, 2001;
El-Agamey et al., 2004). The
antioxidant action of carotenoids occurs through the scavenging of
free-radicals (Burton and Ingold,
1984; Mortensen and Skibsted,
1996) and the quenching of singlet oxygen
(Conn et al., 1991;
DiMascio et al., 1989).
Moreover, epidemiological studies have shown that dietary carotenoids can be
associated with protection from certain age-associated diseases, such as
cancer, cardiovascular and inflammatory diseases
(Schabath et al., 2004;
Tamimi et al., 2005;
Walston et al., 2005). Other
studies have, however, failed to find such an association and, therefore, we
still do not have a complete picture of the importance of carotenoids as
antioxidants in vivo (El-Agamey
et al., 2004; Hartley and
Kennedy, 2004). In addition, carotenoids can even have a
pro-oxidant activity (Burton and Ingold,
1984) at high doses (higher than the amount normally
ingested).
Based on the findings that carotenoids do not always have a protective role
against free radicals, and that oxidation alters or destroys their colour
(thus reducing their sexual signalling function), it was suggested that
carotenoid-based sexual traits might signal the abundance of the
non-pigmentary antioxidant molecules that protect carotenoids from oxidation
and make them accessible for sexual signalling
(Hartley and Kennedy, 2004). A
complex antioxidant machinery is indeed available to scavenge free radicals.
These antioxidant defences include enzymatic (superoxide dismutase, catalase,
glutathione peroxidase and glutathione reductase) as well as non-enzymatic
free radical scavengers (vitamins C and E, uric acid, melatonin, cysteine,
glutathione), and minerals (selenium, zinc)
(Prior and Cao, 1999;
Fang et al., 2002).
The hypothesis that carotenoid-based sexual traits signal the abundance of non-pigmentary antioxidants provides testable predictions. In particular, it is straightforward to predict that by increasing the availability of non-pigmentary antioxidants we should enhance the expression of carotenoid-based sexual traits.
We tested the prediction of Hartley and Kennedy in zebra finches
(Hartley and Kennedy, 2004).
Male zebra finches have red bills that have been shown to be the targets of
female choice (Burley and Coppersmith,
1987; Blount et al.,
2003) (see also Collins and
ten Cate, 1996). Moreover, the colour of the bill depends on the
availability of carotenoids in the environment
(Blount et al., 2003;
Alonso-Alvarez et al., 2004;
Bertrand et al., 2006) and
immune activation reduces the availability of carotenoids for the sexual
signal (Alonso-Alvarez et al.,
2004). We manipulated the availability of carotenoids and of a
non-pigmentary antioxidant, melatonin, in the drinking water. Melatonin is a
secretory product of the pineal gland, and other organs, which has multiple
functions (Hardeland and Pandi-Perumal,
2005). Among its functions, melatonin has been shown to be both a
direct free radical scavenger (Tan et al.,
2002) and also to stimulate a number of antioxidant enzymes
including superoxide dismutase (SOD), glutathione peroxidase (GPx) and
glutathione reductase (GRx) (Reiter et
al., 2000; Anisimov,
2003; Rodriguez et al.,
2004). If the antioxidant properties of melatonin protect
carotenoids from oxidation, we predict that birds given melatonin should have
redder bills than birds not given melatonin, and that birds given supplements
of carotenoids and melatonin should have redder bills than birds given
carotenoids alone.
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Materials and methods |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Birds were randomly assigned to one of four treatments (N=10 males
per group): carotenoid supplementation in the drinking water [100 µg
ml-1; Oro GloTM liquid, 11 mg ml-1 lutein and
zeaxanthin (20:1, w/w); Kemin France SRL, Nantes, France
(Alonso-Alvarez et al., 2004)],
melatonin supplementation in the drinking water [50 µg ml-1
(Moore and Siopes, 2000;
Moore and Siopes, 2002)],
carotenoid and melatonin supplementation in the drinking water (100 µg
ml-1 and 50 µg ml-1, respectively), control group
receiving tapwater. All drinks were prepared freshly each day using cool
water, provided in opaque dispensers, at the same hour of the day (13:00
h).
Body mass (±0.1 g), the amount of carotenoids in plasma, and bill colour were measured twice for each bird during the experiment (day 0 and day 30). Initial values of body mass, amount of carotenoids in plasma and bill colour did not differ between supplementation groups (all measurements, P>0.2).
Measuring plasma carotenoids
To assess the amount of carotenoids in the plasma, blood was collected from
the brachial vein into heparinized microcapillary tubes (
150 µl). The
blood was centrifuged, and plasma stored at -20°C for later measurements
of total carotenoid concentration.
Colorimetry was used to determine the amount of plasma carotenoids. Plasma
(20 µl) was diluted in 180 µl of absolute ethanol. The dilution was
mixed in a vortex and the flocculent protein precipitated by centrifuging the
sample at 1500 g for 10 min. We examined the supernatant in a
spectrophotometer and determined the optical density of the carotenoid peak at
450 nm. Carotenoid concentration was determined from a standard curve of
lutein. We have previously shown that spectrometric and HPLC measurements of
plasma carotenoids are highly correlated in zebra finches
(Alonso-Alvarez et al.,
2004).
Measuring bill colour
Bill colour was assessed using a Dulux Trade Colour chart (Dulux,
Asnières, France) under the same light conditions. The following
specific scale, ranging from less red to redder colours, was used: 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
first number and letters indicate the hue, the numerator is the brightness,
and the denominator is the saturation
(Blount et al., 2003).
Measurements of bill colour were always performed by the same person (S.B.)
blind with respect to the treatments. We have previously shown that bill
colour scores and hue values provided by image analysis software (LUCIA G 4.81
Finale Software, Nikon, Paris, France) are highly correlated in zebra finches
(r=-0.867, P<0.0001, N=15), and that colour
scores are highly repeatable both between and within observers (intraclass
correlation coefficient: R=0.96, N=39, P<0.0001,
R=0.93, N=64, P<0.0001, respectively) (P.
Gautier, M. Barroca, S. Bertrand, C. Eraud, M. Gaillard, M. Hamman, S.
Motreuil, G. Sorci and B. Faivre, manuscript submitted for publication).
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)]. Both
variables were log10-transformed to ensure the normality of the
residuals (Shapiro-Wilk test, P>0.05). ANOVAs were performed on
differences (post-experimental - pre-experimental values). To assess the
effect of treatments on bill colour we used an ordinal model for multinomial
data with a cumulative logit link function [PROC GENMOD
(SAS Institute, 2001)]. As for
body mass and plasma carotenoids, we computed the difference in
post-experimental and pre-experimental bill colour index and used it as the
dependent variable in the model. |
Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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As expected, plasma carotenoids significantly increased in birds that received carotenoid-supplemented water, whereas the melatonin supplementation had no effect on the amount of circulating carotenoids (Fig. 2, Table 2).
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Birds that received carotenoid-supplemented water had redder bills at the end of the experiment (Table 3, Fig. 3). Interestingly, melatonin supplementation also affected bill colour, with melatonin-supplemented birds having redder bills at the end of the experiment (Table 3, Fig. 3). The interaction between carotenoid and melatonin supplementation was not statistically significant (Table 3), showing that the two treatments had an additive effect on the expression of the sexual signal.
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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The role of carotenoids as antioxidants has received much attention in
recent years (for example, see Krinsky,
2001). Behavioural ecologists interested in the signalling
function of coloured secondary sexual traits took advantage of the supposedly
antioxidant function of carotenoids to suggest that carotenoid-based signals
might be used by females to assess the overall quality of mates
(von Schantz et al., 1999).
Recently, a modified version of this hypothesis was proposed
(Hartley and Kennedy, 2004).
According to this version, carotenoid-based sexual traits would indicate the
antioxidant status of their bearers not because carotenoids participate in the
antioxidant machinery, but because they can only be used for the sexual signal
in their unbleached form. Carotenoids are very sensitive to oxidation
(Woodall et al., 1997), which
alters and destroys their colour. Therefore, their signalling function can
only be ensured if they are protected from the oxidation. Hartley and Kennedy
suggested that only individuals that have a very effective antioxidant
machinery (vitamins C and E, catalase, superoxide dismutase) would have enough
unbleached carotenoids available for the sexual signal
(Hartley and Kennedy, 2004).
Therefore, although carotenoid-based signals might still indicate the overall
antioxidant status of their bearer, the mechanisms would be slightly different
from the one originally envisaged. Our results are in agreement with the
hypothesis of Hartley and Kennedy that antioxidant defences can prevent the
bleaching of carotenoids and allow the organism to allocate them to the
production of sexual signals (Hartley and
Kennedy, 2004), since supplementation with melatonin, a potent
non-pigmentary antioxidant, affected the expression of bill colour in male
zebra finches.
Although the results reported in this study are in agreement with the
hypothesis of Hartley and Kennedy (Hartley
and Kennedy, 2004), we cannot completely discard another
explanation. By providing birds with melatonin, we might have increased the
overall availability of antioxidant molecules, and individuals might have
invested more carotenoids in the sexual trait. According to this scenario, we
might have made carotenoids `less needed' for the antioxidant system. The
experimental design used in this study does not allow us to tease apart the
two explanations (the `protection' and the `carotenoid less needed'
hypotheses). However, we believe that the finding that the amount of
circulating carotenoids was not affected by the melatonin supplementation is
supportive of the `protection' hypothesis. Indeed, if melatonin
supplementation increased the pool of antioxidants available for the organism,
we might have expected the amount of circulating carotenoids to increase.
Nevertheless, further work is clearly needed to tease apart the two
hypotheses, as well as to identify the rules that govern the oxidation of
carotenoids and their allocation to secondary sexual traits.
In spite of the considerable attention that has been devoted to the
information content of carotenoid-based sexual traits
(Olson and Owens, 1998), we
still have relatively few empirical data in support of the hypothesis that
individuals trade carotenoids against antioxidant protection or immune
functioning. Most of this evidence comes from studies on birds and fish
(Alonso Alvarez et al., 2004;
Blount et al., 2003;
Faivre et al., 2003;
Grether et al., 2004). In
zebra finches, an experiment in which birds were given variable doses of
carotenoids in the drinking water showed that bill colour became redder as
carotenoid availability increased until a certain dose, beyond which a further
increase in carotenoid availability did not produce any change in bill colour
(Alonso Alvarez et al., 2004).
In the same study, activation of the immune system by means of
lipopolysaccharide injections resulted in depressed bill colour and decreased
amount of plasma carotenoids, whatever the availability of carotenoids in the
environment. Finally, plasma carotenoids were positively correlated with the
antioxidant status in these birds suggesting that there might be a trade-off
between the amount of carotenoids that are allocated to the expression of a
secondary sexual trait, immune functioning and the antioxidant machinery
(Alonso Alvarez et al., 2004).
Unfortunately, as non-pigmentary antioxidants were neither manipulated nor
assessed in this study, one cannot exclude that the observed results are due
to the protection of carotenoids by vitamins or antioxidant enzymes. These
results undoubtedly call for more experimental work in order to have a clearer
picture on the trade-off between carotenoids allocation to sexual traits and
the antioxidant function.
In this study we chose melatonin as a supplement for the birds, instead of
other antioxidants, for three main reasons. First, melatonin has been reported
to be a very powerful antioxidant even when compared to other free radical
scavengers. In vitro, melatonin scavenges hydroxyl radicals,
peroxides, singlet oxygen and nitric oxide
(Reiter et al., 2001;
Tan et al., 2002), and it has
been shown that melatonin is superior to vitamin E as a peroxyl radical
scavenger (Pieri et al.,
1994). Compared with other major antioxidants (ascorbate and
vitamin E), melatonin is also 60- and 70-fold more effective, respectively, in
reducing oxidative DNA damage (assessed as the production of
8-hydroxy-2'-deoxyguanosine) (Qi et
al., 2000). Second, melatonin has an indirect effect on the
antioxidant machinery by stimulating antioxidant enzymes such as superoxide
dismutase, glutathione peroxidase, glutathione reductase, catalase, and other
antioxidant molecules, such as ascorbate, trolox and NADH
(Gitto et al., 2001), but also
by inhibiting pro-oxidant enzymes such as nitric oxide synthase and
lipoxygenase (Reiter et al.,
2000; Anisimov,
2003; Rodriguez et al.,
2004). Moreover, melatonin can also directly affect the production
of reactive oxygen species by reducing electron leakage through the
mitochondrial membrane (Reiter et al.,
2001).
Although, in the light of these previous findings, melatonin acts as a
powerful antioxidant, this hormone also intervenes in many other regulatory
functions of the organism (Anisimov,
2003). Because of these multiple functions, we cannot completely
discard the possibility that the observed effect on the expression of the
secondary sexual trait was due to something unrelated to the antioxidant
properties of melatonin. We will briefly discuss here these possible
alternatives.
Melatonin has a well known function in the regulation of the circadian and
seasonal rhythm (Cassone, 1990;
Gwinner et al., 1997). As
such, it could be that birds given melatonin might have been stimulated to
enhance their secondary sexual trait as a response to a seasonal signal.
However, unlike mammals, birds do not seem to use melatonin as a signal to
tune their reproduction to a particularly favourable time of the year
(Storey and Nicholls, 1978;
Chakraborty, 1995). Moreover,
in many studies on birds, reptiles, amphibians and fish melatonin
administration usually suppress reproductive parameters
(Mayer et al., 1997), such as
testis and ovary development and spermatogenesis.
Melatonin might also have an effect on glucose and lipid metabolism.
However, the results on this issue are rather controversial
(Bizot-Espiard et al., 1998;
Rasmussen et al., 1999;
Wolden-Hanson et al., 2000;
Fabis et al., 2002;
Mustonen et al., 2002;
Picinato et al., 2002), which
makes it difficult to have a clear-cut prediction on the expected direction of
the effect. We found that the body mass of birds given supplements of both
melatonin and carotenoids increased substantially during the course of the
experiment, compared with the birds in the other three experimental groups
whose body mass remained constant. Although this result might suggest that
indeed, melatonin affected either food intake, or metabolic activity of birds,
it is unclear why this effect was restricted to the group receiving both
melatonin and carotenoids. If melatonin had an effect on glucose and/or lipid
metabolism, we should also have found a difference in body mass of birds given
only melatonin.
Finally, melatonin has a regulatory effect on the immune response
(Srinivasan et al., 2005).
Melatonin increases the production of antibodies against T-dependent antigens,
activates Natural Killer (NK) cells and monocytes, and the release of
cytokines (IL-1, IL-2, IL-6, IL-12, and IFN)
(Hardeland et al., 2006).
Given that carotenoids also have an immunostimulatory effect, one might
speculate that by supplementing melatonin, carotenoids were more available for
the sexual advertisement, not because they were protected from oxidation but
because they were less needed by the immune system. Of course this is an
appealing alternative explanation that surely deserves further investigation.
This could be done by assessing immune functioning, the antioxidant status and
the sexual signal of melatonin-supplemented birds. As another way to assess
the generality of these preliminary results, it would be interesting to
explore whether any of the other non-pigmentary antioxidants (such as
vitamins) can also affect the expression of carotenoid-based signals.
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Acknowledgments |
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Footnotes |
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Present address: address 2 
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