Behavioral Ecology Vol. 13 No. 2: 169-174
© 2002 International Society for Behavioral Ecology
Immune response of male barn swallows in relation to parental effort, corticosterone plasma levels, and sexual ornamentation
a Dipartimento di Scienze dell' Ambiente e del Territorio, Università di Milano-Bicocca, via Emanueli 15, I-20126 Milano, Italy b Dipartimento di Biologia, Università degli Studi di Milano, via Celoria 26, I-20133 Milano, Italy c Dipartimento di Etologia, Ecologia ed Evoluzione, Università di Pisa, via Volta 6, I-56126 Pisa, Italy d Laboratoire d'Ecologie, CNRS UMR 7625, Université Pierre et Marie Curie, 7 quai St. Bernard, Case 237, F-75252 Paris Cedex 05, France
Address correspondence to N. Saino, Dipartimento di Biologia, Università degli Studi di Milano, via Celoria 26, I-20133 Milano, Italy. E-mail: n.saino{at}mailserver.unimi.it .
Received 14 April 2000; revised 2 April 2001; accepted 2 April 2001.
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ABSTRACT |
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Life-history theory posits trade-offs between fitness components. Reproduction negatively affects physiology and immune system functioning, and the effect of this form of stress may be mediated by glucocorticosteroids. We manipulated brood size of barn swallows (Hirundo rustica) to study the effect of stress arising from reproductive effort on corticosterone levels of males. We also measured T-cell—mediated immunocompetence by intradermally injecting birds with phytohemagglutinin, which is mitogenic to T-lymphocytes. The results confirmed the prediction of a negative effect of parental effort on lymphoproliferative response. We found no covariation between immune response and corticosterone levels. Males with long tails, an ornament currently under directional sexual selection, had a relatively large T-cell response to the mitogen, consistent with models of parasite-mediated sexual selection predicting higher levels of immune defense in highly ornamented males. In addition, males with large sexual ornaments had relatively low corticosterone levels at the end of the parental period. These results can be reconciled with the hypothesis proposing a trade-off between parental activities and adaptive immunity and suggest that highly ornamented males are less exposed or less susceptible to stress arising from parental effort.
Key words: barn swallows, corticosterone, Hirundo rustica, immunity, parental effort, secondary sexual characters, stress.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Stress is a ubiquitous phenomenon resulting from nonspecific responses of the body to any demand made on it, providing correction mechanisms of homeostatic processes (review in von Holst, 1998
). In its widest sense, stress is produced by a broad
range of factors as different as exposure to extreme temperatures and
xenobiotics, food deprivation, social interactions, or reproduction, and it
can result in suppressed immunity (Bijlsma
and Loeschcke, 1997; Hoffmann
and Parsons, 1989;
Møller and Swaddle,
1997; Møller et al.,
1998c). There is ample evidence, both in humans and other
vertebrates, that stress affects immune system function (for a review, see
Apanius, 1998; se also
Friedman et al., 1996;
Ottaviani and Franceschi,
1996). Temporary activation of the immune system may follow acute
stress episodes, but suppression of immune function generally ensues within
days or weeks, resulting in lowered capacity of raising an adaptive immune
response to parasites and pathogens (see
Apanius, 1998;
Sapolski, 1992;
Wingfield et al., 1998). At
the mechanistic level, the relationship between stress and immunity is thought
to be mediated by neurological as well as endocrine links
(Sapolski, 1992;
Wingfield, 1994). An increase
in circulating levels of glucocorticosteroids, the so-called adrenocortical
response, for example, is a frequently documented effect of intense stress
that eventually leads to immune suppression (for reviews, see
Apanius, 1998;
Wingfield et al., 1998).
Recent evolutionary studies of life history have started to tackle the
issue of the existence of trade-offs between life-history traits such as
survival and reproduction, as mediated by the ability to mount an adaptive
immune response to an experimental challenge to the immune system (e.g.,
Deerenberg et al., 1997;
Moreno et al., 1999;
Nordling et al., 1998;
Saino et al., 1999) and fend
off parasites (e.g., Richner et al.,
1995; Wiehn et al.,
1999). Because resistance to and clearance of pathogens have
important effects on individual fitness (e.g.,
Clayton and Moore, 1997;
Loye and Zuk, 1991;
Pastoret et al., 1998;
Price, 1980), adaptive immune
processes that have evolved to serve this function should be considered as
life-history traits, just like other traits that have received attention from
ecologists (Roff, 1992;
Stearns, 1992). Life-history
theory posits that reproduction imposes costs in terms of reduced chances of
survival and future reproduction, and the literature showing that such costs
exist is ample (Partridge,
1989; Roff, 1992;
Stearns, 1992;
Williams, 1966). In altricial
bird species, for example, intense exercise, such as that determined by
attending an experimentally enlarged brood, has been repeatedly shown to
negatively affect survival and the ability to further invest in reproduction
(see Newton, 1989;
Partridge, 1989 for a review;
Saino et al., 1999). Increased
exercise also impairs an individual's ability to raise an immune response to
an experimental challenge to its immune system
(Deerenberg et al., 1997;
Moreno et al., 1999; see also
Sheldon and Verhulst, 1996)
and reduces resistance to or clearance of parasitic infections
(Møller, 1997;
Roitt et al., 1996).
Two not mutually exclusive hypotheses can been invoked to explain the
observation that increased parental effort, as a form of stress, causes
depression of immune function (for a recent review, see
Råberg et al., 1998).
The resource limitation hypothesis suggests that downregulation of the immune
system during intense exercise occurs as the inevitable consequence of
competition for limited resources (energy or nutrients) between immune defense
and other costly activities. Increased investment in parental care would be
obtained at the cost of a reduced allocation of resources to immune function.
The adrenocortical axis, via the production of glucocorticosteroids, might
provide the required mechanism for the regulation of the immune system. Thus,
immunosuppressive stress hormones could have the function of producing an
adaptive resource reallocation among competing activities (see
Wedekind and Folstad,
1994).
The avoidance of immunopathology hypothesis
(Råberg et al., 1998)
stems from the observation that, under stressful conditions, animals are
relatively more exposed to the risk of hyperactivation of their immune system
against self, possibly having noxious immunopathological consequences (see
Råberg et al., 1998 and
references therein). Depression of immune function during stress might reflect
another kind of trade-off between adaptive immune response and avoidance of
nonadaptive autoimmune processes, thus reducing the risk of incurring in
immunopathology at the expense of defense against parasites.
In this experimental study we tested the prediction that increased parental
effort ultimately impairs functioning of an important component of acquired
immunity, the ability to raise a T-cell—mediated immune response
(Pastoret et al., 1998;
Roitt et al., 1996;
Wakelin, 1996). We manipulated
parental workload of barn swallows by either increasing or reducing the size
of their brood by one nestling soon after hatching. On average, a few days
after fledging of the nestlings, we recaptured male parents and collected a
blood sample within 1 min after capture. Males were then subjected to a
cutaneous hypersensitivity test by injecting their wing web with a lectin,
phytohemagglutinin (PHA), which has a mitogenic effect on T-lymphocytes. The
extent of swelling of the wing web while controlling for the effect of
inoculation per se is considered an index of T-cell—mediated
immunocompetence (Lochmiller et al.,
1993; Saino et al.,
1997a,
1999;
Sorci et al., 1997).
Both the resource limitation and the avoidance of immunopathology hypotheses led us to predict that males with an enlarged brood should have weaker immune responses than males with a reduced brood. We also predicted that males with an enlarged brood would have larger concentrations of circulating corticosterone compared to males with a reduced brood. Finally, the intensity of T-cell—mediated response to mitogenic stimulation of T-cells was expected to negatively covary with corticosterone level, which is considered to be a stress marker.
Barn swallows are socially monogamous, with females exerting a sexual
preference for males with relatively long outermost tail feathers both as
social mates and as extrapair fathers of their offspring (Møller,
1988,
1994;
Saino et al., 1997b).
Ornamental tail feathers of males reliably signal the phenotypic quality of
their bearer, including viability, freedom from parasites, and the ability to
raise a humoral immune response (Møller,
1991a,b,
1994;
Møller et al., 1998a;
Saino and Møller, 1994,
1996). In addition, we
therefore predicted that long-tailed males would be less susceptible to
stress. In particular, we expected that corticosterone levels would negatively
covary, while response to PHA would positively covary with tail length.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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This experiment was carried out during spring-summer 1999 in four barn swallow colonies in our study area east of Milano, Italy. We used mist nets to capture adults arriving from migration, starting in early April. Individuals were sexed according to the shape of the cloacal protuberance and marked with unique combinations of color rings on tarsometatarsi and color markings on breast and belly feathers to allow later assignment to broods. Assignment to sex was confirmed by observation of sexual and breeding behavior and inspection at later captures for presence (female) or absence (male) of an incubation patch. At first capture we measured a number of morphological characters including length of ornamental outermost tail feathers, and their length was expressed as the mean of the right and left character (hereafter "tail length"; for general field procedures, see also Møller, 1994
).
Brood size manipulation
We inspected nests every second day and more frequently around the
estimated hatching date. The size of broods was experimentally altered (either
enlarged or reduced by one nestling) as soon as hatching was completed by
swapping an unbalanced number of randomly chosen nestlings according to a
predetermined scheme between pairs of broods (dyads) hatching in the same
colony on the same day. The brood due to be reduced or enlarged was chosen
randomly within each dyad. Thus, for example, when two synchronously hatching
broods of five nestlings were found, three nestlings of the brood due to be
reduced were transferred to the brood due to be enlarged, while two nestlings
of the brood due to be enlarged were transferred to the brood due to be
reduced (for further details on the procedure, see
Saino et al., 1999), thus
resulting in an (enlarged) brood of six and a (reduced) brood of four
nestlings within that dyad. Manipulation resulted in a significant difference
in postmanipulation brood size between experimental groups of approximately
1.9 nestlings. Reduced broods of males assayed for corticosterone contained on
average 3.28 nestlings (SE = 0.16, n = 25 broods), whereas enlarged
broods contained 5.15 nestlings (SE = 0.18, n = 20 broods; t
test; t = 7.78, df = 43, p <.001). A qualitatively
similar difference persisted until the age of fledging (t = 7.04, df
= 43, p <.001). Similarly, postmanipulation brood size differed
significantly among groups of broods whose attending males were tested for
immunocompetence [size of reduced broods: 3.14 (SE = 0.21, n = 14);
enlarged broods 5.20 (SE 0.25, n = 10)]. For the analyses of
T-cell—mediated immune response, we also considered a set of males with
unmanipulated broods that had just fledged or were about to fledge their
offspring (mean brood size = 4.09, SE = 0.34, n = 11). Also in this
case, postmanipulation brood size varied significantly among groups of males
(F2,32 = 15.10, p <.001), as did brood size
around the age of fledging (F2,32 = 12.34, p
<.001). Hence, brood size manipulation produced the desired effect on mean
number of nestlings in a brood from the time of hatching throughout the
nestling period, with unmanipulated broods having intermediate size between
that of enlarged and reduced broods.
Crucial for our study was showing that our experimental manipulation
affected parental workload of the fathers. In two previous brood size
manipulation experiments carried out with the same procedures used in the
present study (Saino et al.,
1997a,
1999), we collected data on
feeding rate (feeding trips/h) of parents of enlarged or reduced broods. We
made 1-1.25 h of daily (excluding Sundays) observations in the morning
(0600-1100 h) from the day of hatching until nestlings were 13 days old. Those
data sets show that males of enlarged broods visit their nests more frequently
than males of reduced broods, while controlling for potentially confounding
effects of breeding date and colony by comparing males of dyads of broods that
were partially cross-fostered [mean (SE) male feeding trips/h to reduced
broods = 6.01 (0.56), to enlarged broods 7.11 (0.63); t test for
paired data: t = 2.88, df = 25, p =.008, n = 26
pairs of synchronously breeding males]. Hence, males with an enlarged brood
made approximately 18% more trips to the nest than males of reduced broods,
indicating that brood size manipulation actually affected parental workload
(see, e.g., Richner et al.,
1995, for qualitatively similar results). We assume here that
brood size manipulation influenced paternal feeding rate in a way
qualitatively similar to the two previous experiments in the same study
area.
Blood sampling and corticosterone assay
Barn swallows usually spend the night in the stables where they breed and
start leaving the stable at dawn. We put up nets at doors and windows before
dawn and captured birds when they flew out of the stable. Because all
individuals considered in this study were captured between 0440 and 0700 h, we
minimized potentially confounding effects of circadian variation in hormone
concentrations. We tried to capture males around the estimated day of fledging
of their nestlings by opportunely timing our capture sessions. However, we did
not perform frequent capture sessions to minimize the potentially confounding
effect of variation in frequency of capture among individuals. As a result,
males considered in corticosterone analyses were captured 4.18 (SE = 0.96,
n = 45) days after they had fledged their offspring. The difference
in time elapsed between blood sampling date and fledging date did not differ
between males with a reduced or an enlarged brood (t = 0.34, df = 43,
p =.73) Similarly, males considered in the analyses of effect of
brood size manipulation on immune response were captured on average 1.94 (SE =
1.07, n = 35) days after fledging their offspring, and the difference
in time elapsed between fledging and blood sampling among groups of males with
a reduced, unmanipulated, or an enlarged brood was far from statistical
significance (F2,32 = 0.25, p =.78). Because barn
swallow parents are known to attend and feed their offspring for some days
after fledging (Møller,
1994), blood sampling for corticosterone analyses and the
immunocompetence test were performed, on average, approximately at the end of
parental care of the brood. In addition, mean fledging date did not vary
significantly among groups of males assayed for corticosterone levels
(t = 0.09, df = 43, p =.93) or T-cell response
(F2,32 = 0.63, p =.54), indicating that the three
groups of males were homogeneous with respect to breeding date.
However, in all the analyses we also statistically controlled for the potentially confounding effects of time of the day, time elapsed between capture and blood sampling or cutaneous hypersensitivity test and calendar date. These variables were generally found not to affect the results significantly (see Results). When a male due to be entered in the study was captured, a first blood sample of approximately 100 µl was taken in heparinized capillary tubes by puncturing the ulnar vein within 1 min after the bird fell in the net. Time of day at capture was then recorded before putting the bird alone in a standard ringer's cloth bag. Forty minutes after capture, a second blood sample (which has not been used for the purposes of this study) of approximately 90 µl was taken. In this way we standardized the stressful conditions to which males were exposed in captivity before starting a cutaneous test to measure T-cell—mediated immunocompetence.
The right wing web was injected with 0.2 mg of PHA in 0.04 ml of
phosphate-buffered saline (PBS), the left wing web was injected with the same
volume of PBS, and the birds were then released. The next morning, we tried to
recapture as many of the injected birds as possible and measured the thickness
of both wing webs again. Measures of wing web thickness were made blind to
brood size manipulation of the particular male under consideration. An index
of intensity of the response to the mitogenic stimulation of T-cells was
estimated as the change in thickness, measured with a pressure-sensitive
micrometer, of the right wing web minus the change in the left wing web
(Lochmiller et al., 1993;
Saino et al. 1997a,
1999;
Sorci et al., 1997). This
immunocompetence test was also performed on a set of males that had just
fledged or were about to fledge the offspring of their unmanipulated broods.
Corticosterone levels were not assayed in these males. However, males with an
unmanipulated brood were subjected to one blood sampling immediately after
capture and restrained for approximately the same time as males with enlarged
or reduced broods. Hence, male parents of unmanipulated broods experienced a
similar level of stress as males of the other groups.
Thus, corticosterone plasma concentration for the purposes of the present study was assessed in males of two groups (brood enlargement or reduction), and T-cell—mediated immune response was measured in males of three groups (brood enlargement, reduction, or no manipulation). Corticosterone levels were loge-transformed to achieve normality. Variances of corticosterone plasma levels and index of T-cell—mediated immune response were homogeneous among experimental groups of males according to Bartlett-Box F tests (p >.05).
We assayed corticosterone concentration in the plasma by using a 125I radioimmunoassay kit purchased from ICN Biochemical (Costa Mesa, California). Samples were processed in four different assays, and individuals were assigned randomly to assays. We assessed intra- and interassay variation in corticosterone concentration estimates by including in each assay three samples for each of two different pools of plasma taken from barn swallows in the same colonies and dates of the individuals considered in the study. Mean estimated concentration in the two pools (A and B) were 19.33 and 28.55 ng/ml, respectively. Mean within-pool coefficient of variation in estimated concentration was 2.39% (pool A) and 1.35% (pool B). Interassay coefficient of variation was 8.17% for pool A and 6.23% for pool B.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Corticosterone plasma concentration of males in relation to brood size manipulation and secondary sexual characters
Corticosterone plasma concentration at the end of the parental period did not differ significantly between males with reduced and enlarged broods [mean (SE) for males with reduced broods: 21.49 (3.01) ng/ml; enlarged broods: 26.22 (3.78); t test on loge-transformed values, t = 0.77, df = 43, p =.45)]. Corticosterone concentration covaried negatively with tail length of males while controlling for the effect of brood size manipulation in an ANCOVA (effect of brood size manipulation: F1,42 = 1.25, p =.27; tail length: F1,42 = 4.78, p =.034, slope = -0.028; Figure 1). When we included the interaction term, we found no significant effect (F1,41 = 0.02, p =.89). These results were qualitatively confirmed when we controlled for the effects of time of day, calendar date, and deviation from fledging date (analyses not shown).
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Immunocompetence in relation to brood size manipulation and male tail
length
Lymphoproliferative challenge with the mitogenic PHA revealed that males
with reduced broods responded more intensely than those with an unmanipulated
or enlarged broods, and the latter groups were similar in intensity of
response (ANOVA; F2,32 = 4.07, p =.027;
Figure 2).
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In an analysis of covariance, intensity of response to PHA positively covaried with male tail length (effect of brood size manipulation: F2,31 = 4.45, p =.020; tail length: F1,31 = 6.88, p =.013; Figure 3). These results were confirmed when we controlled for the effects of time of day, calendar date, and deviation from fledging date (analyses not shown).
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Finally, ANCOVAs testing for an effect of corticosterone concentration on response to PHA while controlling for potentially confounding variables indicated that wing web swelling did not significantly covary with corticosterone concentration when the effect of brood size manipulation was taken into account (effect of corticosterone concentration: F1,19 = 0.61, p =.45). Hence, no detectable effect of corticosterone profile on response to PHA existed.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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We observed an increase of a particular component of immunity as a consequence of an experimental reduction of brood size. Previous brood size manipulations in the same study area showed that males with reduced broods have lower feeding rates of nestlings compared to males with enlarged broods, indicating that reduction of brood size resulted in smaller paternal workload of male barn swallows (see Methods; Saino et al., 1997a
). The demonstration that males with reduced broods
had a stronger response of T-lymphocytes to a mitogenic stimulus implies that
an important component of their acquired immune function was enhanced
(Pastoret et al., 1998;
Roitt et al., 1996;
Wakelin, 1996). These results
are consistent with those of recent studies on birds. For example,
manipulation of brood size in the pied flycatcher (Ficedula
hypoleuca) had the same effect on response to PHA as that observed in the
present study (Moreno et al.,
1999). Experimental increase of parental effort has also been
shown to depress humoral response against immunogens such as sheep red blood
cells in zebra finches (Taeniopygia guttata;
Deerenberg et al., 1997) or the
vaccine against the virus that causes Newcastle disease in the collared
flycatcher (Ficedula albicollis;
Nordling et al., 1998). Hence,
our results lend support to the idea that working hard at parental activities
has a cost in terms of another important life-history trait, immune defense
against pathogens. Brood size manipulation had no effect on concentration of the glucocorticosteroid corticosterone, which is considered one of the principal mediators of the adrenocortical response to stress in vertebrates. Hence, a prolonged (chronic) stress did not apparently alter corticosterone plasma levels of males, thus contradicting our prediction.
Was the positive effect of brood reduction on the ability to raise a T-cell response under mitogenic stimulation mediated by an effect on corticosterone plasma levels of males? This mechanism of immune depression under stress is explicitly invoked by the avoidance of immunopathology hypothesis, which posits that the adaptive function of elevated levels of circulating glucocorticosteroids under stress is to depress the immune system. However, we found no evidence that response to PHA injection was affected by corticosterone levels.
Immune processes are strongly dependent on nutritional condition as
affected by both energy content of food and availability of particular dietary
components (e.g., amino acids; Chandra and
Newberne, 1977; Dietert and
Golemboski, 1994; Gershwin et
al., 1985; Lochmiller et al.,
1993; Tsiagbe et al.,
1987). The resource limitation hypothesis envisages depression of
immune function as a consequence of limited availability of resources critical
to both immunity and physical performance (i.e., parental workload).
Present findings are compatible with the general idea of depression of
immune function ensuing because of reallocation of critical resources to
competing activities, although the physiological mechanisms mediating such a
trade-off still remain obscure. As far as we are aware, no specific endocrine
or neurological mechanisms mediating this trade-off have been proposed,
although one potentially effective mechanism could be mediated by
corticosterone, which would elicit gluconeogenesis from proteins and fats (see
Wingfield, 1994). Critical
resources might thus be allocated to reconstitution of tissues affected by
gluconeogenesis and subtracted from immunity.
A general proposition of current models of sexual selection is that male
ornamental traits subjected to sexual selection are reliable signals of male
genetic quality (Heywood,
1989; Iwasa et al.,
1991; Møller et al.,
1998b; Pomiankowski et al.,
1991). In particular, parasite-mediated models of sexual selection
suggest that condition-dependent male ornamental traits signal freedom from
parasites (see Andersson, 1994;
Hamilton and Zuk, 1982).
Because immunity is one of the main mechanisms mediating host defense against
parasites, we predicted that male barn swallows with a long ornamental tail, a
trait currently under intense sexual selection (Møller,
1988,
1994,
Saino et al., 1997b), should
exhibit a large response to PHA inoculation. This prediction was confirmed, as
intensity of response to PHA was larger in long-tailed compared to
short-tailed males after controlling for the effect of brood size
manipulation. These results are consistent with a recent study on the red
jungle fowl (Gallus gallus; Zuk
and Johnsen, 1998), where wing web swelling in response to PHA
inoculation positively correlated with size of the sexually selected male
combs. However, a negative relationship was found between response to PHA
during the breeding season and size of the bib of black feathers of male house
sparrows (Passer domesticus), a secondary sexual character under
directional female preference (see
Gonzalez et al., 1999; but see
also Griffith et al.,
1999).
Long-tailed males had lower corticosterone plasma concentration compared to
short-tailed males. This might be due to a relatively low susceptibility of
long-tailed males to stress of parental activities, which might provide a
physiological basis for the positive association between viability and feather
ornamentation documented for the barn swallow (e.g.,
Møller, 1994;
Saino et al., 1999).
In conclusion, we showed that a smaller effort in parental activities ultimately results in a beneficial effect to one particular aspect of immune function of male barn swallows, but we could find no evidence that this effect was mediated by corticosterone plasma levels. These results can be reconciled with the idea of a nutritional trade-off between parental effort and immunity based on limiting resources necessary for both processes. Males of high phenotypic quality had relatively large immunocompetence, as predicted by parasite-mediated models of sexual selection, and had lower levels of corticosterone at the end of the parental period compared to low-quality males, suggesting that susceptibility to stress and immune response may be revealed by male secondary sexual characters subject to female preference.
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ACKNOWLEDGEMENTS |
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We are grateful to Stefano Calza and several students for assisting during field work. We are also indebted with Emilio Bombardieri for lab facilities and Adalberto Cavalleri for running corticosterone analyses. This study was supported by Italian Consiglio Nazionale delle Ricerche and Ministero dell'Università e della Ricerca Scientifica e Tecnologica grants to N.S. and a grant from CNRS (Atipe Blanche) to A.P.M.
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