Parasites and Male Ornaments in Free-Ranging and Captive Red Jungle Fowl

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Parasites and Male Ornaments in Free-Ranging and Captive Red Jungle Fowl Author(s): Marlene Zuk, Kristine Johnson, Randy Thornhill and J. David Ligon Source: Behaviour, Vol. 114, No. 1/4, Behavioural Ecology Symposia (Sep., 1990), pp. 232-248Published by: BRILLStable URL: http://www.jstor.org/stable/4534878Accessed: 14-08-2014 18:26 UTC

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Behaviour 114 (1-4) 1990, E. J. Brill, Leiden

PARASITES AND MALE ORNAMENTS IN FREE-RANGING AND CAPTIVE RED JUNGLE FOWL

by

MARLENE ZUK'), KRISTINE JOHNSON2)3), RANDY THORNHILL2) and J. DAVID LIGON2)4)

(Department of Biology, University of California, Riverside, CA 925211, and Depart- ment of Biology, University of New Mexico, Albuquerque, NM 871312, U.S.A.)

(With 2 Figures) (Acc. 1-XII-1989)

Introduction

Since its presentation several years ago, the hypothesis that parasites play a crucial role in sexual selection has been the subject of much speculation, some controversy, and a few empirical tests (HAMILTON & ZUK, 1982, 1989; READ, 1987, 1988; READ & HARVEY, 1989; ENDLER & LYLES, 1989; ZUK, 1989). The idea that parasites as an important evolutionary force have been largely and wrongfully ignored by behavioural ecologists and

ethologists is becoming virtually uncontested (DOBSON & HUDSON, 1986; SCOTT & DOBSON, 1989), and study of the behavioral effects of parasitism is increasing (BARNARD & BEHNKE, 1990). Several researchers have suggested that pathogens and avoidance of infection have affected such

aspects of ecology as population dynamics, predator-prey relations, or the evolution of social groups (HUDSON, 1986; FREELAND, 1976).

More problematic is the issue of how parasite-host interactions may have caused selection for exaggerated male secondary sex characters and

3) Present address: Department of Ecology, Ethology, and Evolution University of Illinois, Urbana, Illinois 61801, U.S.A.

4) We are grateful to the people who assisted with care of the birds and helped run

experiments: C. BLANCO-MONTERO, C. COSTIN, D. KELLER, C. KROPEK, S. LIGON, J. McCONACHIE, M. MELLOY, S. PORTMAN, D. SHIPPERT, A. THORNHILL, N. THORNHILL, and P. THORNHILL. A. RISSER and the San Diego Zoo kindly supplied us with jungle fowl, and L. R. McDougald provided Ascaridia galli eggs. The Zoo pathology department was very cooperative in helping us to obtain culled birds. J. T. ROTENBERRY gave useful statistical advice, and S. GARDNER helped identify helminths. This research was funded by NSF grants to R.Th., J.D.L. and M.Z. and received support from D. DUSZYNSKI and the UNM biology department and from P. RISSER.



PARASITES AND MALE ORNAMENTS IN RED JUNGLE FOWL 233

female choice of healthy males. Some studies have taken a comparative approach, attempting to determine if intense sexual selection as manifested by showy male ornaments is related to the intensity of

parasites in various taxa (HAMILTON & ZUK, 1982; READ, 1987; READ &

HARVEY, 1989; WARD, 1988, 1989; ZUK, in press a). These analyses are

by necessity indirect, and while suggestive of a relationship between high levels of parasites and the present-day existence of bright coloration or other exaggerated traits, they do not tell us how females might use cues about male health to make mating decisions in natural populations of animals (ENDLER & LYLES, 1989). In addition, it is important to

distinguish HAMILTON & ZUK'S (1982) hypothesis about parasites and

mate choice from a more prosaic avoidance by females of sexually- transmitted diseases, or of a weakened male who will simply be less

capable of giving parental care. These latter mate choice criteria, while

plausible, require no special genetic interactions between host alleles for resistance or susceptibility and parasite alleles for virulence, an essential

part of HAMILTON & ZUK'S (1982) hypothesis. Previous studies of the effect of parasites on male ornamentation and

mating success have generally shown that females prefer uninfected

males, and in some cases an effect of pathogens on the same male trait used by females to make mating decisions has been demonstrated

(KENNEDY et al., 1986; MILINSKI & BAKKER, 1990; MOLLER, 1990; ZUK et

al., 1990). Swallows with low ectoparasite loads were preferred by females, and their offspring appeared to be more resistant than those with

heavily parasitized parents (MOLLER, 1990). Laboratory work on three-

spined sticklebacks also revealed a preference for males with redder throat patches, and experimental infection with the ciliate Ichthyophthirius multifiliis decreased both brightness and attractiveness of male fish

(MILINSKI & BAKKER, 1990). In a series of experiments performed on a

captive flock of red jungle fowl (Gallus gallus), ZUK et al. (1990) found that roosters experimentally infected with the roundworm Ascaridia galli differed significantly from control males in the degree of development of the ornamental traits females preferred in mate choice trials, but not in non- ornamental characters such as bill size. These results suggest that

parasites may affect secondary sex characters, particularly facultative ones such as eye color and comb size, more than they affect growth characters. Other studies relied on correlative data mainly from field populations, some of which showed a negative relationship between parasites and a measure of mating success, and some of which did not (BORGIA, 1986; BORGIA & COLLIS, 1989; ZUK, 1987, 1988; BURLEY et al., in press; READ & WEARY, 1990).



234 ZUK, JOHNSON, THORNHILL & LIGON

Badly needed now are more studies that combine the precision possible in the controlled environment of the laboratory with the realism of work-

ing in the field with natural populations subject to predation, weather, and other biotic and abiotic forces in addition to parasites. Such studies will hopefully provide tests of the HAMILTON & ZUK hypothesis that

distinguish it from the more general ones outlined above. In this paper, we attempt to achieve this balance by combining data on morphology and parasite levels from a feral population of red juncle fowl at the San

Diego Zoo in California with results obtained from experiments performed on captive-bred birds. Although the zoo birds are obviously not in their native habitat, they are free-ranging and subject to natural selection (see below). By comparing both the appearance and the parasite burdens of our experimental jungle fowl with those of the zoo birds, we

attempted to obtain a realistic picture of what females might be expected to choose under natural conditions, and how well worm burdens in our

artificially parasitized birds reflect natural levels of infection. In addition, we report the results of an additional analysis of mate choice in our

experimental population, again with the goal of greater relevance to field

conditions, by treating the effects of parasitemia as a continuous rather than a categorical variable. The results of more general observations on the role of ornaments and courtship behavior in aspects of sexual selection in red jungle fowl are reported elsewhere (ZUK et al., 1990a, b, c; LIGON et al., in press).

The research presented here addressed the following questions: 1. How does the appearance of roosters in our experimental popula-

tion compare with that of feral roosters at the zoo? 2. What is the distribution of helminth parasites in the feral popula-

tion? How does it compare with the parasite burden induced in the

experimentally infected jungle fowl? 3. Is there a relationship between parasite burden and male mor-

phology in the feral population? 4. How does mating success in the experimental trials reflect, not the

membership of a rooster to a control or parasitized group, but his score on an axis representing a multivariate preference for traits?

Materials and methods

Feral population sampling. In 1942, 32 jungle fowl were introduced in the San Diego Zoo in southern California

(COLLIAS et al., 1966). The zoo has extensive wooded canyons and hills where the birds can range unmolested by humans; by the 1960's the zoo population consisted of several




hundred birds (COLLIAS et al., 1966). Previous studies both in the jungle fowl's native southeast Asia and of the unconfined zoo populations have revealed a mating system similar to other non-lekking polygynous pheasants. Both sexes are philopatric and move in small flocks consisting of a dominant rooster, several hens, and several subordinate roosters (COLLIAS et al., 1966; COLLIAS & COLLIAS, 1967, 1985). Hens are free to move within and between flocks, and they mate often but not exclusively with the dominant rooster in their flock (COLLIAS et al., 1966; COLLIAS & COLLIAS, 1967, 1985; THORNHILL,

1988). During a culling program conducted by the zoo in 1987, we obtained sacrificed adult

roosters in March-June for morphological measurement and necropsy. All birds were frozen and thawed before examination. For determination of parasite burdens, the entire gut of the bird was removed and flushed with tap water. The gut contents were then floated in a dissecting tray half-filled with water and examined both visually and under a dissecting microscope. Counts were made of the number of entire roundworms iden- tified as Ascaridia galli, worms in the genus Heterakis, and the number of tapeworm scoleces. Because each tapeworm tended to separate into numerous proglottids upon dis- turbance, the number of scoleces or head capsules was used in calculating worm numbers.

Morphological measurements were made by two observers indoors under standardized

lighting conditions. Longest sickles (curved tail feathers) and saddles (lanceolate feathers

extending over the back) were measured to the nearest mm using a metal ruler. The

length of the spur, the hornlike projection on the tarsus that grows with age in many pheasant species, was measured along the longest curve to the nearest 0.1 mm. Testis volume was calculated by measuring the length and width of the left testis with dial

calipers, and using the formula for volume of a sphere to calculate volume. The length of the comb at its longest span was measured with dial calipers to the nearest 0.1 mm. Because the birds had been frozen, their combs had shrunk from the natural size; for

comparison with roosters used in our experimental trials, comb lengths of frozen birds were transformed in some analyses to their extrapolated natural length using a regression generated by measuring 14 roosters' combs before and after they had been frozen for a time roughly equal to that of the zoo birds. The regression gave a significant, though not

perfect, predictor of natural comb length (r = 0.79, p< 0.001). The colors of hackle (lower neck feathers) tips, head and upper neck feathers, saddle

tips, and saddle base feathers were scored for each rooster. We evaluated colors using the Munsell system, which gives each color a score for hue, value (darkness or amount of black), and chroma (brightness or saturation with pigment) (BURLEY & COOPERSMITH,

1987). We measured tarsus length with dial calipers to the nearest 0.1 mm. We were unable to measure colors of soft body parts such as the comb and eye, as we had in the roosters used for mate choice experiments (see below), because these change almost

instantaneously after death.

Mate choice trial procedure. The captive flock used in sexual selection experiments was derived from 150 jungle fowl acquired from the San Diego Zoo in 1984-1985. The protocol followed in mate choice trials, as well as the procedure for infecting and measuring the experimental roosters, is given in detail elsewhere (ZUK et al., 1990a, b, c). Briefly, 30 sexually mature 10-month- old roosters that had been inoculated with A. galli as chicks were paired randomly with 30 uninfected control roosters. A. galli, which occurs commonly in both domestic chickens and jungle fowl, has a direct life cycle and causes significant juvenile mortality in domestic poultry (RUFF, 1978; IKEME, 1971a, b, c). Worm eggs ingested by the host develop in the intestine, exerting most damage to chicks (IKEME, 1971a; ACKERT et al., 1931; RUFF, 1978).




Each male was used twice, but never with the same partner, generating 60 unique pairs. The tests were run in outdoor enclosures measuring approximately 5.3 x 5.3 m. The test roosters were tethered in the center of individual compartments separated by a wood partition, and a single hen was placed in a wire pen that ran the length of the enclosure. The males were thus visible to the hen, but not to each other. After one hour, the hen was released to interact with the roosters. An observer in a blind fitted with one-

way glass outside the enclosure recorded the identity of the chosen male. A trial ended and a choice was scored after the female copulated with, or gave a clear

solicitation crouch to, one of the test males within half an hour of her release. If neither occurred, we discarded the trial. A male was never used more than one in a day, and a different hen was used in each of the 60 trials. Hens used were year-old birds that were unfamiliar with the test roosters, and had not been part of the parasite infection experiment. All trials were run blind, without the observer knowing which bird was parasitized and which was control.

Measurement of experimental roosters.

Measurement of male morphology was identical to that described above, with the addition of color scoring for the comb and iris (which is orange to red in mature males), and estimation of the amount of yellow or whitish pigment on the wattle. Testis volume and

spur length were not measured; because all roosters were the same age, their spurs were small (<3 mm) and relatively uniform in size.

At 11 weeks of age, infected and control hens that had been maintained along with the

experimental roosters were sacrificed and their worm burdens determined using the procedure described, to obtain data on both the effectiveness of the experimental infection and the uninfected nature of control birds.

Results

Parasite burden in the zoo and experimental populations.

A total of 50 roosters were examined for parasites. As is typical for many helminths, each parasite type alone as well as total parasite levels in

general showed an over-dispersed distribution in the population, with

many individuals harboring few or no parasites, some harboring a moderate number (4-10 A. galli), and a very few birds possessing extremely heavy worm burdens (> 30 A. galli) (Fig. 1). A. galli was the most prevalent parasite, with 32% (n = 16) of the roosters having 1 or more of these worms, compared with 22 % (n = 11) of individuals harbor-

ing Heterakis and 10% (n = 5) harboring tapeworms. Only 25% of the roosters had no parasites at all. There was no relationship between the numbers of the different types of parasite in an individual; the Spearman rank correlation was 0.09 between A. galli and Heterakis, 0.18 between A.

galli and tapeworms, and -0.03 between tapeworms and Heterakis, p>0.22 in all cases.




36

32

28

24

20

12

8

0 4 8 12 16 20 24 28 32 36 40

Number of Ascaridia

24

20

16

1 2

4

0 5 10 15 20 25 30 35 40 45 50

Number of helminths

Fig. 1. Frequency distribution of (la) A. galli and (Ib) total helminth parasites (A. galli, Heterakis, and tapeworms) in 50 adult roosters collected at the San Diego Zoo in late

spring of 1987.

In those jungle fowl with one or more worms, average burdens for each

type were as follows: A. galli, 7.4 (range 1-37); Heterakis, 8.4 (range 1-50); tapeworms, 1.0 (all birds with tapeworms had only one). These incidences are roughly comparable with those found in the sacrificed birds from the experimentally infected group used in our study. The 36

experimentally infected individuals that were examined showed a mean of 18.3 A. galli, with a range of 2-47 worms, while no control sacrificed birds had any Ascaridia.




Relationship between morphology and parasites in zoo roosters.

Because the distribution of parasites in the zoo birds was highly skewed

(Fig. 1), and because our intent was to compare our results to the

experimental work using "parasitized" and "control" groupings, analyses of the zoo roosters were similarly performed on two groups. Those individuals with 0, 1, or 2 parasites of any kind were considered in the "low" parasite group (n = 20), while those with 3 or more worms

(n = 11) were classified as having "high" parasite burdens. The division is obviously somewhat arbitrary, but seems to reflect a natural break in the distribution of parasites (Fig. 1); the use of 0 us 1 or more parasites, or 0 and 1 vs 2 or more parasites, gave qualitatively similar results. Some of the individuals for which we had parasite measurements could not be used in the analysis because one or more of their morphological characters was damaged or otherwise unable to be calculated - e.g., hackle feathers were broken at the tips.

A canonical discriminant analysis was performed using the two classes of parasite burden, to determine if the two groups differed significantly in morphology (TABACHNIK & FIDELL, 1983). This technique allows the simultaneous assessment of several traits. The two parasite classes

separated significantly based on three characters: hackle color, comb

length, and testis volume. Using these traits yielded a squared canonical correlation coefficient (analogous to a multivariate r2) of 0.37, with Wilks' lambda = 0.63 with 3 degrees of freedom and a p-value of 0.0055. Addition of other characters did little to increase the significance of the discriminant function. The most important predictor of parasite burden was testis volume; a plot of this variable against the total number of

parasites is shown in Fig. 2.

Separation of A. galli burdens alone into similar "high" and "low"

groups also resulted in a significant assignment of group membership based on the same three traits; here individuals were classified as "low" if they had 0 Ascaridia (n = 19) and "high" if they had 1 or more. This distinction was again based on a natural break in the distribution of

parasites (Fig. 1), and again, use of other classifications gave similar results. The squared canonical correlation coefficient was 0.25, Wilks' lambda = 0.75 with 3 degrees of freedom and a p-value of 0.05.

Discriminant analyses were not performed on either Heterakis or

tapeworm levels because the number of individuals harboring each of these worms was too small to allow meaningful statistical treatment.




18000

1 6200

E 14400

u 12600

10800 -

i 9000 *

0 7200

,_ 5400* .

3600 *

1800

0 ,

,

. . . . . . . . . . . . . . ...; 0 5 10 15 20 25 30 35 40 45 50

NUMBER OF HELMINTHS

Fig. 2. Relationship between total number of helminth parasites (A. galli, Heterakis, and

tapeworms) and testis volume in 50 roosters collected at the San Diego Zoo.

Comparison of morphology in experimental and zoo

populations.

Mean values of the traits measured in the zoo population, the 60 uninfected roosters used in mate choice and male competition tests in

1988, and the 60 parasite and control roosters from the experiments discussed here are given in Table 1. The feral birds had generally similar traits to the birds used in our experiments, although the roosters from the

parasite experiment had shorter combs and tail feathers than other birds.

Many tail feathers of the parasitized and control birds had broken during the roosters' confinement in pens during the winter in New Mexico. Sad- dle feathers were also longer in the zoo birds, probably because these con- tinue to develop even after sexual maturity, and the zoo birds contained

many roosters older than the yearlings used in our mate choice tests. The traits listed are not generally correlated among themselves,

although the various feather color measures tend to vary positively. The discriminant analysis takes into account the correlations among charac-

ters, but it is worth noting that spur length, which increases with age, is not correlated with testis volume (r = 0.16, p>0.35). Individuals with

larger testes are therefore not merely older than individuals with smaller testes. Testis volume also did not covary with time of year when the birds were collected; all were sacrificed during the early part of the breeding season.




TABLE 1. Comparison of means (SD) for male characters in feral (San

Diego Zoo) and captive red jungle fowl

Trait Source of roosters Zoo Parasite expt. Sexual selection expt.

n = 52 n = 60 n = 48

Tarsus length (mm) 76.2 (4.9) 71.6 (4.3) 76.6 (3.7) Comb length (mm) 70.1* (13.7) 70.2 (8.0) 75.7 (6.9) Tail length (mm) 396 (107) 284 (74) 234 (30.4) Hackle color (Munsell

score) 21.05 (1.45) 21.3 (1.3) 22.7 (1.3) Head feather color

(Munsell score) 13.2 (1.2) 15.1 (1.0) 14.6 (1.9) Saddle tip color

(Munsell score) 17.7 (2.4) 18.8 (1.6) 19.4 (1.9) Saddle base color

(Munsell score) 11.6 (1.7) 12.9 (1.8) 12.2 (2.0)

Color scores are measured in Munsell units, which decrease in these cases with increasing redness of hue. Measurements for both parasitized and control individuals were pooled to give the mean values shown for roosters in the parasite-control experiment. * = Mean comb length in the zoo sample is that of frozen individuals; it may be transformed into the extrapolated "live" length using the following regression: y= .78x + 12.66, which gives a transformed mean value of 73.8 mm.

Mating success and score on the discriminant axis.

Control roosters were chosen in 39 of the 60 mate choice trials, which constitutes a significant preference (p < 0.025, one-tailed binomial proba- bility) (ZUK et al., 1990a). Using canonical discriminant analysis, control roosters could be separated from parasitized roosters on the basis of six traits: sickle length, comb length, hackle color, saddle feather tip color, comb color (chroma or saturation with pigment) and iris color (ZUK et al., 1990a). An analysis of covariance using parasite-control status as a 0-1 class variable and the six secondary sex characters as independent variables, with mating success as the dependent variable, showed that the characters contributed to a significant model with an r2 of 0.38 and a p- value of 0.0009.

The discriminant analysis yields an axis that can be viewed as a one- dimensional summary of the traits used to assign group membership (TABACHNIK & FIDELL, 1983). Each male thus has a score on that axis

representing his overall appearance in relation to that of the other males. To obtain a direct measure of the relationship between male appearance and mating success, we calculated the rank correlation between males'




scores on the canonical axis and the number of times they had been chosen by females in the mate choice trials (0, 1, or 2 times, since each rooster was used twice); this correlation was highly significant (rs = 0.47, p < 0.001). By using parasite-control status only indirectly, the biological relevance of the test is enhanced; females are obviously unaware of the

group assignment of the roosters they see, and in nature of course are confronted with a continuously varying population, not one in two distinct groups.

Discussion

The combination of experimental and observational results reported here

helps shed light on the role of parasites in red jungle fowl ecology. Our results also point the way toward future experiments that may provide critical tests of not only the HAMILTON & ZUK hypothesis of sexual selec-

tion, but of a wide range of ideas regarding the evolution and maintenance of secondary sex characteristics.

Comparison of feral and experimental populations.

The roosters from the San Diego Zoo were generally similar in

appearance to those used in our sexual selection study, although the zoo

birds, being of a variety of ages, had a wider range of values for age- related characters such as spur length and saddle feather length. This information indicates that our previously reported results showing that males with longer, redder combs and redder irises were preferred by females, and that males with longer combs were more successful in male- male competition (LIGON et al., in press; ZUK et al., 1990b, c) were not an artifact of an unusual distribution of characters in our captive flocks.

Unfortunately, some of the most critical characters in our mate choice tests, especially comb and eye color, could not be measured in the zoo

specimens. Likewise, testis volume was not measured in the experimental roosters. It is precisely these facultative characters that appear to be

important in jungle fowl mate choice, and which also are sensitive to the effects of experimental infection (ZUK et al., 1990c). Taken together, however, and seen in conjunction with the data on parasites, the two sets of results suggest a dynamic relationship between sex hormones, parasites, and male ornaments (LIGON et al., in press).

Likewise, although three kinds of helminth parasites were recorded in the zoo sample versus only one, A. galli, in the experimental roosters,




overall worm burdens in infected individuals were at least roughly com-

parable in the two populations, and completely or nearly completely parasite-free individuals were common in the feral group, suggesting that our artificial infection treatment resulted in a range of variation that is realistic in terms of what females in natural populations actually see.

Clearly, a demonstration that males so crippled by parasites that their

appearance was completely unlike most wild jungle fowl receive less attention from females and are less likely to dominate other males would be of limited interest. Instead our results imply that females are likely to

prefer less parasitized males as mates, and that those individuals are available at least in feral, if not field, populations. Further research on the behavior of red jungle fowl in their native habitat would be useful to

complete the picture of sexual selection in the wild; such research has hitherto been hindered by the elusive behavior and impenetrable habitat of the birds in the parts of Asia where they have been studied (COLLIAS & COLLIAS, 1967).

Correlation of mating success and canonical axis score.

The highly significant correlation between the number of times a rooster was chosen by the test hen in our mate choice trials and his score on the discriminant function axis confirms the notion that females are using a continuous variable incorporating many characters when they make

mating decisions. Because it bypasses the dichotomy of parasitized or control group membership, the analysis gives a means of assessing what females do when faced with a quantitatively, rather than qualitatively, varying population. This approach may prove useful to other studies of the effects of a manipulated character on female choice of males that vary in more than just the manipulated trait.

Sex hormones, parasites, and sexual selection.

The negative relationship between testis volume and parasite burden seen in the San Diego Zoo roosters adds to the accumulating evidence for a possible physiological mechanism for the operation of HAMILTON & ZUK's (1982) hypothesis about parasites and sexual selection. It also suggests that female choice for ornamented males, and male production of facultative secondary sex characters, may occur in a previously little- considered context of parasite resistance and energetics.




Testis recrudescence in birds is highly correlated with the increased

production of male sex hormones, especially testosterone, in the breeding season (LOFTS & MURTON, 1973; WINGFIELD & MOORE, 1987). Larger

gonads generally indicate higher circulating hormone levels (LOFTS &

MURTON, 1973; WINGFIELD & MOORE, 1987). Similarly, male comb

length (and probably other characters such as comb color and iris color) is a reflection of male hormone titers, so much so that comb growh in domestic poulty following injection of an unknown solution was used as an assay for testosterone (ALLEE et al., 1939). Several other instances of

testosterone-dependent development of secondary sex characters in birds have been demonstrated (LOFTS & MURTON, 1973), and in at least one

study, testis size was related to mating success as well JOHNSON, 1988a,

b). Also well documented is an immunosuppressive effect of male sex hor-

mones (SOLOMON, 1969; GROSSMAN, 1985; ZUK, in press b). Although

exceptions exist, males in many vertebrate species are more susceptible than are females to many different parasites and diseases, and when

experimentally challenged with a variety of antigens, mount a weaker immune response than do females. Testosterone itself appears to inhibit

lymphocyte transformation (ALEXANDER & STIMSON, 1989). Sex hormones, male ornaments, and parasites are thus interrelated

(LIGON et al., in press). There are at least three potential ways in which these relationships may account for our findings in the zoo birds and their relevance to our previously reported results regarding mate choice and the effect of A. galli on both the development of male secondary sex characters and female response to those characters.

First, as suggested by FOLSTAD & KARTER (in review), testosterone level

and the immune responses and ornaments that depend on this hormone

may be regulated by a feedback loop in response to parasites. According to this view, male ornaments such as combs and showy plumage are "honest" signals of a male's ability to withstand the obligatory immunosuppressive effects of high testosterone titers. Cheating is

unlikely because the cost of doing so, of presenting showy characters when viability or fitness is low, is an automatic loss of immune function that makes the male too vulnerable to pathogenic effects of parasites for it to be maintained. Males with highly-developed secondary sex characters are therefore indicating their capacity to resist the effects of prevalent parasites even on a compromised immune system.

If this model is operating in the jungle fowl, roosters with large testes are those which are initially better able to withstand helminth infections,




and are producing more developed secondary sex characters such as

longer combs because they can afford the costs of high testosterone levels.

They have fewer parasites because of this initial capacity. This idea does not distinguish between the effects of genetic immunity

and those of acquired immunity, the latter being the result of facultative cell-mediated and humoral responses on the part of the host to invasion

by a foreign substance. Testosterone presumably affects this second

aspect of immunity, because genetic resistance or suspectibility is an inherited all-or-none phenomenon. FOLSTAD & KARTER'S model offers no

suggestions of how some males might be better able to afford expenditure of energy and deal with the effects of immune suppression. A second, albeit related, explanation of the finding that testis volume and parasite burden are negatively correlated is that females benefit most by mating with males that are genetically resistant to parasites. Males with this "bonus" resistance are spared the effort of mounting as complete an

acquired immune response as are males that lack such genetic capability. Females choosing such males are therefore gaining heritable benefits of

parasite resistance for their offspring, as well as the more immediate benefits of mating with a vigorous male. This heritable fitness gain is of course the advantage postulated by HAMILTON & ZUK (1982) in their

original hypothesis. The results reported here suggest that males with both genetic and acquired immunity might thus be most likely to produce well-developed secondary sex characters, which requires high testosterone production and larger testes.

An alternative explanation examines the situation from the parasites' point of view. Reducing the sexual competitiveness of a host by retarding the development of his secondary sex characters might well be advan-

tageous to individual Ascaridia. Like most male pheasants, red jungle fowl roosters are extremely aggressive during the breeding season (LIGON et al., in press), and injuries from the sharp spurs and bill are not uncom- mon. Rival males are attracted to courting roosters that are about to mate or have just done so, and potentially competitive males appear to be attracted to the post-ovulation calls of receptive hens (THORNHILL, 1988). Roosters in any of these situations presumably run a greater tisk of physical harm than subordinate individuals not entering the competition. Parasite survival and transmission might thus be greater in less dominant males, and the suppression of testosterone could be seen as a facultative adaptation of the parasite rather than having any relation to female choice. Parasite fitness would be especially enhanced if such non-

competitive males spent time near chicks, which are particularly




vulnerable to infection. The disproportionate effect of A. galli on ornamental characters, as opposed to body and bill size, may also be

interpreted in this light (ZUK et al., 1990a); assuming that the less- decorated males can still obtain food and other resources needed for somatic maintenance, a fair-sized male with relatively inferior secondary sex characters is perhaps the best kind of host for a parasite to have.

Resolution of these at least partially conflicting notions requires further experimentation and, ideally, observation and sampling of jungle fowl in their native habitat. Future experiments should manipulate both the hormone levels and parasite burdens of roosters. Are birds with high testosterone titers more susceptible to infection with parasites than those with lower testosterone levels? Does testosterone titer drop following infection? How does infection affect behavior patterns of males under natural conditions?

Our work as well as that of other researchers in sexual selection points to the need for synthesis of several disciplines in attempting to answer

major questions in evolutionary biology. Testing HAMILTON & ZUK'S

hypothesis is difficult, if not impossible, without some understanding of

parasite biology, an understanding that may often require experiments under controlled laboratory conditions. Other fields, such as

endocrinology, may also provide new insight into proximate factors

affecting the development of secondary sex characters, and again careful

manipulation may be required. The interactions between different facets of the immune response and parasites must be examined on a very mechanistic level. Equally necessary, however, is the study of how

parasites affect the lives of animals in the wild, and both depend in turn on the development of realistic theoretical models that put proximate and ultimate factors into perspective.

Summary The morphology and parasite burdens of culled free-ranging red jungle fowl (Gallus gallus) from the San Diego Zoo were compared with those of captive roosters used previously in sexual selection experiments, to determine if results obtained with the captive birds were relevant to more natural situations. Zoo roosters had three helminth gut parasites: Ascaridia galli, tapeworms, and Heterakis. Parasite distribution was generally over-dispersed, with most individuals having none or few worms and some having heavy parasite burdens. These levels were comparable to those artificially induced in test roosters. The appearance of the zoo birds was similar to test roosters as well. Higher parasite burdens in the zoo birds was negatively related to hackle feather redness, comb length, and especially testis volume. The latter finding is discussed in light of information about the relationship between testosterone levels, sexual selection, and the immune system. A new analysis of female choice of uninfected controls versus experimentally infected roosters suggests that females prefer a multivariate array of traits perceived as a continuous, rather than categorical, variable.




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Parasites and Male Ornaments in Free-Ranging and Captive Red Jungle Fowl