Behavioral Ecology Vol. 13 No. 2: 248-253
© 2002 International Society for Behavioral Ecology
Condition dependence, multiple sexual signals, and immunocompetence in peacocks
a Laboratoire d'Ecologie Evolutive Parasitaire, CNRS UMR 7103, Université Pierre et Marie Curie, Bât. A, 7ème étage, 7 quai St. Bernard, Case 237, F-75252 Paris Cedex 05, France b Evolution and Behaviour Research Group, Department of Psychology, University of Newcastle, UK
Address correspondence to A.P. Møller. E-mail: amoller{at}hall.snv.jussieu.fr .
Received 17 July 2000; revised 22 May 2001; accepted 25 May 2001.
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ABSTRACT |
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Condition-dependent expression of secondary sexual characters and measures of immune function in a cohort of similarly aged male blue peafowl Pavo cristatus was used to test whether different sexual signals provide information about different aspects of phenotypic quality. A measure of cell-mediated immunity and the heterophil—lymphocyte ratio demonstrated condition dependence, but a measure of humoral immunity was not condition dependent. Only train length demonstrated condition-dependent expression, while the number and the size of ocelli in the train did not show significant condition dependence. Although residual train length (after controlling for the number and the size of ocelli in the train) reliably reflected the magnitude of two condition-dependent measures of immunocompetence (positively with cell-mediated immunity and negatively with humoral immunity), residual size of ocelli was negatively related to cell-mediated immunity. Different features of the complex train were related in different ways to measures of immunocompetence.
Key words: cell-mediated immunity, humoral immunity, multiple ornaments, Pavo cristatus, sexual selection.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Many secondary sexual characters demonstrate condition dependence because only males in prime condition are able to develop the most exaggerated ornamentation (Andersson, 1994
). Such condition dependence of sexual signals may reveal
either direct, material or indirect genetic benefits to females
(Andersson, 1994).
Condition-dependent expression of secondary sexual characters may reflect
either general condition (Andersson,
1986) or an ability to cope with debilitating parasites
(Hamilton and Zuk, 1982). Only
hosts that are resistant to virulent parasites will be able to develop extreme
ornamentation.
Although parasite-mediated sexual selection, and in particular good genes
versions of this hypothesis, has been subject to intense scientific enquiry
during recent years, there is only relatively weak overall evidence in favor
of the hypothesis (review in Møller
et al., 1999). A major reason for this conclusion appears to be
that many parasites investigated with respect to the hypothesis have no
consequences or very weak fitness consequences for their hosts. A recent
emphasis on host antiparasite defenses such as the ability to raise an immune
response provides much stronger support for the hypothesis that hostparasite
interactions play an important role in sexual selection (review in
Møller et al., 1999).
Immune function often demonstrates strong condition dependence, with only
individuals in prime condition being able to produce strong immune responses
(reviews in Chandra and Newberne,
1977; Gershwin et al.,
1985; Møller et al.,
1998a). If both secondary sexual characters and immunocompetence
are condition dependent, it seem likely that the two types of traits should
demonstrate positive covariation.
Most animals use multiple signals in sexual communication. The reason for
such complexity of signals remains far from clear. Møller and
Pomiankowski (1993) reviewed a
number of alternative explanations for the evolution of such multiple signals.
These include (1) the multiple message hypothesis, which suggests that each
different component of a signal reflects different aspects of the overall
quality of an individual; (2) the redundant signal hypothesis, which posits
that each ornament gives a partial indication of condition; and (3) the
unreliable signal hypothesis, which states that some ornaments are unreliable
indicators of overall condition but can be maintained because they are not
costly and subject to weak female mate preferences. Comparative evidence from
feather ornaments is consistent with the latter hypothesis
(Møller and Pomiankowski,
1993).
Studies of mallards Anas platyrhynchos and jungle fowl Gallus
gallus both suggest that only some of the multiple ornaments in these
species are used by females in mate choice
(Omland, 1996; Zuk et al.,
1990a,
b,
1992). A study of the barn
swallow Hirundo rustica revealed positive phenotypic correlations
between ornaments, and females used both a feather ornament and song rate as
cues to their choice of their mate relative to extrapair males as sires for
their offspring (Møller et al.,
1998b). There are only two previous studies of immune function and
multiple signals. Saino et al.
(1999) reported that tail
length and red coloration, which both are sexually dimorphic, reflected immune
status of male barn swallows. Here we present the results of extensive
analyses of multiple signals and multiple components of immune function in a
single species.
The aims of the present study were to assess whether different aspects of a
complex secondary sexual character reflect different aspects of phenotypic
quality, using male blue peafowl Pavo cristatus as a study organism.
Peacocks develop an extravagant feather display during the breeding season,
including an exaggerated train with feathers containing ocelli; an iridescent
blue ventral color; an iridescent green dorsal color; an exaggerated crest;
bare, white facial skin patches; long spurs; and several other features.
Females of this lekking species are known to prefer males with a larger number
of symmetrically positioned ocelli in the train, as demonstrated by several
observational and experimental studies
(Hasegawa, 1995;
Petrie et al., 1991;
Petrie and Halliday, 1994;
Yasmin and Yahya, 1996). Males
show considerable variation in train elaboration independent of age
(Petrie, 1993). In this study,
we assessed condition dependence of three components of the elaborate train
and three measures of immunocompetence of a cohort of similarly aged males.
Furthermore, we determined to which extent different aspects of the train
reflected different components of immunocompetence.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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We studied male blue peafowl at a commercial farm. Males of 2 years of age were housed together in large outdoor pens, where they were provided with shelter and provided with water and commercial poultry feed ad libitum. Two-year-old males are able to reproduce. The feed had a protein content of 18%. Animals had free access to invertebrates in the soil and to green vegetation.
We captured 30 males on 10 April 1997 at the start of the breeding season when males were regularly seen displaying their upper tail coverts. Upon capture we measured the combined length of the tarsus, central toe, and claw to the nearest millimeter using a ruler, as a measure of skeletal body size. Body mass was measured on a balance to the nearest 100 g. We assessed the train ornament in three different ways: (1) the length of the longest feather recorded with a measuring tape to the nearest millimeter; (2) the number of ocelli in the train; and (3) the mean diameter of 10 randomly chosen ocelli measured to the nearest 0.1 mm with a caliper. If males had less than 10 ocelli, we measured the number available. Males were penned overnight to facilitate recapture after 24 h for the measure of cell-mediated immunity. Males were recaptured after 2 weeks for a second blood sample. All handling, blood sampling, and immunocompetence testing were done with a permit from under home office license (project license PPL 60/2065).
For each individual we took a blood sample in two capillary tubes after puncturing the ulnar vein. Blood was stored in a cool bag with frozen cooling blocks in the field (for a maximum of 30 min) before being stored in a refrigerator. Blood samples were then centrifuged for 10 min at 11,500 rpm, and hematocrit was measured with a digital caliper to the nearest 0.1%. Plasma was subsequently stored at -20°C.
Experienced personnel counted leukocytes and erythrocytes on blood smears
that had been air dried, fixed in methanol, and stained by the
May-Grunwald-Giemsa method. Blood smears were scanned at 630x
magnification following standard routines. In each microscopic field we
counted red blood cells and leukocytes classified as lymphocytes, monocytes,
eosinophils, heterophils, and basophils—in total 95-160 leukocytes. The
number of each leukocyte type per 10,000 erythrocytes was multiplied with the
hematocrit to obtain a concentration of leukocyte types. These measurements
are all highly repeatable within samples (see also
Ots et al., 1998;
Saino et al., 1995). Because
the phytohemagglutinin and sheep red blood cell challenge tests may directly
affect the amount of circulating lymphocytes, we based our analyses on
heterophil-lymhocyte ratios obtained before challenging the immune system.
We estimated three components of immunocompetence: a measure of T-cell
response, a measure of T- and B-cell response, and the
heterophil—lymphocyte ratio
(National Research Council,
1992). We assessed T-lymphocyte immune responsiveness using
injection with phytohemagglutinin (PHA), which is a standard method to assess
cell-mediated immunity in poultry (Cheng
and Lamont, 1988). The thickness of the left and right wing webs
(patagium) of peacocks at premarked sites was measured by a pressure-sensitive
caliper, a spessimeter (Alpa S.p.A., Milano, cod. SM112), to the nearest 0.01
mm. To avoid any problems of decline in wing web thickness during subsequent
measurements due to repeated pressure on the soft tissue, we removed the
spring from the spessimeter and replaced its pressure with that from a 16-g
weight placed on top of the instrument. The right wing web was injected with
0.2 mg of PHA (Sigma, L-8754) in 0.04 ml of phosphate-buffered saline (PBS).
The left wing web was injected with 0.04 ml PBS only. Twenty-four hours later
we re-measured the thickness of wing webs at the inoculation sites. The
measure of immune response is simply the difference in wing web thickness
between day 2 and day 1 for the PHA-inoculated wing minus the difference in
wing web thickness between day 2 and day 1 for the PBS-inoculated wing (see
Saino et al., 1997b, for
details). This difference in skin thickness is highly repeatable among
repeated measurements of the same individual (R =.80, F =
8.78, df = 28,29, p <.0001). The PHA response that we measured is
a primary immune response that is considerably weaker than the secondary
response (Roitt et al., 1996);
however, it still significantly explains considerable amounts of individual
variation in survival prospects (Christe et al.
1998,
2001;
González et al., 1999;
Hörak et al., 1999;
Saino et al., 1997a;
Soler et al., 1999). Given
that the secondary response is stronger than the primary response, we did not
subject peacocks to a second challenge for ethical reasons.
Humoral immunity was assessed from antibody response to a single injection
with heterologous erythrocytes (Roitt et
al., 1996). We injected peacocks intraperitoneally with 0.5 ml of
a 5% solution of sheep red blood cells (SRBC) after the first blood samples
had been taken. A second blood sample was obtained after 14 days, the
capillaries were centrifuged as described above, and the plasma was separated
from the red blood cells after measurement of hematocrit and the buffy coat
(the layer of leukocytes and fibrinogen separating plasma and erythrocytes).
Hemagglutinating antibody titers were estimated by the micro-hemagglutination
assay (Wegmann and Smithies,
1966). This method consists of serial twofold dilutions of
heat-inactivated serum (56°C for 30 min.) in PBS mixed with an equal
volume of a 1% SRBC solution (in PBS) and incubated at 40°C for 1 h.
Titers were expressed as the log2 of the reciprocal of the highest
dilution of serum showing positive hemagglutination. The results of the
hemagglutination test of multiple samples from the same individual were
significantly repeatable at 0.80 (F = 8.78, df = 14,15, p
<.0001). We measured the primary SRBC response, which is considerably
weaker than the secondary response (Roitt
et al., 1996); however, it still significantly explains
considerable amounts of individual variation in survival prospects
(Saino et al., 1997a). Again,
we did not subject peacocks to a second challenge for ethical reasons. We
calculated the repeatability of the hematological and immunological variables
between the two sampling events, but only for variables that could be assessed
on both occasions (i.e., challenge tests were not included because only a
single response was measured).
We measured three components of the exaggerated train ornament, but because these components were positively correlated, we estimated residual ornament size for each variable by calculating the residuals from a multiple regression with the variable of interest as the dependent variable and the two other variables as independent variables. However, five males had no ocelli in their trains, and these males were excluded from all analyses of diameter of ocelli.
Body condition was estimated as residual body mass from a regression of body mass on the combined length of tarsus, toe, and claw because these residuals reflect relative body mass corrected for differences in structural body size (the combined length of tarsus, toe, and claw). This regression was positive and statistically significant [F = 8.30, df = 1,28, r2 =.23, slope = 12.64 (4.39), p =.0075].
We tested variables for normality using Lilliefors' test, and since no
significant deviations were found, we used parametric tests throughout. A
large number of statistical tests were made, and the overall level of
significance was Bonferroni adjusted for multiple tests to control the type I
error rate (Holm, 1979;
Wright, 1992). Strict
application of this method severely reduces the power of statistical tests
(Wright, 1992), but such
sacrificial loss of power can be avoided by choosing an experimentwise error
rate higher than the usually accepted 5%. We used 10% as suggested by Wright
(1992) and Chandler
(1995). Values are presented as
means with standard errors in parentheses. All tests were two-tailed.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Condition dependence of secondary sexual characters and immune variables
Mean values and coefficients of variation of ornament and immune function variables are reported in Table 1. All variables demonstrated a high level of phenotypic variation, ranging from 24% to 84% for the train variables and from 29% to 73% for the immunological and hematological variables, with the exception of hematocrit, which had a low coefficient of variation of 9%.
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The three components of immunocompetence that were estimated were significantly correlated with each other. The heterophil—lymphocyte ratio was significantly negatively related to humoral immunity estimated from the SRBC injections (Table 2) but was positively related to cell-mediated immunity estimated from the PHA injection (Table 2). Humoral and cell-mediated immunity were not significantly related to each other (Table 2). Although PHA response was weakly, but significantly positively related to combined tarsus, toe, and claw length [F = 4.16, df = 1,28, r2 = 0.07, slope = 0.016 (0.008), p =.046], this was not the case for heterophil—lymphocyte ratio or SRBC response (F < 0.33, df = 1,28, r2 <.01, p >.57). Residual PHA response after controlling for the combined length of tarsus, toe, and claw was significantly negatively related to the SRBC response [F = 6.23, df = 1,28, r2 =.187, slope = -2.6017 (1.044), p =.019]. The heterophil—lymphocyte ratio was significantly positively related to residual PHA response [F = 4.75, df = 1,28, r2 =.15, slope = 1.007 (0.462), p =.038].
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The three measures of the train were positively related to each other. This was the case for train length and number of ocelli [F = 30.80, df = 1,28, r2 =.52, slope = 0.37 (0.07), p <.0001], train length and mean diameter of ocelli [F = 26.97, df = 1,23, r2 =.49, slope = 1.67 (0.32), p <.0001], and number and mean diameter of ocelli [F = 32.80, df = 1,23, r2 =.60, slope = 0.18 (0.03), p <.0001].
We investigated condition dependence of secondary sexual characters and the immune response variables using residual body mass as an estimate of body condition. Of the train descriptors, only residual train length was positively related to body condition [Figure 1a; F = 8.96, df = 1,28, r2 = 0.24, slope = 25.35 (8.47), p =.0057], while the relationships for the two other characters were weak and far from statistical significance (residual number of ocelli: F = 0.38, df = 1,28, r2 =.01, p =.54; residual diameter of ocelli: F = 1.36, df = 1,23, r2 =.06, p =.26).
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The repeatability of hematological and immunological variables between the two sampling events are reported in Table 1. The concentration of monocytes, heterophils, eosinophils, and the hematocrit demonstrated statistically significant repeatability. SRBC and PHA were only estimated once for each individual. This suggests that these variables at least remain similarly ranked among individuals, despite the fact that the immune system was challenged by SRBC.
Several of the immunocompetence and hematological variables showed evidence of condition dependence. Phytohemagglutinin response was significantly positively related to body condition [Figure 1b; F = 5.35, df = 1,28, r2 =.16, slope = 0.75 (0.32), p =.028]. The heterophil—lymphocyte ratio was also positively related to body condition [F = 6.67, df = 1,28, r2 =.19, slope = 1.93 (0.75), p =.015], whereas the SRBC response was not significantly associated with body condition (F = 2.64, df = 1,28, p =.12). Among the hematological variables, hematocrit was positively related to condition [F = 5.94, df = 1,28, r2 =.18, slope = 8.46 (3.47), p =.021], but the size of the buffy coat was negatively related to condition [F = 4.87, df = 1,28, r2 =.15, slope = -1.25 (0.57), p =.036]. The latter relationship is as predicted because individuals in prime condition should have small amounts of circulating leukocytes. After adjusting for multiple tests, only the relationship for heterophil—lymphocyte ratio remained statistically significant.
Sexual ornamentation and immune function
We investigated whether components of the sexual ornament reflected
immunocompetence by means of regression analysis. The PHA response was
predicted by train length [F = 8.85, df = 1,28,
r2 =.24, slope = 0.011 (0.004), p =.006]. The
heterophil—lymphocyte ratio was significantly predicted by train length
[F = 10.82, df = 1,28, r2 =.28, slope = 0.030
(0.009), p =.0027]. The estimate of humoral immunity was
significantly negatively related to train length (F = 6.86, df =
1,28, r2 =.20, slope = -0.058 (0.022), p =.014].
These relationships remained significant after adjusting for multiple
tests.
Any correlation between train variables and immunocompetence does not take
partial correlations with other train variables into account, so we used
residual train values for subsequent analyses because these values would
reflect the independent effect of each variable after taking the other two
variables into account (cf. Arnold and
Wade, 1984). Residual train length predicted cell-mediated
immunity as estimated by the PHA response
[Figure 2a; F = 22.55,
df = 1,23, r2 = 0.50, slope = 0.023 (0.005), p
<.0001]. This was also the case for residual PHA response after controlling
for body condition [F = 22.63, df = 1,23, r2
=.50, slope = 0.022 (0.005), p <.0011]. The
heterophil—lymphocyte ratio was not significantly related to residual
train length [F = 1.12, df = 1,23, r2 = 0.05,
slope = 0.017 (0.016), p =.30], whereas humoral immunity as estimated
from the SRBC test was negatively related to residual train length
[Figure 2b; F = 9.40,
df = 1,23, r2 =.28, slope = -0.11 (0.03), p
=.0023]. These relationships remained statistically significant after
adjusting for multiple tests.
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The residual number of ocelli was not significantly related to humoral immunity, as shown by response to SRBC [F = 2.48, df = 1,23, r2 = 0.10, slope = 0.036 (0.023), p =.13], and the two other regressions were far from statistically significant (PHA: F = 0.58, df = 1,23, r2 =.02, p =.46; heterophil—lymphocyte ratio: F = 1.42, df = 1,23, r2 =.06, p =.25).
For residual diameter of ocelli, there was a negative relationships with residual PHA response before and after controlling for the effect of body condition [Figure 2c; F = 7.21, df = 1,23, r2 =.24, slope = -0.043 (0.016), p =.013; F = 9.17, df = 1,23, r2 =.29, slope = -6.353 (2.107), p =.006], but the other two regressions were weak and nonsignificant (F < 0.68, df = 1,23, p >.42). The relationship for PHA remained significant after adjusting for multiple tests.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Of the three different aspects of ornamentation of peacocks, only train length demonstrated condition-dependent expression (Figure 1a); the number and the size of ocelli were not significantly related to body condition. Cell-mediated immunity and the heterophil—lymphocyte ratio showed condition dependence, but this was not the case for the estimate of humoral immunity. These findings are consistent with previous evidence from the poultry literature and the literature on wild birds showing condition-dependent expression of cell-mediated immunity, but little or no evidence of humoral immunity being affected by body condition or feed quality (Glick et al., 1981
,
1983;
Klasing, 1988;
Lochmiller et al., 1993;
Tsiagbe et al., 1983). Similarly, the relationship between
heterophil—lymphocyte ratio and condition is well substantiated in the
literature (Dein, 1986;
Gross and Siegel, 1983). The
significantly negative relationship between cell-mediated and humoral immunity
is consistent with a trade-off between the two arms of the immune system. Such
a trade-off may be more evident when individuals live in stressful
environments with frequent social interactions because stress may affect
immune function (Apanius, 1998;
Friedman et al., 1996;
Ottaviani and Franceschi,
1996). This might also have been the case in the present study,
although we did not directly quantify this effect. Johnsen and Zuk
(1999) have reported a
negative correlation between PHA response and immunoglobulins, consistent with
a trade-off between the two arms of immune function. However, alternative
interpretations cannot be excluded without direct manipulation of either (or
both) of these components of the immune system.
Peacocks have multiple ornaments, such as an exaggerated train with
feathers containing ocelli; an iridescent blue ventral color; an iridescent
green dorsal color; an exaggerated crest; bare, white facial skin patches; and
long spurs. Here we investigated only three components for logistic reasons.
These three components were positively correlated, but still only one, train
length, demonstrated condition dependence. In an investigation of the
relationship between residual train parameters and the three measures of
immunocompetence, we found that train length was significantly positively
related to cell-mediated immune response and negatively related to humoral
immunity. The number of ocelli was not significantly related to the measures
of immunocompetence, but the size of the ocelli was significantly negatively
related to cell-mediated immunity. Thus, the immune variables were
significantly related to different components of the train. These findings are
most consistent with the multiple message hypothesis, which suggests that
different parts of a multiple ornament signal different aspects of general
quality (Møller and Pomiankowski,
1993). This appeared to be the case because train length reflected
cell-mediated and humoral immunity, whereas the size of ocelli reflected
cell-mediated immunity. Female peafowl are known to use the number of ocelli
in their mate choice (Petrie et al.,
1991; Petrie and Halliday,
1994; Yasmin and Yahya,
1996), but it remains unknown whether train length or size of
ocelli are important in mate choice. However, choosy females will trade
genetic fitness benefits from their mate choice in terms of cell-mediated
immunity against benefits in terms of humoral immunity. A large number of
studies have considered to which extent secondary sexual characters reliably
reflect parasite load or immune function of individual males (review in
Møller et al., 1999).
Saino et al. (1999) reported
that both tail length and red coloration reflected immune status in male barn
swallows.
In conclusion, components of immunocompetence and sexual ornamentation were condition dependent, and different features of the complex train of the peacock were related to different aspects of immunocompetence, but other features were unrelated to measures of immune function.
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ACKNOWLEDGEMENTS |
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C. Haussy kindly made the sheep red blood cell tests. Q. Spratt provided excellent care for the peacocks. D. Maisey helped to catch and hold the birds. A.P.M. was funded by an ATIPE BLANCHE from CNRS.
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