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Song and Female Mate Choice in Zebra Finches: A Review
Abstract
Zebra finches are an important model for vocal learning and avian mate choice. The two are contingent on each other: males' learned songs are addressed at females with learned preferences. This review documents the recent changes away from a purely mechanism-orientated approach of song learning toward the question of how variation in male phenotypic quality is reflected by variation in male song. The substantial evidence for female song preference learning is reviewed and compared to what is known to about unlearned preference biases. From the complementary evidence, a picture emerges that shows how cultural transmission of the male mating signal is paralleled by sensory learning processes on the receiver's side. The question of how the trait and preference might react in concert to environmental change and how learned receiver biases affect the evolutionary dynamics of culturally transmitted song emerge as exciting future research prospects.
... Females that did not start key pecking spontaneously within the first day were given training sessions twice daily for 20 min until operant responses were logged. During shaping, the experimenters (K.R., I.A., C.P.H.E., outside the test chamber behind a one-way mirror) initially drew females' attention to the keys by flashing the LED lights before playing the song reward and then gradually rewarding all behaviour leading to closer approach and exploration of the keys, taking care to reinforce the keys on both sides (details on training, see 31 ). During initial training (involving 10 females and 10 stimulus sets), songs were randomly chosen from the pool of pre and post singing prevention to see whether females were motivated to peck for either stimulus category. ...
... During initial training (involving 10 females and 10 stimulus sets), songs were randomly chosen from the pool of pre and post singing prevention to see whether females were motivated to peck for either stimulus category. During this first testing round 7/10 females learned to peck the keys and were highly motivated to hear songs ( > 30 key pecks/day) and as previously reported for this species females preferred longer songs 29,31 . For the second, actual preference test all successfully trained females plus 3 additional females were tested with the actual test songs. ...
... Preference analysis. The pecking events and cumulative learning curves of each female were checked daily and preference testing began the day after the initial pecking had changed from incidental pecking to an exponential increase of frequent operant responses on both sides 31 . Each test lasted 4 days and each night we switched the assignment of the stimulus songs between left and right keys to control for side preferences. ...
Vocal signals, including human speech and birdsong, are produced by complicated , precisely coordinated body movements, whose execution is fitness-determining in resource competition and mate choice. While the acquisition and maintenance of motor skills generally requires practice to develop and maintain both motor circuitry and muscle performance, it is unknown whether vocal muscles, like limb muscles, exhibit exercise-induced plasticity. Here, we show that juvenile and adult zebra finches (Taeniopygia castanotis) require daily vocal exercise to first gain and subsequently maintain peak vocal muscle performance. Experimentally preventing male birds from singing alters both vocal muscle physiology and vocal performance within days. Furthermore, we find females prefer song of vocally exercised males in choice experiments. Vocal output thus contains information on recent exercise status, and acts as an honest indicator of past exercise investment in songbirds, and possibly in all vocalising vertebrates. Producing complex learned vocalizations, such as human speech and birdsong, comprises some of the most intricate, temporally precisely coordinated movements of the vertebrate body. The precise motor control and execution of these vocal motor skills ultimately plays a decisive role in mate choice and resource competition 1,2. The acquisition and maintenance of motor skills requires motor practice i) to develop and maintain motor circuitry and ii) to improve and maintain muscle performance. In vocal learners, vocal skills are typically acquired over postnatal development, when the body is growing, and maintained over adulthood. Especially for songbirds-widely accepted as the closest animal analogue for human speech acquisition 3,4-the critical contribution of reshaping sensory and motor circuits to song learning is well established 3,5-8. However, whether vocal muscles require motor practice to improve and maintain performance, and if such changes directly affect vocal output remains unknown for any vocalizing vertebrate, including humans 9 .
... Females that did not start key pecking spontaneously within the first day were given training sessions twice daily for 20 min until operant responses were logged. During shaping, the experimenters (K.R., I.A., C.P.H.E., outside the test chamber behind a one-way mirror) initially drew females' attention to the keys by flashing the LED lights before playing the song reward and then gradually rewarding all behaviour leading to closer approach and exploration of the keys, taking care to reinforce the keys on both sides (details on training, see 31 ). During initial training (involving 10 females and 10 stimulus sets), songs were randomly chosen from the pool of pre and post singing prevention to see whether females were motivated to peck for either stimulus category. ...
... During initial training (involving 10 females and 10 stimulus sets), songs were randomly chosen from the pool of pre and post singing prevention to see whether females were motivated to peck for either stimulus category. During this first testing round 7/10 females learned to peck the keys and were highly motivated to hear songs ( > 30 key pecks/day) and as previously reported for this species females preferred longer songs 29,31 . For the second, actual preference test all successfully trained females plus 3 additional females were tested with the actual test songs. ...
... Preference analysis. The pecking events and cumulative learning curves of each female were checked daily and preference testing began the day after the initial pecking had changed from incidental pecking to an exponential increase of frequent operant responses on both sides 31 . Each test lasted 4 days and each night we switched the assignment of the stimulus songs between left and right keys to control for side preferences. ...
Vocal signals, including human speech and birdsong, are produced by complicated, precisely coordinated body movements, whose execution is fitness-determining in resource competition and mate choice. While the acquisition and maintenance of motor skills generally requires practice to develop and maintain both motor circuitry and muscle performance, it is unknown whether vocal muscles, like limb muscles, exhibit exercise-induced plasticity. Here, we show that juvenile and adult zebra finches (Taeniopygia castanotis) require daily vocal exercise to first gain and subsequently maintain peak vocal muscle performance. Experimentally preventing male birds from singing alters both vocal muscle physiology and vocal performance within days. Furthermore, we find females prefer song of vocally exercised males in choice experiments. Vocal output thus contains information on recent exercise status, and acts as an honest indicator of past exercise investment in songbirds, and possibly in all vocalising vertebrates.
... Females that did not start key pecking spontaneously within the first day were given training sessions twice daily for 20 min until operant responses were logged. During shaping, the experimenters (K.R., I.A., C.P.H.E., outside the test chamber behind a one-way mirror) initially drew females' attention to the keys by flashing the LED lights before playing the song reward and then gradually rewarding all behaviour leading to closer approach and exploration of the keys, taking care to reinforce the keys on both sides (details on training, see 31 ). During initial training (involving 10 females and 10 stimulus sets), songs were randomly chosen from the pool of pre and post singing prevention to see whether females were motivated to peck for either stimulus category. ...
... During initial training (involving 10 females and 10 stimulus sets), songs were randomly chosen from the pool of pre and post singing prevention to see whether females were motivated to peck for either stimulus category. During this first testing round 7/10 females learned to peck the keys and were highly motivated to hear songs ( > 30 key pecks/day) and as previously reported for this species females preferred longer songs 29,31 . For the second, actual preference test all successfully trained females plus 3 additional females were tested with the actual test songs. ...
... Preference analysis. The pecking events and cumulative learning curves of each female were checked daily and preference testing began the day after the initial pecking had changed from incidental pecking to an exponential increase of frequent operant responses on both sides 31 . Each test lasted 4 days and each night we switched the assignment of the stimulus songs between left and right keys to control for side preferences. ...
Vocal signals mediate much of human and non-human communication. Key performance traits - such as repertoire size, speed and accuracy of delivery - affect communication efficacy in fitness-decisive contexts such as mate choice and resource competition1. Specialized fast vocal muscles2,3 are central to accurate sound production4, but it is unknown whether vocal, like limb muscles5,6, need exercise to gain and maintain peak performance7,8. Here, we show that for song development in juvenile songbirds, the closest analogue to human speech acquisition9, regular vocal muscle exercise is crucial to achieve adult peak muscle performance. Furthermore, adult vocal muscle performance reduces within two days of abolishing exercise, leading to downregulation of critical proteins transforming fast to slower muscle fibre types. Daily vocal exercise is thus required to both gain and maintain peak vocal muscle performance, and if absent changes vocal output. We show that conspecifics can detect these acoustic changes and females prefer the song of exercised males. Song thus contains information on recent exercise status of the sender. Daily investment in vocal exercise to maintain peak performance is an unrecognized cost of singing and could explain why many birds sing daily even under adverse conditions10. Because neural regulation of syringeal and laryngeal muscle plasticity is equivalent, vocal output may reflect recent exercise status in all vocalizing vertebrates.
... Our findings on the extensive singing by paired males are inconsistent with the idea of inter-sexual selection such as mate attraction being the primary function of song. Clearly, singing in zebra finches has been shown to play a key role in mate preferences in laboratory-based studies 12 and in the wild when individuals need to find a new partner. 26 However, this ''directed'' song in mate choice is far less common than the so-called undirected song produced outside the mating context. ...
... 26 However, this ''directed'' song in mate choice is far less common than the so-called undirected song produced outside the mating context. 12,69 Acoustically, directed and undirected songs are almost identical in structure, carrying the same individual signature, but with directed song having more introductory notes and being sung marginally faster than undirected song. 70 The main difference is that directed song is combined with visual displays directed at a female, whereas undirected song lacks the visual display. ...
... 70 The main difference is that directed song is combined with visual displays directed at a female, whereas undirected song lacks the visual display. 70 However, both song types function in mate choice, 12 weakening the often implied functional difference between directed and undirected song. Previously, undirected song has been attributed to function in motor-practice, 71 as well as being socially inhibited, 72 but our data do not support these ideas as our transect and nest recordings showed that song changed with context and our song playback attracted conspecifics. ...
Male songbirds sing to establish territories and to attract mates.¹,² However, increasing reports of singing in non-reproductive contexts³ and by females⁴,⁵ show that song use is more diverse than previously considered. Therefore, alternative functions of song, such as social cohesion³ and synchronization of breeding, by and large, were overlooked even in such well-studied species such as the zebra finch (Taeniopygia guttata). In these social songbirds, only the males sing, and pairs breed synchronously in loose colonies,⁶,⁷ following aseasonal rain events in their arid habitat.⁸,⁹ As males are not territorial, and pairs form long-term monogamous bonds early in life, conventional theory predicts that zebra finches should not sing much at all; however, they do and their song is the focus of hundreds of lab-based studies.¹⁰,¹¹,¹²,¹³,¹⁴,¹⁵,¹⁶,¹⁷,¹⁸,¹⁹,²⁰,²¹,²² We hypothesize that zebra finch song functions to maintain social cohesion and to synchronize breeding. Here, we test this idea using data from 5 years of field studies, including observational transects, focal and year-round audio recordings, and a large-scale playback experiment. We show that zebra finches frequently sing while in groups, that breeding status influences song output at the nest and at aggregations, that they sing year round, and that they predominantly sing when with their partner, suggesting that the song remains important after pair formation. Our playback reveals that song actively features in social aggregations as it attracts conspecifics. Together, these results demonstrate that birdsong has important functions beyond territoriality and mate choice, illustrating its importance in coordination and cohesion of social units within larger societies.
... Other species such as the zebra finch however, that sing only a single song type, could be suitable models to investigate this question. Moreover, zebra finches are already an established model for song and song preference learning where the timing of the sensitive phase for song preference learning is well known (Riebel, 2003b) and suitable song preference testing paradigms are available (Holveck and Riebel, 2007;Riebel, 2009). An additional advantage is that only males produce the elaborate courtship song in this species (although both sexes are very vocal throughout the day and seasons, Zann, 1996), meaning that song preference learning in females can be studied without the added confounds arising from perceptual biases resulting from song production learning (Riebel et al., 2002;Gobes et al., 2009). ...
... However, preferences for females' fathers' songs were weaker when they were tested against a structurally more similar song. As all subjects were raised by their biological fathers, within family sharing of perceptual biases could explain aligning song and song preferences, but subsequent studies using cross-fostering or tape tutoring demonstrated preference learning beyond doubt (reviewed in Riebel, 2003bRiebel, , 2009. Several of the earlier song preference studies reported observations suggestive of generalisation: preferences for learned tutor songs were weaker when paired with structurally more similar songs in phonotaxis tests (Miller, 1979;Clayton, 1988). ...
... In this study, we investigated whether female zebra finches generalised learned song preferences for their tutor's song along a gradient of songs edited to share decreasing number of syllables with the originally learned song. Overall, female zebra finches preferred their tutor's (here their father's) song which is according to expectation arising from earlier studies in this species (reviewed in Riebel, 2003bRiebel, , 2009. Across the test song gradient, the number of syllables shared with the father's song affected females' preferences: the more familiar tutor song syllables there were in the songs, the more and the longer birds visited the perches triggering playbacks of these songs. ...
Song learning is a prime example for cultural transmission of a mating signal. Local or individual song variants are socially learned early in life and adults sing and prefer these songs. An unresolved issue in this context is the question of how learned preferences for specific variants generalise to songs sufficiently similar to the original model. Here we asked whether female zebra finches would generalise early learned song preferences along a similarity gradient based on syllable sharing between test and tutor songs. For each female, this gradient consisted of their tutor’s (father’s) song (F), two variants of unfamiliar songs edited to share 2/3 (F2/3) and 1/3 (F1/3) of syllables with father’s song and an unfamiliar song (UF) not sharing any syllables with the father’s song. Females’ preferences were measured in a 4-way operant choice arena where birds could perch on different operant perches to trigger playbacks of the four different songs. Number and duration of perch visits were positively associated with the number of syllables that the assigned stimuli shared with fathers’ songs. These results suggest that female zebra finches generalise early learned song preferences to songs sharing syllables (and/or voice characteristics) with songs learned early in life.
... Partly due to these shared features with human speech, neuroethology of birdsong has primarily focused on the signalers. As a result, neural mechanisms of song learning and production in males have been more intensively studied than those of song perception and recognition in either sex (Hernandez et al., 2008;Riebel, 2009). ...
... Although relatively less attention has been paid to song receivers compared to signalers, investigation into the mechanisms of song perception and recognition should also be an important focus as we seek to attain a deeper understanding of vocal behavior. It has been demonstrated in several species that adult and juvenile birds of both sexes can discriminate songs of different categories or acoustic and temporal features (Searcy and Yasukawa, 1996;Riebel, 2009;Rodríguez-Saltos, 2017). Their sensitivity to differences between song stimuli has been measured by behavioral, physiological, and molecular methods, and their acuity suggests the ability to recognize species, local populations, and individuals based on song features (Miller, 1979;Dooling and Searcy, 1980;Clayton, 1988;Gentner and Hulse, 2000;Maney et al., 2003;Woolley and Doupe, 2008). ...
... Strong influence of postnatal experience on the signal preference is one of the most interesting features in songbirds compared to other vertebrate or Frontiers in Physiology | www.frontiersin.org April 2022 | Volume 13 | Article 876205 invertebrate taxa (Riebel, 2009;Verzijden et al., 2012), and experience-dependent changes in song preferences can occur throughout life (Riebel, 2009). Recent studies in adult female zebra finches showed the involvement of the dopaminergic system in the acquisition of song preference using pharmacological manipulation (Day et al., 2019;Barr et al., 2021), but the neural mechanisms by which song preference is shaped early in development is still unclear. ...
Birdsong has long been a subject of extensive research in the fields of ethology as well as neuroscience. Neural and behavioral mechanisms underlying song acquisition and production in male songbirds are particularly well studied, mainly because birdsong shares some important features with human speech such as critical dependence on vocal learning. However, birdsong, like human speech, primarily functions as communication signals. The mechanisms of song perception and recognition should also be investigated to attain a deeper understanding of the nature of complex vocal signals. Although relatively less attention has been paid to song receivers compared to signalers, recent studies on female songbirds have begun to reveal the neural basis of song preference. Moreover, there are other studies of song preference in juvenile birds which suggest possible functions of preference in social context including the sensory phase of song learning. Understanding the behavioral and neural mechanisms underlying the formation, maintenance, expression, and alteration of such song preference in birds will potentially give insight into the mechanisms of speech communication in humans. To pursue this line of research, however, it is necessary to understand current methodological challenges in defining and measuring song preference. In addition, consideration of ultimate questions can also be important for laboratory researchers in designing experiments and interpreting results. Here we summarize the current understanding of song preference in female and juvenile songbirds in the context of Tinbergen’s four questions, incorporating results ranging from ethological field research to the latest neuroscience findings. We also discuss problems and remaining questions in this field and suggest some possible solutions and future directions.
... In the zebra finch, song plays a crucial role in mate choice and the link between song and female 56 preference is well studied (for a review, see Riebel, 2009). Under natural conditions, each male 57 zebra finch has a unique song, which constitutes an individual signature (Clayton, 1988;Cynx 58 & Nottebohm, 1992) and is recognized by his sexual partner (Clayton, 1988). ...
... Female zebra 59 finches also have a sensitive phase for song preference learning (Riebel, 2003) Riebel, 2000). Females, when adult, do 64 prefer the song they heard when they were young over other songs (Clayton, 1988(Clayton, , 1990Miller, 65 1979aMiller, 65 , 1979bRiebel, 2009). In the wild, female mate choice is based on different signal 66 modalities, but it has been demonstrated that the song could potentially provide sufficient 67 information about a male for females to assess his quality and allow them to make their choice 68 (Holveck & Riebel, 2007). ...
... However, there is no convincing 510 evidence so far that female zebra finches exhibit preferences for particular song features. It 511 rather seems that experience-dependent song preferences of a female zebra finch might 512 interplay with song features of the male's song (such as syllable diversity and spectro-temporal 513 details) to determine which song that female finds attractive (Riebel, 2009). Nevertheless, we 514 cannot exclude that some females in the current study preferred certain N-CST stimuli because 515 of particular sound characteristics. ...
Birdsong is culturally transmitted, and geographical variations of song have been found in several songbird species. There is evidence that such dialects contribute to reproductive isolation through variation in female preference. In the wild, there is no report of consistent dialects in populations of zebra finches. However, under laboratory conditions, we were able to artificially create different colony‐wide song dialects. In this species, song plays a crucial role in mate choice and the importance of both subadult and adult song experience in shaping song preferences has been well documented. Therefore, we expected females to prefer songs corresponding to their colony's dialect. We measured this preference using an operant test: females could either trigger a song corresponding to their Colony Song Type (CST) sang by an unfamiliar individual, or another conspecific song, corresponding to a Non‐Colony Song Type (N‐CST). Most females preferred the CST over the N‐CST, supporting the idea that zebra finch females exhibit a preference for songs similar to their colony's song. It also reveals that song dialects matter to female zebra finches. It has been proposed that song could be used as an affiliative signal in highly social species. Therefore, preferring the colony dialect could be the consequence of a sexual preference, but also of a social preference. We discuss the potential role of song dialects in the context of social learning. Dialects do not exist in wild zebra finches, but we succeeded to create two colony‐wide song types. In a two‐choice experiment, we observed that females exhibited a preference for their colony song type. This study suggests that dialects matter to zebra finches.
... Yet, by far, the most song produced by males is after pair formation, where zebra finch males keep singing in various social contexts [54]. Songs produced outside of courtship contexts are so-called undirected songs [48,84], mainly because these songs do not elicit an obvious and apparent immediate response from others. There are subtle acoustical differences between undirected and directed song, with undirected song having fewer introductory notes, being sung slower than directed songs [85] and being more variable [86]. ...
... This singing behaviour makes a fascinating case for the wider role of individually distinct vocalizations in the social organization of animal societies and widens the required considerations to understand the evolution of birdsong and animal communication, to be more integrative across a wider range of contexts and selection pressures. It will be interesting to see in the future if mated females attend to variation in their mate's song in the same way as they do when tested in a mate choice paradigm [84] because sexual and social selection after mate choice, rather than during mate choice, might pose the strongest selection pressure on their singing [24]. ...
Acoustic signalling is crucial in affecting movements and in social interactions. In species with dynamic social structures, such as multi-level societies, acoustic signals can provide a key mechanism allowing individuals to identify and find or avoid each other and to exchange information. Yet, if the spacing between individuals regularly exceeds the maximum signalling range, the relation between movements and signals becomes more complex. As the best-studied songbird in captivity, the zebra finch (Taeniopygia castanotis) is a species with individually distinct songs that are audible over just a few metres and a widely ranging dynamic multi-level social organization in the wild, raising questions on the actual role of its song in social cohesion and coordination. Here, we provide an overview of birdsong in social organizations (networks) and use the ecology of the zebra finch and male song to discuss how singing can facilitate social cohesion and coordination in species where the signal range is very short. We raise the question of the extent to which zebra finches are a representative species to understand the function of song in communication, and we broaden current views on the function of birdsong and its individual signature.
This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.
... Song production is sexually dimorphic as only males sing, but both sexes memorize tutor song as juveniles and as adults prefer to hear the songs they were exposed to early in life (Clayton, 1988;Houx and ten Cate, 1999;Riebel et al., 2002;Riebel, 2003aRiebel, , 2009). Song preference learning thus provides a unique opportunity to investigate tutor song memorization independent of motor learning (Riebel et al., 2002). ...
... To test whether FoxP1 expression in HVC or CMM is required for females to recognize and prefer songs, FoxP1 was knocked down in these areas either before (in juveniles) or after (in adults) the sensitive period for song preference learning (Riebel, 2003b(Riebel, , 2009). Subsequently, auditory memories were assessed in operant preference tests (Riebel, 2000;Holveck and Riebel, 2007). ...
The search for molecular underpinnings of human vocal communication has focused on genes encoding forkhead-box transcription factors, as rare disruptions of FOXP1, FOXP2, and FOXP4 have been linked to disorders involving speech and language deficits. In male songbirds, an animal model for vocal learning, experimentally altered expression levels of these transcription factors impair song production learning. The relative contributions of auditory processing, motor function or auditory-motor integration to the deficits observed after different FoxP manipulations in songbirds are unknown. To examine the potential effects on auditory learning and development, we focused on female zebra finches ( Taeniopygia guttata ) that do not sing but develop song memories, which can be assayed in operant preference tests. We tested whether the relatively high levels of FoxP1 expression in forebrain areas implicated in female song preference learning are crucial for the development and/or maintenance of this behavior. Juvenile and adult female zebra finches received FoxP1 knockdowns targeted to HVC (proper name) or to the caudomedial mesopallium (CMM). Irrespective of target site and whether the knockdown took place before (juveniles) or after (adults) the sensitive phase for song memorization, all groups preferred their tutor’s song. However, adult females with FoxP1 knockdowns targeted at HVC showed weaker motivation to hear song and weaker song preferences than sham-treated controls, while no such differences were observed after knockdowns in CMM or in juveniles. In summary, FoxP1 knockdowns in the cortical song nucleus HVC were not associated with impaired tutor song memory but reduced motivation to actively request tutor songs.
... One of the main model bird species is the Australian zebra finch (Taeniopygia guttata castanotis), providing the primary avian model organism in laboratory studies world-wide (Griffith and Buchanan 2010;Griffith et al. 2021). Zebra finches have been key in studies on mate choice (Slater et al. 1988;Riebel 2009;Kniel et al. 2015), long term effects of early developmental stress (Spencer et al. 2005;Monaghan et al. 2012;Honarmand et al. 2015), and specifically are a textbook model for the physiology, neurobiology and genetics of the song system (Haesler et al. 2004;Gil et al. 2006;Warren et al. 2010;Ma et al. 2020) including song development and learning (Slater et al. 1988;Kriengwatana et al. 2016;Hauber et al. 2021;Tchernichovski et al. 2021). Yet, very few studies have addressed zebra finch song in the wild Zann 1996a, 1996b;Woodgate et al. 2012), so that the ecological context and perspective on the findings from laboratory studies is largely lacking and often based on anecdotal observations (Immelmann 1968;Zann 1996). ...
... Advantages of using zebra finch song under laboratory conditions as a model for animal communication and the neural basis of song learning, are that males sing all year round, individuals sing a unique single motif (song) produced with only small variation across repetitions (Sturdy et al. 1999), and males sing reliably when exposed to females (Riebel 2009). Whilst the latter characteristic has made the zebra finch song a major focus of work on mate choice, wild males continue to sing outside breeding events (Zann 1996;Griffith 2019), and indeed most males are paired for life from an early age (Zann 1996). ...
Birdsong is typically seen as a long-range signal functioning in mate attraction and territory defense. Among birds, the zebra finch is the prime model organism in bioacoustics, yet almost exclusively studied in the lab. In the wild, however, zebra finch song differs strikingly from songbirds commonly studied in the wild as zebra finch males sing most after mating and in the absence of territoriality. Using data from the wild, we here provide an ecological context for a wealth of laboratory studies. By integrating calibrated sound recordings, sound transmission experiments and social ecology of zebra finches in the wild with insights from hearing physiology we show that wild zebra finch song is a very short-range signal with an audible range of about nine meters and that even the louder distance calls do not carry much farther (up to about fourteen meters). These integrated findings provide an ecological context for the interpretation of laboratory studies of this species and indicate that the vocal communication distance of the main laboratory species for avian acoustics contrasts strikingly with songbirds that use their song as a long-range advertisement signal.
... 104,118 Substantial research exists on the importance of male song for mate attraction and female choice in zebra finches and other songbirds. 104,[138][139][140][141] There is considerably less research on the large repertoire and use of male and female calls. ...
... When establishing a pair bond, male song is essential for courtship, and females select mates based heavily on these songs. 104,[138][139][140] Males that are unable to sing are unlikely to successfully attract a mate. 153 However, female zebra finches do not simply make mate choice decisions based on static assessements of a male signal. ...
Organisms filter the complexity of natural stimuli through their individual sensory and perceptual systems. Such perceptual filtering is particularly important for social stimuli. A shared “social umwelt” allows individuals to respond appropriately to the expected diversity of cues and signals during social interactions. In this way, the behavioral and neurobiological mechanisms of sociality and social bonding cannot be disentangled from perceptual mechanisms and sensory processing. While a degree of embeddedness between social and sensory processes is clear, our dominant theoretical frameworks favor treating the social and sensory processes as distinct. An integrated social-sensory framework has the potential to greatly expand our understanding of the mechanisms underlying individual variation in social bonding and sociality more broadly. Here we leverage what is known about sensory processing and pair bonding in two common study systems with significant species differences in their umwelt (rodent chemosensation and avian acoustic communication). We primarily highlight that (1) communication is essential for pair bond formation and maintenance, (2) the neural circuits underlying perception, communication and social bonding are integrated, and (3) candidate neuromodulatory mechanisms that regulate pair bonding also impact communication and perception. Finally, we propose approaches and frameworks that more fully integrate sensory processing, communication, and social bonding across levels of analysis: behavioral, neurobiological, and genomic. This perspective raises two key questions: (1) how is social bonding shaped by differences in sensory processing?, and (2) to what extent is sensory processing and the saliency of signals shaped by social interactions and emerging relationships?
... Results suggest that males calling with a high rate attract more flying females and more females on the ground. Similar results have been found in mammals and birds (McComb, 1991;Riebel, 2009). ...
... Results suggest that males calling with a high rate attract more flying females and more females on the ground. Similar results have been found in mammals and birds (McComb 1991;Riebel 2009). One possible explanation would be that males producing many frequent calls are easier to locate in dense and noisy colonies (up to two burrows per m 2 : Brothers 1984) because the repetition of calls helps the female walking on the ground to locate the source of emission . ...
Comme Bradbury et Verhencamp (1998) l’ont joliment dit, la communication est « la colle maintenant les sociétés animales » car elle est le fondement de nombreux comportements sociaux chez la majorité des espèces. Les pétrels fouisseurs offrent une excellente opportunité d’étudier la communication vocale dans un environnement qui, de prime abord, semble désavantageux. En effet, ces oiseaux marins se regroupent au cours de la saison de reproduction en denses colonies. En dépit des turbulences climatiques (ex. vents violents), des interférences vocales liées à la présence d’autres oiseaux et de la présence de prédateurs qui chassent à l’ouïe, les vocalisations sont à la base des interactions sociales. Durant ma thèse, je me suis intéressée à deux espèces de pétrels fouisseurs phylogénétiquement proches : le pétrel bleu Halobaena caerulea et le prion de la Désolation Pachyptila desolata, tous deux connus pour leurs capacités olfactives développées. En dépit des contraintes environnementales, de la pression de prédation et la possibilité de communiquer via des signaux olfactifs, la communication vocale devrait procurer des bénéfices jusqu’alors méconnus. A l’aide d’expériences de repasse et d’attractivité menées sur un site de reproduction des oiseaux, à Kerguelen, mon objectif a été d’étudier les déterminismes et implications des cris des mâles dans le choix de partenaire des femelles. Les résultats de la présente thèse soulignent : (i) la stratégie de codage de l’information statique (morphologie et identité individuelle) et dynamique (motivation) au niveau des caractéristiques spectrales et temporelles des cris de mâles ; (ii) en quoi la détectabilité du cri et surtout l’information contenue influencent le choix du partenaire par les femelles : et (iii) le rôle joué par le terrier dans la propagation du cri et le choix du partenaire par les femelles. Les deux espèces étudiées ici montrent des similarités dans leurs stratégies vocales et de codage de l’information, ce qui suggère que les mêmes contraintes environnementales sur la communication longue distance ont modifié les signaux de manière similaire. Ces résultats enrichissent nos connaissances sur la manière dont les oiseaux nichant en terriers, très peu étudiés, communiquent dans un environnement contraignant.
... Since Darwin highlighted sexual selection as a driving force in the evolution of such signals (Darwin 1859), many studies have provided evidence that individuals with more elaborate signals on average are preferred by the opposite sex and have a fitness benefit (Andersson and Simmons 2006). Yet more recent studies have emphasised that females also vary in their preferences (Riebel 2009;Buchanan et al. 2013) and that males with the most elaborate signals thus might not always be the most preferred mate. Moreover, under natural conditions females will never have perfect information, make errors, and also will differ individually in the information they have available. ...
... To understand the broader principles of animal communication and specifically its role in mate choice, bird song has played a key role as it is important for both territory defence against other males and mate attraction (Searcy and Yaukawa 1996;Catchpole and Slater 2008;Naguib and Riebel 2014). Yet despite decades of research, our understanding of how female birds use song to assess and choose mates in their natural environment is surprisingly limited, as many studies on female preference for male song have been conducted in highly standardised laboratory situations (Riebel 2009;Leboucher et al. 2012;Honarmand et al. 2017). Studies in the wild linking female choice to male characteristics have either correlated male traits with the timing of mating or mating success, or related female extra-pair mating decisions to male traits (Catchpole and Slater 2008). ...
The behavioural decisions animals take directly influence their fitness and thus have a fundamental impact on evolutionary processes. In many animals, acoustic signals play an important role in social decisions with mate choice being among the most apparent ones. Male bird song has played a key role along this line, yet the understanding of how female birds use song to prospect, assess and choose mates in their natural environment is surprisingly limited. A main reason for this limited understanding is that it is very difficult to follow a female during her prospecting and decision process and quantify her experience with different males before she makes a final decision. Here we integrate insights from communication networks, male song traits and female prospecting behaviour to stimulate a more integrative approach on the role of signalling in behavioural and reproductive decisions.
... It is paramount to consider the different pressures that influence territoriality in temperate and tropical regions while testing the effect of local density on vocal behaviour. It is well known that males in temperate regions sing to defend resources that allow them to attract breeding partners during a relatively short breeding season (Searcy 1992;Nowicki and Searcy 2005) and females use song output and song features to evaluate potential mates (Reid et al. 2004;Riebel 2009). Therefore, we anticipate a stronger response to variation in local density for males compared to females in the temperate zone (Fig. 1A). ...
Among territorial birds, the number of conspecific neighbours sets the social context of communication. There have been many investigations of vocal behaviour and its important role in territory defense and mate attraction in birds; however, the effect of the density of conspecific neighbours on avian communication has received little attention. In this study, we reviewed the literature on the influence of local density on vocal communication in birds, exploring how the number of conspecific neighbours influences avian vocal behaviour, by conducting a literature review following the guidelines of the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) in two databases: Web of Science and Scopus. We also included additional articles from a more flexible search in Google Scholar. We found 19 studies of birds that included data on vocal behaviour in relation to the number of conspecific neighbours. The majority of these studies (14 of 19) showed that local density influences avian vocal behaviour. Overall, these studies revealed an effect of local density of conspecifics on song rate (expressed as song rate, syllable rate, solo song rate, or singing rate). Other vocal behaviours that were shown to vary with local density included song-type switching, song duration, peak frequency, and song variation. Most studies focused on temperate-zone species where males are the predominant singers. Our results reveal a bias towards the study of male songs in the context of local density, with very few studies on female song; this corresponds with a historical geographical focus on temperate birds. We present experimental design suggestions for future investigations, including predictions for males and females of tropical and temperate species. Finally, we argue that more research on this topic is needed, and that investigations of vocal communication will benefit from further study of the influence of density on avian vocal behaviour.
... Animals might use physical characteristics to select their mate, like coloration (Baube et al. 1995;Rowland et al. 1995;Pryke and Griffith 2007;Gomez et al. 2010) or size (McKaye 1986;Howard et al. 1998;Shine et al. 2001;Romero-Pujante et al. 2002;Hoefler 2007). They can also use behavioral traits such as song characteristics (Searcy 1992;Wagner and Reiser 2000;Byers and Kroodsma 2009;Riebel 2009;Caro et al. 2010;Iglesias and Hasson 2017), courtship behaviors (Zuk et al. 1990;Sargent et al. 1998;Kallman et al. 2015;Ota et al. 2015), personality (van Oers et al. 2008;Schuett et al. 2011;Bierbach et al. 2015;Chen et al. 2018;, or cognitive abilities (Boogert et al. 2011;Kavaliers and Choleris 2017). Even the chooser's own phenotype, such as its condition, coloration, or size (Hunt et al. 2005;Holveck and Riebel 2010;Rueger et al. 2016;Caro et al. 2021), can play a decisive role at the time they decide with whom to mate. ...
Do females modify their reproductive investment if they do not succeed in pairing with a male that matches their preference? In a two-year experiment, we asked female blue tits (Cyanistes caeruleus) to select among six males, and then successively paired them with their preferred and their most avoided male. We monitored female reproductive investment through nest building activity, timing of breeding, size and number of eggs, number of fertilized eggs, and brood sex ratio. We found that females preferred males with a chromatic coloration (blue UV chroma of the head crown) that matched their own, but also that they preferred males with a lower achromatic coloration (less bright color of the cheeks and head crown). Although females paired with their preferred males tended to build heavier nests during the breeding season, we found no evidence of an effect of the pairing treatment on timing of breeding, or any other aspects of female reproductive investment. We however found that laying dates, clutch sizes, egg sizes, and brood sex ratio were significantly repeatable within females between the two years, despite the opposite pairing treatments. These findings show that in female blue tits, the males with which they are paired do not substantially alter their reproductive decisions.
... Previous investigations on the courtship of Java sparrows in captivity revealed that the presence of duet dancing is more important for successful mating than song alone (Soma and Iwama 2017). This may come as a surprise, considering that individual variations in songs are typically a major factor in mate choice among songbirds (Searcy 1992;Riebel 2009;Byers and Kroodsma 2009;Soma and Garamszegi 2011; see also Snyder and Creanza 2019). It is likely that dance, as a visual signal, would be of greater use in close-distance communication than in vocalization. ...
Courtship singing in songbirds is often accompanied by gestural displays, similar to human vocalization or music that solicits body movements. This suggests that sound communication can potentially function in multimodal contexts; however, prior songbird research has primarily focused on the acoustic domain solely. In an effort to understand the multimodal signaling associated with singing, we analyzed the simultaneous singing and dancing courtship displays of Java sparrows. Specifically, we investigated the degree of singing-dancing temporal coordination in males as well as individual variability in dance sequences in males and females, as only males sing, but both sexes engage in courtship duet dancing. The results revealed a strong temporal relationship between the commencement of hopping and the production of song notes in males, which was affected not only by song learning but also by the identity of the female that received the courtship display. In addition, the dancing sequence was more complex in males than in females. Although it remained unexplained how such among- and within-individual variations contribute to the message content of courtship in the Java sparrow, multimodal courtship was not merely a byproduct of singing and warrants further scrutiny in future investigations.KeywordsAudio-visual communicationEstrildid finchDanceMutual courtshipSexual signal
... Courtship displays may allow individuals to identify and choose between potential mating partners, and in some cases to maintain a pair bond. Avian courtship behaviours can involve displays of different sensory modes; from visual signals, such as plumage pattern or colouration (e.g., Goodwin, 1982;Naguib and Nemitz, 2007;Soma and Garamszegi, 2015), acoustic signals, such as bird song (e.g., Catchpole and Slater, 2003;Riebel, 2009), to olfactory signals (e.g., Caro and Balthazart, 2010;Whittaker et al., 2013;Caspers et al., 2015a;Grieves et al., 2022), and specific movements, such as courtship dances (e.g., Goodwin, 1982;Zann, 1996;Soma and Garamszegi, 2015). ...
Avian courtship behaviour is essential to attract potential mating partners. Courtship behaviours can involve displays of different sensory modes. Sex discrimination is a crucial step and in many bird species, sexes differ in acoustic and visual traits, allowing sex discrimination. It has been shown only recently that in some species of Estrildid Finches, chemical cues are involved in social communication. Here, we investigated whether olfaction also plays a role in sex discrimination in Estrildid Finches. Investigating olfactory sex preferences as an indicator behaviour in six different Estrildid Finch species, we aimed to understand whether sex- and/or species-specific differences in olfactory preferences exists and whether olfactory sex preferences correspond to species-specific differences in sex-specific acoustic and visual displays, e.g., singing, plumage dimorphisms and courtship dance. Olfactory sex preferences were tested in a Y-Maze test. We found differences in scent preferences among the different species of Estrildid Finches. We discussed the behavioural pattern with respect to other species-specific traits. And their potential implications in a broader mate choice context.
... Studies of songbirds provide a key experimental advantage in that song is a unimodal stimulus. Even though mate choice involves information obtained through a variety of modalities, song is so influential that females will solicit copulation by performing a copulation solicitation display (CSD) in response to song even if no male is physically present Searcy and Andersson, 1986;Candolin, 2003;Riebel, 2009;Byers et al., 2010;Dunning et al., 2014). Female perception and mate choice are best measured through CSD production, but other behaviors may also serve as proxies of female mate preference. ...
Animals use a variety of complex signaling mechanisms to convey an array of information that can be detected by conspecifics and heterospecifics. Receivers of those signals perceive that information and use it to direct their subsequent actions. Thus, communication such as that which occurs between senders and receivers of vocal communication signals can be a powerful model in which to investigate the neural basis of sensory perception and action initiation that underlie decision-making. In this study, we investigated how female songbirds perceive the quality of acoustic signals (songs) performed by males and use that information to express preference for one song among many possible alternatives. We use behavioral measurement of song preference before and after lesion-induced alteration of activity in an auditory processing area (caudal nidopallium, NC) for which we have previously described its interconnections with other auditory areas and downstream reward pathways. Our findings reveal that inactivating NC does not change a female’s ability or willingness to perform behavioral indicators of mate choice, nor does it change their ability to identify the songs of individual males. However, lesioning NC does induce a decrease in the strength of song preference for specific males more than others. That decrease does not result in a complete elimination of preference, as female preferences for specific males are still evident but not as strongly expressed after lesioning of NC. Taken together, these data indicate that NC plays a role in a female’s strength of preference in song evaluation and mate choice, and activity in NC is an important facet of mate choice.
... stressors, parasites, or developmental historyon courtship performance underlies a large number of sexual selection studies (Andersson, 1994;Grafen, 1990;Johnstone, Rands, & Evans, 2009;Kokko, Jennions, & Brooks, 2006). For instance, developmental stress has been shown to impact repertoire size and copying fidelity in songbirds (Boogert, Fawcett, & Lefebvre, 2011;Buchanan, Spencer, Goldsmith, & Catchpole, 2003;Podos, Lahti, & Moseley, 2009;Riebel, 2009). Moreover, phenotypic plasticity and the deployment of alternative courtship tactics have been identified across diverse taxa (Gross, 1996;Oliveira, Taborsky, & Brockmann, 2008;Patricelli, Krakauer & McElreath, 2011). ...
Research into learning of courtship behavior remains largely confined to birdsong and vocal learning studies. Yet, visually communicated aspects of courtship displays are widespread and prominent, and also deserve consideration. Postural displays, choreographies, and construction of display arenas are all visual signal components mediated by motor activity of the displayer. The goal of this review is to present growing evidence for learning of courtship motor patterns other than song. We tackle two main challenges: we first highlight criteria that can be used to determine whether visual courtship components are learned, and if so, we then assess the type of learning involved. In line with the vocal learning literature, we suggest applying a distinction between usage learning and production learning of motor patterns: usage learning refers to a change in the context in which pre-existing display patterns are used, whereas production learning involves modification in trait structure, i.e. the acquisition of novel display patterns from a model. The effects of imitation, social feedback, and practice are described in detail, drawing on multiple examples from birdsong research. Our goals are to illustrate the learning processes which may affect motor development of courtship signals, to formulate testable predictions for each learning category and related mechanisms, and to suggest possible lines for future research. Although most of the evidence we review here is indirect and not yet conclusive about learning, recent technological advances now provide novel tools to quantify courtship motor patterns, and thus have the potential to produce more direct insights into whether, and how, courtship displays are learned.
... Zebra finches sing a complex, rhythmic song that is a multicomponent signal. High syllable repertoire is among the song traits preferred by females (for a detailed review of song function and sexual selection in zebra finches, see Riebel, 2009). Included in our review were six studies that analyzed syllable repertoire (also referred to as number of unique syllables or elements; Table 3). ...
Many sexually selected traits exhibit phenotypic plasticity. Despite a growing appreciation for the ecological context in which sexual selection occurs, and for the role of plasticity in shaping traits associated with local adaptation and divergence, there is an important gap in knowledge about the onset and duration of plasticity in sexual trait expression. Integrating this temporal dimension of plasticity into models of sexual selection informs our understanding of the information conveyed by sexual traits and our predictions related to trait evolution, and is critical in this time of unprecedented and rapid environmental change. We conducted a systematic review of 869 studies to ask how trait modalities (e.g., visual and chemical) relate to the onset and duration of plasticity in vertebrate sexual signals. We show that this literature is dominated by studies of coloration in birds and fish, and most studies take place during the breeding season. Where possible, we integrate results across studies to link physiology of specific trait modalities with the life stage (e.g., juvenile, breeding, or nonbreeding) during which plasticity occurs in well-studied traits. Limitations of our review included a lack of replication in our dataset, which precluded formal analysis. We argue that the timing of trait plasticity, in addition to environmental context, is critical for determining whether and how various communication signals are associated with ecological context, because plasticity may be ongoing or occur at only one point in an individual's lifetime, and determining a fixed trajectory of trait expression. We advocate for careful consideration of the onset and duration of plasticity when analyzing how environmental variation affects sexual trait expression and associated evolutionary outcomes.
... In contrast to clumping, we found a negative relationship between D1 over D2 mRNA ratios in NAc and undirected song production. Whereas female-directed song in zebra finches is known to be critical for mate attraction (Riebel, 2009;Tomaszycki & Adkins-Regan, 2005), the function of undirected song in zebra finches remains elusive. Undirected song is produced at higher rates by unpaired males than by paired males (Bolund et al., 2012) and in paired males is positively correlated with extra-pair directed song but not partner-directed song (Dunn & Zann 1996), suggesting a role in mate attraction. ...
Long-term social bonds are critical for survival and reproductive success in many species. Although courtship and pair-bond formation are relatively well studied, much less is known about the neural regulation of behaviors that occur after pair bonding that reinforce the bond and contribute to reproductive success. Dopamine and opioids in the nucleus accumbens (NAc) alter motivational state and reward by binding to receptor subtypes that engage distinct and opposing second messenger systems, and there is evidence that receptor ratios may influence social behavior. We used quantitative real-time PCR to explore relationships between messenger RNA ratios for dopamine D1 and D2 receptors (D1:D2) and mu and kappa opioid receptors (MOR:KOR) in NAc and behaviors implicated in reproductive investment and pair-bond maintenance in established male-female zebra finch pairs. In males, D1:D2 expression in NAc related negatively, whereas MOR:KOR related positively, to undirected song production. D1:D2 receptors also related positively to physical contact with a female. For females, D1:D2 expression was lower in females exposed to high compared to low rates of the partner's undirected song, and MOR:KOR expression in females related positively to undirected song exposure and allopreening. Analyses of single genes did not yield the same results. These findings suggest that the ratio of D1 to D2 and MOR to KOR receptor signaling in NAc causes differences in behavior or that behavior (or the partner's behavior) causes receptor ratio changes to modulate behaviors that maintain pair bonds and promote reproductive investment. (PsycInfo Database Record (c) 2021 APA, all rights reserved).
... This species, an important laboratory model for animal behavior research (Immelmann 1965;Zann 1996;Griffith and Buchanan 2010), typically pairs for life, and both sexes contribute substantially to nest building and defense, incubation/brooding, and feeding of offspring (Delesalle 1986;Burley 1988a;Zann and Rossetto 1991;Zann 1996;Gilby et al. 2011). Previous studies have reported that female zebra finches have consensus mate preferences for sexually dimorphic traits, including acoustic (song) traits (Collins et al. 1994;Tomaszycki and Adkins-Regan 2005;Riebel 2009) and visual traits (beak color: Simons and Verhulst 2011 and references therein; cheek patch size: Tschirren et al. 2012;Burley et al. 2018). Males also have mating preferences for female beak color (Burley and Coopersmith 1987;Bennett et al. 1996;Templeton et al. 2014), and both sexes have latent preferences for novel ornamental traits (Burley et al. 1982). ...
Understanding the dynamics of mutual mate choice requires investigation of mate preferences of both sexes using a variety of designs, but fewer studies have focused on male choice in avian models. Here we conducted two experiments on preferences of male zebra finches to study the impact of trial design on results. Experimental design varied in number of trial participants, inclusion of observer (“audience”) males, and housing design for stimulus females. Females were reared on one of two diets to enhance variation in mating quality: those reared on a protein-supplement diet (HI-diet) were predicted to be more attractive to males than (LO-diet) females that did not receive supplements. Results differed among trial types. Notably, males showed the predicted preference for HI-diet females only in the Group Choice experiment, where two male subjects simultaneously chose from a field of four females, and all six birds interacted freely. In the Dyadic Preference (DP) experiment, a single male was allowed to interact with two stimulus females that were physically isolated; in half of these trials, audience males were present. In DP trials without audience males, test males did not express a preference consensus; however, with audience males present, test males preferred LO-diet females. Results are consistent with a small but growing literature indicating that results of mate choice experiments can be highly sensitive to design considerations.
... The importance of studying female zebra finches 482 Female zebra finches only slowly and partially assumed a role in some of the earlier behavioral 483 and developmental studies on sexual imprinting (e.g., Collins et al., 1994), but now maintain a 484 co-lead position. This is because mate choice is mutual in this species and females participate in 485 the ever-important initial pair-bonding decisions, as well as in all aspects of collaborative 486 biparental care (Riebel, 2009). As such, females make a critical contribution to the phenotype of Finally, the behavioral, the neurophysiological and gene-activational bases of perceptual 513 learning of conspecific song features appear to be both species-specific in song-naïve (mother-514 only parent raised) female zebra finches and dependent on early social experience with con-or 515 cross-fostered heterospecific male songs (Hauber et al., 2013;Louder et al. 2018). ...
The zebra finch ( Taeniopygia guttata ) is a socially monogamous and colonial opportunistic breeder with pronounced sexual differences in singing and plumage coloration. Its natural history has led to it becoming a model species for research into sex differences in vocal communication, as well as behavioral, neural and genomic theories of imitative auditory learning. As scientists tap into the genetic and behavioral diversity of both wild and captive lineages, the zebra finch will continue to inform research into culture, learning and social bonding, as well as adaptability to a changing climate.
... Zebra finches (Taeniopygia guttata) are small Australian songbirds frequently studied in the context of mate choice (reviewed in Riebel, 2009). Despite thorough examination, it remains unclear how zebra finches select their mates. ...
In species with long-term pair bonds, such as zebra finches, evaluating the quality of potential mates is critically important. Courtship is an opportunity to evaluate information from dynamic behavioural cues. Personality traits, as stable individual differences in behaviour, could predict the quality of a potential mate. How might personality traits influence mate choice? We examined the influence of several personality traits, including exploration, aggression, and social preference, on pair formation in zebra finches. We provided birds with a variety of potential mates and allowed them to select a pair partner. Our semi-naturalistic mate choice paradigm allowed birds to observe social information over an extended period, simulating the challenges of social evaluation that birds encounter in the wild. We found that pairing is influenced by personality, with birds selecting mates similar to them in exploration. The partner’s exploration score relative to their own was more important than the absolute exploration score.
... Juvenile males learn their song during a sensitive period early in life often from their father (Immelmann, 1969;Zann, 1996). Song is used by females for mate choice decisions (Riebel, 2009; but see Wang et al., 2017) but might also serve for intra-group communication in this species. Under typical conditions, males of a given colony would not all produce the same song type, as they would have different male tutorssinging different song typesfrom which to learn their song or different parts of their song. ...
Vocal communication is essential for social interactions in many animal species. For this purpose an animal has to perceive vocal signals of conspecifics and is often also required to discriminate conspecifics. The capacity to discriminate conspecifics is particularly important in social species in which individuals interact repeatedly. In addition, auditory perception of self plays an important role for vocal learners. It allows a vocal learner to memorise vocalisations of conspecifics and to subsequently modify its own vocalisations in order to match the memorised vocalisations. Here we investigated auditory perception of self and others in zebra finches (Taeniopygia guttata), a highly gregarious songbird species and vocal learner. We used laboratory colonies in which founder males had been previously trained to produce the same song type. This resulted in artificial dialects in the song of founders and their offspring. We investigated whether those birds would be able to discriminate between familiar and unfamiliar conspecifics based on song. Furthermore, we examined whether they would classify their own song as familiar or unfamiliar. We found that birds were able to discriminate between songs of familiar versus unfamiliar conspecifics, despite the fact that all songs were imitations of the same song type. This suggests that such discrimination is possible even based on songs with a high acoustic similarity. None of the subjects classified their own song as unfamiliar. Three out of eight males classified their own song as familiar. Thus zebra finches might recognise their own song. Further experiments are needed to confirm such self-recognition.
... Results suggest that males calling with a high rate attract more flying females and more females on the ground. Similar results have been found in mammals and birds (McComb 1991;Riebel 2009). One possible explanation would be that males producing many frequent calls are easier to locate in dense and noisy colonies (up to two burrows per m 2 : Brothers 1984) because the repetition of calls helps the female walking on the ground to locate the source of emission (Storey 1984). ...
In blue petrels (Halobaena caerulea), females are supposed to be particularly choosy and mate choice can take a couple of years. In these lifelong monogamous seabirds, choosing a good mate is crucial and has a strong influence on their fitness. Due to their nocturnal habits, the absence of sexual dimorphism, and the physical barrier between males calling from their burrow and females flying above the colony, vocal signals seem to be one of the main channels for males to communicate with potential mates. In a previous study, we investigated whether acoustic parameters of male calls carry information about morphological characteristics that might be indicators of males’ qualities. Here, we experimentally test whether these acoustic parameters linked to male characteristics are actually attractive to females. To do so, we played back modified calls of males to females in a colony of blue petrels of the Kerguelen archipelago. We found that flying females were more attracted by high-pitched calls, and by calls broadcasted at a high call rate. Previous studies showed a relationship between pitch and bill depth and length. In filter-feeding birds, such as blue petrels, bill morphology influences feeding efficiency. A high call rate is an indicator of sexual motivation and makes the caller easier to locate by potential mates and predators in the hubbub of the colony. We thus hypothesized that producing frequent high-pitched calls appeared to be preferable for a conspicuous sexual signaling although it may increase predation risks.
Significance statement
Mate selection process is largely unknown in burrowing petrels due to their cryptic life at the colony. Here, we examined the implication of vocal signals in mate choice in the blue petrel Halobaena caerulea. We used an experimental setting based on a two-choice test to show that male calls are sexual signals attracting females. As expected, broadcasting male calls attracted females. Despite the apparent stereotypy of male calls, their acoustic parameters transmit pieces of information that may influence females’ preference. We found that females are more attracted by high call rate and high-pitched calls. This is the first evidence of the implication and influence of vocal signals in mate choice in burrowing petrels.
... "Topic" searches title, abstract, author keywords and keywords plus. The Zebra Finch has become established as the main model species for understanding the neuronal mechanisms of song and vocal learning [9,10], and more recently the female perception of song [11]. The utility of the Zebra Finch in this research field followed the early discovery of the clearly defined sensitive period in development for the acquisition of phenotypes relating to acoustic production and perception [12]. ...
Zebra Finches have become the most widely researched bird species outside of those used in agricultural production. Their adoption as the avian model of choice is largely down to a number of characteristics that make them easy to obtain and use in captivity. The main point of our paper is that the very characteristics that make the Zebra Finch a highly amenable laboratory model species mean that it is by definition different from many other passerine birds, and therefore not a good general model for many research areas. The Zebra Finch is likely to be particularly resilient to the effects of stress early in life, and is likely to show great flexibility in dealing with a wide variety of conditions later in life. Whilst it is tempting for researchers to turn to species such as the Zebra Finch, that can be the focus of manipulative work in the laboratory, we caution that the findings of such studies may confound our understanding of general avian biology. The Zebra Finch will remain an excellent species for laboratory work, and our paper should help to direct and interpret future work in the laboratory and the field.
... If we can determine the signal component(s) to which receivers respond, we can identify the relevant selective force(s) and make informed predictions about the evolution of the signal. Important advances in this regard have been made in a few model systems, notably in acoustic (Ryan and Rand 2003;Riebel 2009) and visual (Endler 1992;Grether et al. 2004;Price et al. 2008) signaling, while other taxa (e.g., reptiles) and sensory modalities (e.g., chemical) remain deeply understudied (Coleman 2009). ...
Most animal signals across sensory modalities are multicomponent traits that can be broken down into discrete elements. If different elements are perceived as unique, independent units (elemental perception), instead of as integrated percepts (configural perception), single changes in the presence/absence or the abundance of specific elements of a multicomponent signal may be enough to impact communication. Here, we found that male Yarrow’s spiny lizards (Sceloporus jarrovii) can discriminate single compounds of a multicomponent chemical signal (femoral gland secretions), different concentrations of a signaling compound, and a single compound from a mixture of compounds. In addition, one chemical compound elicited a response similar to that evoked by the complete natural scent. We conclude that perception of chemical signals in S. jarrovii lizards is elemental but also configural. The elemental perception of signaling compounds seems to occur with high sensitivity and narrow resolution, so that minor changes in single key elements may affect chemical communication. Given the multicomponent nature of most animal signals, hypotheses regarding signal function and evolution would be enhanced if researchers could determine whether these results apply to signals in other sensory modalities and identify the key elements of complex signals, from a receiver’s perspective.
Significance statement
Most signals in animal communication are quite complex. For example, odors are mixtures of multiple volatile chemical compounds, and the way in which receivers perceive and process these mixtures to extract relevant information influences the structure and evolution of chemical signals. In a series of behavioral trials, we investigated how male Sceloporus jarrovii lizards may perceive conspecific odors by testing their response to individual and combined mixtures of two compounds present in femoral gland secretions at two different concentrations. We demonstrate that lizards can discriminate structurally similar compounds and that the response to a compound changes when said compound is part of a larger mixture. Compound concentration affected the perception of individual compounds but not complex mixtures. Deciphering what elements and/or configurations are perceived in an odor mixture is the only way to understand the role of mixture composition and its impact on communication.
... These signals may influence receivers over varying temporal and spatial scales, and multiple components of a single signal may be the target of selection (Candolin 2003;Bro-Jørgenson 2009). Conversely, signals with multiple components such as songs and complex visual signals may be evaluated in a gestalt fashion (Riebel 2009), although the operation of this method of signal evaluation and processing would be difficult to demonstrate empirically, especially in fieldbased studies (Weatherhead et al. 1991). Our methods and results support the current trend of focusing on more than one single conspicuous trait in mate choice analyses and instead taking into account the full range of signals transmitted by individuals of the chosen sex, possibly spanning multiple sensory modalities (Scheffer et al. 1996;Fusani et al. 1997). ...
Sexual selection theory maintains that traits under selection honestly advertise qualities of signaling individuals and that only individuals in the best condition can survive while displaying maximally elaborated secondary sexual ornaments. Recent trends in mate choice studies have favored the consideration of the effects of multiple traits on mating success, including suites of traits transmitted in different sensory modalities. Sexual selection is expected to be especially strong in lek-mating species. The lesser prairie-chicken (Tympanuchus pallidicinctus) is a grouse species which breeds on leks. Males of this species perform audio and locomotor displays and exhibit two pairs of brightly colored ornaments. We performed an observational study of mate choice in spring 2016–2018 and noted 40 copulations on seven leks. We quantified behavioral, territorial, and morphological characteristics of males along with ornament color properties. We found that variables from all categories considered predicted female choice. Age had the strongest effect, with adult males experiencing higher female choice relative to yearlings. Allocation of aggressive behavior and comb color properties were also strongly correlated with female choice. Our results show that modulating behavior depending on whether females are present contributes to male mating success and highlight the importance of the size and color properties of secondary ornaments. Further research is required to determine how the variables most strongly associated with mate choice relate to one another and which aspects of individual quality, if any, are signaled by color ornaments. Future studies could also incorporate variables related to females to determine if selection on females occurs.
Significance statement
The choice of a mate can help determine the survival and reproductive success of offspring. In species where males do not care for offspring, mate choice can be highly consistent among females, and mate choice decisions are often based on the evaluation of multiple traits such as vocalizations, behavior, and morphological trait size. Based on measurements of captured males and observations of breeding behavior, we demonstrate that mate choice in lesser prairie-chickens (Tympanuchus pallidicinctus) correlates with male behavior, morphology, skin patch color, and territorial characteristics. Our findings represent a rare demonstration of mating success being influenced by how male behavior (including aggression) changes when females are present or absent. Our results show how multiple traits can transmit information about individual quality and support theoretical links between mate choice and increased male age or male-male competition.
... One possibility is that song memory guides female attraction to songs with specific features during mate choice by sexual imprinting (19,20,21,22). ...
Auditory learning is a prerequisite step for acoustic communication learning, which was previously assumed to be restricted to animals with high levels of cognition, such as humans, cetaceans, and birds. How animals that rely on auditory learning for acoustic communication form sound preferences is not known. Fruit flies are a recently proposed novel animal model for studying experience-dependent auditory perceptual plasticity because of their ability to acquire song preferences via song exposure. Whether fruit flies have innate courtship song preferences, however, is unclear. Here we report that, similar to songbirds, fruit flies exhibit an innate preference for conspecific courtship songs. Maintenance of innate song preference requires song input, reminiscent of the song learning process in songbirds. Our findings also indicate that the response to conspecific and heterospecific songs manifests temporal and experience-dependent differentiation, which may underlie innate song preference and its plasticity. In addition, we find that flies have a robust ability to reacquire song preference during aging. Fruit flies thus offer a novel and simple approach for studying sound preference formation and its underlying mechanisms.
... Humans develop lifelong auditory skills based on infant experiences with native-language sounds 9,10 , and childhood experience with a language predicts adult proficiency 11 . Similarly, songbirds develop lifelong auditory preferences for 12 and vocal copies of 13 adult songs that they hear as juveniles, and adults discriminate among songs of their own species better than those of other species 3 . ...
Vocal learners use early social experience to develop auditory skills specialized for communication. However, it is unknown where in the auditory pathway neural responses become selective for vocalizations or how the underlying encoding mechanisms change with experience. We used a vocal tutoring manipulation in two species of songbird to reveal that tuning for conspecific song arises within the primary auditory cortical circuit. Neurons in the deep region of primary auditory cortex responded more to conspecific songs than to other species’ songs and more to species-typical spectrotemporal modulations, but neurons in the intermediate (thalamorecipient) region did not. Moreover, birds that learned song from another species exhibited parallel shifts in selectivity and tuning toward the tutor species’ songs in the deep but not the intermediate region. Our results locate a region in the auditory processing hierarchy where an experience-dependent coding mechanism aligns auditory responses with the output of a learned vocal motor behavior.
... In the wild, zebra finches are flock birds and females often select mates from among familiar males (Zann 1996). One benefit of this approach, besides testing for mating preferences in a more biologically relevant context, is that we avoided making assumptions about which sexual signal (e.g., beak color or song) females use to make decisions (Riebel 2009b). Because males were familiar, song served as a cue to male identity and was not the only information available. ...
A female’s cognitive ability may influence her mate preferences through various mechanisms. These mechanisms include the direct effect of cognitive ability on the information-processing skills used during mate choice, and the indirect effect of cognitive ability on quality when females mate assortatively. Here, we examined whether the ability to learn a novel foraging task, a cognitive skill which has been associated with reproductive success in other capacities, was correlated with song preferences in female zebra finches (Taeniopygia guttata). Female preferences were measured in an operant testing chamber where hops on a perch triggered song playback. Females were given the choice of (1) conspecific vs. heterospecific song and (2) high-quality male vs. low-quality male conspecific song. We found that female performance on the novel foraging task was positively correlated with preference for conspecific song, but not with preference for high-quality male song. Instead, female mass was positively correlated with preference for high-quality male song, potentially signifying that female mass is a stronger predictor of female quality in assortative mating than female cognitive performance. Female mass and cognitive performance were unrelated. Our results suggest that the particular traits of a female that affect conspecific preference do not necessarily affect preference for high-quality males.
Animals from every taxon invest significant energy into reproduction. Research on reproductive decision making often focuses on how females choose mates and the features that attract them, but there is much more to reproductive decision making than simple mate choice. In this chapter, we highlight the diversity of reproductive decisions that males and females make, with an emphasis on the timing of mating, and means by which to mate. We discuss a central network of brain areas known as the social decision making network (SDMN) as an anchor for the modulation of reproductive decisions. We also promote the idea that the SDMN works intimately and reciprocally with other brain networks and neuroendocrine signaling pathways that are necessary for sensory/perceptive processing and motor output to enable reproductive decisions. Throughout, we (1) highlight examples that take place over different timescales and contexts, (2) take a comparative approach to emphasize common themes across animals, and (3) show the pervasiveness of neuroendocrine mechanisms that impact this profoundly important process. The decisions of when and with whom to mate are surely among the most important that any animal will make. Therefore, a deeper understanding of the mechanisms that influence and shape reproductive decisions is critical.
Vocal learning in songbirds is thought to have evolved through sexual selection, with female preference driving males to develop large and varied song repertoires1–3. However, many songbird species learn only a single song in their lifetime⁴. How sexual selection drives the evolution of single-song repertoires is not known. Here, by applying dimensionality-reduction techniques to the singing behaviour of zebra finches (Taeniopygia guttata), we show that syllable spread in low-dimensional feature space explains how single songs function as honest indicators of fitness. We find that this Gestalt measure of behaviour captures the spectrotemporal distinctiveness of song syllables in zebra finches; that females strongly prefer songs that occupy more latent space; and that matching path lengths in low-dimensional space is difficult for young males. Our findings clarify how simple vocal repertoires may have evolved in songbirds and indicate divergent strategies for how sexual selection can shape vocal learning.
Birdsong is a longstanding model system for studying evolution and biodiversity. Here, we collected and analyzed high quality song recordings from seven species in the family Estrildidae . We measured the acoustic features of syllables and then used dimensionality reduction and machine learning classifiers to identify features that accurately assigned syllables to species. Species differences were captured by the first 3 principal components, corresponding to basic frequency, power distribution, and spectrotemporal features. We then identified the measured features underlying classification accuracy. We found that fundamental frequency, mean frequency, spectral flatness, and syllable duration were the most informative features for species identification. Next, we tested whether specific acoustic features of species’ songs predicted phylogenetic distance. We found significant phylogenetic signal in syllable frequency features, but not in power distribution or spectrotemporal features. Results suggest that frequency features are more constrained by species’ genetics than are other features, and are the best signal features for identifying species from song recordings. The absence of phylogenetic signal in power distribution and spectrotemporal features suggests that these song features are labile, reflecting learning processes and individual recognition.
Current climate change is leading to increasingly unpredictable environmental conditions and is imposing new challenges to wildlife. For example, ambient conditions fluctuating during critical developmental periods could potentially impair the development of cognitive systems and may therefore have a long-term influence on an individual’s life. We studied the impact of temperature variability on zebra finch cognition, focusing on song learning and song quality (N = 76 males). We used a 2 × 2 factorial experiment with two temperature conditions (stable and variable). Half of the juveniles were cross-fostered at hatching to create a mismatch between pre- and posthatching conditions, the latter matching this species’ critical period for song learning. We found that temperature variability did not affect repertoire size, syllable consistency, or the proportion of syllables copied from a tutor. However, birds that experienced variable temperatures in their posthatching environment were more likely to sing during recordings. In addition, birds that experienced variable prenatal conditions had higher learning accuracy than birds in stable prenatal environments. These findings are the first documented evidence that variable ambient temperatures can influence song learning in zebra finches. Moreover, they indicate that temperature variability can act as a form of environmental enrichment with net positive effects on cognition.
Birdsong is a longstanding model system for studying evolution, and has recently emerged as a measure of biodiversity loss due to deforestation and climate change. Here, we collected and analyzed high quality song recordings from seven species in the family Estrildidae . We measured the acoustic features of syllables and then used dimensionality reduction and machine learning classifiers to identify features that accurately assigned syllables to species. Species differences were captured by the first 3 principal components, corresponding to basic spectral features, spectral shape, and spectrotemporal features. We then identified the measured features underlying classification accuracy. We found that fundamental frequency, mean frequency, spectral flatness, and syllable duration were the most informative features for species identification. Next, we tested whether specific acoustic features of species’ songs predicted phylogenetic distance. We found significant phylogenetic signal in syllable spectral features, but not in spectral shape or spectrotemporal features. Results indicate that spectral features are more constrained by species’ genetics than are other features, and are the best signal features for identifying species from song recordings. The absence of phylogenetic signal in spectral shape and spectrotemporal features suggests that these song features are labile, reflecting learning-processes and individual recognition.
Song learning is a prime example for a culturally transmitted mating signal. Local or individual song variants are socially learned early in life and adults sing and prefer these songs. An unresolved issue in this context is the question of how learned preferences for specific variants generalise to songs sufficiently similar to the original model. Here we asked whether female zebra finches would generalise early learned song preferences along a similarity gradient based on syllables sharing between test and tutor songs. For each female, this gradient consisted of their tutor's (father's) song (F), two variants of unfamiliar songs edited to share 2/3 (F2/3) and 1/3 (F1/3) of syllables with father's song and an unfamiliar song (UF). Females' preferences were measured in a 4-way operant choice arena where the birds could perch on different operant perches to trigger playbacks of the four different songs. Number and duration of perch visits were positively associated with the number of syllables that the assigned stimuli shared with fathers' songs. These results suggest that female zebra finches generalise early learned song preferences to songs sharing syllables (and/or voice characteristics) with songs learned early in life.
Individual-specific mate preferences are thought to be widespread, but they are still poorly understood in terms of mechanisms and function. Earlier work on a songbird (the zebra finch, Taeniopygia guttata) showed predominantly individual-specific mate preferences and signs of behavioural incompatibility with certain partners. However, the phenotypic target of preference or aversion remains unclear. A previous study suggested that female preferences may be related to variation in male song. Male zebra finches have individually distinct songs and together with individual-specific female song preferences they could function according to a ‘key–lock principle’. Here we report on a preregistered study in which we tested the hypothesis that individual females respond to males with highly similar songs in a similar way. We selected 18 duos of males with nearly identical songs and released them with females in communal breeding aviaries. We scored female preference as the female's responsiveness to male courtship and confirmed that females indeed had strong individual-specific mate preferences. However, female responsiveness scores were not positively correlated across males closely matched for their song, thereby rejecting the idea of a song-based ‘key–lock principle’ as an explanation for the observed individual-specific preferences. We suggest researchers should focus on details of the interactions between potential partners to elucidate the cause of behavioural incompatibility.
Global climate change is causing heatwaves to increase in number, length and intensity. These extreme temperatures can reduce fitness when mating behaviours are affected. An important mating behaviour for many organisms is sexual signalling. For example, songbirds, such as the zebra finch, Taeniopyggia guttata, use song to attract mates. Here, we test how an acute period of extreme heat affects song production in male zebra finches. We then ask whether female zebra finches discriminate between songs produced at different temperatures. We find that males significantly reduce song output at temperatures that induce heat dissipation behaviours. We also find that males produce song bouts with shorter syllables when thermally challenged. Furthermore, the relative acoustic and structural consistency of songs changes with temperature. Finally, we find that female zebra finches discriminate between songs produced at different temperatures, and the strength of discrimination is associated with changes in syllable duration. Altogether, we demonstrate that heatwave-like conditions can impact communication via alterations in signaller behaviour and the signal itself. We also discuss the potential compounding effects of reduced song production and other physiological declines on fitness in free-living zebra finches, which increasingly experience these high temperatures.
It is the female response to male signals that determines courtship success. In most songbirds, females control reproduction via the copulation solicitation display (CSD), an innate, stereotyped posture produced in direct response to male displays. Because CSD can be elicited in the absence of males by the presentation of recorded song, CSD production enables investigations into the effects of underlying signal features and behavioral state on female mating preferences. Using computer vision to quantify CSD trajectory in female brown-headed cowbirds (Molothrus ater), we show that both song quality and a female's internal state predict CSD production, as well as the onset latency and duration of the display. We also show that CSD can be produced in a graded fashion based on both signal strength and internal state. These results emphasize the importance of underlying receiver state in determining behavioral responses and suggest that female responsiveness acts in conjunction with male signal strength to determine the efficacy of male courtship.
Birdsong is an important signal used in intra- and intersexual communication in a reproductive context. Strong sexual and natural selective forces act on this behaviour, such that singing individuals can be viewed as vocal athletes whose performance is critical for reproductive success. In this review, I argue and illustrate how a solid understanding of song production mechanisms can enhance our investigations of performance. From a production perspective, temporal and spectral features of song are relatively well understood and therefore are discussed in detail. Performance ranges of temporal and frequency characteristics can be broad, but often involve different production mechanisms, with different constraints and trade-offs underlying their generation. Based on these multifaceted features, I argue that song may be perceived as an ‘acoustic gestalt’, which for each syllable represents a specific location in a complex multidimensional parameter space characterized by differential contributions of individual features. Derived from this view, I also propose that individual males may be showing specialization for exceptional performance of some, but not all, features of song. To illustrate this possibility for a future research focus, I quantify some song features of seven male European robins, and, although the data set is limited, it shows that different individuals exhibit different performance levels across a number of song features.
Variation in the acoustic structure of vocal signals is important to communicate social information. However, relatively little is known about the features that receivers extract to decipher relevant social information. Here, we took an expansive, bottom-up approach to delineate the feature space that could be important for processing social information in zebra finch song. Using operant techniques, we discovered that female zebra finches can consistently discriminate brief song phrases (“motifs”) from different social contexts. We then applied machine learning algorithms to classify motifs based on thousands of time-series features and to uncover acoustic features for motif discrimination. In addition to highlighting classic acoustic features, the resulting algorithm revealed novel features for song discrimination, for example, measures of time irreversibility (i.e., the degree to which the statistical properties of the actual and time-reversed signal differ). Moreover, the algorithm accurately predicted female performance on individual motif exemplars. These data underscore and expand the promise of broad time-series phenotyping to acoustic analyses and social decision-making.
Zebra finch (Taeniopygia guttata) is a songbird species in which males sing their unique songs to attract females who then select their preferred male. Acoustic features in the songs of individual males are important features for female auditory perception. While the male of this species is a classic model of vocal production, it has been little known about auditory processing in female. In the higher auditory brain regions, the caudomedial mesopallium (CMM) and nidopallium (NCM) contribute to female's sound recognition, we, therefore, extracted acoustic features that induce neural activities with high detection power on both regions in female finches. A multiple linear regression analysis revealed that neurons were sensitive to mean frequency and Wiener entropy. In addition, we performed an experiment with modified artificial songs and harmonic songs to directly investigate neural responsiveness for deriving further evidence for the contribution of these two acoustic features. Finally, we illustrated a specific ratio combining these two acoustic features that showed highest sensitivity to neural responsiveness, and we found that properties of sensitivity are different between CMM and NCM. Our results indicate that the mixture of the two acoustic features with the specific ratio is important in the higher auditory regions of female songbirds, and these two regions have differences in encoding for sensitivity to these acoustic features.
Learned aspects of song affect female mating preferences in a number of species of songbirds, including swamp sparrows, Melospiza georgiana. One explanation for why female songbirds attend to such song features is that these song attributes convey information on the general cognitive ability of singers. The fact that song attributes and cognitive ability are affected during development by the same stressors makes a connection between the two plausible. Here we test the hypothesis that song is a signal of cognitive ability by relating five measures of song quality to five measures of cognitive performance in 49 captive male swamp sparrows. The five song measures are repertoire size, mean and minimum vocal deviation (measures of vocal performance), and mean and maximum typicality (measures of song learning). Cognitive performance was measured as the speed with which five cognitive tasks were mastered: a novel foraging task, a colour association, a colour reversal, a spatial learning problem and a detour-reaching test. In general linear mixed models controlling for neophobia, none of the song measures were predictive of any of the cognitive performance measures. Thus the results do not support the hypothesis that song attributes signal general cognition in swamp sparrows.
Vocal communication is critical for reproduction and survival across a wide range of species. For vocal communication systems to function, receivers must perform a range of auditory tasks to decode and process acoustic signals. In songbirds, learned vocal signals (songs) can be used by receivers to gain information about the species, sex, identity, and even motivation of the singer. Moreover, young songbirds must hear and memorize songs during development to use them as templates for song learning. This chapter reviews research on the structure and function of the songbird auditory system. In particular, the relationships between the organization, connections, and information-coding properties of the auditory pallium are described and how the functions of those circuits allow birds to perform a range of auditory tasks is considered, including individual recognition, tutor song learning, auditory memory, and mate choice processes.
In many ways, the complement of cell subtypes determines the information processing that a local brain circuit can perform. For example, the balance of excitatory and inhibitory (E/I) signaling within a brain region contributes to response magnitude and specificity in ways that influence the effectiveness of information processing. An extreme example of response changes to sensory information occur across Critical Periods (CPs). In primary mammalian visual cortex, GAD65 and parvalbumin inhibitory cell types in particular control experience-dependent responses during a CP. Here, we test how the density of GAD65- and parvalbumin-expressing cells may inform on a CP for complex behavioral learning. Juvenile male zebra finch songbirds (females cannot sing) learn to sing through coordinated sensory, sensorimotor, and motor learning processes distributed throughout a well-defined neural network. There is a CP for sensory learning, the process by which a young male forms a memory of his “tutor’s” song, which is then used to guide the young bird’s emerging song structure. We quantified the effect of sex and experience with a tutor on the cell densities of GAD65- and parvalbumin-expressing cells across major nodes of the song network, using ages that span the CP for tutor song memorization. As a resource, we also include whole-brain mapping data for both genes. Results indicate that inhibitory cell populations differ across sex, age, and experiential conditions, but not always in the ways we predicted.
Zebra finches (Taeniopygia guttata) use their voices for communication. Song structures in the songs of individual males are important for sound recognition in females. The caudomedial mesopallium (CMM) and nidopallium (NCM) are known to be essential higher auditory regions for sound recognition. These two regions have also been discussed with respect to their fundamental functions and song selectivity. To clarify their functions and selectivity, we investigated latencies and spiking patterns, and also developed a novel correlation analysis to evaluate the relationship between neural activity and the characteristics of acoustic factors. We found that the latencies and spiking patterns in response to song stimuli differed between the CMM and NCM. In addition, our correlation analysis revealed that amplitude and frequency structures were important temporal acoustic factors for both regions. Although the CMM and NCM have different fundamental functions, they share similar encoding systems for acoustic factors.
Chemical signalling is widespread across animal taxa. Even birds, once thought to have little or no sense of smell, are now known to possess a fully functional olfactory system and may thus respond to conspecific and heterospecific chemical signals. In birds, body odour derives primarily from preen oil, a complex chemical mixture that is potentially rich in information: for example, preen oil chemical composition differs between the sexes and among species. Hypothesizing that songbirds attend to preen oil odour cues in the contexts of intra- and interspecific communication, we presented breeding-condition adult song sparrows, Melospiza melodia, with preen oil odour cues in two-choice tests. We compared time spent in a Y-maze arm scented with preen oil from same-sex conspecifics relative to the absence of such odour; from opposite-sex relative to same-sex conspecifics; and from female brown-headed cowbirds, Molothrus ater (frequent brood parasites of song sparrows), relative to the absence of such odour. The time spent with same-sex conspecific preen oil was not significantly different than time spent without odour. However, both males and females spent more time with opposite-sex than same-sex preen oil. We found a sex-by-stimulus interaction with respect to female cowbird odour: male song sparrows spent more time with cowbird preen oil than without odour, but female song sparrows showed the opposite pattern. Our findings show that even relatively nonsocial species can attend to the information contained in preen oil secretions.
Understanding the regulation of social behavioural expression requires insight into motivational and performance aspects. While a number of studies have independently assessed these aspects of social behaviours, few have examined how they relate to each other. By comparing behavioural variation in response to live or video presentations of conspecific females, we analysed how variation in the motivation to produce courtship song covaries with variation in performance aspects of courtship song in male zebra finches (Taeniopygia guttata). In agreement with previous reports, we observed that male zebra finches were less motivated to produce courtship songs to videos of females than to live presentations of females. However, we found that acoustic features that reflect song performance were not significantly different between songs produced in response to videos of females, and those produced in response to live females. For example, songs directed at video presentations of females were just as fast and stereotyped as songs directed at live females. These experimental manipulations and correlational analyses reveal a dissociation between motivational and performance aspects of birdsong and suggest a refinement of neural models of song production and control. In addition, they support the efficacy of videos to study both motivational and performance aspects of social behaviours.
Bill-color variability has the identical range and similar distributions in free-living Australian Zebra Finches (Taeniopygia guttata) and their wild-type domesticated descendants. Individual differences in bill color exist among adults of both sexes, both in nature and captivity. In laboratory birds, bill color changed over the course of the five-week breeding cycle, with lowest bill-color scores expressed at the end of the cycle. Longer-term patterns included a gradual decline of bill color over the course of multiple clutch attempts, followed by a rapid increase when resources for breeding were withdrawn. Among laboratory males, survivorship was clearly independent of bill color. Among females, bill color changed more rapidly in birds that subsequently died than in those that survived a two-year breeding experiment. High rates of reproduction were significantly associated with decline of male bill score, but not female bill score. The bill-color scores of laboratory males maintained on supplemented and basic seed diets for eight weeks did not diverge. Crowding of laboratory birds was associated with decreased bill color. For birds in nature, bill color tended to decline over the breeding season. Bill color of captive wild birds became more red over a six-week period when birds were fed ad libitum on the laboratory diet. Data for both laboratory and wild birds indicate that reproduction is associated with a decline of bill color in both sexes. Results of diet experiments were inconclusive, but helped to establish that the range of bill colors displayed by domesticated birds is similar to that encountered in nature. Our results, when considered in light of previous findings, suggest the possibility that bill color has different costs and benefits for the sexes and that genetic and/or physiological constraints prevent optimal phenotypic expression of bill color in Zebra Finches.
Vocal learning has evolved in several groups of animals, yet the reasons for its origins and maintenance are controversial, with none of the theories put forward appearing to apply over a broad range of species. The theory of gene-culture coevolution is applied to this problem taking the speci¢c case of the mainte-nance of song learning in birds. The interaction between genes underlying the ¢lter for recognizing and learning conspeci¢c song and the culturally transmitted songs themselves sets up an evolutionary force that may maintain vocal learning. We evaluate this hypothesis using a spatial simulation model. Our results suggest that selection that would maintain song learning exists over a wide range of conditions. Song learning may persist due to an evolutionary trap even though the average ¢tness in a population of learners may be lower than in a population of non-learners.
One way that sexual selection for genetic benefits could operate in
monogamous species is through female choice during extra-pair
copulations (EPCS). EPCS are common in monogamous species, and field
studies are consistent with the hypothesis of females choosing
genetically attractive males for EPCS. Here I show that female zebra
finches actively solicit and perform EPCS with males that are more
attractive than their mates. Attractive males have higher song rates,
have sons with higher song rates, and fledge heavier offspring. This
provides a mechanism for sexual selection in monogamous species, and is
consistent with `good genes' models of sexual selection.
Recent work suggests that coloured plastic leg bands may alter the sexual attractiveness and reproductive success of zebra finches (Poephila guttata). For example, males wearing red bands are more attractive to females and have enhanced reproductive success compared with males that have light green bands. Colour bands have been widely used in studies of avian behaviour and therefore could introduce bias if they regularly have a significant impact on social interactions among individuals. We carried out an experiment to assess the proximate effects of colour bands on zebra finch behaviour. Male zebra finches maintained in a large indoor aviary were given either red or light green bands and then scored for their ability to compete for a limited number of nest boxes and to attract females. The same males were randomly reassigned either red or light green bands and tested for their ability to regain boxes and attract new females. We found no correlation between band colour and a male's ability to gain either a nest or female. However, there was an association between male activity level and success. Also, those males that attracted a female in the first part of the experiment were more likely to do so in the second part of the experiment. We conclude that any immediate advantages conferred by attractive band colours may be masked under conditions of strong intermale competition for nests and mates.
Songs from 402 Zebra Finches (Taeniopygia guttata castanotis) were sampled in order to describe the structure of the song phrase and the relationship of its elements to the call repertoire. The song of wild birds was also compared to that of 47 domesticated Zebra Finches from two European laboratories in order to examine the effects of domestication on song structure. The stereotyped phrase, which is the repetitive unit of the song, had a mean number of 6.75 elements and a mean duration of 0.86 s in wild birds. Elements were sung in sequence that defined three parts to the phrase-a start, a middle and an end. Fourteen types of elements were identified of which four were sung by the vast majority of males; three of these "primary" elements were "borrowed" unmodified from the call repertoire, and formed the start and end sections of the phrase. "Secondary" elements, which were less frequently represented across males, constituted the middle of the phrase and appeared to be modified versions of the Distance-call Element, the loudest element in the phrase. I tentatively conclude that Zebra Finch song may have evolved from the calls associated with flight intention and take-off. Domestication has led to changes in element morphology, frequency of occurrence, and rate of singing (elements/s), but not in number of elements per phrase.
Sensory experience during sensitive periods in development may direct the organization of neural substrates, thereby permanently influencing subsequent adult behavior. We report a sensitive period during the imitative motor learning phase of sensorimotor integration in birdsong development. By temporarily and reversibly blocking efference to the vocal muscles, we disrupted vocal motor practice during selected stages of song development. Motor disruption during prolonged periods early in development, which allows recovery of vocal control prior to the onset of adult song, has no effect on adult song production. However, song disruption late in development, during the emergence of adult song, results in permanent motor defects in adult song production. These results reveal a decreased ability to compensate for interference with motor function when disturbances occur during the terminal stage of vocal motor development. Temporary disruption of syringeal motor control in adults does not produce permanent changes in song production. Permanent vocal aberrations in juveniles are evident exclusively in learned song elements rather than nonlearned calls, suggesting that the sensitive period is associated with motor learning. (C) 2000 John Wiley & Sons, Inc.
Studies of female mate preference in zebra finches (Taenopygia guttata) have shown that male beak colour and song rate are important. However, the two characters are correlated. Here the effect of beak colour and song rate on female choice are examined independently. In mate choice tests involving two males, beak colour was manipulated artificially using nail varnish. The results showed that females showed a significant preference for males with a high song rate, but not with a red beak. Females did not prefer males with a red beak if song rate was low and females preferred males with orange beaks who expressed a high song rate. Female preference for males with red beaks was not found when beak and song characters were no longer correlated.
Abstract Individual differences in sexual behavior have received much attention by evolutionary biologists, but relatively little is known about the proximate causes of this variation. We studied the quantitative genetics of male and female sexual behavior of captive zebra finches and found surprisingly strong maternal effects (differing between individual mothers) on the aggressiveness and song rate of sons and on the daughters' mating preferences for these male traits. We also found that daughters differed in their choosiness during mate-choice experiments depending on whether they originated from eggs produced early or late within the laying sequence of a clutch. Because this effect of laying order occurred independently of hatching order in cross-fostered broods, it must have been caused by consistent within-mother variation in maternal effects transmitted through the egg. Our findings raise the question whether these maternal effects might represent strategic programming of offspring behavior in response to the environment experienced by mothers or whether they are merely nonadaptive byproducts of developmental processes.
Zebra finch ( Taeniopygia guttata ) song syllables often include harmonically related frequency components. These harmonics may be suppressed, and this differential emphasis varies between the syllables in a song and between individual birds' songs. These patterns of harmonic suppression are timbre. Individual syllables' patterns of harmonic suppression are constant within adult males' songs. Young males that imitate the songs of older males also imitate their patterns of harmonic suppression. Syringeal denervation distorts these patterns, which suggests that they are produced through active control of the vocal organ. The selective suppression and emphasis of some harmonics creates a great number of possible timbre variants for any one syllable. These add signal diversity to the limited array of frequency modulations and range of fundamental frequencies found in zebra finch song. Analyses of bird song that disregard timbre may overlook a feature that is important in vocal communication. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
Zebra Finch (Taeniopygia guttata castanotis) songs from 33 colonies in two geographic zones of Australia (central and southeastern) were investigated in order to describe variation from macrogeographic to microgeographic levels. Canonical discrimination classified songs according to 31 measurements of the song phrase and clearly distinguished those from the two zones. Songs from regions within the southeastern zone fell into two groups on element sequence and frequency of element types. The two song groups came from habitats that differ in aridity and tree cover; both factors affect dispersal. Song variation within and among colonies in a region occurred in the frequency of "labile" elements. Movements of birds among colonies are extensive, but patterns are still far from clear. Despite resemblance in song structure between sons and their fathers, dispersal to and from colonies prevents the formation of colony-specific versions of the song.
Songs from 402 Zebra Finches (Taeniopygia guttata castanotis) were sampled in order to describe the structure of the song phrase and the relationship of its elements to the call repertoire. The song of wild birds was also compared to that of 47 domesticated Zebra Finches from two European laboratories in order to examine the effects of domestication on song structure. The stereotyped phrase, which is the repetitive unit of the song, had a mean number of 6.75 elements and a mean duration of 0.86 s in wild birds. Elements were sung in sequence that defined three parts to the phrase--a start, a middle and an end. Fourteen types of elements were identified of which four were sung by the vast majority of males; three of these "primary" elements were "borrowed" unmodified from the call repertoire, and formed the start and end sections of the phrase. "Secondary" elements, which were less frequently represented across males, constituted the middle of the phrase and appeared to be modified versions of the Distance-call Element, the loudest element in the phrase. I tentatively conclude that Zebra Finch song may have evolved from the calls associated with flight intention and take-off. Domestication has led to changes in element morphology, frequency of occurrence, and rate of singing (elements/s), but not in number of elements per phrase.
Two way choice tests show a preference of female zebra finches for male songs four standard deviations longer than normal song. Further tests show the ontogeny of this preference to parallel song learning in general as well as a preference for songs with entirely heterogeneous notes compared to songs with four note repeats. These findings are discussed in relation to a theory of the evolution of bird song from bird calls due to female preferences for longer, more complex vocalizations.
Geographic variation in the Zebra Finch Taeniopygia guttata was examined by comparing live wild-caught and captive T. g. guttata from the Lesser Sunda Islands in Indonesia and T. g. castanotis from the Australian mainland and confirmed by museum skin measurements of guttata and castanotis. (1) T. g. castanotis is significantly larger than T. g. guttata, as measured by wing length, weight and bill length. (2) castanotis have redder, darker, brighter bills than T. g. guttata. (3) T. g. castanotis males have larger breast- bands than T. g. guttata males, even when the size difference is taken into account, with strongly pronounced black bar- ring on the throat and upper breast which are absent from T. g. guttata males on Lombok, Sumbawa, Flores and Timor. (4) T. g. castanotis produce lower frequency distance calls and the males differ from T. g. guttata males in having a noise part to this call. (5) The songs of captive T. g. castanotis males are lower in frequency and their song phrases are shorter, with fewer elements per phrase, than captive T. g. guttata males from Timor. In contrast to the differences between T. g. castanotis and T. g. guttata, little geographic variation was found within T. g. guttata on the four islands studied, although there was a cline of decreasing size in bill depth from west (Lombok) to east (Timor). The status of the two forms, T. g. guttata and T. g. castanotis, is discussed.
The acoustic profile of the zebra finch song is characterized by a series of identical repeating units, each comprising a distinctive sequence of acoustic elements, called syllables. Here, we perform an analysis of song pattern deviations caused by variabilities in the production of song syllables. Zebra finches produce four different kinds of syllable variabilities-syllable deletions, single or double syllable insertions, syllable alterations, and syllable repetitions. All these variabilities, with the exception of repetitions, are present in songs of more than two-thirds of the normal adult birds; repetitions are present in less than one-fifth of birds. The frequency of occurrence of these variabilities is independent of the amount of singing, suggesting that they are unlikely to result simply from singing-induced physiological changes such as fatigue. Their frequencies in tutor-deprived birds are not significantly different from those in normal birds, indicating that they are unlikely to be acquired due to deficiencies in tutor-dependent learning. The types, patterns of occurrence and relative frequencies of these song syllable variabilities might reveal insights into the functioning of the song motor control pathway.
Taeniopygia guttata guttata is found on the Lesser Sunda Islands, Indonesia, and males differ from their Australian counterparts, T. g. castonotis, in having a thinner breast-band and grey chin and throat instead of the black and white throat bars. The songs of male guttata are longer and sung at a higher frequency than those of male castanotis with subspecies. Members of the two subspecies were observed to mate assortatively, ie guttata and castanotis did not form mixed pairs. Findings suggest that difference between the two subspecies in both song and breast-band size could play a role in mate choice and subspecies discrimination, thus leading to assortative mating between the two subspecies in captivity. Cross-fostered zebra finches resemble normally raised members of their own subspecies in size and plumage, and hybrids were intermediate. In multiple mate choice tests, females preferred normally raised birds of their own subspecies over those that had been cross-fostered and over those of the other subspecies. Since cross-fostered males do not appear to differ from normally raised birds of the same subspecies in plumage, size or song, results suggest that females may discriminate between guttata and castanotis males on the basis of behavioural cues. -from Author
This chapter discusses the song syntax in Bengalese finches. Bengalese finch song has a unique type of complexity. The syntactical rules underlying it by statistical methods are analyzed and found that the songs of these birds could be expressed as finite state syntax. In general, two to five song notes are arranged in fixed order to form “chunks” and several chunks are arranged with probabilistic rules into variable song phrases. Through song development, it is found that the phonological characteristics appeared first and syntactical characteristics were then established. The song development follows the hierarchical path from song phonology to song syntax. To understand the evolution of the song complexity, songs of the wild strain of the Bengalese finch, the white-backed munia are examined. Their songs are linear strings of notes in a highly stereotyped order, neither hierarchical nor complex like those of Bengalese finches. The brain mechanism by which this complex syntax was enabled is investigated in the chapter. It is suggested that song complexity in Bengalese finches may have been initiated as a sexually selected trait in the wild, and then enhanced in a domesticated environment that relaxed several selection pressures in the wild.
Undirected Song is commonly performed in wild and captive zebra finches and is typically given by males partly isolated from other members of the flock or colony. It has no territorial function nor it is used during precoital courtship; its frequency varies strongly among individuals. However, its rate of performance is severely limited by the close proximity of conspecifics, and this study investigated what social factors are responsible for this constraint in first-generation offspring of wild-caught zebra finches. The close presence of females caused a greater reduction in singing than did that of males. Familiarity between companions and the singer was also a factor that reduced the rate of singing. The more familiar the singer became with a female the more often he would sing in her presence, whereas the opposite occurred with males - singing was more prevalent with strangers than with familiar companions. Pair formation reduced a singer's sensitivity to inhibitory factors associated with the close proximity of conspecifics. Simple visual and auditory contact with a conspecific was not sufficient to constrain Undirected Singing, but intense, close range interactions appear to be necessary. It is hypothesised that Undirected Singing is used to attract females for pair formation or extra-pair mating, but the close proximity of male companions and/or the mate hampers this. However, in a competitive mate choice experiment there was no significant correlation between the rate at which a male gave Undirected Song and order of the pair formation. This suggests that Undirected Singing may not be crucial in the ultimate choice of a mate, but it may still be a useful cue at the outset of pair formation.
Laboratory experiments were designed to examine the influence of previous acoustic experience on later song preferences in female domesticated canaries (Serinus canaria). Young females were reared in acoustic isolation (five groups). In these five groups, one was reared without tutoring and four were exposed to taped tutoring songs (playbacks of three different songs, two conspecific and one heterospecific). One of the four tutored groups was exposed to all three songs, while each of the remaining groups was exposed to one of the three songs. When adult, all females were tested using copulation solicitation displays as an index of their song preferences. We demonstrated that females reared without tutoring were especially responsive to a particular domesticated canary song. This song contained a special song phrase type (Vallet & Kreutzer, 1995) that elicits high levels of sexual response. In general, a similar preference was also observed in the groups reared with tutoring. In addition, the females' preferences in tutored groups were also positively and strongly affected by conspecific songs, when these songs had been heard during the previous tutoring. In fact, females seemed to be able to selectively respond to a song containing a special song phrase, but were also able to learn conspecific songs.
SONNEMANN & SJÖLANDER (1977) found that zebra finch females raised by their own species (Zz females) differ in mate preference from females raised by Bengalese finches (Zb females) when given the choice between a Z male and a B male. Their data also showed an own species bias (Zz females strongly preferred Z males, whereas Zb females showed about equal interest in Z and B males). Several authors mentioned the existence of a preference for species-specific characteristics independent of early experience (a so called 'innate' preference) as a cause for an own species bias. This conclusion can be doubted for theoretical and methodological reasons and the question for the processes leading to an own species bias in zebra finch females seems completely open. We investigated several possible causes of the own species bias. Our experiments suggest that the final preference in Z females may be influenced by three independent processes. First, visual stimuli are involved. Information on these seems to stem exclusively, or at least largely from parental influence. No initial preference for visual characteristics, independent of experience with Z or B has to be assumed. Second, experiments indicate that a preference for actively courting males is present. The process underlying this is unknown but seems independent of the one giving rise to a preference for visual stimuli. Third, during the period between raising and testing (during which the females were visually isolated) the preference changes with age. Here too, the underlying process is unclear. Several possible causes for this change are discussed. The process underlying it is probably different from the other two. Altogether the results indicate that the own species bias may be the result of several independent developmental processes, which in combination led to a bias in testing.
Sexually mature zebrafinch males show a sexual preference for the species which has raised them. IMMELMANN (1972 a, b) stated that such a preference develops more readily if zebrafinch males were exposed to their own species than to Bengalese finches. The explanation for this phenomenon has been the supposition that an initial bias for the own species exists which is independent of post hatch experience. This hypothesis presupposes the absence of differences in behaviour between zebrafinch and Bengalese finch parents raising zebrafinch offspring. To investigate this supposition, the parental behaviour of zebrafinch and Bengalese finch (foster)parents raising zebrafinch offspring was observed. This was done in pure pairs (male and female of the same species) as well as in mixed pairs (male and female of different species). Differences between both species were found in parental care, and in clumping, allopreening, aggressive and sexual behaviour directed to zebrafinch young; most clearly in mixed, but often in pure pairs too. These differences were present from a few days after hatching till the moment of separating parents and young at about day 57. The kind of differences gradually changed during this period. Zebrafinch young are thus not exposed to equivalent experience with zebrafinch and Bengalese finch parents. The observed differences in experience may underly the more readily developing preference for zebrafinch than for Bengalese finch. This alternative should be explored more thorougly before the initial bias hypothesis is accepted.
The Zebra Finch (Poephila guttata) is a small Australian Ploceid which is ideal for the laboratory study of bird behaviour. Its attacking, fleeing, threatening and submissive behaviour are described and discussed. In this species there is no elaborate code of signals involved in this behaviour. Most disputes are settled mainly by actual fighting. This species builds a domed nest with a side entrance, the material for which is collected by the male. A special ceremony exists which apparently serves to strengthen the relationship between a pair in relation to a particular nest or nest-site. The pre-copulatory behaviour is described and analysed. The courtship of the male consists of an upright pivoting dance, during which it always sings and advances towards the female. The courtship of the latter takes the form of a horizontal body posture accompanied by a rapid quivering of the tail. The courtship of both sexes involves the three conflicting drives of attacking, fleeing and mating. In different species, the relative importance of these three drives will vary. In the Zebra Finch, the main conflict in pre-copulatory behaviour is between fleeing and mating. The female is more active than the male in incubating and rearing the young. The nestling possess brightly marked mouths which presumably facilitate feeding by the parents in the dark nest. Under certain circumstances, males were seen to perform the female courtship display and occasionally females responded with male behaviour, resulting in the occurrence of reversed mountings. The possible causation of this behaviour is discussed. It appears that the pseudofemale behaviour of the male is caused by strong sexual thwarting (as a result of the unresponsiveness of the female) in combination with the arousal of the drive to flee. Displacement activities which occur in this species are enumerated and described. They include various comfort movements, sleep, feeding, mounting, foodbegging and nest-building. Some of these occur as True, and other as Apparent, Alternative Displacement Activities. In the case of displacement beak-wiping it is possible to analyse accurately the differences between the displacement activity and its autochthonous form. There are differences in orientation, amplitude, velocity, and in the number of wipes per wiping-bout. This last difference is analysed quantitatively. Various other aspects of the reproductive behaviour are briefly mentioned, particularly the nature of territory and the strength of the pair-bond. The family Ploceidae show many degrees of socialisation and the defence of the territory by the Zebra Finch is often spasmodic, except when actually rearing young. The occurrence of attempted
Wild zebra finches, Taeniopygia guttata, sing frequently throughout the year but the function of undirected song, the most prevalent type, is unknown. Paired males commonly sang undirected song in feeding flocks where it occurred more frequently in the non-breeding season than in the breeding season. Song rate varied greatly among males. The context of the singer and the absence of any overt responses from flock members excludes direct aggressive and mate-attracting functions. Performance of undirected song may have energetic costs and predatory risks. The finding that singers are active individuals with ‘spare time’, that are neither hungry, nor tired, nor sexually motivated, suggests that singers are advertising their ‘quality’ as potential mates and/or participants for extra-pair copulations. When the female partner in non-breeding pairs was experimentally removed, the rate of undirected song of the ‘widower’ increased significantly. Males quickly re-paired. This experiment supports the hypothesis that singing in the flock has a mate-attracting role.
In zebra finches,Taeniopygia guttata, females prefer males that display at a high rate. In these experiments the effect of a female's experience on this preference was tested. Females were presented with a pair of males before and after being exposed to one of three treatments: (1) males with a low display rate, (2) males with a high display rate, or (3) no new males. Female preference for the male of the initial pair that displayed more was affected by the above treatments. Females increased their relative preference for this male if they had been exposed to males with a low display rate, decreased their preference if exposed to males with a high display rate, and did not change their preference if exposed to no new males. To test whether the changes in preference were sexual, the experiment was repeated with female pairs before and after the intervening treatments. There was no effect of the treatments on female preference for female pairs. The implications of these results for models of sexual selection and mate-choice strategies are discussed.
Zebra finch subspecies, Taeniopygia guttata guttata and T. g. castanotis, were cross-fostered to members of the other subspecies and their subsequent mating preferences measured. In multiple matechoice tests, an individual could show a preference for perching near a particular bird but physical contact was not possible: in one-way mate-choice tests, stimulus birds were prevented from seeing the individual being tested by one-way mirrors; in two-way mate-choice tests, wire-mesh screens allowed visual interaction between the test individual and the stimulus birds. In subsequent pair-formation tests, the same birds could form pairs freely in an aviary. When both sexes were cross-fostered, the birds preferred members of the foster subspecies in mate-choice tests and formed mixed pairs in the aviary. However, when only one sex was cross-fostered and the other was raised normally by members of their own subspecies all the cross-fostered males, and the majority of cross-fostered females, paired with members of their own subspecies in the aviary, irrespective of their preferences in one-way mate-choice tests. Birds spent more time with the individual they later mated with in the aviary in two-way than in one-way matechoice tests in all studies. In mate-choice tests, when both sexes were cross-fostered significantly more females than males chose their future mate. However, when only one sex was cross-fostered more normally raised than cross-fostered birds chose their future mate, irrespective of sex: this suggests that rearing experience has an important influence on which member of the pair ultimately chooses the mate.
The songs of captive Taeniopygia guttata guttata from Timor, T. g. castanotis from the Australian mainland and hybrid zebra finch males were analysed sonagraphically and the response of females was measured in playback experiments. Guttata and Castanotis young were either raised normally by members of their own subspecies or cross-fostered to members of the other subspecies. Hybrid young were raised by Guttata male-Castanotis female pairs. Guttata songs were significantly longer than Castanotis songs, with more elements per phrase, and were sung at a higher frequency, irrespective of whether males had been raised normally or cross-fostered. Hybrid songs were intermediate between Guttata and Castanotis songs. The results suggest that rearing experience has little, if any, effect on these macrostructural differences between the songs of the two subspecies. Females implanted with oestradiol preferred songs of males of their foster-father subspecies, irrespective of whether these males had been cross-fostered or raised normally, indicating that females use macrostructural song features for subspecies recognition and that their song preferences are learnt. It is suggested that these macrostructural differences in song function in subspecies recognition.
Mate choice and pair formation of captive zebra finches from the Australian mainland, Taeniopygia guttata castanotis, and from Timor, T. g guttata, were compared. In the multiple mate-choice test, an individual could show a preference for perching near a particular bird but could not form a pair bond (e.g. by clumping together). In the pair-formation test, individuals in a flock in an aviary were allowed to form pairs freely. The two subspecies preferred members of their own subspecies in mate-choice tests and mated assortatively in the aviary. When females were presented with Timor males, half of whom had been painted to resemble Mainland males, Timor females both preferred and paired with unpainted Timor males whereas Mainland females approached both unpainted and painted Timor males but paired with the latter. When Mainland males were introduced into the aviary only three out of 10 of these Mainland females re-paired with Mainland males, reflecting the stability of the pair bond. Males and females generally paired with the bird they preferred in the initial mate-choice tests, if that individual was not already paired. In mate-choice tests conducted after pair formation, mott birds preferred the individial they had already paired with. However, those that paired last and had not laid eggs preferred the bird they had chosen in the first mate-choice test rather than the individual they paired with in the aviary.
Wild zebra finches sing frequently during the breeding season, but the vast majority of song is of the undirected song type that is not directed at any individual, and the function of which is obscure — it appears to be ignored by all potential recipients. It is sung close to the nest-site, has a peak in production during the egg-laying period, and diminishes thereafter. The incidence of undirected song is positively correlated with extra-pair courtship, a finding consistent with the hypothesis that it is a means of advertising availability for extra-pair matings. Typically, undirected song occurred outside the nest when the female was inside, and a positive relationship was found between the amount of singing given by the male during the 5-min interval immediately after the female entered the nest and the time she subsequently spent inside the nest. Keeping the partner inside the nest during her fertile period is an advantage to the male: it serves as a form of paternity protection against other males and it allows him opportunities to pursue his own extra-pair matings. Occupancy of the nest during laying is also a means of guarding against intraspecific brood parasitism, which was high at this colony.
Zebra finch males may, depending on early experience with con-specifics and/or with Bengalese finches, develop a preference for either conspecific or Bengalese finch females. This preference is usually measured in choice tests, using directed song of the males as a criterion. So far, experiments are lacking on whether preferences measured in this way are indicative of social and aggressive behaviour and pair formation when zebra finch males are given the opportunity to show these behaviour patterns. Therefore, the preference of 19 males was first measured in choice tests. Thereafter the males were placed individually in a cage with one zebra finch and one Bengalese finch female and observations on social behaviour were made (free choice experiments). There appeared to be a clear relationship between the preference as measured in the choice tests and both the later orientation of social behaviour to the two females, as well as pair formation shown in the free choice experiment. Directed song during choice tests therefore is a useful predictor of other social behaviour and of pair formation.
To find out whether a mating preference could have initially evolved for adaptive reasons, one must determine whether the preferred trait could have provided useful information about mate quality at the time when the preference first arose.
One way to do so is to determine whether the preference evolved before or after the preferred trait. If the preference evolved first, then it cannot initially have served an adaptive function in mate choice, rather it must have arisen by random drift, or as a pleiotropic consequence of selection acting on other aspects of individual perceptual abilities.
A number of studies have shown that females exhibit a mating preference (e.g. for movement) in non‐sexual contexts also, which suggests that it may have evolved for reasons unconnected to mate choice. In addition, phylogenetic analyses have revealed that in several cases, females of a certain taxon exhibit a preference for a male trait that is absent in a sister taxon and in outgroup taxa, and that this preference is shared by females of the sister taxon tacking the male trait. The principle of parsimony suggests that such a preference has been inherited from a common ancestor, while the preferred trait arose only once in the lineage exhibiting the trait, i.e. that the preference predates the attractive trait.
While the above evidence indicates that females may possess ‘hidden’ preferences for male traits that are not exhibited by members of their own species, and that in at least some cases males have later evolved display traits that exploit preexisting preferences of this kind, there have been too few historical studies of preference evolution to allow one to assess the frequency of such exploitation. Moreover historical studies cannot provide strong support for the adaptive origin hypothesis, because coevolution of trait and preference (as opposed to exploitation of a pre‐existing bias) is compatible with Fisherian models of preference evolution as well as with honest advertisement and the handicap principle. One can conclude only that while some mating preferences did not originally evolve for adaptive reasons, others may or may not have done so.
To find out whether a mating preference is currently maintained by natural selection because the preferred trait provides useful information about mate quality, one must investigate the phenotypic and genotypic correlates of display, and the fitness consequences of mate choice.
A review of the published data reveals some support for the ideas of adaptive choice and honest advertisement. In a number of species, preferred display traits are correlated with putative measures of quality, and in a small proportion of these, there is evidence that reproductive success and/or offspring performance are higher for individuals mated to attractive partners. Very few studies report a failure to find any such correlates of display or any such benefits.
While the above result suggests that honest advertisement does sometimes occur in extant populations (which does not necessarily imply that preferred traits originally evolved as reliable indicators of mate quality), the possibility of publication bias means that one cannot assess how widespread it is. More data is needed to remedy this problem, particularly regarding the fitness consequences of mate choice for females. Experimental rather than observational methods are the best means to gather such data. Studies that look for correlates of display, for instance, should rely on experimentally induced rather than natural variation in ‘quality’.
The most common correlates of male display are age and dominance. The latter observation suggests that there may often be interactions between the processes of intersexual and intrasexual selection.
There is considerably more evidence to support the idea of female choice for direct than for indirect benefits. At the same time, however, it is apparent that mating decisions are commonly influenced by more than one measure of quality, so that these two kinds of choice need not be independent. To assess this possibility will require more studies of the relationship between male attractiveness and offspring performance.
Mate choice is frequently based on more than one display trait, and each trait is frequently influenced by more than one aspect of quality. ‘One quality, one trait’ views of honest advertisement are simplistic, and must be abandoned.
Honesty in sexual displays is sometimes maintained by cost (as in strategic handicap models) and sometimes, with approximately equal frequency, by physical necessity (as in revealing handicap models). In some cases, both mechanisms are involved in a single signalling system. To further distinguish between these possibilities will require experimental investigation of display cost, based on manipulation of display traits.
Young male and female zebra finches, Taeniopygia guttata, were tested for their ability to discriminate between the song of their father or tutor and that of another male in two types of preference test, one with a male whose song was dissimilar to that of the father or tutor and one with a male who sang a similar song, on removal from the father, at 4 months and at 6 months of age. Birds that were isolated from their father at 25 days (group A) did not show a preference for their father's song whereas those isolated from the father at 35 days (groups B and C) learnt to prefer their father's song. In addition, group C, which were housed with tutor 1 from 35 to 70 days and with tutor 2 from 4 to 6 months of age, preferred their tutors' songs to those of other males. If one compares the strength of preference in the two types of test, group B showed a weaker preference for the father in tests with the father and a similar male. Further, group C showed a weaker preference in the test with tutor 1 versus a similar male. The possible influence of tutor, sibling and own song on the discrimination of the father's song is discussed, and the results are compared with those for song performance learning. Finally, the mother birds preferred their mate's song.
This chapter discusses the physiology, ecology, and behavior of hormones in avian eggs. The main source of hormones found in avian eggs is the maturing follicles of the female ovary that contain specialized cells creating different hormones during their development. The granulosa cells of the largest preovulatory follicles (F1) are the main source of circulating progesterone. Theca cells produce both estrogen and androgens, and the production decreases with increasing follicular maturation. Postovulatory follicles continue to produce steroids before final atresia, and their low androgen production during incubation is brought about by a decrease in luteinizing hormone stimulation rather than by a reduction of the steroidogenic capacity of the theca interna cells at that stage. Although sexual differentiation takes place in the early embryo by the means of processes based on estradiol, the development of sexually selected characters in birds is tightly linked to hormonal processes in adulthood, of both androgenic and estrogenic nature. While within‐brood distributions of yolk androgens can be highly species‐specific, many differential patterns can be found within the same species. Given the effects of androgens in chick competitiveness, females could use within‐clutch distributions of androgens to balance or reinforce the effects of hatching asynchrony.
This chapter discusses on the recent findings in song learning in zebra finches and brings them together with earlier studies of song learning in this species, as well as recent physiological work on this species that is relevant to song development. Zebra finch song also affords excellent prospects for further advances in our understanding of principles of behavioral development; the review concludes by considering some of these remaining questions. The chapter summarizes briefly on what is known of the way of life of the zebra finch in the wild, where it occurs in Australia and the Lesser Sunda islands. It is an intensely sociable species, occurring in large flocks and breeding colonially in response to the rainfall, which is essential if there is to be sufficient food for feeding chicks. Zebra finch song seems largely to act as a signal between the sexes, although it is simple in structure and does not therefore fit easily into the scheme of song function. Rather than being concerned primarily with mate attraction or rival repulsion, its major role may be in stimulating ovarian development, including ovulation, a function song is known to possess in other species. This chapter describes what is known about the song-learning system in zebra finches and suggest ways in which the timing, accuracy, and selectivity of learning is affected by the environment that the young bird experiences during its development.
Zebra finches (Taeniopygia guttata) learn song primarily at 35-65 days of age, but birds deprived of experience at that stage may modify their songs later. Experiments on 5 groups examined the effect of varying early social experience on the plasticity of adult song. Major changes of song in adulthood were rare, and new syllables were memorized only in the more socially impoverished groups. Most songs underwent minor changes, in syllable structure or stereotypy, as well as in the addition or deletion of syllables. Two factors appeared to be important in determining the amount of change: the extent of social deprivation that the bird had experienced and, in the case of group-reared birds, the degree of song matching between social companions.
Although bird song is thought to be important in mate attraction, little is known about how females perceive differences in song and which specific elements of song females prefer. Most studies, to date, have examined female choice during preference tests for song stimuli, and most have treated females with oestrogen prior to testing. At present, it is unclear whether song preferences during such tests reflect actual mate preferences. This study tested the hypothesis that experimentally altering male courtship vocalizations (song) would affect female mate choice and the formation of long-term socially monogamous relationships. Male zebra finches, Taeniopygia guttata, were vocally distorted using two minor and reversible techniques. Females in a two-choice paradigm preferred control males over vocally distorted or muted males. In a pair bond formation experiment, all control males had paired 5 days into the study, whereas only one vocally distorted male had paired. By the end of 2 weeks, however, four nerve-transected males and one air-sac-punctured male had paired. These results suggest that females do use song quality as a basis for choosing males. However, other male qualities may eventually override vocal quality as the basis for female choice.
Songbirds are able to receive communications in networks because both senders and receivers are equipped with impressive auditory perceptual abilities. Here, we examined the effects of isolation from adult males and other conspecifics in the communication network on the development of auditory perception in zebra finches. We tested male and female zebra finches in laboratory auditory operant discriminations known to test zebra finches' abilities to perceive absolute pitch (frequency range discrimination) and relative pitch (frequency ratio discrimination), and to identify individual song notes (song note discrimination). Compared to normally reared zebra finches, birds reared apart from adult males but with siblings and the female parent (tutor-only isolates) had deficits in the frequency range discrimination. Birds reared apart from adult males and apart from all conspecifics after 35 days of age (tutor-brood isolates) had deficits in all three auditory discriminations. Analyses of song production revealed that tutor-only isolate males directed their aberrant songs at female conspecifics, whereas tutor-brood isolate males did not. These results support the hypothesis that male and female zebra finches require specific experience with conspecifics in a communication network to develop normal auditory perceptual abilities.
In a laboratory study the effect of brood size manipulations on the sexual attractiveness of offspring was investigated. Zebra finches,Taeniopygia guttata, were reared in small or large broods. Young were exchanged so that natural siblings from different rearing conditions could be compared. Birds of both sexes reared in small broods were larger and heavier as adults; furthermore, they developed the adult bill colour sooner than birds reared in large broods. Males reared in small broods had a redder beak as adults. Males but not females reared in small broods were more attractive to opposite sex individuals, as measured in choice tests. Males with redder beaks were more attractive to females. No relation was found in females between attractiveness and measured traits. Sexual attractiveness may thus be a potentially important mechanism by which brood size affects fitness.
Laboratory experiments were conducted to assess the extent to which female zebra finches (Taeniopygia guttata) respond preferentially to the song of their own mate versus the song of a neighbouring conspecific male. Following a 2 to 3 day period of separation from their mates, 20 females were tested individually in 30-min simultaneous auditory choice tests. Of the birds that showed clear preferences as assessed via approach duration scores, 14 strongly preferred the song of their mate, and two preferred the song of a neighbour. Thus, one possible function of male zebra finch song, which is highly variable inter-individually, is to provide his mate with an acoustic basis of individual recognition that may serve to strengthen and/or maintain the pair band.
Previous research has shown that acoustic experiences in early life influence song preferences in female domesticated canaries, Serinus canaria. We do not know, however, if they can modify song preferences in adulthood. In the experiments reported here, one group of young female domesticated canaries was reared in acoustic isolation in early life without song tutoring, while two groups were tutored with a playback song (one with wild canary song and one with domesticated canary song). We tested these three groups of females once they had reached adulthood, prior to breeding, using copulation-solicitation displays as an index of their song preferences. The females were then placed in an aviary with males during the breeding period, after which they were retested. We observed that the song preferences of females reared in acoustic isolation and those tutored with wild canary song had changed. These females were able to develop new song preferences in adult life. These results are discussed in relation to current views on song preferences and sexual imprinting.
Songbirds are known for their vocal versatility and the great developmental plasticity that permits or even makes it normal that adult signals are shaped by social learning processes. The chapter describes the vocal perception learning and vocal production learning in female songbirds. Song functions as an important mate attraction signal. Hence, it is often sexually dimorphic, with males typically the vocally displaying and advertising sex. The vocal perception learning in female song birds depends on recognition, song preferences, and perpetual fine tuning. Bird vocalizations are traditionally divided into calls and songs. The categorization is based both on physical characteristics of the signal (calls are shorter and less complex than songs) and also on its function. The chapter describes song learning and call learning in female song birds. Female song seems rare in comparison, and these behavioral dimorphisms also seem to map onto neuroanatomical differences in the specialized brain nuclei involved in singing. Consequently, there has been an emphasis on studying song acquisition in male songbirds. However, with female song described in a growing number of species, a new interest in the form and function of female song has surged. Likewise, theory has spawned interest in causes of variation on the receiver's side but also increasingly in the extent and function of female ornaments. With a culturally transmitted mating signal, learned preferences arise as an additional dimension next to genetically inherited and condition-dependent variation in female preferences and signaling.