Behavioral Ecology Vol. 11 No. 2: 146-153
© 2000 International Society for Behavioral Ecology
Social environment and immunity in male red jungle fowl
Department of Biology, University of California, Riverside, CA 92521, USA
Address correspondence to M. Zuk. E-mail: mzuk{at}citrus.ucr.edu .
Received 18 May 1999; accepted 28 July 1999.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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We examined the relationship between social dominance, immune response, and ornamentation in captive red jungle fowl by comparing these variables in males housed individually with a single female to those in the same males after they were placed in flocks with an unfamiliar male and three unfamiliar females. Males with larger combs before being placed in the flocks were more likely to become dominant, and dominant males' combs grew after flock formation, whereas subordinate males' combs shrank. Immune response as reflected in hematocrit, immunoglobulin levels, and wing web swelling (a measure of cell-mediated immunity) was stronger in males that later became dominant, both before and after flock formation, although the difference between dominant and subordinate birds was more pronounced after males were housed in the multi-male groups. Dominant and subordinate males also differed in the relationship between comb length and wing web swelling. Among dominant males, individuals with larger combs had significantly larger swellings after flock formation, whereas within the subordinate males, those with relatively larger combs had worse cell-mediated immunity than those with smaller combs. These results suggest that males of different quality pay different costs to maintain both ornamentation and immune defense.
Key words: dominance, Gallus gallus, immune response, ornamentation, red jungle fowl.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The social environment has a profound effect on many aspects of an animal's biology. Dominance status, for example, can influence access to food, mating success, and fecundity, all of which in turn may be important determinants of fitness. The social environment can also affect an animal's internal state: physiological variables such as hormone profiles and growth or maturation rates may potentially be modified in response to the presence of conspecifics. Disease resistance has been a recent focus of the effect of social interactions on individuals; the ability to fend off parasites and pathogens is likely to be important for most organisms at some point in their lives, and the role of parasite resistance in host behavioral ecology has been increasingly recognized over the last decade (Folstad and Karter, 1992
;
Sheldon and Verhulst, 1996;
Zuk, 1994). In some species,
social rank may change susceptibility to disease, and parental effort involved
in feeding offspring may also limit an animal's ability to fight off pathogens
(Barnard et al., 1993;
Gustafsson et al., 1994;
Richner et al., 1995).
Studies of this interaction between social behavior and disease resistance
have generally taken one of two approaches. First, several researchers have
examined immune suppression or vulnerability to parasite infection as one of
the factors mediating the cost of reproduction
(Gustafsson et al., 1994;
Nordling et al., 1998;
Richner et al., 1995). This
life-history approach looks for a trade-off between reproductive effort and
immune function, so that animals investing heavily in producing young may
become more vulnerable to disease. Experimental manipulation of parental
effort or brood size in collared flycatchers (Ficedula albicollis),
zebra finches (Taeniopygia guttata), and great tits (Parus
major) showed that birds forced to work harder either had a decreased
ability to respond to an immune system challenge (flycatchers,
Nordling et al., 1998; zebra
finches, Deerenberg, 1996) or
developed higher levels of avian malaria (tits:
Nordling et al., 1998;
Richner et al., 1995). This
response is consistent with the idea that individuals cannot maximize both
immune defense and parental effort and suggests that at least in the short
term animals must pay a price for increasing their offspring production and
that such trade-offs are potentially important in evolution. Svensson and
Sheldon (1998) point out that
placing these life-history studies in a social context, such as that of sexual
selection or dominance, is potentially fruitful.
A second approach is more physiologically based and examines the immediate
effect and proximate causes of changes in disease resistance when animals are
under different social conditions, such as changes in dominance status or
stress. A variety of laboratory and field studies have determined that
acquiring or maintaining dominance is stressful and that immune competence
declines under such stressful conditions
(Barnard et al., 1998;
Fox et al., 1997;
Sapolsky et al., 1997;
Tuchscherer et al. 1998). In
particular, low-ranking individuals in mammals such as laboratory mice
(Mus musculus) and baboons (Papio anubis) appear to have
higher levels of stressrelated hormones that may make them more vulnerable to
disease (Barnard et al., 1998;
Sapolsky and Spencer, 1997).
The picture is complex; dominant and subordinate animals may differ not simply
in their stress hormone levels but in the modulation of those hormones
(Barnard et al., 1998), and the
relationship between dominance and stress can be seasonal
(Kotrschal et al., 1998). In
addition, a few field studies have contradicted the generally inverse
relationship between dominance and stress, perhaps because animals measured in
the field are under different constraints than those measured in captivity
(Creel et al., 1996). In any
case, the literature on psychoneuro-immunology in both humans and nonhumans
underlines a strong connection between the social experiences of an individual
and its ability to resist disease (Ader et
al., 1991; Blanchard et al.,
1993).
Here we attempt to bring these two approaches together by examining the
consequences of changes in social environment for immune defense in male red
jungle fowl (Gallus gallus) and placing the individual-level results
in an evolutionary context. We were particularly interested to see how
dominant and subordinate individuals responded to changes in their social
situation because, although a trade-off between investment in immune defense
and reproductive behavior is expected, it may take place differently in
individuals of different quality. High quality may be considered as roughly
equivalent to high fitness, as reflected in traits such as immunocompetence as
well as mating success. Although within a given individual immune defense is
decreased when reproductive effort is increased and vice versa, high-quality
individuals may perform this trade-off differently because they have more
resources overall to allocate to either task. Conversely, low-quality
individuals may simply have poorer immune responses and poorer ability to
perform reproductive behaviors. Variation in these individual-level responses
has important implications for the way in which natural selection acts on life
history (Roff, 1992;
van Noordwijk and de Jong,
1986).
Previous work on immunity and sexual selection in red jungle fowl has
revealed a connection between sexually selected ornaments and immune status
(Zuk and Johnsen, 1998;
Zuk et al., 1995). During the
breeding season, males with large combs, a trait important in both mate choice
and male competition, have lower levels of lymphocytes but greater
cell-mediated immunity, as indicated by a cutaneous hypersensitivity response
(Zuk and Johnsen, 1998).
Before the breeding season, however, both cell-mediated immunity and
proportion of lymphocytes are positively correlated with comb length. These
results suggest that males may not all show the same patterns of allocation to
ornamentation and immune defense, displaying an immunocompetence handicap
(Folstad and Karter, 1992).
Other ornaments used by females in mate choice, such as comb color and eye
color, also appear to reflect immune status
(Zuk et al., 1995).
In this study we assessed immunity in the context of behavior by examining
how immune response changes when males are placed in social groups with
another male and three females after having been housed in male-female pairs.
In the wild as well as in free-ranging captive populations, jungle fowl live
in flocks consisting of a dominant male, one or a few subordinate males, and a
number of females (Collias and Collias,
1967; Collias et al.,
1966). Dominance interactions are frequent, and social status has
important consequences for both sexes
(Collias et al., 1994;
Zuk et al., 1998). Changing
the social group composition from male-female pairs to multimale groups
therefore alters the competitive environment in a biologically meaningful way.
We were particularly interested in whether males responded differently after
their social environment was changed depending on the dominance status they
attained. Do dominant males pay more or less of a price to maintain
immunocompetence? We also examined the relationships among ornamentation,
dominance status, and immune function. The condition of a male's immune system
obviously cannot be directly detected by another individual, so any response
presumably is mediated by morphology and behavior. Males with longer combs are
preferred as mates and are more likely to win in aggressive encounters
(Ligon et al., 1990;
Zuk et al., 1990), so we
wanted to see if changes in immune status were reflected in comb length or
other ornamental characters.
We measured immunity in several different ways to obtain a more complete
picture of immune competence. First, we measured the hematocrit, the
proportion of red blood cells in the whole blood. Hematocrit often reflects
general health, and in male red jungle fowl it is higher in birds with greater
aerobic capacity, or ability to maintain vigorous exercise
(Chappell et al., 1997).
Second, we examined the agglutination response of the birds to injection of
sheep red blood cells (SRBC), a common immune system stimulant. The
hemagglutination results from a reaction between antibodies formed against the
SRBC and the SRBC themselves, so a higher agglutination score indicates a
higher level of antibody formation. Third, we measured the total amount of
immunoglobulin G (IgG) produced in the blood in response to phytohemagglutinin
and SRBC injections; immunoglobulins are the molecules that are the source of
specific antibodies, and higher levels indicate a more vigorous immune
response. Finally, we measured cell-mediated immunity using a cutaneous
hypersensitivity test.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Origin and maintenance of jungle fowl
Our study population is descended from 150 individuals obtained in 1985-1986 from a free-ranging population at the San Diego Zoo, which imported 30 red jungle fowl from Asia in 1942 (Zuk et al., 1995
). Chicks were hatched in incubators and kept indoors
in brooders for the first 6 weeks of their life. At 6 weeks of age, the chicks
were moved outside and kept in large communal cages in flocks of up to 80
birds. When they were approximately 5 months old, the males began to exhibit
aggression toward each other, and we separated the birds into male-female
pairs and housed them in smaller cages (1 m high, 2 m wide, and 1 m deep). The
birds all received water and commercial poultry feed (18-21% protein) ad
libitum, supplemented with scratch, a mixture of seeds, after they were moved
outside. Individual males could thus see and hear, but not contact, other
males, a treatment which equalizes the perceived dominance of each individual
(Ligon et al., 1990). When the birds reached sexual maturity at 9-11 months of age, they were put into 37 mixed-sex flocks each consisting of two males and three females. The flocks were housed in large group cages (2 m high, 3 m wide, and 6 m deep) with 10 permanent perches to allow subordinates the opportunity to escape when chased by dominant birds. Sample sizes are <37 for some measures either because certain individuals were not measured for some variables on a given day or because a member of the flock died.
Timetable of experiment
We obtained six blood samples from each male, with four taken before the
males were placed in the flocks and two afterward, as
follows:
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The "alone" samples 1-4 in the figures therefore corresponded to those on days 0, 11, 18, and 44, whereas the "flock" samples 1 and 2 were taken on days 56 and 63.
Behavioral observations
To form the mixed-sex flocks, we first placed three females in each cage.
On the next day, we added the two males to each flock and observed them as
they fought for dominance. Male pairs were chosen at random, and none of the
birds in the flock had interacted before. The dominance relationship between
the males in each flock was determined by observing the behavior of the males
immediately after they had been placed in a common cage as well as once the
flocks had been together for several days. In most cases, the males interacted
within seconds of being introduced to the cage. These conflicts ended with one
male persistently chasing and pecking the other male, and we determined that
the winner was dominant and the loser was subordinate. If the aggression
continued until it looked as if the subordinate male could become injured, we
separated the males before this occurred and gathered no data from that flock.
In flocks where the males did not fight, we observed pecks and displacements
between the males, and we determined that the winner in these aggressive
encounters was dominant to the loser in the same manner as Zuk et al.
(1998).
Morphological measurements
We measured tarsus length and comb length to the nearest 0.01 mm using
digital calipers. Mass was recorded to the nearest 0.1g using a digital
scale.
We measured colors of the comb and iris using the Munsell system. Although
we and others have employed a more quantitative technique for color
measurement of feathers using a spectroradiometer
(Zuk and Decruyenaere, 1994),
the eye and comb are virtually impossible to reliably and safely measure using
this device. The Munsell system consists of a series of color chips that give
each color a score for hue (e.g., red or yellow), value (darkness, or amount
of black), and chroma (brightness, or saturation with pigment). For data
analysis, we used the variable that varied most among individuals. This was
hue for iris color and chroma for comb color; for the other scores, most males
had the same iris chroma and value and the same comb hue and chroma. Iris hue
and comb chroma were also the color measures of these traits that were most
likely to be important in mate choice in previous studies
(Zuk et al., 1990).
Immune system assays
We took blood from the alar vein in the wing by inserting a needle into the
vein and drawing blood into a vacutainer containing the anticoagulant lithium
heparin. The blood was stored on ice for up to 3 h before it was centrifuged,
the plasma separated from the hematocrit, and the plasma stored at -20°C.
Later the same day, we brought the birds into the laboratory and took a second
blood sample. We placed the needle in the vein and collected blood in a
capillary tube as it emerged from the needle.
Hematocrit
Blood drawn into a capillary tube was spun at 2000 rpm in a centrifuge for
5 min. We determined the percentage of red blood cells, or hematocrit, in the
capillary tube by measuring the length of the column of red blood cells
relative to the total column of blood.
Hemagglutination assay
We measured the relative concentration of antibodies to SRBC using a
hemagglutination assay (Hudson and Hay,
1989). Briefly, 25 µl of PBS buffer was added to the wells rows
2-11 of a 96-well plate (concave bottom). For each sample, we added 50 µl
plasma to the well in the first row. We prepared a gradual dilution of the
plasma in PBS buffer by transferring 25 µl from the first well into the
second well, mixing the solution in that well before we continued to dilute
the plasma until we discarded the last 25 µl taken from row 10. We then
added 25 µl of SRBC antibody solution to the wells in the twelfth row.
Finally, we added 25 µl of a 10% SRBC solution to all the wells. When
enough antibodies were present in solution, a matrix formed between the
antibodies and the SRBC, preventing the cells from accumulating at the bottom
of the wells. When the concentration of antibodies was low, the blood cells
accumulated at the bottom of the well and could be seen as a well-defined
spot. We scored the plates by determining the lowest concentration of plasma
at which the hemagglutination reaction had not occurred. We then used the
log(2) of the inverse of the concentration in our analysis. This
calculation allowed us to score the plates as 0 if no reaction takes place at
a plasma concentration of 1, 1 at a concentration of 0.5, 2 at a concentration
of 0.25, and so on. This number is the reaction score used in analyses.
Immunoglobulin G
We used a sandwich ELISA assay to measure IgG concentrations in plasma
samples taken from the males after the challenges with phytohemagglutinin and
SRBC. Briefly, chicken anti-IgG (100 µl, 12.5 ng/ml) was allowed to bind to
the walls of Corning 96-well polystyrene flat-bottom plates. Nonbinding
anti-IgG was washed off and further binding to the walls was blocked by
saturating the wells with bovine serum albumin (BSA). Excess BSA was washed
off, and IgG (standard curves and plasma samples) was then added to the wells
and allowed to bind with its antibody. After washing, chicken anti-IgG labeled
with peroxidase (100 µl, 1:4000 dilution) was added to all wells. The wells
were washed to remove unbound anti-IgGx. The addition of
3,3',5,5'-tetramethylbenzidine (TMB) and peroxidase in buffer
produced a color change from clear to blue. The reaction was stopped after 10
min by adding 50 µl 2N sulfuric acid, which also changed the color from
blue to yellow, and light absorption was measured at 450 nm.
The standard curve consisted of a dilution series from 0.01 to 0.0008 mg/ml-1 of chicken IgG, and a duplicate of the curve was added to rows 2 and 11 of each of the 27 plates in the assay. We plotted the log-linear relationship for the standard curve and calculated the least-squares best fit (r ranged from.75 to.97). Rows 1 and 12 and the remaining outer edge of the plates were filled with buffer, both as blanks and to provide a more constant environment for the inner wells on the plate. Plasma samples were diluted by a factor of 1:1000, 1:5000, and 1:50,000, and 100 µl of the solution was added in duplicate in one of the remaining rows. We plotted a least-squares best fit log-linear curve for the plasma samples and calculated light absorption at dilutions of 1:1000 or 1:5000. For most samples, we used the 1:1000 dilution, and we used the 1:5000 when necessary. We calculated IgG concentrations after comparing absorption readings with the standard curve and accounting for the dilution of the sample. Before beginning the assay, we made a pool of plasma and included a subsample on each plate.
Cell-mediated immunity
We evaluated cell-mediated immunity, a generalized shortterm response to
grafts, allergens, and wounds, using a delayed cutaneous hypersensitivity
response (Benjamini and Leskowitz,
1991; Roitt et al.;
1989; Saino et al.,
1997; Sorci et al.,
1997). This response is a measure of T-cell reactivity and is
assessed by subcutaneously injecting an inert protein and measuring the
swelling that occurs within 24 h (Benjamini
and Leskowitz, 1991). The immune system is thus stimulated without
any accompanying pathology. Our procedure is the same as that used in Zuk and
Johnsen (1998) and is adapted
from Parmentier et al. (1993,
1994). The birds were given a
sensitizing injection of 400 µg PHA, suspended in 0.4 ml of PBS,
administered subcutaneously into the abdominal region. The thickness of the
wing web, a thin layer of skin between the radius and humerus, was measured to
the nearest 0.01 mm using digital calipers after placing a metal disc 1 mm
thick and 18 mm in diameter on both sides of the extended wing to standardize
the measurements. For all measurements, we measured the wing web three times
and used the mean in subsequent analyses; as in a study by Sorci et al.
(1997), the measures were
highly repeatable (Zuk and Johnsen,
1998). A week after the sensitizing injection, the wing web was
measured and the birds were injected at the wing web with 0.1 ml of the same
solution, and the wing web measurements were repeated 6 and 24 h after this
injection. Larger localized swelling indicates a more robust immune
response.
Data analysis
All data were analyzed using SAS version 6.12 for personal computer. To
compare overall immune response in dominant and subordinate birds, we used
canonical discriminant analysis. This multivariate technique uses several
characters simultaneously to determine if group membership (i.e., whether a
bird is dominant or subordinate) can be successfully predicted
(Tabachnik and Fidell,
1983).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Ornaments, body size, and dominance status
At male-female pair formation, before the flocks were formed, males that later became dominant had significantly larger combs than males that became subordinate (Figure 1; Student's t = 2.764, n = 37 in each group, p =.007). The mean difference between birds that eventually were paired was 4.97 mm, with a range of -30.63 to 27.66 mm. At 17 days after flock formation, this difference was even more pronounced (Figure 1; t = 4.351, n = 27 in each group, p =.0001). The mean difference between dominant and subordinate birds was 5.75 mm; in 24 of 36 pairs, the dominant bird had the larger comb. In addition, comb size increased significantly in dominant males after flock formation (Figure 1; paired t-test, T = 2.19, p =.0375), whereas the combs of subordinate males became significantly smaller (Figure 1; paired t-test, T = -2.17, p =.0394).
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Iris color and comb color were both duller in subordinate birds before flocks were formed, but not after (Figure 2; iris hue before flocks: Student's t = -4.351, n = 37 in each group, p =.001; iris hue after flocks: t = -0.669, n = 27 in each group, p =.50; comb chroma before flocks: t = 2.357, n = 37 in each group, p =.02; comb chroma after flocks: t = 0.250, n = 27 in each group, p =.80). Note that Munsell scores have lower magnitude for redder hues and higher magnitude for higher chroma or saturation.
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Neither tarsus length nor mass differed in dominant versus subordinate males before flock formation (tarsus: Student's t = 1.321, n = 27 in each group, p =.19; mass: t = 0.927, n = 27 in each group, p =.36). Tarsus was not measured again after flock formation, and mass was still not significantly different in the two groups (t = 0.85, n = 27 in each group, p =.39). Both groups, however, lost a significant amount of weight after they were put in flocks (dominant males: paired t-test, T = -4.53, p =.0002; subordinate males: paired t-test, T = -4.735, p =.0001). Neither group lost more weight than the other (Student's t = 1.035, n = 20 in each group, p =.31).
Immune response and dominance status
We evaluated immune response in the context of dominance in two ways.
First, we compared dominant and subordinate males using a canonical
discriminant analysis to see if a combination of all immune system measures
could be used to distinguish between the two groups. When IgG levels,
hemagglutination scores, wing web swelling, and hematocrit from the blood
samples taken just before flock formation were compared in the two classes of
males, dominant males had slightly stronger immune responses, but the
discrimination was not quite significant (Wilks' 
= 0.878, canonical
correlation coefficient =.35, n = 36 dominant and 31 subordinate
individuals, p =.08). At day 17 after flocks were formed, however,
the two groups were statistically distinct, with dominant males showing
substantially higher scores in each of the measures (Wilks' = 0.795,
canonical correlation coefficient =.45, n = 27 dominant and 27
subordinate individuals, p =.02).
We also examined changes in the immune system measures over time by performing a repeated-measures ANOVA on IgG levels, hemagglutination scores, and hematocrit using dominance status as the class variable. Because wing web swelling was only measured once before and once after flock formation, we compared this response in the two groups of males using t tests. The effect of status on both IgG and hematocrit was significant, while dominant and subordinate males did not differ in hemagglutination score (Table 1; Figure 3). The ANOVA also revealed a significant effect of time of measurement, so that all males increased their responses during the experiment, as is expected when their immune system is sensitized by previous exposure to the antigen. No significant time x status interaction effect was seen, however, suggesting that the dominant males' more robust responses were present before the multi-male groups were formed.
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Wing web swelling size was similar in dominant and subordinate males before they were put in the multi-male flocks (Figure 4). After flock formation, however, dominant males had significantly larger swellings at 24 h after injection than did subordinate males (Figure 4; Student's t = 2.276, n = 27 in each group, p =.027).
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Comb size and immune response
Our previous study showed that males with larger combs also had more robust
cell-mediated immunity, as indicated by larger wing web swellings
(Zuk and Johnsen, 1998). Here,
dominant and subordinate males differed in the relationship between comb
length and wing web swelling (Figure
5). Before flock formation, comb length was unrelated to web
swelling when all birds were pooled (F1,78 = 2.174,
r =.09, p =.144). Among dominant males, individuals with
larger combs again had significantly larger swellings after flock formation
(r =.48, n = 26, p =.01). Subordinate males,
however, showed the opposite effect, with a significantly negative
relationship (r = -.47, n = 26, p =.01), so that
subordinate males with relatively larger combs had worse cell-mediated
immunity than those with smaller combs. If the single subordinate individual
with the smallest comb is removed from the analysis, the relationship between
comb size and swelling is no longer significant for subordinate males but is
still different from that apparent in the dominant males.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Our results suggest that males of different quality pay different costs to maintain both ornamentation and immune defense. At least in the short term, male red jungle fowl show a "rich get richer" response, so that males with large combs became dominant and even increased their comb size, as well as having more robust immune responses. The disparity between males that achieved dominance and those that became subordinate was only exacerbated by being placed in a presumably more stressful social environment.
This study also provides an example of the car-house paradox, a phenomenon
well-described in life-history theory
(Roff, 1992;
van Noordwijk and de Jong,
1986; Zuk et al.,
1996). Although limited funds available for any individual would
suggest that funds put into a house would restrict the amount put into a car,
the expected negative trade-off does not appear when examining the population
as a whole, and people with large houses also tend to drive expensive cars.
The paradox occurs because of the differing amounts of resources individuals
start out with; people who are wealthy to begin with have more money to spend
on everything. Similarly, although allocation of resources to immune defense
may come at the expense of investment in ornamentation, this trade-off is not
apparent because individuals are of different quality
(Qvarnström
and Forsgren, 1998).
Support for such a trade-off comes from Verhulst et al.'s
(1999) study of artificially
selected lines in domestic chickens. Lines selected for high antibody
responsiveness showed a correlated decrease in comb length, while lines
selected for low responsiveness had large combs
(Verhulst et al., 1999).
Presumably, the lines are obtained by selecting individuals already at the
extremes of the distribution of both comb size and immune response, which
allows the trade-off to be exhibited because the selected population is a
subgroup of the variation originally present. The males selected for their
particularly robust immunity therefore consisted of a subgroup that exhibited
the negative correlation between comb length and responsiveness. Our birds
were under no such constraints and hence were able to show both dominance and
immune competence. This natural spread in variation in quality among
individuals may mean that in nature, trade-offs are unlikely to result in
selection for either extreme ornamentation or extreme immune competence, but
instead may help maintain differences in resources available to individuals
within the population.
What caused the initial differences among males? Unlike the situation in
field studies, males in our experiment were the same age, had the same rearing
environment, and were housed in the same circumstances, making it unlikely
that individuals were in very different conditions at the start of the
breeding season. It would be interesting to determine if genetic differences
were at least partially responsible for both the eventual dominance status and
immune response of the jungle fowl. The relatively rapid response of the
domestic chickens in Verhulst et al.'s
(1999) study suggests that
antibody responsiveness, at least, is highly heritable.
It is also possible that the dominant males pay their costs at a different
time of year, perhaps after the breeding season is over. Seasonal effects on
immune response, social status, and the relationship between ornamentation and
both of these measures, are well known
(Kotrschal et al, 1998;
Nelson and Demas, 1996;
Zuk and Johnsen, 1998).
Because jungle fowl live in year-round flocks in nature, however, it seems
unlikely that dominant birds simply collapse at the end of the breeding
season; the birds appear to maintain most aspects of their social system even
when chicks are not being produced (Collias
and Collias, 1967; Collias et
al., 1966).
Although immune defense is frequently presumed to be costly
(Deerenberg et al., 1997;
Sheldon and Verhulst, 1996;
Wedekind and Folstad, 1994),
relatively little evidence exists to support this assumption. Demas et al.
(1997) found that when
laboratory mice were immunized with keyhole limpet antigen, they had
significantly higher metabolic rates, a difference not simply due to a rise in
body temperature, and which seems to reflect the actual cost of producing
antibodies. Svensson et al.
(1998) suggested that any
trade-off between immune defense and energetically costly activities may not
necessarily be based on energy or nutrient limitation but instead may occur
either through the adaptive avoidance of autoimmunity or via the damaging
effects of free oxygen radical production. Results such as ours support the
idea of costly immune competence, but until the mechanisms are better
understood, the exact nature of the trade-off and how it is executed by
individuals of different quality remains unclear.
Perhaps somewhat more clear is the cost of maintaining sexual ornaments
such as the comb. The finding that dominant males have larger combs than
subordinates is consistent with previous studies
(Ligon et al., 1990;
Zuk et al., 1990).
Furthermore, the significant increases in comb size by dominant males and
decrease in comb size of subordinate males after flock formation suggests that
the comb is a powerful social signal with an accompanying social cost; it
seems unlikely that subordinate males gained any physiological, rather than
social, benefit by reducing their comb size. The maintenance of a few
millimeters more or less of soft tissue is unlikely to significantly alter the
energy budget of an individual. Instead, males with larger combs may be
challenged more by other males, increasing the risk of injury during fights
(Ligon et al., 1990;
Zuk and Johnsen, 1998).
Therefore, the shrinking of combs in subordinate individuals could have
reduced the likelihood of social interactions with the accompanying risk of
wounding.
Additional support for the idea that males of different quality pay
different costs for ornaments comes from the finding that only dominant males
showed a positive relationship between comb length and wing web swelling; for
subordinate males, in contrast, having a large comb was costly in terms of
immune defense (Figure 5). The
failure of dominant males to maintain their brighter comb and eye colors after
the birds were placed in the multi-male flocks suggests that these ornaments
are secondary to comb length in importance in sexual selection, a conclusion
supported by these traits being less important to females in mate choice
experiments (Zuk et al.,
1990). Apparently all ornaments cannot be maintained at their peak
during social competition.
In our experiment, dominant males had better immune defense than
subordinate males, a finding somewhat different from those of Barnard et al.
(1993,
1998), who suggested that
high-ranking, aggressive laboratory mice modulate their immune responses
differently from low rankers, but that the dominant individuals are not
uniformly better or worse. Several other studies suggest that subordinate
individuals have suppressed immunity, probably mediated through stress-related
hormonal changes (Blanchard et al.,
1993; Sapolsky et al.,
1997; Stefanski and Engler,
1998; Tuchscherer et al.,
1998). The timing and stability of a social situation can also
influence the degree of stress and stress-related responses
(Fox et al., 1997). The
generally more robust immune responses of the dominant jungle fowl males even
before the flocks were formed and the lack of a significant time x
status interaction effect on immune responses in the repeated-measures ANOVA
argues against the lower immunity of subordinates being an artifact of a
social situation in which they were unable to escape the aggression of
dominant individuals. The differences among studies may reflect the degree of
variation in initial quality of individuals; where fewer high-quality males in
an absolute sense are present, even dominant individuals may not be able to
maintain both immune defense and high levels of aggression or
ornamentation.
Social dominance has many repercussions. Moore et al.
(1997) point out that such
interacting phenotypes, or traits that exist exclusively as a product of
interactions, have unique genetic effects, both through direct and indirect
contributions to the trait itself. They suggest further that the relative rate
of evolution in interacting phenotypes may be different from that of more
"standard" characters such as morphology
(Moore et al., 1997). In the
situation described here, one can envision not one but two sets of interacting
phenotypes occurring together: the social status that results from
interactions with conspecifics and the immune system response that results
from interactions with pathogens. Rapid evolution has been proposed for traits
expressed in social situations, such as those associated with courtship
(West-Eberhard, 1983), as well
as for traits associated with immune defense
(Ebert, 1998). Whether traits
such as comb size in jungle fowl, which are linked to both, show even more
exaggerated responses to selection, or whether the need for coevolution with
pathogens is antagonistic toward the evolution of ornamentation, remains to be
seen.
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ACKNOWLEDGEMENTS |
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We are grateful to the students who helped with maintaining the jungle fowl colony and with data collection. The research reported here is supported by grants to M.Z. from the U.S. National Science Foundation and the UCR Academic Senate. This manuscript was prepared while M.Z. was a visiting professor at Uppsala University, Sweden, funded by the Swedish Natural Science Research Council, and their support is greatly appreciated. M. Andersson, L. Gustafsson, A. Qvarnström, B. Sheldon, and S. Ulfstrand provided helpful discussion and comments on an earlier version of the manuscript. Three anonymous reviewers also made useful comments.
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REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
|---|
Ader R, Felten DL, Cohen N (eds), 1991. Psychoneuroimmunology. San Diego, California: Academic Press.
Barnard CJ, Behnke JM, Gage AR, Brown H, Smithurst PR, 1998. The role of parasite-induced immunodepression, rank and social environment in the modulation of behaviour and hormone concentration in male laboratory mice (Mus musculus). Proc R Soc Lond B 265: 693-701.[Medline]
Barnard CJ, Behnke JM, Sewell J, 1993. Social behaviour, stress and susceptibility to infection in house mice (Mus musculus): effects of duration of grouping and aggressive behaviour prior to infection on susceptibility to Babesia microti. Parasitology 107: 183-192.
Benjamini E, Leskowitz S, 1991 Immunology, a short course. New York: Wiley and Sons.
Blanchard DC, Sakai RR, McEwen B, Weiss SM, Blanchard RJ, 1993. Subordination stress: behavioral, brain and neuroendocrine correlates. Behav Brain Res 58: 113-121.[Web of Science][Medline]
Chappell MA, Zuk M, Johnsen TS, Kwan TH, 1997. Mate choice and aerobic capacity in red junglefowl. Behaviour 134: 511-530.[Web of Science]
Collias NE, Collias EC, 1967. A field study of the red jungle fowl in north-central India. Condor 69: 360-386.[Web of Science]
Collias NE, Collias EC, Hunsaker D, Minning L, 1966. Locality fixation, mobility and social organization within an unconfined population of red jungle fowl. Anim Behav 14: 550-559.[Web of Science][Medline]
Collias NE, Collias EC, Jennrich, R, 1994. Dominant red junglefowl (Gallus gallus) hens in an unconfined flock rear the most young over their lifetime. Auk 111: 650-657.
Creel S, Creel NM, Monfort SL, 1996. Social stress and dominance. Nature 379: 212.
Deerenberg C, 1996. Parental energy and fitness costs in birds (PhD thesis). Groningen: University of Groningen.
Deerenberg C, Apanius V, Daan S, Bos N, 1997.
Reproductive effort decreases antibody responsiveness. Proc R Soc Lond
B 264:
1021-1029.
Demas GE, Chefer V, Talan MI, Nelson R, 1997.
Metabolic costs of mounting an antigen-stimulated immune response in adult and
aged C57BL/6J mice. Am J Physiol 273:
R1631-R1637.
Ebert D, 1998. Experimental evolution of parasites.
Science 282:
1432-1435.
Folstad I, Karter AJ, 1992. Parasites, bright males and the immunocompetence handicap. Am Nat 139: 603-622.[Web of Science]
Fox HE, White SA, Kao MH, Fernald RD, 1997. Stress and
dominance in a social fish. J Neurosci
17: 6463-6469.
Gustafsson L, Nordling D, Andersson MS, Sheldon BC, Qvarnström A, 1994. Infectious diseases, reproductive effort and the cost of reproduction in birds. Phil Trans R Soc Lond B 346: 323-331.[Web of Science][Medline]
Hudson L, Hay FC, 1989. Practical immunology. Oxford: Blackwell Scientific.
Kotrschal K, Hirschenhauser K, Möstl E, 1998. The relationship between social stress and dominance is seasonal in greylag geese. Anim Behav 55: 171-176.[Web of Science][Medline]
Ligon JD, Thornhill, R, Zuk, M, Johnson K, 1990. Male-male competition in red jungle fowl and the multiple roles of testosterone in sexual selection. Anim Behav 40: 367-373.
Moore AL, Brodie III ED, Wolf JB, 1997. Interacting phenotypes and the evolutionary process: I. Direct and indirect genetic effects of social interactions. Evolution 51: 1352-1362.[Web of Science]
Nelson RJ, Demas GE, 1996. Seasonal changes in immune function. Q Rev Biol 71: 511-548.[Medline]
Nordling D, Andersson M, Zohari, S, Gustafsson, L,
1998. Reproductive effort reduces specific immune response and
parasite resistance. Proc R Soc Lond B
265: 1291-1298.
Parmentier HK, Schrama JW, Meijer F, Nieuwland MJB, 1993. Cutaneous hypersensitivity responses in chickens divergently selected for antibody responses to sheep red blood cells. Poultry Sci 72: 1679-1692.[Web of Science][Medline]
Parmentier HK, Siemonsma R, Nieuwland MJB, 1994. Immune responses to bovine serum albumin in chicken lines divergently selected for antibody responses to sheep red blood cells. Poultry Sci 73: 825-835.[Web of Science][Medline]
Qvarnström A, Forsgren E, 1998. Should females prefer dominant males? Trends Ecol Evol 13: 498-501.
Richner H, Christe P, Oppliger A, 1995 Paternal
investment affects prevalence of malaria. Proc Natl Acad Sci
USA 92:
1192-1194.
Roff DA, 1992. The evolution of life histories. New York: Chapman & Hall.
Roitt I, Brostoff J, Male D, 1989. Immunology, 2nd ed. New York: Harper and Row.
Saino N, Calza S., Møller, AP, 1997. Immunocompetence of nestling barn swallows in relation to brood size and parental effort. J Anim Ecol 66: 827-836.
Sapolsky RM, Alberts SC, Altmann J, 1997.
Hypercortisolism associated with social subordinance or social isolation among
wild baboons. Arch Gen Psych 54:
1137-1143.
Sapolsky RM, Spencer EM, 1997. Insulin-like growth factor I is suppressed in socially subordinate male baboons. Am J Physiol 273: R1346-R1351.
Sheldon BC, Verhulst S, 1996. Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11: 317-321.
Sorci G, Soler JJ, Møller AP, 1997. Reduced immunocompetence of nestlings in replacement clutches of the European magpie (Pica pica). Proc R Soc Lond B 260: 1593-1598.
Stefanski V, Engler H, 1998. Effects of acute and chronic social stress on blood cellular immunity in rats. Physiol Behav 64: 733-741.[Medline]
Svensson E, R
berg L, Koch C,
Hasselquist D, 1998. Energetic stress, immunosuppression and the
costs of an antibody response. Funct Ecol
12: 912-919.
Svensson E, Sheldon BC, 1998. The social context of life history evolution. Oikos 83: 466-477.[Web of Science]
Tabachnick BG, Fidell LS, 1983. Using multivariate statistics. New York: Harper and Row.
Tuchscherer M, Puppe B, Tuchscherer A, Kanitz E, 1998. Effect of social status after mixing on immune, metabolic, and endocrine responses in pigs. Physiol Behav 64: 353-360.[Medline]
van Noordwijk AJ, de Jong G, 1986. Acquisition and allocation of resources: their influence on variation in life history tactics. Am Nat 128: 137-142.[Web of Science]
Verhulst S, Dieleman SJ, Parmentier HK, 1999. A
trade-off between immunocompetence and sexual ornamentation in domestic fowl.
Proc Natl Acad Sci USA 96:
4478-4481.
Wedekind C, Folstad I, 1994. Adaptive or nonadaptive immunosuppression by sex hormones? Am Nat 143: 936-938.[Web of Science]
West-Eberhard MJ, 1983. Sexual selection, social competition, and speciation. Q Rev Biol 58: 155-183.[Web of Science]
Zuk M, 1994. Immunology and the evolution of behavior. In: Behavioral mechanisms in ecology (Real L, ed). Chicago: University of Chicago Press; 354-368.
Zuk M, Bryant MJ, Kolluru GR, Mirmovitch V, 1996. Trade-offs in parasitology, evolution and behaviour. Parasitol Today 12: 46-47.
Zuk M, Decruyenaere JG, 1994. Measuring individual variation in colour: a comparison of two techniques. Biol J Linn Soc 53: 165-173.
Zuk M, Johnsen TS, 1998. Seasonal changes in the
relationship between ornamentation and immune response in red jungle fowl.
Proc R Soc Lond B 265:
1631-1635.
Zuk M, Johnsen TS, MacLarty T, 1995. Endocrine-immune
interactions, ornaments and mate choice in red jungle fowl. Proc R Soc
Lond B 260:
205-210.
Zuk M, Kim T, Robinson S, Johnsen TS, 1998. Parasites influence social rank and morphology, but not mate choice, in female red jungle fowl (Gallus gallus). Anim Behav 56: 493-499.[Web of Science][Medline]
Zuk M, Thornhill R, Ligon JD, Johnson K, Austad S, Ligon S, Thornhill N, Costin C, 1990. The role of male ornaments and courtship behavior in female choice of red jungle fowl. Am Nat 136: 459-473.[Web of Science]
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