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Behavioral Ecology Vol. 14 No. 5: 593-601
© 2003 International Society for Behavioral Ecology
Food, vigilance, and sperm: the role of male direct benefits in the evolution of female preference in a polygamous bird
Evolutionary Ecology Group, Animal and Plant Sciences Department, University of Sheffield, Sheffield S10 2TN, UK
Address correspondence to T. Pizzari, who is now at the Section of Ethology, Department of Animal Environment and Health, Swedish University of Agricultural Sciences, PO Box 234, SE-532 23 Skara, Sweden. E-mail: tom.pizzari{at}hmh.slu.se.
Received 3 September 2001; revised 4 June 2002; accepted 1 October 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The adaptive significance of female selection of copulation partners remains unresolved, particularly in polygamous species where males do not provide paternal care. In these species the possibility that direct benefits other than paternal care may play an important role in the evolution of female choice has received little attention. I tested whether direct benefits are associated with female choice in the polygamous feral fowl, Gallus g. domesticus, where females prefer socially dominant copulation partners and males do not care for the young but do provide females with three commodities: food, vigilance, and sperm. I used a combination of empirical and experimental data to show that male propensity to offer food and vigilance, but not sperm, was positively associated with male social status, suggesting that the provision of these resources may be costly and condition dependent in males. Copulation success was correlated with male status but not with the number of feedings a female received from a male, indicating that a female preferred dominant partners that in general provided any female with more food, rather than partners that provided only her with more food, consistent with the idea that females may use male resource provisioning as a proximate mechanism to assess male condition. Together, these results indicate that male resources provisioning is (1) tightly linked to male social status, (2) a potential indicator of male condition and possibly genetic quality, and (3) a potential criterion for females to select dominant partners, thus playing an important role in the evolution of partner choice even in polygamous species lacking paternal care.
Key words: condition dependence, courtship feeding, ejaculate size, mate choice, social dominance, vigilance.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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One of the most debated issues in evolutionary biology concerns the mechanisms that promote and maintain nonrandom mating. Part of the variance in male reproductive success is often explained by variation in a male's ability to compete for copulation (Andersson, 1994
; Darwin, 1871) and by variation in fertilization opportunities (Birkhead and Pizzari, 2002; Pizzari and Birkhead, 2002). However, it is well established that variation in paternity is also caused by females that may consistently prefer to copulate with and use the sperm of certain males (Andersson, 1994; Birkhead and Pizzari, 2002). Although male–male competition and female selection often operate in unison, with females favoring inseminations from socially dominant males (Andersson, 1994; Pizzari et al., 2002), this is not always the case (Moore and Moore, 1999; Qvarnström and Forsgren, 1998), and the evolution of female preference for dominant copulation partners is unresolved (Qvarnström and Forsgren, 1998).
A potential mechanism driving the evolution of female preference is the pursuit of direct benefits (Gwynne, 1984; Gray, 1997; for reviews see Andersson, 1994; Choe and Crespi, 1997; Reynolds, 1996), and thus females might prefer dominant males because such males trade copulations for high-quality resources. However, the evidence that dominant males provide females with resources of superior quality remains inconclusive (Qvarnström and Forsgren, 1998; Sæther et al., 1999). The pursuit of direct benefits seems even less likely in polygamous species where males typically do not provide the most obvious of resources, paternal care, and where direct male contribution to reproduction is assumed to be limited to the provision of semen (Kirkpatrick and Ryan, 1991). This assumption has led to the hypothesis that female preference in polygamous species may be explained by genetic benefits (Birkhead and Parker, 1997; Bradbury and Gibson, 1983; Kirkpatrick and Ryan, 1991). Preference for socially dominant males may thus be driven by the pursuit of alleles associated with superior fitness. However, although there is some evidence that social dominance can be transmitted from parents to offspring in some species (e.g., Craig et al., 1965; Moore, 1990), few studies have found convincing evidence that genetic benefits explain female partner choice (David et al., 2000; Wilkinson et al., 1998), while others have produced more ambiguous results (Brooks, 2000; Griffith et al., 1999; Holland, 2002; Holland and Rice, 1999) or have identified environmental mechanisms confounding results consistent with genetic benefits (reviewed by Sheldon, 2000). Theoretically, males of polygamous species may influence female reproductive success directly even without providing paternal care (Reynolds and Gross, 1990; Sheldon, 1994), and the few studies that have tested this idea have focused on the possibility that female preference evolves to reduce direct costs such as sexual harassment (e.g., Sæther et al., 1999).
In the typically polygamous fowl, Gallus gallus, paternal care does not occur but males provide females with three types of resources: (1) food, through courtship feeding (Evans and Evans, 1999; Kruijt, 1966; Stokes, 1971), (2) vigilance against predators (Johnson, 1963; McBride et al., 1969; Sullivan, 1991), and (3) sperm. However, the relationship between the provision of these commodities and male fitness has never been clarified (e.g., Evans and Evans, 1999). Female fowl preferentially copulate with socially dominant males (Johnsen et al., 2001; Pizzari, 2001; Pizzari and Birkhead, 2000) and eject the ejaculates of subordinates when these overcome female resistance (Pizzari and Birkhead, 2000). However, the adaptive significance of this female preference remains unclear. A previous study (Pizzari, 2001) showed that female fowl may reduce sexual harassment from subdominant males by associating with dominant males, indicating a potential role for direct effects in the evolution of female preference.
In the present study I investigated the role of male provision of food, vigilance, and sperm in the evolution of the female preference for socially dominant copulation partners. First, if male provision of food, vigilance, and/or sperm contributes to the evolution of female preference for dominant partners, I expected social status and the propensity to provide some or all of these resources to be positively associated. Second, subdominant males may resort to the provision of resources to compensate for impaired attractiveness, generating a negative relationship between male status and propensity to provide resources. Third, male provision of resources may not covary with male status, for example, because it may have lost its effect on male reproductive success. This is a correlational approach that does not test the causality of a potential relationship. However, if an association between male resource provisioning and status is found, the propensity of dominant and subdominant males to provide resources can be further demonstrated experimentally.
Female preference can be associated with male resource provisioning (first scenario) through two mechanisms: (1) females prefer dominant males because they obtain superior resources from them (i.e., the pursuit of direct benefits is the ultimate mechanism driving female preference), and/or (2) because of genetic benefits potentially associated with high status and the provision of superior resources (i.e., the pursuit of indirect benefits is the ultimate mechanism driving female preference, and resource provisioning may be a proximate clue used by females to select partners providing better indirect benefits). To the extent to which the provision of food, vigilance, and sperm is costly to males, the propensity of a male to provide these resources may reliably indicate male condition. Because male condition may be heritable (David et al., 2000; Kotiaho et al., 2001), females may prefer to copulate with males that provide more food, vigilance, and sperm because of the genetic benefits that such males may convey to the offspring. These two mechanisms are not necessarily mutually exclusive (female preference may result in both direct and indirect effects), but generate diverging predictions. The direct benefit hypothesis predicts a positive association between the benefits delivered to a female by a male and her propensity to preferentially copulate with him, regardless of whether resource provisioning is costly to males. The indirect benefit hypothesis predicts that male resource provisioning is costly and condition dependent, indicating that propensity to provide resources is higher in dominant males and that a female prefers to copulate with the male with the highest propensity to provide commodities, regardless of whether his efforts are preferentially directed to her or to other females. Therefore, by determining the extent to which copulation success is explained by the resources provided by a male to a female, and by male status, which is reflected by the propensity to provide any female with resources, it is possible to establish the role played by male resource provisioning in female preference.
The aims of the present study were to (1) test the phenotypic relationship between male social dominance and male provision of food, vigilance, and sperm, (2) measure the propensity of dominant and subdominant males to provide these resources under experimental conditions, and (3) establish the relative importance of direct effects in female preference for dominant males in the case of courtship feeding, where male investment in individual females is more easily quantified, by measuring the extent to which individual females favor males that provide them with more food or males that in general provide females with more courtship feeding.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Study populations
I studied a feral, free-ranging population of domestic fowl of a breed (Bankiva or Swedish bantam) from South Asia (Harrison, 2001
), morphologically and behaviorally close to the red junglefowl, Gallus gallus (Harrison, 1987; Pizzari and Birkhead, 2000; 2001; Schütz and Jensen, 2001), at the research station of the University of Stockholm (Sweden). From April to July 1998 the study population comprised 13 males and 21 females; from April to July 1999 the population comprised 10 different males and 13 different females (Pizzari and Birkhead, 2001); and from June to July 2000 the study population comprised 11 males and 28 females.
Male social dominance
I assessed male social status on the basis of the outcome of naturally occurring pairwise interactions. Because the aim this study was to determine the effect of social status on male reproductive strategies, competitive interactions over females and copulation opportunities were not used to assess male dominance. The status of each male was estimated according to Clutton-Brock et al. (1979):
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b is the total number of males defeated by the losers, L is the number of males that on average outcompeted the focal male, and l is the total number of males that outcompeted them. In experimental trials, where males were divided in pairs, I assessed social dominance between male pair members on the basis of the number of times one male avoided the other. The male that was significantly more likely to be avoided was regarded as dominant (Pizzari, 2001).
Copulation behavior
The behavioral sequence leading to a copulation has been extensively described in the domestic fowl (Etches, 1996; Guhl, 1962; Wood-Gush, 1971). The birds were fully habituated, and most copulations were observed at 
5 m distance. I monitored copulation behavior through focal watches and ad libitum observations of the whole population (see Pizzari, 2001; Pizzari and Birkhead, 2000, 2001). I used two measures of female choice of copulation partners: (1) copulation success, which is mainly determined by direct and indirect selection of males by females (Pizzari, 2001; Pizzari and Birkhead, 2000) and (2) female resistance to copulations (Pizzari, 2001). I defined a copulation as solicited by the female when she crouched in front of the male. Copulations in which the male forcefully mounted the female in the absence of female solicitation were regarded as forced. A copulation was resisted if the female avoided the male or lowered her tail once the male had mounted her. A female passively accepted a copulation when she raised the tail to facilitate cloacal contact after mounting. Copulation attempts were behaviorally successful when cloacal contact was observed directly or when it was assumed to occur when the male's tail was lowered over the female's cloaca.
Courtship feeding
When courtship feeding, male fowl use a specific call (food call) to signal the presence of a food item that they feed to the female attracted by such call (Collias, 1987; Evans and Evans, 1999; Kruijt, 1966; Stokes, 1971). Courtship feeding is stimulated by the presence of females (Evans and Marler, 1994) and, in turn, attracts females that are then fed and courted (Marler et al., 1986a). I observed male courtship feeding behavior as signaled by food calls and recorded male identity, the number of females attracted, and their identity. Sometimes males may cheat, uttering food calls in the absence of food (Stokes, 1971). I established the honesty of a food call by recording whether food was present. During a food call the food item is visible, as males hold the food in their beak while calling or point to it with a specific behavior (tid-bidding; Kruijt, 1966). When calls were dishonest, males would use inedible objects like twigs to mimic a food item (see also Stokes, 1971), and neither the attracted female(s) nor the calling male ate the item.
Courtship feeding and copulation may be tightly or loosely associated in time. I tested both possibilities by investigating the relationship between the frequency of copulation and courtship feeding of a male with individual females within 10 min after courtship feeding and over the whole reproductive season.
Upon finding a food item, a male can either eat it or call a female to feed it to her. I conducted an experiment to test whether the probability of a male eating a food item rather than feeding it to a female covaried with his social status.
To control for the effect of food quality on the probability of courtship feeding, I experimentally provided males with food items of the same size and nutritional quality (one boiled pasta noodle, mass = 0.70 g). One male at a time was provided with a noodle when isolated from other birds to prevent other males and females from detecting the presence of food and influencing the behavior of the focal male (Marler et al., 1986b) and to prevent females from knowing the honesty of a food call. A male was provided with a noodle when other males and females were at least 10 m away from him, and the noodle was left on the ground, in proximity of the focal male and hidden from the other birds. In each trial, which lasted for 20 min, I recorded the time of the day to establish whether this had an effect on male propensity of courtship feeding. Because fowl fed throughout most of the day, the cost of feeding a food item to a female rather than eating it is expected to decline with time as males become satiated.
Vigilance
Male fowl are often vigilant, and they use two types of alarm call to signal aerial and terrestrial predators (Collias, 1987). Females respond to both types of male alarm calls by becoming alert and seeking cover (Evans and Marler, 1994; Pizzari, personal observation). In 1998 I investigated differential investment in vigilance by monitoring the alarm calling behavior of the males in the free-ranging population. Because the population acted as a single social unit (Pizzari and Birkhead, 2001), the probability of detecting the alarm calls of different males was equally high. The type of alarm call and the identity of the calling male were recorded. In some cases other males would join in calling: when this occurred only the identity of the male that called first was recorded. However, estimating vigilance effort on the basis of alarm calling makes the assumption that alarm calling is a reliable indicator of vigilance effort. I experimentally tested this assumption in 1999.
The aims of the vigilance experiment were to test (1) whether dominant males spent more time being vigilant than their subordinates, (2) whether the rate of alarm calling was proportional to the time spent vigilant, and (3) whether females benefited from male presence by allocating less time to vigilance. From 27 April to 5 August 1999, 11 pairs of males were housed in outdoor pens (3 x 6 m), and 9 of them were kept in visual contact with a female in a similar, adjacent pen. I assessed the social relationship between members of each male pair by recording the outcome of competitive interactions (see above). The male that defeated his opponent was considered the dominant of the pair and the other his subordinate. Interactions were monitored through observation periods varying in duration (see below) and ad libitum throughout the duration of experiment to investigate the repeatability of interaction outcomes. In no case was the dominance relationship reversed, and in each pair one male consistently won over the other (n male pairs = 11, Exact sign test: p <.001). To reduce fighting I used males that were familiar with each other and with each other's competitive ability.
In every trial, I used a stopwatch to measure the time spent vigilant by both males of each male pair to the nearest 0.6 min and recorded the number of alarm calls to both terrestrial and aerial predators produced by each male. The amount of time spent vigilant by females was also recorded. I considered a bird vigilant if both eyes were kept fully open and it did not exhibit frontal fixation (Evans and Evans, 1999) toward the ground, toward his- or herself, or toward the interior of the nest-box. Both dominant and subdominant males allocated a repeatable (sensu Lessells and Boag, 1987) proportion of time to vigilance (dominant males: F = 7.74, df = 10, 165, r =.29, p <.001; subdominant males: F = 12.4, df = 10, 166, r =.41, p <.001). To exclude the possibility of a male calling in response to the other males' alarm calls rather than to potential predators, an alarm call was ignored if uttered within 10 s the call of the other male.
A constant observation time may translate into a bird spending a similar amount of time being vigilant, thus limiting the potential to establish the relationship between vigilance time and the frequency of alarm calling. To test whether the frequency of alarm calling covaried with vigilance, I increased the variance in the time spent vigilant by individual males by varying the duration of the observation period, randomly assigning individual observation periods the duration of 10, 20, 30, 40, 50, or 60 min. Male pairs were then randomly assigned to have either the dominant or the subdominant male removed. I monitored the vigilance and alarm calling behavior of the remaining male and female as described above. Subsequently the remaining male was removed and the behavior of the female alone was observed. If females adjusted the time spent vigilant to male vigilance time, female vigilance should be negatively correlated with male vigilance and should increase when one male is removed, increase more when the most vigilant male of the pair is removed, and increase further when both males are removed.
Birds were given one day to settle down when first introduced in the experimental pens. Similarly, after a male was removed from the pen a day elapsed before the observations started again on the remaining birds. On average, 1.50 ± 0.18 vigilance trials a day were carried out on each group (i.e., 2 males and 1 female) from 25 April to 30 July 1999. Because some days were relatively overrepresented, I tested whether there was a day effect on the vigilance behavior of males in those pairs that were observed more then once in a day. The proportion of time that dominant and subdominant males spent vigilant did not vary significantly between days (MANOVA; dominants' vigilance, F8,30 = 0.44, p >.50; subdominants' vigilance, F8,30 = 1.12, p >.50).
Sperm
Natural ejaculates were obtained by presenting males with a live female in a soliciting position fitted with a harness for collecting the male's ejaculate (Ishikawa, 1930; Pizzari and Birkhead, 2000). Ejaculates were collected and their volume measured (±0.5–1.0 µl) with a 200-µl pipette (Gilson Pipetman®), and the sperm contained in an ejaculate were counted following Bakst and Cecil (1997). Male sperm reserves are depleted through successive copulations (Birkhead et al., 1988; Dewsbury, 1982; Nakatsuru and Kramer, 1982); therefore, male sperm investment may vary dramatically depending on the copulation frequency. Sperm investment by dominant and subdominant males was quantified when males were not sexually rested but exposed to their natural copulation frequency in free-ranging population in 1999. Sperm collection was concentrated between 1700 h and 2000 h local time, the time of the day when copulations are most frequent in the fowl (Cheng and Burns, 1988; Pizzari and Birkhead, 2001) and when the largest ejaculates are produced (Lake and Wood-Gush, 1956). Sperm collection trials lasted about 20 min, and multiple ejaculates could be obtained from the same male, and the individual males were sampled in multiple trials over successive days. To avoid the pseudoreplication of those males that produced more ejaculates within a trial, I analyzed the effect of social dominance on sperm number, considering exclusively the largest ejaculate produced by a male during a trial, averaged for all the trials (mean number of trials per male: 9.2 ± 1.10). The mean number of sperm contained in the largest ejaculate produced during a trial was used. In addition, I experimentally tested differential sperm investment in 10 of the 11 sexually rested males from June to July 2000.
In the sperm investment experiment, 10 males were kept free-ranging in an enclosure (30 m2) isolated from females, and after each trial, males were sexually rested for at least 2 days to allow them to replenish their sperm reserves (Parker et al., 1942). I exposed males to two series of experimental trials: trials with competition (mean number of trials per male: 2.3 ± 0.26), and trials without competition and successive females (2.5 ± 0.31 trials/male). In competition trials three males were isolated and presented with a female. All males except the focal individual(s) were removed from the study area and enclosed in a pen 2 h before the trial. I allowed each male to copulate ad libitum with a single female in the presence of the other two males. To avoid male–male competitive interactions influencing male copulatory behavior, only one male a time was allowed to mount the female, while the other two were kept at about 5–10 m from the copulating pair. Each male was able to observe his competitors copulate with the female. In multiple-female trials, a single male was isolated 2 h before the trial and was then given the opportunity to copulate ad libitum with a female.
Because this experiment standardized the conditions under which different males produced ejaculates (i.e., sexual rest, ad libitum number of copulations, presence of competitors), the cumulative number of sperm produced by a male during a trial reflected his sperm investment in a particular female and/or in a series of copulation opportunities. Therefore, I investigated the effect of social dominance on the cumulative sperm investment, both with and without sperm competition.
Data analysis
Statistical tests were conducted with SPSS 10.0.7. I analyzed correlations and tests for difference in means of relatively small data sets nonparametrically (Siegel and Castellan, 1988). Larger data sets that spanned over 2 years of study were transformed to achieve normality and analyzed parametrically, through ANOVAs in which male status was entered as a covariate and year was entered as factorial independent variable to control for between-year differences. I analyzed the results of the courtship-feeding experiment with a logistic regression where the probability of courtship feeding in each trial was entered as the dependent dichotomous variable and male status and time of day were entered as independent variables. Female vigilance effort in the presence of two, one, and no male was analyzed with a repeated-measures ANOVA where the arcsine-transformed proportion of time invested in vigilance by females was entered as the dependent variable and the experimental treatment (i.e., number of males) was entered as the within-subject independent variable with three levels (i.e., two males, one male, no males), and the status of the male left as between subject variable (a nonparametric Friedman ANOVA of the results of this experiment generated identical results). Means are expressed ±1 SE, and all probabilities are two-tailed.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Courtship feeding
High-ranking males produced more, and proportionally more honest feedings than their subordinates (number of courtship feedings, status: F = 16.43, df = 1, 22, p =.001; year: F = 1.20, df = 1, 22, p >.20, Figure 1; proportion of honest courtship feeding, status: F = 4.68, df = 1, 22, p =.043; year: F = 0.39, df = 1, 22, p >.50). When experimentally provided with food, dominant males were more likely than subordinates to feed females rather than eating the food themselves (logistic regression analysis, log-likelihood = 121.85,
2 = 30.6, df = 1, n trials = 112, n males = 13, status: b = 2.66 ± 0.54, Wald = 15.72, p <.0001; time of day was excluded by the regression model: b = 0.00 ± 0.00, Wald = 0.09, p >.50). These results are consistent with the idea that honest courtship feeding is condition dependent and positively correlated with status.
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There was a nonsignificant tendency for the probability of a successful copulation with a female to be higher in the 10 min after an honest (mean probability of copulation: 0.006 ± 0.003) rather than a dishonest food call (0.12 ± 0.004, Wilcoxon paired test: T = 1.0, n males = 13, p =.078). The number of females attracted by a food call over the whole reproductive season covaried positively with male social status (status: F = 9.29, df = 1, 22, p =.006; year: F = 0.005, df = 1, 22, p >.90). The mean number of successful copulations correlated significantly and positively with male social status (Spearman rank correlation: rs =.54, n males = 23, p =.008; Figure 2), but only weakly with the mean number of honest courtship feedings after controlling for the effect of male status (partial correlation: rs =.36, n males = 23, p =.10). Moreover, the number of successful copulations that a male had with different females over the whole reproductive season was not positively associated with the number of times he provided them with honest courtship feeding. In fact, I found only one male for which there was a significantly positive association between the number of honest courtship feedings and number of successful copulations (in 1999, Spearman rank correlation: rs =.59, p =.04, n females = 12). A significant and positive association between number of successful copulation and number of honest courtship feedings was less likely to occur than expected by chance (1 of 11 males, 9.1%, binomial test: p =.002; only males that copulated with and/or provided at least 10 females in 1998 and 4 females in 1999 with honest courtship feeding were considered). In addition, the probability of the relationship between honest courtship feedings and successful copulations was not more likely to be positive than negative across males (number of positive relationships: 6 out of 11, 55%, binomial test: p = 1.0). Similarly, the probability of female resistance to a copulation was not associated with the number of honest feedings received by any male (i.e., no male had a significantly negative correlation between the number of honest courtship feedings and probability of female resistance, number of negative relationships: 5 out of 11, 45%, binomial test: p = 1.0).
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Together, these results indicate that honest courtship feeding is positively associated with male status and with copulation success only to the extent to which honest courtship feeding is correlated with male social status. Therefore, the results are consistent with the hypothesis that female preference for dominant males is associated with male provision of food and suggest that females use male propensity to provide food primarily to assess male condition and status rather than to obtain direct benefits.
Vigilance
In 1998 I found a nonsignificant trend for high-ranking males to utter more alarm calls than their subordinates (Spearman rank correlation: rs =.48, n males = 13, p =.09). Under experimental conditions dominant males allocated on average a higher proportion of time to vigilance than their subordinates (mean: dominants = 0.62 ± 0.04, subdominants = 0.38 ± 0.05, Wilcoxon paired test, T = 65, n pairs = 11, p <.005; Figure 3), which in turn did not spend more time vigilant than females (mean females = 0.35 ± 0.03, Wilcoxon paired test, T = 35 n pairs = 9, p >.10). The frequency of alarm calling of all dominant males was positively correlated with the amount of time spent vigilant (least significant correlation Spearman rank correlation: rs =.46, p =.05). However, in only 2 subdominant males out of 11 (18%, binomial test: p = 1.0; Table 1) was alarm-calling frequency positively correlated with vigilance. A lack of a positive correlation between alarm calling and vigilance time in subdominants was due to subdominant males giving few alarm calls regardless of their vigilance time, limited time invested in vigilance, and dishonest alarm calls. Indeed, in some cases, subdominant males alarmed while resting with their eyes closed. Alarm calling at a rate proportional to vigilance was not randomly distributed relative to male status, as dominant males were significantly more likely to call at a honest rate (Fisher's Exact test, p <.0001).
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When dominant males were removed, the proportion of time their subordinates spent vigilant did not increase significantly (mean proportion of time allocated to vigilance: before = 0.39 ± 0.06, after = 0.43 ± 0.03, Wilcoxon paired test: T = 5.5, n = 6, p >.10); however, they alarmed at a significantly higher rate (mean n alarm calls/s before = 0.03 ± 0.03, after = 0.07 ± 0.06, Wilcoxon paired test: T = 15.5, n = 6, p <.05). When subdominant males were removed, dominants showed a nonsignificant tendency to spend more time vigilant (mean proportion of time allocated to vigilance: before = 0.61 ± 0.06, after = 0.69 ± 0.07, Wilcoxon paired test: T = 15, n = 5, p =.07), but their rate of alarm calling did not change significantly (mean n alarm calls/s before = 0.002 ± 0.001, after = 0.002 ± 0.001, Wilcoxon paired test: T = 7, n = 5, p >.10).
When both males were present, the average female vigilance was not correlated with the average vigilance of the most vigilant male of the pair (Spearman rank correlation: rs =.23, n = 9, p >.10). Females spent less time being vigilant when at least one male was present than when they were alone (mean proportion of time invested in vigilance, two males: 0.32 ± 0.003, one male: 0.38 ± 0.004, no male: 0.64 ± 0.005), but the status of the male removed did not significantly affect female vigilance (repeated-measures ANOVA: female vigilance with two, one, and no males [within-subject variable]: F = 24.39, df = 1, 7, p =.002, status of male removed [between-subject variable]: F = 0.29, df = 1, 7, p >.50, within x between subject interaction: F = 5.32, df = 1, 7, p =.50; Figure 4). However, there was no difference in the time allocated to vigilance by individual females when they were with two or with only one male (Wilcoxon signed test, T = 29, n = 9, p >.10). Furthermore, there was no difference in vigilance between those females that were deprived of the subdominant (0.36 ± 0.005) and those that were deprived of the dominant male of the pair (0.40 ± 0.007, Mann-Whitney U test, U = 5, n subdominants = 5, n dominants = 4, p >.10). These results indicate that male vigilance effort is positively associated with social dominance and are thus consistent with the hypothesis that the provision of reliable vigilance is associated with female preference for dominant copulation partners.
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Sperm
In the free-ranging population, the mean number of sperm produced was not predicted by male status (Spearman rank correlation: rs =.08, n males = 10, n ejaculates = 92, p =.90; top half of the hierarchy: 5.84 x 105 ± 31,632 sperm; bottom half of the hierarchy: 6.20 x 105 ± 59,753 sperm, Mann-Whitney U test: U = 11, p >.10; Figure 5).
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Consistent with the results obtained in the free-ranging population, I found that the mean cumulative sperm investment did not covary with social status either in trials with sperm competition or in trials in the absence of sperm competition (trials with sperm competition: Spearman rank correlation: rs =.15, p >.10; without sperm competition: Spearman rank correlation: rs = -.41, p >.10, n males = 10, n ejaculates = 255). In addition, males of the top half of the hierarchy did not produce more sperm relative to the males of the bottom half of the hierarchy (trials with sperm competition, top: 7.14 x 106 ± 106,520 sperm; bottom: 8.25 x 106 ± 1,262,294 sperm, Mann-Whitney U test: U = 10, p >.10; without sperm competition, top: 1.2 x 107 ± 586,045 sperm; bottom: 1.0 x 107 ± 635,627 sperm, U = 4, p =.10). Together these results indicate that inseminations from dominant males did not deliver more sperm than inseminations from subdominant males and thus are not consistent with the hypothesis that female preference for dominant males is associated with differential provision of sperm.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The main findings of the present study were, first, that the propensity to provide females with food and vigilance, but not sperm, is positively associated with male social status and thus with female preference. Second, under experimental conditions, male propensity to provide females with both food and vigilance is positively correlated with male status, consistent with the idea that male provisioning of resources may signal male condition. Third, consistent with the indirect benefits hypothesis but not with the direct benefits hypothesis, male copulation success is only weakly associated with courtship feeding after controlling for male status.
The potential role played by the provision of direct benefits in the evolution of female preference has been neglected in species lacking paternal care (but see Reynolds and Gross, 1990; Sæther et al., 1999; Sheldon, 1994). The present study shows that the male phenotype preferred by females, social dominance, is closely associated with male propensity to provide females with two of the three commodities studied: food and vigilance.
Because of the tight link between status and the provision of food and vigilance, it is difficult to establish the causality of this relationship. However, the fact that subdominant males were constrained in their ability to provide honest vigilance and courtship feeding is consistent with the idea that not all males can afford to provide these commodities, suggesting that the provision of food and vigilance may be costly and condition dependent in male fowl and therefore unlikely to be selectively neutral. Furthermore, female fowl did not choose copulation partners according to the number of feedings obtained from individual males but according to male propensity to provide any female with honest feedings. This suggests that courtship feeding may be used to assess the condition of potential partner(s) rather than to obtain benefits and is consistent with the indirect benefits hypothesis of female preference. In several taxa courtship feeding may increase female fecundity, egg weight, and offspring survival (Brown, 1997; Eisner et al., 1996; Gwynne, 1988; Thornhill and Alcock, 1983; Wedell and Arak, 1989). However, courtship feeding varies greatly in the extent to which it is costly to males and beneficial to their partners (Brown, 1997; Gwynne, 1993; Wedell, 1993; Sadowski et al., 1999). In the fowl courtship feeding typically consists of invertebrate prey (Pizzari, personal observation; Stokes, 1971), which may be important for the fecundity and viability of female fowl. However, in the study population females had unlimited access to invertebrate prey, and it is uncertain whether the supplement of nutrients obtained through courtship feeding may increase female fitness.
Courtship feeding is a trait shared by several members of the galliforme clade (Hagelin, 2002; Stokes and Williams, 1971). Consistent with the finding of the present study, courtship feeding performance has been shown to be status mediated and to attract females in the pheasant Phasianus colchicus (Mateos and Carranza, 1999), although the relationship between courtship feeding and male copulation success was not investigated in this species. Similarly, Hagelin (2002) found that in male–male contests, only winners performed courtship feeding (tid-bitting) in both Gambel's quails (Callipepla gambelii) and scaled quails (C. squamata). However, no association was found between courtship feeding and female preference in a study of captive red junglefowl based on mate-choice trials (Zuk et al., 1990); this study also did not detect female preference for dominant partners. However, in Zuk et al.'s study courtship feeding involved exclusively inedible objects, and it is unclear whether males had access to food during a trial. The absence of food would have eliminated a potential effect of honest courtship feeding on female choice. In addition, in the same study mate-choice trials were designed to minimize social interactions between the males presented to a female (males were tethered to different corners of the enclosure and visually separated from each other) and female social information of the experimental males (females had not previously encountered the males of a trial; Zuk et al., 1990). The combination of the lack of meaningful courtship feeding opportunities and of competitive interactions between males may have prevented females from selecting partners on the basis of their status and/or on the basis of status-linked courtship feeding performance.
The fact that females adjusted to male vigilance by increasing their own vigilance effort in the absence of males is consistent with the idea that females may depend on males for vigilance. A trade-off often occurs between foraging and vigilance (Brown, 1999), and male vigilance may be critical for efficient and safe foraging by female fowl. However, females should only rely on the vigilance of dominant males, and thus male vigilance ability may convey further information on male condition and competitive ability. This may explain the nonsignificant trend for females to be more vigilant in the presence of a subdominant rather than a dominant male. The lack of a stronger dominance effect on female vigilance investment may be explained by a combination of limited sample size and the fact that female vigilance may be partly adjusted to group size alone and partly fine-tuned to the vigilance efficiency of group members.
The importance of sperm as a direct benefit varies greatly across mating systems. Based on artificial insemination experiments in birds, where unnaturally high numbers of sperm are inseminated to maximize the fertilizing efficiency of an insemination (Pizzari and Birkhead, 2000), one ejaculate is often assumed to contain enough sperm to fertilize a whole clutch of eggs (Lake, 1975). However, in a more natural situation, and particularly when males are sperm depleted or limit the number of sperm inseminated to avoid sperm depletion (Dewsbury, 1982; Warner et al., 1995), sperm may be a limiting factor in female reproductive success (Nakatsuru and Kramer, 1982; Sheldon, 1994; Warner et al., 1995). Furthermore, copulations may be considerably costly to females in several species (Chapman et al., 1995; Stutt and Siva-Jothy, 2001). Therefore, obtaining large ejaculates may allow females to reduce the number of copulations necessary to fertilize their eggs. However, contrary to the idea that female fowl prefer males that inseminate more sperm (fertility hypothesis; Sheldon, 1994), I did not find an effect of social dominance on the number of sperm ejaculated by males. Two factors may explain the lack of an effect of social status on sperm investment: small sample size and differential sperm allocation driven by sperm competition. The combination of few (10) males sampled and the high variation in ejaculate size both within and between individuals (see below) may have limited the power to detect a significant effect of social status on sperm provisioning. Additionally, when sperm competition is intense, males are expected to use their sperm reserves economically (Parker, 1998). Male fowl are able to invest sperm differentially according to levels of sperm competition and to the novelty of copulation partners (Pizzari et al., unpublished data), suggesting that the number of sperm invested by a male in an insemination or in a female is not necessarily a good indicator of his sperm reserves. Many tests of the fertility hypothesis have assumed no differential sperm investment by males and used measures of male sperm reserves, such as testes mass, as indirect measures of the number of sperm inseminated by a male (e.g., Birkhead et al., 1997). The present study is one of the first tests of the fertility hypothesis based on variation in natural ejaculates.
In conclusion, this study demonstrates a tight phenotypic link between a male trait targeted by female choice, social dominance, and male provision of two resources: food and vigilance. Because the propensity to provide these resources also covaries with male status, it is possible that it may convey information on male condition as well as on status. In addition, the fact that females prefer to copulate with males providing any female with more food, rather than males providing only them with more food, is consistent with the idea that females may use male resource provisioning as a proximate mechanism to select males of high status and good condition who thus possibly carry genes for superior fitness. However, whether preferential mating with socially dominant males translates into indirect fitness benefits to females is not known. Together, these results strongly indicate that the role of male provision of direct benefits in the evolution of female preference in species lacking paternal care may be more important than currently realized.
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ACKNOWLEDGEMENTS |
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I am grateful to C. K. Cornwallis for invaluable help in the field and in sperm counting, to A. Bylin, C. K. Cornwallis, E. Aberg, and N. Anbjer for technical assistance and for taking care of the birds, to T. R. Birkhead and S. Jakobsson for providing facilities, and to T. R. Birkhead, B. J. Hatchwell, M. Petrie, and two anonymous referees for helpful comments. Part of this work was supported by a Patrick & Irwin Packington Fellowship at the University of Sheffield. This work is dedicated to the memory of the late Anders Bylin, without whose dedication my research would not have been possible.
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REFERENCES |
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