Dominance hierarchy formation in a model organism, the zebra finch ...

Research Article

Dominance hierarchy formation in a model organism, the zebra finch (Taeniopygia guttata), and its potential application to laboratory research Rachael Bonoan, Felecia Clodius, Annie Dawson, Sara Caetano, Elsa Yeung, and Guillermo Paz-y-Mino-C. ˜ Biology Department, University of Massachusetts Dartmouth, North Dartmouth, MA 02747

Abstract. Social animals often rely on hierarchical dominance relationships to avoid costly agonistic encounters resulting from competition for resources with conspecifics. We demonstrate that zebra finches do form dominance hierarchies in the laboratory under a food competition setting. Birds were placed into single-sex groups and competed against each other for food in repeated dyadic encounters. The dominant and subordinate behaviors each bird displayed towards another were recorded and analyzed in order to determine the dominance hierarchy of each group of birds. Each hierarchy was further validated by analyzing differences in feeding behaviors of dominant and subordinate birds. As zebra finches are a model organism used in genetics and neurobiology, further studies can examine the link between proximate mechanisms and ultimate explanations behind dominant/subordinate interactions. Studying dominance hierarchies in the laboratory can also help us understand the evolution of social structure and associated cognitive abilities.

ual’s rank within an established dominance hierarchy has a direct effect on the fitness of that individual, as dominant individuals are more likely to have larger territories, breed more frequently, and survive for longer periods of time in the wild than subordinate individuals (Arcese and Smith, 1985). Many social animals recognize where in the dominance hierarchy they rank and keep mental track of the dominance relations within and among conspecifics (Cheney et al., 1986; Emery and Clayton, 2004; Paz-y-Mino-C. et al., 2004). This infor˜ mation about group members can be used to behave strategically in social interactions and increase fitness (Emery and Clayton, 2004). Dominance hierarchies have been studied in various taxa. Primates seem to take into account a conspecific’s rank within the social group

Introduction

S

ocial animals may possess higher intelligence than less social animals due to the complex daily interactions with each other that are necessary for survival (Humphrey, 1976; Jolly, 1966). In order to survive in a social group, individuals must compete with group members for mates, food, and territories (Emery, 2006; Paz-y-Mino-C. et al., 2004). By ˜ adopting organized and structured social dominance hierarchies, animals avoid costly injuries through agonistic encounters with group members (Paz-y-Mino-C. et al., 2004). An individ˜

Correspondence to: [email protected]

201 BIOS 84(4) 201–209, 2013 Copyright Beta Beta Beta Biological Society

202 when competing for food (Cheney et al., 1986; Hare et al., 2000). Ravens (Corvus corax; Bugnyar and Heinrich, 2005; 2006) and scrub jays (Aphelocoma californica; Dally et al., 2006) have been compared to primates in their ability to distinguish between conspecific competitors’ identities and dominance relationships, and adjust behaviors accordingly when pilfering from another’s food cache. Paz-y-Mino-C. et al. ˜ (2004) found that pinyon jays not only recognize which individuals within a social group are dominant or subordinate to themselves, but can also use transitive reasoning (i.e. the ability to infer that if bird A is dominant to B, and bird B is dominant to C, it follows that A is dominant to C) to infer where they rank in relation to an unknown bird after watching its interaction with a known bird. Dominance hierarchies have also been observed and formed in crayfish, mountain goats, and hens, suggesting that animals not typically considered ‘‘intelligent’’ can have the cognitive ability required to make and remember judgments about conspeciﬁcs within social groups (Cot ˆ e,´ 2000; Herberholz et al., 2007; Hogue et al., 1996; Issa et al., 1999). This study examines dominance hierarchy formation in zebra finches, which live in large, complex social groups (Zann, 1996). Like many birds, zebra finches rely heavily on visual cues to distinguish between members of their flock, and discriminate between potential mates based on the color of the beak as well as the symmetry of the chest plumage (Cuthill et al., 1997; Fagot and Cook, 2006; Swaddle and Cuthill, 1994). Zebra finches also interact with each other in complex ways, and are able to understand thirdparty relationships among conspecifics using auditory cues (Vignal et al., 2004). This ability to recognize individuals based on visual cues, in conjunction with experience with complex social interactions, makes the zebra finch a good candidate in which to study dominance hierarchy formation and its related cognitive functions. Zebra finches often compete with each other for food in the wild, and we mimic this using a food competition setting to form a dominance hierarchy in the lab.

Volume 84, Number 4, 2013

BIOS

Materials and Methods Subjects Zebra finches, Taeniopygia guttata, are social birds native to Australia (Zann, 1996). They feed mainly on grass seeds and are capable of going days without water. Although they nest in trees, zebra finches prefer open grassy habitats with bushes and spend much of their time on the ground. Zebra finches have relatively complex social interactions including a mating ritual that involves an elaborate nest ceremony where pairs cooperatively decide on a site for the nest. Nests are built in colonies. Although hierarchies found in the field are not rigid, subordinate and dominant roles are formed within the colony (Zann, 1996).

Procedures The protocol was approved by the University of Massachusetts Dartmouth IACUC (UMD 0704). Zebra finches were purchased from certified pet stores in Southeastern Massachusetts and Rhode Island, USA. Finches were assigned to one female group and one male group of six birds each. Finches were given unique bands and maintained in individual cages (35.6 · 21.6 · 27.9 cm) which were placed next to each other alternating in a male-female pattern. Birds were kept in a temperature-controlled room on a 12 hour light-dark cycle. Each bird was fasted for eight hours before each testing trial and all birds were fed after each trial was completed. All bird encounters were digitally recorded using a Sony Handicam HDR-SR1 camera. Encounters were scored by watching the videos in slow motion ( 0.5x speed) using Sony Vegas Movie Studio HD Platinum 10.0. Training trials were performed first to habituate finches to a testing Plexiglas box (15.2 · 17.8 · 38.1 cm), which was separated into three compartments by sliding opaque and transparent doors (Fig. 1). During training trials, finches were placed alone in either end compartment of the box (placement was alternated for each trial). The opaque doors were raised and the bird had visual access to the entire apparatus through the transparent doors.

Dominance hierarchy formation in the zebra finch

Figure 1. Testing box apparatus, made of Plexiglas and separated into three chambers with both clear and opaque dividers. The finches were habituated to the box on their own before being paired with a conspecific for observation as shown.

These transparent doors were then lifted and the bird was allowed to explore the entire box. Exploration lasted a maximum of five minutes or until the bird successfully fed from a feeder full of birdseed located in either the front, or the back, of the apparatus (center chamber). Feeding was defined as when the finch fed from the top of the feeder while on the adjacent perch (as opposed to feeding off the side of the feeder while standing on the ground). Both feeders were full during this first stage of habituation. Each bird underwent training trials until it fed consistently in less than five minutes. The birds were then presented with training trials in which only one feeder had food. Latency time to feeding was recorded for each training session (Figure 2).

203

After being habituated to the testing box, the hierarchy for each group of birds was determined during hierarchy formation trials. In these trials, only one feeder (front or back) was half filled with food to simulate food competition. One bird was placed in the left compartment of the apparatus, and another bird was placed in the right compartment. The side of entry for each bird was randomly assigned for each trial. As in the training trials, the opaque doors were first lifted, followed by the transparent doors, allowing the birds simultaneous access to the center chamber, where the food was located. Birds were allowed to interact for three minutes. The total number of dominant and subordinate behaviors (Table 1) displayed by each bird were recorded for each encounter and each finch had a total of three encounters with each of the other finches in its group. Behaviors scored are indicative of dominance or subordinance in social animals and have been observed in the field (Zann, 1996). A dominance index was calculated for each bird by dividing the number of dominant behaviors observed by the number of total (dominant and subordinate) behaviors observed. The bird with the higher dominance index was recorded as the dominant bird of that encounter and the other bird was the subordinate. This was done for each encounter, and the number of encounters ‘‘won’’ and ‘‘lost’’ by each bird was recorded in a matrix (Fig. 3, details in results). By scoring the encounters in this way, we were able to determine the dominance hierarchy of each group of birds.

Table 1. Table of selected, scored behaviors during hierarchy encounters. Category

Behavior

Dominant

Head up Stare Look at Push Supplant Peck Crouch Look away Lower eyes/bill Supplanted/Move away

Subordinate


Description Subject Subject Subject Subject Subject Subject Subject Subject Subject Subject

raises head up higher than other bird’s head directs gaze towards other bird for more than one second directs gaze towards other bird physically contacts other bird with its body and causes other bird to move displaces other bird attempts to contact other bird with beak stands with knees bent, body lower than other bird directs gaze away from other bid directs gaze or beak downward is displaced by other bird

204

Figure 2. Mean time taken by (a) male and (b) female birds to begin feeding as a function of training session. All birds were conditioned to respond in only three trials. Asterisks indicate significant differences in latency time to feeding. (RM-ANOVA; a) males n = 5, F(2, 8) = 4.841 = p = 0.042; b) females n = 6, F(3, 15) = 6.107, p = 0.006; Error bars are – 1standard error).

Statistical analysis For training trials, the latency time taken for birds to begin feeding was recorded and analyzed using repeated-measures ANOVA in order to assess how fast the birds learned to use the feeders in the testing box (Fig. 2). To validate the order determined from the matrix, time spent in the different compartments of the box – left, middle (where food was present), and right – were also analyzed for dominant and subordinate birds using a 2x3 ANOVA (Fig. 4). This, in conjunction with a 2x2 ANOVA of the overall number of behaviors displayed by birds was used to discern differences between dominant and subordinate birds (Fig. 5). A scatter plot of the birds’ behaviors relative to rank within the hierarchy was also


BIOS

Figure 3. Dominance matrix for (a) males and (b) females. The rows and columns show the number of time a bird was dominant (rows) or subordinate (columns) to the bird in the corresponding column or row during three dyadic encounters. By adding across a row, the total times a bird was dominant can be calculated and by adding down a column, the total times a bird was subordinate can be calculated.

constructed to examine how behaviors changed with position in the hierarchy (Fig. 6). In addition, we carried out a regression analysis of feeding time as a function of rank.

Results In successive training trials, latency time decreased, demonstrating that all birds habituated to and learned how to access food in the testing box (RM-ANOVA; males n = 5, F(2, 8) = 4.841, p = 0.042; females n = 6, F(3, 15) = 0.006; Fig. 2). One male failed to respond and was not used in the analysis. To visualize and determine the dominance hierarchies, a matrix was constructed for each group (Fig. 3). Each cell in the matrix indicates the number of times a bird in a corresponding row was dominant to a bird in a corresponding column. The matrix also shows the number of times a bird in a corresponding column was subordinate to a bird in a corresponding row.

Dominance hierarchy formation in the zebra finch

Figure 4. Comparison of the mean percentage time spent in areas of the box when a bird is dominant and when a bird is subordinate for (a) males and (b) females. Note that dominant birds (black bars) spent more time in the middle, where the food is located, than subordinate birds (white bars). Different letters indicate significant differences in mean percentage time (2x3 ANOVA; males F(2, 168) = 4.163, p = 0.017; females F(2, 264) = 8.00, p < 0.001; Error bars are – 1standard error).

The total number of times a bird was subordinate can be calculated by adding up the values down the column for that specific bird. Likewise, the total number of times a bird was dominant can be calculated by adding up the numbers across the row for a specific bird. Each matrix was arranged to show the birds in descending order from most to least dominant


205

Figure 5. Sum of dominant and subordinate behaviors displayed overall by dominant and subordinate (a) males and (b) females. Dominant birds showed significantly more dominant behaviors than subordinate birds and subordinate birds showed significantly more subordinate behaviors than dominant birds. Different letters indicate significant differences in mean number of behaviors (2x2 ANOVA, males F(1, 112) = 41.58, p < 0.001; females F(1, 176) = 38.26, p < 0.001).

(based on number of ‘‘wins’’) according to the numbers in the cells (Martin and Bateson, 1986). Note that the numbers in the matrix increase from left to right, since the matrix is arranged with the most dominant bird on the left along the top row. Similarly, the numbers decrease from top to bottom, since the birds are arranged with the most dominant bird on the top of the leftmost column.

206

BIOS

Figure 6. Total number of dominant behaviors (black diamonds) vs. subordinate behaviors (white squares) shown by males (a, b) and females (c, d). Six females and five males were tested and each bird interacted three times with all other birds. When a male is dominant, r2= 0.6053 (p = 0.121) for the number of dominant behaviors and r2= 0.3852 (p=0.264) for the number of subordinate behaviors. When a male is subordinate, r2=0.881 (p=0.018) for the number of dominant behaviors and r2=0.889 (p=0.101) for the number of subordinate behaviors. When a female is dominant, r2= 0.7275 (p=0.031) for the number of dominant behaviors and r2= 0.3262 (p=0.236) for the number of subordinate behaviors. When a female is subordinate, r2= 0.6233 (p=0.062) for the number of subordinate behaviors and r2= 0.8272 (p=0.012) for the number of dominant behaviors.

Figure 4 shows that birds spent more time in the middle compartment, where food was located, when they were the dominant bird in the pair than when they were subordinate (2x3 ANOVA; males F(2, 168) = 4.163, p = 0.017; females F(2, 264) = 8.00, p < 0.001; Fig. 4). Analysis of the mean number of behaviors displayed by birds overall showed that dominant birds exhibited more dominant behaviors than subordinate birds (2x2 ANOVA; males F(1, 112) = 41.58, p < 0.001; females F(1, 176) = 38.26, p < 0.001; Fig. 5). The results of these analyses were consistent with what would be expected from interactions between dominant and subordinate birds. Scatter plots of the total number of dominant and subordinate behaviors displayed by each bird showed that dominant birds exhibited more dominant than subordinate behaviors as a


function of rank, and the number of both types of behaviors decreased with decreasing position in the hierarchy. This was true for both sexes, but regressions were mostly not statistically significant (linear regression; dominant males r2= 0.6053, F(1, 4) = 4.60, p = 0.121 for dominant behaviors, r2= 0.3852, F(1, 4) = 1.880, p=0.264 for subordinate behaviors; subordinate males r2=0.881, F(1, 4) = 24.121, p=0.018 for dominant behaviors and r2=.889, F(1, 4) = 32.903, p=0.011 for subordinate behaviors; dominant females r2= 0.7275, F(1, 5) = 10.676, p=0.031 for dominant behaviors, r2= 0.3262, F(1, 5) = 1.936, p=0.236 for subordinate behaviors; subordinate females r2= 0.6233, F(1, 5) = 6.619, p=0.062 for dominant behaviors, r2= 0.8272, F(1, 5) = 19.142, p=0.012 for subordinate behaviors; Fig. 6). The scatter plots also showed that the behaviors

Dominance hierarchy formation in the zebra finch of the birds were consistent with what would be expected from the hierarchy produced by the analysis of the matrices. A regression analysis of feeding time as a function of rank also showed trends that dominant birds tended to feed more than subordinate birds, but the effects were not significant (dominant males r2 = 0.058, F(1, 3) = 0.186, p = 0.695; subordinate males r2 = 0.541, F(1, 3) = 3.534, p = 0.157; dominant females r2 = 0.477, F(1, 4) = 3.648, p = 0.129; subordinate females r2 = 0.471, F(1, 4) = 5.460, p = 0.080)

Discussion In the wild, zebra finches form dominance hierarchies (Zann, 1996) which probably help them avoid costly injuries and unnecessary energy expenditure, as suggested for other highly social and/or gregarious birds (Emery, 2006; Paz-y-Mino-C. et al., 2004). Our results ˜ suggest that zebra finches are also able to recognize individual conspecifics and form dominance hierarchies in a laboratory setting. Dominant birds spent more time feeding in the middle of the box than subordinate birds (Fig. 4). This is consistent with the findings that dominant birds also displayed more dominant behaviors overall than subordinate birds (Fig. 5) and that the number of dominant behaviors decreased with decreasing rank in the hierarchy (Fig. 6). Feeding time as a function of rank showed a downward trend but was not statistically significant. This could be an artifact of the laboratory setting but warrants further investigation into the relationship between feeding and dominance behavior. In nature, zebra finches compete for a variety of resources, which may account for the differences in behaviors between dominant and subordinate birds. Indeed, we found that birds tended to behave consistently dominant or subordinate towards specific individuals and all pairs established a clear dominant/subordinate relationship after only 3 trials. Zebra finch hierarchies in nature have been observed to be more dynamic, with birds changing ranks over time depending on their age, sex, reproductive status or social network (Zann, 1996). This


207

could be because finches often spend time together in social settings during which they participate in behaviors such as clumping and allopreening, social bonding, which could minimize aggression with conspecifics, plus seed availability might be plenty in the field rather than restricted to the controlled amount in this study. This complexity of social interactions and hierarchies may be reflected in our findings that though relationships between pairs of birds are clear, some lower-ranking birds did occasionally win encounters against higher-ranking birds. Nonetheless, our hierarchies were relatively stable because we facilitated them in the laboratory, where birds in individual cages did not interact with one another freely, as in the field where food can be abundant. Dominance hierarchies can further be used to investigate various aspects of zebra finch biology, some under investigation in our laboratory, for example, visual perspective taking (VPT), which is the ability to infer what another individual can or cannot see (Michelon and Zacks, 2006). VPT has immediate adaptive value; it can be used to avoid predators and minimize conflict over competition. It can also aid in group navigation and spatial problem solving among social and interactive groups. Studying VPT can lead to a better understanding of how the brain works in zebra finches and, therefore, other birds. Dominance hierarchies generated in the laboratory can and have been applied to studies in animal behavior and cognition (Dally et al., 2006; Hare et al., 2000; Paz-y-Mino-C. et al., ˜ 2004). Rank within a hierarchy can have direct effects on the fitness of an individual, which can be the basis for future studies on the effect of rank on other factors of an individual’s life. For example, the physiology and health of an individual has been shown to be influenced by social rank (Hawley et al., 2007; Sapolsky, 2005). Dominance hierarchies are useful in cognitive studies, and they imply the ability to recognize others as individuals and to remember past interactions. Cognitive skills studied using hierarchies include transitive reasoning, which has been studied in pinyon jays (Gymnorhinus cyanocephalus) as well as prosimians (Maclean

208 et al., 2008; Paz-y-Mino-C. et al, 2004). In ˜ pinyon jays, it has been documented that if bird C is subordinate to bird B and bird B is subordinate to bird A, bird C can infer that it too is subordinate to bird A by observing an interaction between bird A and bird B (Paz-yMino-C. et al, 2004). In prosimians, it has been ˜ shown that highly social ringtail lemurs are capable, like pinyon jays, of transitive reasoning, while the less social mongoose lemurs are not (Maclean et al., 2008). This suggests that social complexity can be an important selective pressure in the evolution of cognitive abilities among social animals. Dominance hierarchies have also been used to explore visual perspective taking in chimpanzees (Pan troglodytes; Hare et al., 2000) and in food caching and pilfering in scrub jays (Dally et al., 2006). Therefore, applying dominance hierarchies in behavioral and cognitive studies can be useful in understanding the animal mind. Our future work will explore these cognitive skills in zebra finches. Because zebra finches are model organisms used in several fields they can be used to further investigate the influence of neurobiology and genetics on the interactions seen within groups of social animals (Keller and Hahnloser, 2009; Warren et al., 2010). The zebra finch genome was recently sequenced, presenting possibilities of studying in detail the genetic component of behavior in these birds (Robinson et al. 2005; Warren et al., 2010). Zebra finches are also often used in vocal learning (Keller and Hahnloser, 2009) and a library of zebra finch brain cDNAs has been under construction in an effort to make experiments linking the genome, brain, evolution, and behavior possible (Replogle et al., 2008). Some past endocrinological work has been done in zebra finches to further illustrate how the brain and behavior can be influenced by hormones (Gurney and Konishi, 1980; Hutchison et al., 1984). Studying such aspects of behavior can lead to better understanding about the connections between neuroendocrinology and cognition. We have shown that dominance hierarchies can be formed in the laboratory with zebra finches, and suggest that they have potential to be incorporated and fully utilized in other


BIOS studies involving not only social behavior, but also other fields that use zebra finches as a model. Studies on cognition may especially benefit from using hierarchies; further investigation is needed into how behavior, cognition and neuroendocrinology are connected. Acknowledgments: The experiments were carried out in compliance with the University of Massachusetts Dartmouth IACUC; protocol UMD 07-04.

References Arcese, P. and Smith, J.N.M. (1985). Phenotypic correlates and ecological consequences of dominance in song sparrows. J. Anim. Ecol. 54, 818–830. Bugnyar, T. and Heinrich, B. (2005). Ravens, Corvus corax, differentiate between knowledgeable and ignorant competitors. Proc. R. Soc. Lond. B. Biol. Sci. 272, 1641– 1646. Bugnyar, T. and Heinrich, B. (2006). Pilfering ravens, Corvus corax, adjust their behavior to social context and identity of competitors. Anim. Cogn. 9, 369–376. Cheney, D., Seyfarth, R., and Smuts, B. (1986). Social relationships and social cognition in nonhuman primates. Science. 234, 1361–1366. Cot ˆ e,´ S. D. (2000). Dominance hierarchies in female mountain goats: stability, aggressiveness, and determinants of rank. Behavior. 137, 1541–1566. Cuthill, I. C., Hunt, S., Cleary, C., and Clark, C. (1997). Colour bands, dominance, and body mass regulation in male zebra finches (Taeniopygia guttata). Proc. R. Soc. Lond. B. Biol. Sci. 264, 1093–1099. Dally, J. M., Emery, N. J., and Clayton, N. S. (2006). Foodcaching western scrub-jays keep track of who was watching when. Science. 312, 1662–1665. Emery, N. J. (2006). Cognitive ornithology: the evolution of avian intelligence. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 361, 23–43. Emery, N. J. and Clayton, N. S. (2004). The mentality of crows: convergent evolution of intelligence in corvids and apes. Science. 306, 1903–1907. Fagot, J. and Cook, R. E. (2006). Evidence for large longterm memory capacities in baboons and pigeons and its implications for learning and the evolution of cognition. Proc. Natl. Acad. Sci. 103, 17564–17567. Gurney, M. E. and Konishi, M. (1980). Hormone-induced sexual differentiation of brain and behavior in zebra finches. Science. 208, 1380–1383. Hare, B., Call, J., Agnetta, B., Tomasello, M. (2000). Chimpanzees know what conspecifics do and do not see. Anim. Behav. 59, 771–785. Hawley, D. M., Jennelle, C. S., Sydenstricker, K. V., and Dhondt, A. A. (2007). Pathogen resistance and immunocompetence covary with social status in house finches (Carpodacus mexicanus). Funct. Ecol. 21, 520–527. Herberholz, J., Mccurdy, C., Edwards, D. H. (2007). Direct benefits of social dominance in juvenile crayfish. Biol. Bull. 213, 21–27.

Dominance hierarchy formation in the zebra finch Hogue, M. E., Beaugrand, J. P., and Lague,¨ P. C. (1996). Coherent use of information by hens observing their former dominant defeating or being defeated by a stranger. Behav. Process. 38, 241–252 Humphrey, N. K. (1976). The social function of intellect. In: Growing Points in Ethology. (Eds. P. P. G. Bateson and R. A. Hinde), pp. 303–317. Cambridge University Press: Cambridge, UK. Hutchison, J. B., Wingfield, J. C. and Hutchison, R. E. (1984). Sex differences in plasma concentrations of steroids during the sensitive period for brain differentiation in the zebra finch. J. Endocrinol. 103, 363–369. Issa, F. A., Adamson, D. J., and Edwards, D. H. (1999). Dominance hierarchy formation in juvenile crayfish, Procambarus clarkii. J. Exp. Biol. 202, 3497–3506. Jolly, A. (1966). Lemur social behavior and primate intelligence. Science. 153, 501–506. Keller, G. B. and Hahnloser, R. H. R. (2009). Neural processing of auditory feedback during vocal practice in a songbird. Nature. 457, 187–190. Maclean, E. L., Merritt, D. J., Brannan, E. M. (2008). Social complexity predicts transitive reasoning in prosimian primates. Anim. Behav. 76, 479–486. Martin, P. R. and Bateson, P. P. G. (1986). Measuring behaviour: An introductory guide. (Cambridge: Cambridge University Press, USA.) Michelon, P., Zacks, J. M. (2006). Two kinds of visual perspective taking. Percept. Psychophys. 68, 327–337.


209

Paz-y-Mino-C. G., Bond, A. B.,Kamil, A. C., and Balda, R. ˜ P. (2004). Pinyon jays use transitive inference to predict social dominance. Nature. 430, 778–781. Replogle, K., Arnold, A., Ball, G., Band, M., Bensch, S., Brenowitz, E., Dong, S., Drnevich, J., Ferris, M., George, J., et al. (2008). The Songbird Neurogenomics (SoNG) Initiative: Community-based tools and strategies for study of brain gene function and evolution. BMC Genomics, 9, 131. Robinson, G. E., Grozinger, C. M. and Whitfield, C. W. (2005). Sociogenomics: social life in molecular terms. Nature Reviews: Genetics. 6, 257–270. Sapolsky, R. M. (2005). The influence of social hierarchy on primate health. Science, New Series. 308, 648–652. Swaddle, J. P. and Cuthill, I. C. (1994). Female zebra finches prefer males with symmetric chest plumage. Proc. R. Soc. Lond. B. Biol. Sci. 258, 267–271. Vignal, C., Mathevon, N., and Mottin, S. (2004). Audience drives male songbird response to partner’s voice. Nature. 430, 448–451. Warren, W. C., D. F. Clayton, et al. (2010). The genome of a songbird. Nature.464, 757–762. Zann, R. A. 1996. The Zebra Finch: A Synthesis of Field and Laboratory Studies (Oxford: Oxford University Press, USA). Received 14 October 2011; accepted 13 November 2012.