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The Role of Male Ornaments and Courtship Behavior in Female Mate Choice of Red Jungle Fowl Author(s): Marlene Zuk, Randy Thornhill, J. David Ligon, Kristine Johnson, Steven Austad,Sandra H. Ligon, Nancy Wilmsen Thornhill and Colleen Costin Source: The American Naturalist, Vol. 136, No. 4 (Oct., 1990), pp. 459-473Published by: for The University of Chicago Press The American Society of NaturalistsStable URL: http://www.jstor.org/stable/2462188Accessed: 14-08-2014 18:30 UTC

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Vol. 136, No. 4 The American Naturalist October 1990

THE ROLE OF MALE ORNAMENTS AND COURTSHIP BEHAVIOR IN FEMALE MATE CHOICE OF RED JUNGLE FOWL

MARLENE ZUK,* RANDY THORNHILL, J. DAVID LIGON, KRISTINE JOHNSON,t STEVEN AUSTAD,t SANDRA H. LIGON, NANCY WILMSEN THORNHILL,

AND COLLEEN COSTIN?

Department of Biology, University of New Mexico, AlbuquerqLle, New Mexico 87131; tDepartment of Ecology, Ethology, and Evolution, University of Illinois, 505 S. Goodwin Avenue, Urbana, Illinois 61801; tDepartment of Organismic and Evolutionary Biology, 16 Divinity Avenue,

Harvard University, Cambridge, Massachusetts 02138; ?Department of Anthropology, University of New Mexico, Albuquerque, New Mexico 87131

Submitted January 23, 1989; Revised June 19, 1989; Accepted November 29, 1989

In many species of birds, males have showy plumage or other ornaments and elaborate courtship displays to attract females for mating. The evolution of these male secondary sex characters is a matter of much discussion among evolutionary biologists, as is the role female choice plays in sexual selection. Do females prefer males exhibiting a particular character or combination of characters? Do they attend to morphology rather than behavior, or vice versa?

Of special interest is the question of whether traits preferred by females might indicate the physical condition or genetic quality of a male; theoretical work offers conflicting viewpoints on this question, with some arguing that traits preferred by females are meaningless in any context of male fitness other than mating success (Lande 1981; Kirkpatrick 1982; Arnold 1983) and others maintaining that females use male ornaments as cues of male fitness that might be passed to offspring (Trivers 1972; Zahavi 1975; Andersson 1982; Hamilton and Zuk 1982; Thornhill and Alcock 1983; Kodric-Brown and Brown 1984; Nur and Hasson 1984). The role of male secondary sex characters is most perplexing in species lacking male parental care because, if females in such species are making adaptive mate choices, they must be doing so from direct indications of male quality contained in male appearance or courtship. Finally, are cues that are used by females in mate choice the same as those that are important in sexual competition among males?

Studying these problems under either field or laboratory conditions alone can pose problems for drawing generalizations about sexual selection. In field popula- tions, small sample sizes and the simultaneous variation of male traits such as age, social status, and nutritional history, along with physical appearance, can make data on the mating success of different morphological types of males difficult to

* Present address: Department of Biology, University of California, Riverside, California 92521.

Am. Nat. 1990. Vol. 136, pp. 459-473. ? 1990 by The University of Chicago. 0003-0147/90/3604-0002$02.00. All rights reserved.

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460 THE AMERICAN NATURALIST

interpret. However, controlled laboratory tests may tell us little about the behav- ior of individuals in their natural habitats, and they often use species that have been subjected to many generations of artificial selection and abnormal levels of inbreeding, making the results obtained by using such species less useful. Perhaps because of these difficulties, little empirical evaluation of theories of sexual selection has been offered relative to the plethora of models and proposed tests of the theories (see Bradbury and Andersson 1987).

In this article, we report the results of a series of experiments designed to overcome at least some of these problems. Using captive red jungle fowl (Gallus gallus) from free-ranging and therefore not artificially selected populations, we performed mate-choice tests to determine the roles of male ornaments and court- ship behavior in female choice. Because male ornamentation and perhaps display behavior continue to develop after the first breeding season in jungle fowl (Collias and Collias 1985; J. D. Ligon, R. Thornhill, and M. Zuk, personal observations), we also examined the potential for female preference for older birds (cocks) over yearlings (cockerels). Female preference for older males has been suggested for several bird species (Weatherhead 1984; Alatalo et al. 1986). In addition, by comparing the results of female-choice trials with those of male competition (Ligon et al. 1990), we were able to see whether traits important in one process are also important in the other.

Red jungle fowl are the ancestors of domestic chickens, and they are well suited for sexual selection studies. Males are elaborately ornamented, both with colorful plumage and with fleshy comb and wattles on the head and neck, whereas females are relatively drab and cryptic. The birds readily become accustomed to humans and exhibit high degrees of sexual competition.

Previous studies of unconfined populations in Asia, in New Mexico, and at the San Diego Zoo have revealed a mating system similar to that of other non- lekking polygynous pheasants. Both sexes are philopatric and move in small flocks consisting of a dominant rooster, several hens, and several subordi- nate roosters (Collias et al. 1966; Collias and Collias 1967, 1985; Thornhill 1988). 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 and Collias 1967, 1985; Thornhill 1988). Attempts by males to copulate forci- bly are usually unsuccessful (Collias and Collias 1985; Thornhill 1988). Fe- males see a small number of males in a season, including few dominant roos- ters.

Jungle fowl courtship and mating behaviors are virtually identical to those of the conspecific domestic fowl (Kruijt 1964), which have been well described (see, e.g., Guhl 1951; Wood-Gush 1971), and several studies have examined the rela- tionship of social dominance and/or morphology to mating success in domestic chickens (Collias 1943; Guhl and Warren 1946; Marks et al. 1960; Lill 1966). These studies have demonstrated the influence of several characters, especially comb size and shape, in mating success and individual recognition. In addition, the sedentary nature and relatively small size of natural flocks of jungle fowl make an experimental design using a single female with a few males reasonably realistic (Collias et al. 1966; Thornhill 1988).

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FEMALE CHOICE IN JUNGLE FOWL 461

MATERIAL AND METHODS

Origin and Maintenance of Jungle Fowl

A population of about 30 jungle fowl was introduced from southeastern Asia to the San Diego Zoo in 1942 and allowed to breed, ranging freely over the extensive zoo grounds (Collias and Collias 1985). Our birds are descended from 150 individ- uals obtained from the zoo in 1984-1985. Most chicks used in mate-choice experi- ments were incubated and hatched in the laboratory and then kept in indoor brooders until 6 wk of age, after which rearing was completed in large outdoor pens containing birds of both sexes (on the property of either R.T. and N.W.T. or J.D.L. and S.H.L.). The birds were fed commercial chicken feed (21% protein) later supplemented with scratch and given water ad lib. Mate-choice trials were performed in the spring, after the jungle fowl were sexually mature, starting at approximately 8-9 mo of age; males in their first breeding season are called cockerels. For trials involving cocks, males used had entered at least their second breeding season and included some birds originally obtained from the zoo 3-4 yr before experiments were performed. Except for 11 second-year hens used in 1987, all females were in their first breeding season.

Measurement of Secondary Sex Characters At sexual maturity, secondary sex characters were measured on all roosters.

Longest sickles (curved tail feathers) and saddles (lanceolate feathers extending over the back) were measured to the nearest 1.0 mm with a metal ruler. Spur length was measured to the nearest 0.1 mm in the set of cocks and cockerels used in the experiment that examined the effect of male age on female preference. The length of the comb at its longest span was measured to the nearest 0.1 mm with dial calipers. In 1987, comb lengths of most males were remeasured in late summer, after the breeding season, to determine whether comb lengths changed after mating activity was over. In addition, the colors of the comb, iris, tips of the hackles (lower neck feathers), head and upper neck feathers, saddle tips, and saddle-base feathers were scored for each rooster. Colors were evaluated with the Munsell system, which gives each color a score for hue (e.g., red or yellow), value (darkness, or amount of black), and chroma (brightness, or saturation with pig- ment) (Burley and Coopersmith 1987). Only hue was recorded for feather colors. The percentage of yellow or white pigment on the wattle area below the eye but above the free-hanging part of the wattle we called the "ear" was also re- corded. Tarsus length was measured with calipers to the nearest 0.1 mm to give an indication of body size, and, in the group of roosters used for the cock and cockerel trials, all individuals were weighed to the nearest 1.0 g. All measure- ments were made by at least two observers indoors under standardized lighting conditions; M.Z. was an observer in all measurements to help ensure consistency. We did not formally score repeatability, but birds remeasured within the same season to score changes in comb length, for example, had color measures identical to those taken previously. All birds were scored before mate-choice trials were performed, thus preventing bias toward individual roosters.

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462 THE AMERICAN NATURALIST

Mate-Choice Trials

In 1987, a pool of 33 yearling roosters was used for all mate-choice trials. For trials examining female preference for cocks (males at least 2 yr old) versus cockerels, 19 cocks were also used. A pair was generated at random from the pool of 33, and, in the trials using all young birds, each individual was used five times, but never with the same partner, for a total of 83 unique pairs. One male was used six times, and his mating-success score was "prorated" to give a proportion of wins out of five trials. In the trials using cocks, each of the 19 cocks was paired with one cockerel, with each male used once. In 1988, the pool of roosters numbered 60, and each male was used 7-10 times, each with a different partner, for a total of 248 pairs.

In both years, the hens were unfamiliar with the test roosters (roosters from the Ligon site were tested at the Thornhill site with Thornhill hens, and vice versa) and were used only once in each set of trials, although hens from the cock-and- cockerel experiment could be rerun in the trials using all cockerels. Rearing or testing site had no effect on the results; statistical tests performed for each site separately yielded the same results as those for pooled samples. Hens had previ- ous sexual experience with the roosters with which they were reared but were isolated in all-female groups in outdoor pens for at least 5 d after they were moved and before they were used in mate-choice tests.

The tests were run in outdoor enclosures measuring approximately 5.3 m x 5.3 m. Test roosters were individually isolated for a few weeks before testing, which reduces subordinate behavior (Ligon et al. 1990). During each trial, two 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. Tethers were long enough to permit the roosters to reach the corners of their compartment but stopped just short of the partition. The males were thus visible to the hen but not to each other. Each male had access to his entire compartment, but a 1-m-wide strip between the males' compartments and the female pen was outside the reach of the tethered males. This provided a neutral area for the female and allowed her to move unmolested from one male's compart- ment to the other's. Although males could hear each other, they probably did not influence each other's behavior; roosters that cannot be approached and chal- lenged visually by other roosters have a high level of "self-confidence" (Ligon et al. 1990). Roosters rapidly became accustomed to moving on the tethers without stumbling or other abnormal locomotion and exhibited the full range of normal courtship behaviors. In 1987, the hen was left in the pen for 1.5 h; for the first and third half-hour periods, the roosters' courtship displays and crowing were re- corded by an observer in a blind fitted with one-way glass outside the enclosure. In 1988, we did not observe roosters before the hen was released, and the hen was left in the pen for 1 h instead of 1.5 h.

The hen was released from the pen without the observer's entering the enclo- sure by ropes attached to the pen and the blind. The observer recorded the courtship behavior of the two roosters as well as the amount of time the hen spent "in residence" (in the same portion of the enclosure and in back of-the partition)

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FEMALE CHOICE IN JUNGLE FOWL 463

with each male. Courtship-behavior scores consisted of the number of times each rooster performed the following behaviors: crowing, wing flapping (a vigorous motion in which the wings meet over the back, usually accompanied by a "pop- ping" sound), waltzing (the male lowers one wing and circles behind the hen), crouching-scratching (the male crouches on the ground and scratches at the substrate with his feet), and "tidbitting" (the male picks up an item such as a twig or stone and drops it several times while emitting a low sound) (Stokes 1971; Stokes and Williams 1971; Gyger and Marler 1988). In 1988 only, behaviors were classified according to whether they were done in the presence (hen resident) or absence of the hen. Behavior data thus consisted of both prerelease and post- release displays for 1987 roosters and of postrelease displays only for 1988 roosters.

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 0.5 h of her release. The solicitation crouch is a distinctive posture in which the hen lowers her tail, spreads her wings, and freezes in a crouched position (Kruijt 1964; Wood-Gush 1971). If neither copulation nor a crouch occurred, we discarded the trial. A male was never used more than once per day.

Multiple regressions were computed with the general-linear-models procedure of SAS (SAS 1985). In all cases Type III sums of squares and their associated P values were used to test hypotheses; unlike the Type I sums of squares used in simple linear regression, Type III sums of squares are not affected by the ordering of independent variables in a model (SAS 1985).

RESULTS

Female Preference for Male Ornaments Trials using all cockerel (yearling) roosters.-Female preference data were

analyzed in two different ways. First, "mating success" was tallied for each rooster by the number of times he was chosen by hens. In 1987, this score was merely the number of matings, ranging from zero to five, since each male was used exactly five times. In 1988, scores were calculated by dividing the number of times a male was chosen by the number of trials in which he was used and then transforming the resulting percentage to the arcsine square root. These mating- success scores were then used in multiple regressions using the male characters as independent variables and mating success as the dependent variable.

Females showed preferences in both years, but the traits preferred were some- what different in the two sets of trials (table 1). In 1987, comb length explained the most variation in mating success, although roosters with redder irises, redder hackle and head feathers, and yellower saddle-feather tips were also preferred. Although the P value associated with the Type III sums of squares for iris hue is not significant, the value was significant in an analysis using ordinary Type I sums of squares and was also significant in the analysis described below; thus, it is included here. Tarsus length, indicating body size, and the lengths of the spur and ornamental feathers were unimportant in explaining variation in mating success, as was the color of the comb and wattles.

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464 THE AMERICAN NATURALIST

TABLE 1

MATING SUCCESS AND MALE MORPHOLOGY

Multiple-Regression Type III Year and Variable Coefficient Sum of Squares P

1987:* Comb length .07 (.02) 6.69 .01 Iris hue - .07 (.07) .70 .35 Hackle hue -.32 (.14) 4.09 .03 Head-feather hue .17 (.09) 2.52 .08 Saddle hue .20 (.10) 3.09 .06

1988:t Comb chroma .09 (.03) .35 .01 Iris value .14 (.08) .14 .09 Hackle hue .05 (.02) .20 .04 Percentage of ear yellow .002 (.001) .17 .06

NOTE.-The dependent variable in both years was mating success; in 1987, this was the number of times chosen by hens, and in 1988, the percentage of the number of times chosen transformed to the arcsine square root. Standard errors are in parentheses. See the text for an explanation of male characters and how they were measured.

* F = 4.79, df = 5, 25, r2 = 0.49, P = .003. t F = 3.78, df = 4, 55, r2 = 0.22, P = .009.

In 1988, comb length was unrelated to mating success, whereas comb chroma (the saturation with pigment, or brightness) was significantly associated with a tendency to be chosen (table 1). Iris value, hackle hue, and percentage of ear yellow were also associated with mating success. As in 1987, tarsus length and feather lengths did not explain significant amounts of variation. In general, prefer- ences were not as strong in 1988 as in 1987; the multiple regression explains only about 20% of the variation in mating success, compared with 50% in 1987.

The data were also analyzed with respect to each trait separately, with each trial as an independent data point and with the differences between winner and loser scores examined for the male characters within each trial. These differences were then subjected to signed-rank tests, with the null hypothesis that the mean of the differences is zero; if females have no preferences for particular traits, combs of winners should be bigger, irises redder, and so forth, than those of losers as often as the reverse.

In 1987, significant preferences were shown for longer combs and redder irises (table 2), but these were the only traits that showed significant departures from the null hypothesis. In 1988, comb chroma, percentage of ear yellow, and hackle-tip hue were all significantly different between winners and losers, but in these trials the winners had yellower hackles rather than redder, as was the case in 1987. Head-feather hue and iris value (darkness) were close to significant in 1988 as well (P = .10). In both years, then, results from the traitwise analysis are consistent with the outcomes of the multiple regressions.

Trials using cocks and cockerels.-Females chose the younger birds in 13 of the 19 trials; this preference is not significant. The cocks-versus-cockerels trials were analyzed with only the second technique of subtracting the loser's score from the

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FEMALE CHOICE IN JUNGLE FOWL 465

TABLE 2

DIFFERENCES IN MALE MORPHOLOGY (WINNER'S SCORE MINUS LOSER'S SCORE) FOR ALL YEARLING ROOSTERS

Year and Trait X Difference Signed-Rank Statistic P

1987 (n = 83): Comb length (mm) 2.95 614 .01 Iris hue (U) -.81 -284 .03

1988 (n = 248): Comb chroma (U) .17 420 .02 Hackle hue (U) .21 749 .05 Percentage of ear yellow 5.02 1,757 .03

NOTE.-All other traits measured showed no significant differences between winners and losers. U, unit value on Munsell scale. See the text for an explanation of male characters and how they were measured.

TABLE 3

WINNER-MINus-LoSER SCORES IN COCK-VERSUS-COCKEREL TRIALS

Trait (n = 19) X Difference Signed-Rank Statistic P

Saddle hue (U) 1.11 22 .01 Sickle length (mm) - 180 - 14 .02 Saddle length (mm) - 34 - 55.5 .03

NOTE.-All other traits measured showed no significant differences between winners and losers. U, unit value on Munsell scale. See the text for an explanation of male characters and how they were measured.

winner's because each individual was used only once. The only color character on which losers and winners differed significantly was saddle-feather hue, with winners having lighter saddles than losers (table 3). Chosen males also had shorter saddles and shorter sickle feathers, although this was probably due not to female preference for shorter feathers but to a preponderance (nonsignificant) of younger birds in the sample of winners (see below).

A comparison of the cocks and cockerels used in the mate-choice trials (table 4) showed that the two groups differed significantly in mean values for several characters: saddle length, sickle length, spur length, comb chroma, and weight. However, no significant differences were found in any of the feather-color traits or in comb length (table 4).

Correlations among male traits.-Table 5 shows the correlations among male traits in the 2-yr period. Correlations were drawn from the group of 48 roosters used in 1987 for both mate-choice and male-competition tests (Ligon et al. 1990). In general, traits were not significantly correlated within the male groups, espe- cially when taking into account the large number of simultaneous tests, and few or no correlated traits were used together in the multiple-regression analyses. In addition to the data in the table, the different comb-color measures (hue, value, and chroma) were correlated in the 1987 data set, and hue and chroma likewise in 1988. Roosters with lighter saddle feathers also significantly tended to have lighter

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466 THE AMERICAN NATURALIST

TABLE 4

COMPARISON OF MORPHOLOGY IN COCKS AND COCKERELS

Trait Cocks X Cockerels X t P

Spur length (mm) 40.28 (2.48) 11.05 (.44) 11.60 <.001 Sickle length (mm) 467.4 (26) 217.3 (44.7) 4.83 <.001 Saddle length (mm) 172.7 (8.2) 130.2 (8.5) 3.61 .001 Weight (g) 1,370 (38) 1,227 (25) 3.12 .004 Comb chroma (U) 8.42 (.33) 10.42 (.84) -5.27 <.001 Comb length (mm) 73.15 (1.40) 75.62 (2.29) -.90 .37 Iris hue (U) 15.13 (1.54) 12.63 (.69) 1.48 .15 Percentage of ear yellow 17.89 (5.34) 14.47 (2.67) .57 .57 Hackle hue (U) 22.83 (.40) 22.83 (.36) .00 1.00 Saddle hue (U) 11.18 (.29) 11.94 (.32) - 1.74 .09

NOTE.-Comparisons used Student's t statistic with correction for unequal variances where appro- priate. n = 19 cocks and 19 cockerels. Standard errors are in parentheses. U, unit value on Munsell scale. See the text for an explanation of male characters and how they were measured.

TABLE 5

CORRELATIONS AMONG MALE TRAITS WITHIN YEARS

1987

Percentage Tarsus Comb Iris Comb of Ear Hackle Saddle Sickle Length Length Hue Chroma Yellow Hue Hue Length

1988: Tarsus length ... .19 -.07 -.18 -.11 -.08 -.25 .24 Comb length .31* - .15 - .12 .37* - .04 - .29 - .23 Iris hue .08 -.05 -.07 -.09 .19 -.26 -.14 Comb chroma .02 .01 .05 -.19 -.09 .26 .04 Percentage of

ear yellow -.20 -.22 -.01 .34** -.32* -.10 -.20 Hackle hue -.17 -.11 -.12 -.10 .07 .54** -.04 Saddle hue - .14 - .22 .06 - .17 .01 .39** .04 Sickle length .23 .04 - .16 .12 - .24 - .01 - .18 ...

NOTE.-All coefficients are Pearson product-moment correlations. Correlations for 1987 appear above the diagonal; those for 1988 appear below the diagonal. n = 60 roosters in 1988, 48 roosters in 1987.

* P < .05. ** P < .01.

hackle feathers in both 1987 and 1988, and head-feather color was positively correlated with hackle-tip color in 1988 only.

Comparison across years.-A comparison of the two groups of males used in the different years shows that males in 1987 had combs that were more saturated with pigment and yellower hackle feathers (table 6); these were the only differ- ences relevant to the mate-choice experiments.

Seasonal changes in comb length.-Of 19 roosters' combs measured in late summer in 1987, after the breeding season was over and molt had begun, all became smaller, with a mean difference of 9.86 mm; this change is highly signifi- cant (paired t = 5.44, P = .0001).

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FEMALE CHOICE IN JUNGLE FOWL 467

TABLE 6

COMPARISON OF ROOSTERS USED IN I987 AND I988

Trait 1987X 1988X t

Tarsus length 76.63 (3.74) 74.45 (4.15) 2.85** Comb length 75.72 (6.94) 75.12 (5.15) .50 Iris hue 11.46 (2.72) 12.06 (2.04) 1.27 Comb chroma 10.58 (1.16) 9.63 (.86) 4.73** Percentage of ear yellow 17.19 (19.9) 26.00 (30.9) 1.79 Hackle hue 22.66 (1.34) 21.52 (1.22) 4.54** Saddle hue 19.38 (1.89) 19.21 (2.03) .44 Sickle length 233.5 (206) 331.4 (78.4) 3.09**

NOTE.-Comparisons used Student's t statistic with correction for unequal variances where appropriate. n = 48 in 1987 and 60 in 1988. Standard deviations are in parentheses. See the text for an explanation of male characters and how they were measured.

** P < .01.

Female Preference for Male Courtship Behaviors

In both years, data were analyzed by using the difference between the winner's and the loser's display-behavior scores in each mate-choice trial and performing signed-rank tests on the differences.

Results from 1987.-The amount of crowing and wing flapping by each male before the hen was released from the pen appeared to be unrelated to the likeli- hood of a male's being chosen (signed-rank statistic, S = - 196 for crows, - 162 for wing flaps; P > .3 in both cases). Hens did spend significantly more time in residence with the male they chose, even after residence times were standardized by dividing by the trial length (S = 753, P = .001). Many trials were too short to contain much courtship behavior at all; in 28 of the 83 trials, females mated in 2 min or less.

In general, waltzing, tidbitting, and crouching scratching were performed only after the female was released and usually while she was in residence. The only courtship behavior that differed significantly between winners and losers was the number of waltzes, which again was standardized by dividing by the amount of time the hen spent in residence with the male in question; scores thus represented the frequency of a behavior corrected for the total opportunity the rooster had for performing that behavior (table 7). No significant differences in numbers of crows or wing flaps performed after the hen was released were detected between winners and losers (S = - 37 for crows, - 1 for wing flaps; P > .7 in both cases).

Results from 1988. -As in 1987, females remained in residence with the chosen male longer than with the rejected male, even after residence time was divided by trial length (S = 6,125, P < .001). None of the courtship displays differed between winners and losers, regardless of whether the hen was in residence with a particu- lar male or not (table 7), except for waltzes performed while the female was out of residence; winners in this instance showed more waltzes than did losers (table 7). It should be noted that roosters sometimes waltzed while a hen was out of residence but still in view. Overall, then, male courtship behavior appeared to be relatively unimportant in determining which rooster was chosen.

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468 THE AMERICAN NATURALIST

TABLE 7

MALE COURTSHIP DISPLAYS IN I987 AND I988 (WINNER-MINUS-LOSER SCORES)

1988 X

BEHAVIOR 1987 X Hen Resident Hen Not Resident

Crowing -.81 (6.30) .25 (.97) -.02 (.97) Waltzing 1.28 (5.16)** .19 (1.52) .11 (.70)* Wing flapping -.66 (8.20) .10 (.63) .01 (.42) Tidbitting .04 (1.05) .04 (1.05) .03 (.28) Crouching-scratching .06 (1.29) .43 (2.07) .03 (.34)

NOTE.-Scores are the number of times a behavior was performed by the chosen male minus the number of times it was performed by the unchosen male. For 1987, scores were standardized by dividing by the amount of time a hen spent in residence with a particular rooster to give a rate of behaviors per minute. For 1988, "hen resident" scores were standardized as for 1987, but "hen not resi- dent" scores were the differences divided by the total trial length minus the residence time; thus, the scores are for solitary displays. Standard deviations are in parentheses. Signed-rank tests tested the null hypothesis that the mean differ- ence is zero. See the text for a description of the behaviors.

* P < .05. ** P < .01.

Relationship between Morphology and Behavior To determine whether roosters with particular physical characteristics tended

to have any consistently associated behaviors, we examined Pearson product- moment correlation coefficients between the morphological traits listed in table 5 and an individual's mean score for the following displays: crows, wing flaps, waltzes, tidbittings, and crouches-scratches. Mean scores were obtained by add- ing the number of instances of each behavior that occurred during trials when a particular male was chosen and dividing by the number of those trials. No signifi- cant association was found between display rates and any of the secondary sex characters.

DISCUSSION

Female red jungle fowl have clear mating preferences that appear from our data to be based almost entirely on morphology. Here we consider the significance of male morphology and behavior separately and discuss both the limitations im- posed by our experimental design and the implications of our results for current models of mate choice and sexual selection.

Female Preference for Male Morphology Hens solicited copulations from males nonrandomly in both years of the study.

Preferences seemed to be most pronounced for various characteristics of the head, including eye color; although in 1987 comb length was the most important correlate of mating success, in 1988 deep comb chroma was the prominent preferred trait. This and other discrepancies between the years (e.g., the impor- tance of percentage of ear yellow in 1988) remain unexplained; perhaps the rearing of hens used in the tests, although seemingly similar between years, inadvertently

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FEMALE CHOICE IN JUNGLE FOWL 469

resulted in the development of different mechanisms of choice in the two groups of females (for a discussion of the effect of female mate-choice mechanisms on sexual selection, see Zuk 1990a). Roosters used in the 2-yr period did differ in hackle hue and comb chroma; comb chroma, which explained a significant amount of variation in 1988, was much more brilliant in the roosters tested that year. Perhaps the available spectrum of males also influenced female preference (Zuk et al. 1990a).

The lack of female preference for older males is consistent with the similarity between our groups of cocks and cockerels in precisely those characters that the hens used to make their choices in 1987. This is to suggest not that cocks in general do not have longer combs or redder feathers than cockerels but that in our small sample the traits did not differ and hence the hens were not choosy, which supports our conclusion that the comb, eye, and feather characters were the critical ones. Females did not seem to respond to any other character intrinsic to older males, although older birds may have other advantages in natural popula- tions of jungle fowl (Ligon et al. 1990). Unlike von Schantz et al. (1989), we found no relationship between spur length and female preference, but the variation within the yearling birds may have been insufficient to allow such a preference to appear.

Nonrandom mating has been observed previously in both unconfined flocks of jungle fowl (Lill 1966; Thornhill 1988) and domestic chickens (Guhl et al. 1945; Guhl and Warren 1946; Guhl 1951), although most of these studies did not relate the variation in mating frequency to any characteristic other than social domi- nance status, and even this distinction was not always made. Guhl attributed the unequal distribution of mating at least in part to female choice rather than to forced copulations by certain roosters; he noted that "although the cocks courted at nearly the same rates, the hens, as a group, responded most readily to one male" (1951, p. 689). Thornhill (1988) observed that most copulation solicitations were directed toward dominant roosters.

The importance to the hens of comb and eye characters rather than feather or body-size traits is meaningful for two reasons. First, research on several breeds of domestic poultry, on unconfined jungle fowl, and on a natural population of rock ptarmigan has linked comb size and, to a lesser extent, comb color to social behavior, dominance, and mating success. Siegel and Dudley (1963) found that pea-combed individuals were subordinate to single- (larger-) combed birds in mixed flocks, and comb shape and size are also apparently important in individual recognition (Guhl and Ortman 1953; Candland 1969). Hens with larger combs won more social encounters than did hens with smaller combs (Collias 1943); each contestant's face "becomes red and flushed" before a fight, and the loser's "pales" afterwards (Collias 1943, pp. 520-521). Hens that had their combs experi- mentally dubbed became subordinate to hens with unaltered combs, even if they had previously been dominant to the undubbed birds (Marks et al. 1960). Comb size and color are thus important in a variety of social interactions in both sexes.

Most directly relevant to our study of the role of ornaments in mate choice is the finding that domestic hens preferentially associate with males with larger combs but are indifferent to the body size of the rooster (Graves et al. 1985); comb size is positively correlated with dominance status, and females familiar with a group of

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470 THE AMERICAN NATURALIST

males prefer the more dominant roosters (Graves et al. 1985). In addition, field observations of a population of rock ptarmigan in Canada showed that males with larger supraorbital combs had more mates than smaller-combed males and that males banded with colors similar to the comb color had more mates the following year than did males with similar-sized combs that had bands with different colors (Brodsky 1988). Among both ptarmigan and jungle fowl, males may peck at each other's combs during fights; damage acquired during fights could therefore in- fluence male mating success by rendering the ornament less attractive.

The second reason that female preference for head ornaments is significant for sexual selection theory is that these traits are facultative and reflect the immediate condition of their bearers more than do feathers (which are molted only once a year). The comb and wattles are used as a general indicator of health in domestic poultry (Hofstad 1978), and illness was associated with combs' shrinking in our roosters (Zuk et al. 1990b). Several "good-genes" models for sexual selection imply or propose this kind of condition-dependent ornament (Zahavi 1975; Hamil- ton and Zuk 1982; Nur and Hasson 1984). Together with the decrease in comb size after the breeding season, these results suggest a cost-physiological, social, or both-of maintaining combs at their healthy, breeding-season length.

Because comb color depends partly on diet, it reflects condition as well; of 17 jungle fowl roosters we reared on a carotenoid-free diet, all had paler combs than a random sample of our test roosters (M. Zuk, unpublished data). Combs were also shorter and less saturated with pigment in jungle fowl roosters experimentally infected with Ascaridia galli, an intestinal roundworm (Zuk et al. 1990b), and comb length and chroma were similarly lower in jungle fowl roosters that had lost fights with other males than they were in the winners of those fights (Ligon et al. 1990). Comb size depends on testosterone level, which may account for this consistency (Ligon et al. 1990). Females using comb length and color as a cue in making mating decisions may therefore be obtaining males in good condition that are capable of supporting the cost of this ornament. If aspects of this good condition are heritable, then females could indeed be selecting "good genes" for their offspring by using ornaments as indicators. Eye color, which also was used by females in making choices, has received less attention in the literature than the comb and wattles, but it seems to be a relatively plastic trait as well, with individuals' iris colors changing within a season (J. D. Ligon, K. Johnson, R. Thornhill, and M. Zuk, unpublished observations).

The Importance of Male Display Behavior

The role of courtship displays in jungle fowl female choice seems minimal. Hens often mated with roosters that had not displayed at all, and the rate or nature of the displays had little bearing on which male was chosen. Several explanations of these results are possible. First, females may use courtship behavior, but only in a coarse way, to ensure that roosters are sexually competent; the performance of several of the displays is at least partially testosterone-dependent in domestic chickens (Davis and Domm 1943). Lill (1966) noted that male waltzing usually precedes female crouching in jungle fowl but drew no conclusions about the effect of waltzing on the hen. Waltzing also occurs in fights between roosters and may signify nothing more than a general level of excitement.

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FEMALE CHOICE IN JUNGLE FOWL 471

Second, displays may function primarily in male-male interactions, and the design of our experiments, which minimized such interactions, may have pre- vented a complete evaluation of their importance. Collias (1987) suggested that crowing might attract females; we suspect it may serve more as a challenge to other males, with hens perhaps attending to the outcome of the challenges but not to the signal itself. It was clear to the observers that the two test roosters crowed at different rates before females were released from the pen, but we obviously cannot assess the response of the hen to any fights that might have resulted had the roosters not been tethered.

Displays may also be used by hens in a manner we were unable to measure. We calculated the rates of the various displays but did not measure vigor or any more subtle variations of the behaviors. The crow is a complex vocalization (Collias 1987) and may contain information about the individual producing it; a more detailed spectrographic analysis of crowing is planned for future experiments. Calls given during tidbitting are likewise variable, and in domestic chickens tidbitting depends on, among other things, the relationship between the male and female (Gyger and Marler 1988). The availability of real food items for tidbitting might also have had a different effect on the hen; in our trials, males used twigs or pebbles for tidbits, and, although this probably also occurs in nature, roosters often provide insects to females.

This distinction between behavior and morphology is, in a sense, artificial since male ornaments change depending on behavior itself, as described above. From a female's perspective, evaluating morphology during several different behavioral conditions may provide a good means of assessing male quality.

In conclusion, females mated more frequently with males possessing particular secondary sex characters, characters that are consistent with the results of previ- ous research and that may potentially indicate male condition. It is, of course, possible that females make arbitrary, nonadaptive choices, and such choices can theoretically be associated with the evolution of exaggerated male ornaments (Lande 1981; Kirkpatrick 1982). Our results suggest that the operation of adaptive mate choice is at least empirically plausible. Experiments examining the role of male ornaments in male competition revealed that larger males and ones with longer combs that were more saturated with pigment were more likely to win fights (Ligon et al. 1990). This concordance between the traits important in male competition and in female choice is predicted by several good-genes models (Hamilton and Zuk 1982; Thornhill and Alcock 1983; West-Eberhard 1983). Ex- amination of the heritability of both male ornaments and female preferences is currently in progress. Future experiments are also intended to elucidate more precisely the nature of female preferences through experimental manipulations of male ornaments.

SUMMARY

Mate-choice experiments allowing a female red jungle fowl (Gallus gallus) to choose between two roosters showed female preferences for several male second- ary sex characters. In 1987, male comb length was most strongly related to mating success, with eye color and the color of some ornamental feathers also being

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472 THE AMERICAN NATURALIST

important in choice. In 1988, males with darker, redder eyes were again chosen more frequently, but comb color explained a significant portion of mating-success variation, whereas comb length was unimportant. Females did not choose older males over younger ones, but, in our sample, older and younger roosters did not differ on the basis of traits used in making choices. Male courtship behavior was generally not significantly different between chosen and unchosen males, and behavior was not correlated with morphological characters. Comb characteristics are facultative and are probably good indicators of individual condition, suggest- ing that females using these traits to distinguish among males could be obtaining good genes for their offspring.

ACKNOWLEDGMENTS

We are grateful to the many people who assisted with the care of the birds and helped run experiments: C. Blanco-Montero, D. Keller, C. Kropek, J. McCona- chie, M. Melloy, S. Portman, D. Shippert, A. Thornhill, and P. Thornhill. A. Risser of the San Diego Zoo kindly supplied us with jungle fowl. S. Arnold, P. Weatherhead, and 6-10 anonymous reviewers made useful comments on the manuscript. J. T. Rotenberry gave useful statistical advice. This research was funded by National Science Foundation grant BSR-8515377 (to R.T. and J.D.L.) and received support from D. Duszynski and the University of New Mexico biology department and from P. Risser.

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