Behavioral Ecology doi:10.1093/beheco/arp178 Advance Access publication 11 December 2009

Effects of singing on copulation success and egg production in brown-headed cowbirds, Molothrus ater David J. White,a Andrew P. King,b Meredith J. West,b Julie Gros-Louis,c and Elaina M. Tuttled Department of Psychology, University of Pennsylvania, 3720 Walnut Street, Philadelphia, PA 19104, b Department of Psychology, Indiana University, 1101 E. 10th Street, Bloomington, IN 47405, c Department of Psychology, University of Iowa, 11 Seashore Hall E, Iowa City, IA 52232, and dDepartment of Life Sciences, Indiana State University, 200 North Seventh Street, Terre Haute, IN 47809, USA

a

We examined the relationship between singing and reproductive success in cowbirds. We amassed data from 17 captive flocks (164 males, 167 females) that we have studied over 4 years. For each flock, we conducted extensive observations on social interactions as the birds competed, courted, and reproduced. We collected and incubated all eggs laid during the breeding season and performed parentage analyses on the 7 flocks with the highest levels of egg production. Finally, we measured males’ song quality in playback tests. Here, we assessed what aspects of singing were associated with 1) copulation success and 2) offspring production. Results differed for these 2 measures of reproductive success because of high variance in egg production within and across groups. The overall amount of songs males directed to females, a measure of courtship persistence, was the one variable strongly associated with males’ copulation success. For offspring production, there was significant between-flock variability that was more pronounced than the within-group variability. The one variable that was found to be strongly associated with eggs laid within and across groups was the amount of countersinging males produced; a measure of male–male singing competition. Song attractiveness did not predict any unique variance in either measure of reproductive success. The relationship between female egg production and male competition suggests that females may be trading off current versus future reproduction based on the opportunities available in groups to evaluate males’ competitive abilities. Key words: birdsong, cowbird, egg production, reproductive success, social behavior. [Behav Ecol 21:211–218 (2010)]

n communication research, much interest has centered on the relationship between signals and reproductive success. Examining the characteristics of signals that lead to enhanced mating success can provide a means to determine how a communication system may have evolved (Searcy and Nowicki 2005) and how sexual selection may operate on signals and signaling (Andersson 1994). Bird song has been a particularly effective model for studying how signals relate to reproductive success. In many species, male birds sing to attract females, and courtship songs elicit females’ copulation solicitation displays (Catchpole 1987). Thus, having an attractive signal is a necessary component of a male’s reproductive success. Males also use song in interactions with other males, and these interactions can influence who is ultimately able to reproduce (Searcy and Andersson 1986; Nowicki and Searcy 2005). Evidence of song’s contribution to reproductive success comes from extensive studies: 1) in the field, where characteristics of song and mating success can be measured (Searcy 1984; Alatalo et al. 1990; Payne and Payne 1993; Rehsteiner et al. 1998; Baker and Boylan 1999; Otter et al. 2001; MacDougall-Shackleton et al. 2002) and 2) in the laboratory where controlled investigations of females’ song preferences can be assessed (King and West 1977; Searcy 1981, 1984, 1992; O’Loghlen and Rothstein 1995; O’Loghlen and Beecher 1997; Holveck and Riebel 2007; Pasteau et al. 2009). This body of research has provided a wealth of data

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Address correspondence to D.J. White. E-mail: whitedj@psych .upenn.edu. Received 28 May 2009; revised 13 November 2009; accepted 17 November 2009.  The Author 2009. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please e-mail: [email protected]

on the wide variety of song and singing characteristics that may be important to reproductive success, such as song quality, song complexity, repertoire size, amplitude, singing effort, song matching, and sharing (Howard 1974; Smith 1977; Searcy and Andersson 1986; Kroodsma and Byers 1991; Catchpole and Slater 1995; Kroodsma and Miller 1996; Nordby et al. 1999; Marler and Slabbekoorn 2004). Song can be an indicator of a male’s resource holding potential, health, learning ability, developmental resilience to stress, attentiveness to females, or social skills. One challenge in examining the link between song characteristics and reproductive success has been in tying together laboratory examinations of female preferences with mating patterns seen in the wild. Often, the relationship between mate preferences and mate choice is not a simple one. The laboratory preparation, removed from the context in which mating occurs, fails to incorporate many aspects of social life. Male or female competition, for example, can influence reproductive success and change the relationships between traits females prefer and traits that are ultimately selected (Searcy 1984; Beecher 1996; Nordby et al. 2000). Alternatively, research in the wild often lacks the control necessary to be able to isolate the important aspects of singing from many of the other covarying factors that may influence mating success. The goal of this work was to examine the relationship between characteristics of song and reproductive success in a controlled laboratory environment but in a context that provided individuals enough freedom to live and breed in groups. We studied brown-headed cowbirds, a gregarious songbird. The cowbird serves as an excellent model for studying relationships between social behavior and reproductive success because wild-caught individuals will breed in large outdoor

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aviaries. There are of course many differences between flocks in captivity and in the wild (e.g., food availability, shelter, range size, and safety from predation). Thus, captive flocks cannot be considered analogous to populations in the wild. They do, however, offer a powerful means to control aspects of social systems that cannot be controlled in the field. In our captive flocks, birds court, copulate, and lay eggs in mock nests. These patterns of behavior do resemble the seasonal patterns of singing, courting, and mating reported in the wild (Friedmann 1929; Ortega 1998; Smith et al. 2000). There is, however, wide variation in field reports of cowbird social demographics and in social behavior (Brainard 1998). In the laboratory, we can have some control over aspects of the social and physical environment, providing a means to assess how social interactions may influence reproductive success. We are also able to examine female preferences for male courtship song by measuring copulation solicitation displays given by females in response to recordings of songs played in sound attenuation chambers (King and West 1977). Thus, we can have controlled measures of females’ preferences for songs, and we can also measure actual mating patterns of birds in groups. Observations of birds during the breeding season provide us with measures of song use; as males use song to compete with other males, to court, and to copulate. Past work has revealed that song use can vary dramatically across males and can be influenced by social experiences during development. For example, juvenile males who had experience with adult males learn to engage in more social singing (to both males and females) than juveniles who do not have social experiences with adult males (White, King, and West 2002a; White et al. 2007). Experienced juveniles also engage in countersinging bouts more often than naive juveniles (White et al. 2007). Cowbird countersinging differs from what is typically considered under this term, which usually refers to males matching song types with neighbors across long distances (Beecher et al. 2000). Male cowbirds are not territorial, so countersinging takes place at very close distances (often within inches). Countersingers alternate songs and can sing flurries of songs rapidly (routinely singing 10 or more songs per minute). Singing to other males is related to dominance (Dufty 1986; Rothstein et al. 1988), but countersinging also seems to have an influence on females. In groups producing high levels of countersinging, females more frequently approach and spend time near the males (West et al. 2002; King, West, and White 2003; King, White, and West 2003). Cowbirds are obligate brood parasites and are therefore not constrained in their reproduction by the burden of parental care. They thus have the potential to lay more eggs than species that must care for their young. In our captive conditions, we are able to collect and incubate all eggs laid in the breeding season to get measures of reproductive output. In the past, we have been struck by the wide variation in egg production we have found across different groups (West et al. 2002; King, West, and White 2003; King, White, and West 2003), but we have never, until now, had a sample size of independent groups large enough to examine this variability in detail. We have not been able, for example, to determine whether the across-group variability was due to a few extremely fecund females or whether females as a group were stimulated to lay eggs as a consequence of overall aspects of the social group. Either way, if females have control over their egg production and vary reproductive output in response to the qualities of the males present, then this could have an effect on reproductive success and on selection. Given a large-enough sample size, we should be able to assess what characteristics of males may be associated with reproductive stimulation. Here, we report on the patterns and relationships among social behavior and reproductive success in captive flocks of

cowbirds, using extensive data sets of the social and singing behavior of 331 birds (164 males, 167 females), the complete egg production of females spanning 4 years for 17 captive flocks, microsatellite parentage analysis on 7 of the flocks with highest egg production, and finally, results of song playback tests examining female preferences for recordings of songs from the majority of the males in the groups. MATERIALS AND METHODS Subjects We caught all birds in Monroe County, IN, from 1999 to 2004, and housed them in 9.1 3 21.4 3 3.4 m aviaries (see Table 1). Aviaries contained trees, perches, ground cover, and indoor shelters. Birds had ad libitum access to water and a modified Bronx zoo diet for omnivorous birds plus canary seed and red and white millet. In the breeding season, we supplemented the diet with one-fourth cup crushed oyster shell per aviary. These flocks have been the subject of several studies in the past. In all cases, the only difference across the groups was in their age class composition (see Table 1). For more details about the social compositions of the flocks, refer to the individual studies (West et al. 2002; White, King, and West 2002a, 2002b; King, West, and White 2003; King, White, and West 2003) MEASURES For all groups, 3 observers took extensive measures of social behavior prior to, and during the breeding season. We used a speech-recognition data collection system to record the timing of behavioral events continuously (White, King, and Duncan 2002). We report data from samples during the time that eggs were collected (May 1–June 10). Song use We noted patterns and amount of male vocalizations in 15-min censuses (White, King, and West 2002a). Within each census, we noted the individual who sang or whistled, whether it was directed to another bird (sung within 60 cm and oriented toward another individual), or was undirected. We Table 1 Flock composition for 17 aviaries

a

Number of males

Number of females

Aviary

Year studied

Total birds

Adult

Juvenile

Adult

Juvenile

1 2 3 4a 5a 6a 7 8 9 10 11 12a 13a 14 15a 16a 17a

2000 2000 2000 2001 2001 2001 2001 2001 2001 2002 2002 2002 2002 2004 2004 2004 2004

22 19 20 20 20 20 20 21 20 16 17 25 24 16 17 17 17

0 0 6 0 0 0 0 11 10 0 0 14 7 0 7 8 8

12 9 4 10 10 10 10 0 0 6 7 0 7 8 0 0 0

6 6 6 6 6 6 6 6 10 10 10 12 10 8 10 9 9

4 4 4 4 4 4 4 4 0 0 0 0 0 0 0 0 0

Indicates groups included in microsatellite analysis.

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programmed our database to determine whether or not song occurred in a countersinging bout. A vocalization occurred in a countersinging bout if the recipient of a directed vocalization responded to the singer with a directed vocalization within 15 s. Past work has suggested that countersinging is a more sensitive measure of male singing competition than is male directed singing alone (King, West, and White 2003; King, White, and West 2003; White et al. 2007). We also recorded all observed copulations. The automated speech-recognition system provided us with high levels of interobserver reliability in song censuses (song per male; r ¼ 0.98, P , 0.001). Because we collected different numbers of censuses across the groups, we controlled for this by transforming all measures to be per 15min data collection block (each individual’s measures divided by the total number of censuses taken on the group). Song playbacks We made breeding season audio recordings of songs of males within the flocks and played them to females in sound attenuating chambers. The 64 female subjects used for playbacks were unfamiliar with the males whose songs were being tested. They were of the same age range as the females in the rest of the study and had been housed in aviaries with males prior to being placed in sound attenuation chambers. We measured each song’s ‘‘potency,’’ or effectiveness at eliciting females’ copulatory postures (see West et al. 2002; White, King, and West 2002a for details of playback procedure). We played back songs from males from 10 of the flocks. We selected one song from each male based on recording quality for playback. Time did not permit us to test multiple songs from each male. Potency scores from different songs of the same male typically do not vary substantially (King AP, West MJ, White DJ, unpublished observations). We conducted playbacks of pairs of aviaries over the course of 4 breeding seasons. Each song was played 6times in total to females, and we scored for each song how often females responded to the playback with a copulation solicitation display. Egg collection At approximately 0530 h each morning in the breeding season, we collected all eggs laid in all groups. We incubated eggs for 10 days to determine whether they were fertile. Mock nests in the aviaries contained grass clippings and yogurt-covered peanuts that served as false eggs. For further details of sampling procedures, refer to the within-year studies (West et al. 2002; White, King, and Duncan 2002; White, King, and West 2002a, 2002b; King, West, and White 2003; King, White, and West 2003). Microsatellite analysis We conducted a parentage analysis on a sample of 7 of the aviaries (a groups in Table 1). The 7 aviaries chosen were ones that produced enough eggs to allow us the possibility of detecting patterns of successful reproduction among individuals within groups. We used microsatellite markers to assign maternity and paternity to each fertile egg. We collected blood samples (50–100 ll) from all putative parents by puncture of the brachial vein, and we stored the blood at 220 C until needed for analysis. Whole embryos were harvested on day 10 of incubation and also stored at 220 C. We extracted DNA from both blood and embryo using standard organic solvent purification (Sambrook and Russel 2001). We determined parentage using 4 pairs of nuclear microsatellite markers (Mal20, Mal25, Mal29, and Dpl16) either developed specifically for brown-headed cowbirds (Alderson et al. 1999) or for yellow warblers (Dendroica petechia) (Dawson

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et al. 1997). We followed Alderson et al. (1999) for polymerase chain reaction (PCR) reaction conditions for all primers. We analyzed amplification products on an ABI PRISM 310 Genetic Analyzer (Applied Biosystems). We then further analyzed the resulting data with the Genescan Analysis 2.0.2 and Genotyper 2.0 software packages. All microsatellite loci were highly variable and averaged 21 alleles/locus. The observed number of heterozygotes did not differ from the expected number of heterozygotes for all 4 loci. Furthermore, the estimated occurrence of null alleles was also correspondingly low. In addition, we were able to genotype another female at only 1 of the 4 loci. All other adults were typed completely. DATA ANALYSIS First, we used generalized linear mixed models (GLMM) testing copulation success as the dependent variable. Copulation success was a continuous variable scored for each bird based on the number of copulations they attained across the duration of the breeding season. Because groups had different total numbers of observations taken, individual’s copulation success was calculated per number of song census blocks taken on each group. We ran models for male and female copulation success separately, using a dummy code for group (aviaries 1–7) as a random factor, and song characteristics as covariates. Although we have a large assortment of different measures of song, for these analyses, we focused on a subset of the song measures in order to reduce the levels of multicollinearity. Thus, we selected song measures that past work have revealed to assess different aspects of social interactions and not to be highly intercorrelated (White, King, and West 2002a; King, West, and White 2003; King, White, and West 2003). As a measure of courtship effort, we used amount of female-directed song males produced per census block taken on the group. To measure male–male singing competition, we used the amount of countersinging males produced per census block. We also entered a measure of song potency for the males from whom we had playback results. This score was the potency score averaged across the playback females. We had song potency measures for 53 of the 68 males in the 7 groups. (Intercorrelation coefficients for female-directed song, countersinging, and potency averaged r ¼ 0.21.) For models testing female copulation success, we used the amount of female-directed song females heard from males per census block, the song potency, and amount of countersinging per census block produced by the male with whom the female copulated. Females only ever copulated with one male; thus, each female had only one value for the dependent variable in the analysis. Some of the males copulated with multiple partners. We entered their results with each of their females as repeated measures and entered individual as a random variable. Next, we ran GLMMs with number of offspring produced as the dependent variable. Offspring produced was a continuous variable calculated as the number of fertile eggs each individual sired across the entire breeding season. Across years, the number of days that we collected eggs varied (between 33 and 37 days). We controlled for this by transforming eggs collected to be per day of egg collection (total eggs collected for each female divided by number of days collecting eggs). We square-root transformed offspring produced per day in order to maintain homogeneity of variance across groups. We again ran separate models for males and females. We entered the same factors and covariates in the offspring production models as in the copulation success models above. Finally, we incorporated all 17 aviaries into a multiple regression using total number of fertile eggs produced per aviary per female as the dependent variable and the per census block totals of female-directed song, countersinging, copulations,

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and average potency of all the males in the group as predictors. Thus, although we did not have information on the within-group variationinmaternity andpaternityinallofthe groups, thistestwas run to examine whether overall characteristics of groups played a role in stimulating the reproductive condition of the females in those groups (using each group as an independent datapoint). RESULTS Overall, across the 17 aviaries, there was wide variation in eggs collected, ranging from 13 to 79 fertile eggs. Among the groups selected for parentage analyses, we were able to measure the parentage of 373 eggs. There was substantial variation in egg laying both within and across these groups. Figure 1a illustrates the number of fertile eggs produced per female in each of the seven groups. Each line represents one group with the order of females sorted from highest egg producer to lowest for each group. Figure 1b illustrates the number of offspring sired per male across the 7 groups. Both males and females had pronounced variation in reproductive success, with males exhibiting more, but not significantly more skew (mean variance in reproductive success for males ¼ 0.17 6 0.08, females ¼ 0.05 6 0.02, paired t-test, t(6) ¼ 1.88, P . 0.10). Males had on average 1.60 6 0.11 partners; females never mated with more than one male in a breeding season. Copulation success No variable in the model significantly accounted for variation in male or female copulation success. For males, the amount of female-directed song produced was not significant in the

model when each female partner was entered individually. However, total female-directed song produced by males (collapsing across all females with whom a male copulated) was significantly related to copulation success. Within the groups, the amount of males’ female-directed song produced had on average a 0.77 (60.07) correlation with copulation success (6/7 groups had significant correlations). Countersinging and song potency were not significantly associated with copulation success within groups. Figure 2 illustrates the relationship between males’ copulation success and total female-directed song they produced seen in the 7 groups. This difference between the results of the model for female-directed song (per partner) compared with total female-directed song (for all partners) indicates that males who can invest in singing to more females are more successful in copulating. Offspring produced Both models using offspring produced as the dependent variable revealed that countersinging was significantly related to offspring produced (male model, F(1, 49) ¼ 8.15, P , 0.01; female model, F(1,47)¼ 6.31, P ,0.02). Also, in both models, there was a significant variance associated with group (male model, F(6,42) ¼ 4.36, P , 0.005; female model, F(6,47) ¼ 3.62, P , 0.005). Female-directed song and song potency failed to predict any unique variance in offspring produced. The significant effect of group in the models for offspring produced suggests that some variance in egg production found across groups was not explained by the variables tested within groups. The subset of groups we used for parentage testing (a restricted range of only the highest egg producing groups) would have grossly underestimated the size of this group effect. We therefore examined egg production across all 17 aviaries. Across groups: egg production The multiple regression model was significant (F(4,6) ¼ 4.98, P , 0.05) and explained 61.4% of the variance (adjusted) in egg production across groups. Countersinging was the only variable that significantly predicted egg production across groups (Beta ¼ 0.812, t ¼ 3.48, P , 0.02). Figure 3a illustrates the relationship between countersinging and egg production. We then removed countersinging from the model. Once countersinging was removed, the regression model was no

Figure 1 Variance in reproductive success for (a) females and (b) males in the 7 groups for which we had parentage information. Reproductive success was measured by the number of offspring produced per day of egg collection. Across conditions, total days of egg collection ranged between 33 and 37 days. Individuals within each group are sorted in descending order based on number of offspring produced.

Figure 2 Scatterplot depicting the relationship between each male’s amount of female-directed song produced per block of data collection and his copulation success. Each regression line represents one of the 7 flocks.

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Copulation success The one characteristic of singing that related to copulation success for males was the overall amount of female-directed song they produced. This is a pattern we have seen in the past groups of cowbirds (Freeberg 1996), and reports in other species have found that courtship persistence and effort relates to mating success (Vinnedge and Verrell 1998; Shamble et al. 2009). The effect could only be found when grouping all of a male’s partners together; thus, males’ copulation success is increased by courting multiple partners. None of our measures proved effective in predicting numbers of copulations achieved by females, suggesting that either we have not measured the characteristics of social interactions important to explain female copulation rates, or else the interactions that predict copulations for females occur earlier in the spring. The focus of current work is in determining whether females who are courted early in spring pair bond earlier and copulate more with their partners. Offspring produced

Figure 3 Scatterplots depicting the relationship across 17 groups between (a) countersinging (CS), and (b) female-directed singing produced in the group per block of data collection with numbers of eggs produced in the groups.

longer significant (F(3,7) ¼ 1.01, P . 0.44), explaining only 0.3% of the variance (adjusted) and no other variables came close to predicting egg production (all Beta t values , 1.6, all Ps. 0.14). In contrast to countersinging, Figure 3b illustrates the (lack of) relationship between female-directed song and egg production.

DISCUSSION The analysis of the relationships between singing and reproductive success in cowbirds revealed 3 notable results: 1) copulation success and offspring production were very different measures of reproductive success owing to the striking variability in egg production within and across conditions; 2) aspects of song use, but not song potency, were important contributors to reproductive success; and 3) the only significant predictor of female egg production between and across groups was countersinging.

Surprisingly, it was the amount of countersinging—male singing interactions with other males—that best predicted offspring production. The pronounced across-group variance in egg production was also a surprise. The significant amount of variance associated with the group factor in the GLMM models suggested that variability in egg production across groups could not be accounted for in its entirety by the singing interactions of the females’ partners. Also, the differences across aviaries could not be attributed to a few females, as there were significant numbers of females in some groups producing more eggs than females in other groups (Figure 1a). This pattern was found even in the restricted range of the highest egg producing aviaries. The multiple regression analysis provided suggestive evidence that it may be the ambient amount of countersinging in the group that stimulates female egg production. Experiments, however, will be needed to elucidate the mechanism of countersinging’s effect on egg production. It could be the temporal patterns of countersinging or the visual displays males produce when countersinging that stimulate females’ reproductive hormones (sensu Lehrman 1965). It is also possible that countersinging covaries with some other unmeasured variable that is critical in driving changes in egg production. The 2 measures of reproductive success—copulation success and egg production—were remarkably disassociated in their relationships with singing. Females have some control over copulation success because females must produce solicitation displays in order for males to copulate successfully (Yokel and Rothstein 1991). The variation in egg production, however, did not relate to copulation success; it was related to male competition and not to courtship persistence. This suggests that females have 2 levels of control over reproduction; one based on copulation success and the other related to regulating egg production. The lack of a relationship between either measure of reproductive success and song potency was unexpected. Having a song a female prefers is necessary for a male to copulate. Also, there is evidence in many species that song quality can serve a stimulatory function for egg production (Brockway 1965; Kroodsma 1976; Leboucher et al. 1998). That song preferences did not correspond to copulation success or reproductive stimulation suggests that something occurring in social contexts may lead females to 1) mate with males whose songs do not correspond to their preferences, 2) assess males based on characteristics other than song potency, 3) change their song preferences in some way (King, West, and White 2003; King, White, and West 2003; Freed-Brown and White 2009), or 4)

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use different criteria for selecting mates in different social contexts. In support for this last possibility, past work has revealed that there have been some social groups where song potency has indeed correlated strongly with mating success (West et al. 1981; White, King, and West 2002a, 2002b). How preferences may vary with social context is at this point unknown. It could be that there are many different characteristics of males that females use for mate selection and that the characteristics that are most important to females in any particular group depend on the assortment of males and the frequency or variance of traits within a group that are being compared. The results suggest that reproductive success for males depends on singing persistently to females and also engaging in male–male singing bouts; 2 song-use behaviors that past work has found to be highly influenced by social learning during development. In past studies, we have found that males can vary dramatically in their propensities for both types of directed singing, and groups of males can be influenced to be more male- or female-directed by other males in their flock (Freeberg et al. 1995; White, King, and West 2002a, 2007, forthcoming). In the past, we have described different groups as ‘‘cultures’’ where different social compositions lead to variation in social behavior and singing patterns (White et al. 2007). In some groups, allocating more time to courtship may account for reproductive success, whereas in other groups, engaging in more male competition may be a more successful strategy. It remains unclear what effect these cultures may have on selection. For example, do different cultures lead specialist males to be more successful in one type of condition and less successful in another, or are the most successful males the ones who are flexible and can change their behavior to match the culture in which they find themselves? To answer these questions, longitudinal studies are necessary where subjects live and breed in different cultures across years. There are 2 points of caution to be noted in interpreting these results: First, as is always a risk with laboratory research, there is the possibility that the characteristics of our captive system are not representative of the characteristics of groups in the wild. Other than knowing that female-directed song and countersinging exist in the wild, there is little information from the wild bearing on the patterns of reproductive success found in this work. It is extremely difficult to assess a female brood parasite’s reproductive success in the wild and impossible to have enough control over the social and physical ecology to determine how social environments may influence reproductive success in the wild. Even if the overall effects differ between the laboratory and the wild, the captive studies provide information about the plasticity in female reproductive behaviors and male abilities. Such plasticity could allow for the potential for different cultures to develop and be maintained in the wild (Freeberg et al. 2001). Second, the associations found here are only correlations, and it is therefore possible that other unmeasured variables account for the relationships found in the analysis. Future experiments under more controlled conditions will allow us to extend the discoveries found here and to move toward statements of causation. One focus of studies of communication systems has been on signal honesty (Bradbury and Vehrencamp 1998; Searcy and Nowicki 2005). Signals are only useful to receivers if they provide reliable information. From this perspective, countersinging may be a more honest indicator of a male’s quality than his song potency. Males can copy songs and can develop high potency song as a consequence of certain developmental experiences (King and West 1977; West and King 1988; White, King, and West 2002a). Thus, whereas any male can develop

a high potency song, not every male can defend singing one in a context with other males. Other males react aggressively to high potency song, so countersinging provides valuable information about the ability of a male to engage with other males. Thus, in conditions where there is an abundance of countersinging, there would be an abundance of reliable information about males for females to evaluate. Thus, if females experience multiple groups in a season or in their lifetimes (if over wintering mortality is not substantial; but see Darley 1971), it could be that females manage tradeoffs in future versus current reproductive success based on the amount of information available in groups to assess male social quality. It could be that the dramatic variation shown here in clutch size may only be found in a brood parasite that does not face increases in parental care resulting from laying high numbers of eggs. Social control of reproduction may be a phenomenon that generalizes beyond brood parasites, however. At the individual level, females in many species have been shown to have control over egg production in response to various types of environmental stimuli (Carey 1996). Also, at the group level, intraspecific variation exists in reports of clutch sizes across populations of several social bird species (Gill 1994; Baicich and Harrison 1997). Furthermore, changing egg production is only one example of a way in which a social context could influence reproductive success (Adkins-Regan and Mackillop 2003; Mazuc et al. 2003; Silk et al. 2003, 2009). The current work implies that understanding how selection acts on an individual of a social species requires measuring 2 types of processes: 1) processes that lead to assortative mating at the individual level and 2), group-dependent processes that create the social context in which the individual must reproduce. FUNDING National Science Foundation operating grants to A.P.K. and M.J.W. Maral Papakhian and Susan Linville assisted with data collection. Deborah Gordon and 2 anonymous reviewers provided thoughtful comments on an earlier version of the manuscript. All work conformed to the Animal Behavior Society guidelines for ethical treatment of animals and was done under Indiana University animal use and care study # 01-085.

REFERENCES Adkins-Regan E, Mackillop EA. 2003. Japanese quail (Coturnix japonica) inseminations are more likely to fertilize eggs in a context predicting mating opportunities. Proc R Soc Lond B. 270:1685–1689. Alatalo RV, Glynn C, Lundberg A. 1990. Singing rate and female attraction in the pied flycatcher - an experiment. Anim Behav. 39: 601–603. Alderson GW, Gibbs HL, Sealy SG. 1999. Parentage and kinship studies in an obligate brood parasitic bird, the brown-headed cowbird (Molothrus ater), using microsatellite DNA markers. J Hered. 90: 182–190. Andersson M. 1994. Sexual selection. Princeton (NJ): Princeton University Press. Baicich PJ, Harrison CJO. 1997. A guide to the nests, eggs, and nestlings of North American birds. San Diego (CA): Academic Press. Baker MC, Boylan JT. 1999. Singing behavior, mating associations and reproductive success in a population of hybridizing Lazuli and Indigo Buntings. Condor. 101:493–504. Beecher MD. 1996. Birdsong learning in the laboratory and field. In: Kroodsma DE, Miller EH, editors. Ecology and evolution of acoustic communication in birds. Cornell University Press. p. 61–78. Beecher MD, Campbell SE, Burt JM, Hill CE, Nordby JC. 2000. Songtype matching between neighbouring song sparrows. Anim Behav. 59:21–27.

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Effects of singing on copulation success and egg ...

Dec 11, 2009 - We then further ana- lyzed the resulting data with the Genescan Analysis 2.0.2 and. Genotyper 2.0 software packages. All microsatellite loci ...

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