Review
CSIRO PUBLISHING
Emu, 2010, 110, 209–218
www.publish.csiro.au/journals/emu
The functional role and female perception of male song
in Zebra Finches
Mark E. Hauber A,C, Dana L. M. Campbell A and Sarah M. N. Woolley B
A
Department of Psychology, Hunter College, City University of New York, NY 10065, USA.
Department of Psychology, Columbia University, NY 10027, USA.
C
Corresponding author. Email: [email protected]
B
Abstract. The song of male Zebra Finches has been the focus of decades of behavioural, developmental, neurobiological
and, increasingly, genomic research. Zann was the first to summarise the immense and integrative research effort in a
landmark synthesis of field and laboratory studies of Zebra Finches, which paralleled his own championing work on the
sociality and vocal behaviour of estrildid finches in the wild and in captivity. The study of the production and perception of
Zebra Finch song has driven theoretical, empirical and technological advances in behavioural ecology, endocrinology and
neuroethology, and led to a greater understanding of the evolution of animal communication systems in general. A survey
of the literature shows that there are still significant gaps in our understanding of the mechanisms underlying the
responses of non-singing females to male sexual displays, including song. We focus on recent insights into the features
and functions of male song that shape female choice, regarding both behavioural and neurobiological measures of selectivity.
This review underscores the need for continued research into the biological mechanisms underlying the perception of male
song by female Zebra Finches and confirms this system as a valuable and productive model for research on animal
communication.
Additional keywords: Bengalese Finch, female choice, genome, Lonchura striata vars. domestica, neuroethology,
sexual selection, Taeniopygia guttata.
Structure and development of Zebra Finch song
The song of the Zebra Finch (Taeniopygia guttata), produced
solely by males, is a short (1–2 s) vocalisation comprised of
harmonic stacks and broadband notes, called syllables, that are
produced in stereotyped sequences called motifs. Song motifs are
repeated in bouts (Sossinka and Bohner 1980). The number,
acoustic features and diversity of syllables that are produced are
stereotyped within individuals but vary between individuals
(Immelmann 1969). Individual differences allow the songs of
male Zebra Finches to be easily distinguished by the human
listener and also enable true individual recognition of mates
(Miller 1979a) and fathers (Miller 1979b; Slater et al. 1988)
by females (see below).
Although the female Zebra Finch typically does not sing,
masculinisation via oestradiol administration during ontogeny
can induce song production, indicating an important role for
gonadal hormones in the organisation of sexual dimorphism of
vocal displays (Adkins-Regan et al. 1994). Genetic determination
of sex (Agate et al. 2003), coupled with neuroendocrine effects
up to the first week after hatching, are most influential for this
development of the species-typical sexual differentiation in
singing and the neuroanatomical basis of male-only song
(Adkins-Regan et al. 1994). However, the administration of
testosterone to adult females can still induce and increase the
frequency of female singing (Adkins-Regan 1999). In parallel,
ontogenetic oestradiol treatment causes female Zebra Finches to
sing in adulthood, and shows that these songs are learned during
Ó Royal Australasian Ornithologists Union 2010
development, in parallel to the development of males’ imitative
learning of song displays (Simpson and Vicario 1991).
The male Zebra Finch copies his song from an adult tutor
during well-defined developmental stages (Slater et al. 1988;
Zann 1996). Song ontogeny comprises memorising a song
template, followed by motor production of subsong and plastic
song, until the song becomes crystallised at ~100 days of age.
Following the crystallisation, typically only minor adjustments
are made in the acoustic characteristics of the song. Such
plasticity can include some transient deviations in song pattern,
including syllable deletions or alterations, that are likely to reflect
changes in the neural motor control pathway in the forebrain
(Helekar et al. 2000), or amplitude modulation in response to
the distance of the intended recipient of the vocal display
(Brumm and Slater 2006). But the likelihood and functional
relevance of these anatomically and socially induced aspects of
acoustic plasticity remain untested in the wild. In parallel with
males, female Zebra Finches learn to remember the song of
their fathers and familiar brothers during development in
captivity (Riebel et al. 2002; Riebel 2003), and also learn to
recognise the songs of their mates during adulthood
(Miller 1979a) but, again, the function of familiarity-based
discrimination of songs by females in nature remains unclear.
Zebra Finches of both sexes are able to learn about
conspecific song from playbacks of vocalisations (Bolhuis et al.
1999), although males will more thoroughly and accurately
imitate songs of tutors with whom they can vocally and visually
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interact (Eales 1989). Evidence from blindfolded juvenile males
has further shown that physical interaction itself, even in the
absence of vision, enhances the learning of song (Adret 2004).
This is in contrast to the social inhibition of song imitation
by several brothers in the same cage (Tchernichovski and
Nottebohm 1998) and presents a strong case for further
investigations into the role that the sex and numbers of siblings
might play during development in both male imitation of, and
female preference for, tutor songs.
In the absence of a live song tutor, a male Zebra Finch will
develop a rudimentary version of the adult species-typical song
that is characterised by abnormally high frequencies and long
syllables, often repeated in bouts that lack the normal stereotypy
in syllable order of adults (Williams et al. 1993). This type of song
is referred to as isolate song. Previously untutored adult Zebra
Finches have also been shown to copy new syllables from tutors
or exemplars to which they are exposed at an age that is beyond
the typical sensitive period of song learning in this species
(Eales 1985; Morrison and Nottebohm 1993). Imitation and
improvisation occur in each generation of males to produce
normal (social) adult song. A recent experiment tracked the
change in features of male song across multiple generations,
but started with males that sang isolate songs as tutors (Fehér
et al. 2009). The results were unexpected in that normal,
species-typical song structure re-established themselves within
approximately four generations in a closed microcosm where
males of the previous generation served as song tutors for the
next generation of males.
Such novel experimental paradigms and surprising findings
also have critical implications and require new theory to explain
the evolutionary benefit and cost of investment into the neural
substrates of imprinting, copying and learning to generate
song cultures. For example, pinpointing the relative roles of
species identity versus tutoring experience in shaping
generational cultural shifts could involve documenting the
process of cultural evolution of song, and the impacts on
female perception, across generations, starting with male
Zebra Finch tutors singing heterospecific songs (e.g. through
cross-fostering with Bengalese Munias (or Bengalese Finches,
Lonchura striata vars. domestica) as parents; Clayton 1989;
Campbell and Hauber 2009a). Using cross-fostered males as
initial tutors would be especially valuable because male Zebra
Finches are imperfect mimics of Bengalese Munia songs:
whereas they copy syllable structure closely, they retain some
syntax and rhythm of Zebra Finch songs (e.g. Woolley et al.
2010). In turn, the neurophysiological basis of preferences in
female Zebra Finches between normal songs and Bengalese
Munia-like songs of conspecific males is still unresolved
(Campbell and Hauber 2010b). Such new manipulations
would thus both inform and challenge traditional hypotheses
for the roles and consequences of early experience and learning
in shaping species specificity in female choice for conspecific
songs (see below).
Song and female mate-choice
Male song is one of the important cues for mate-choice in female
Zebra Finches. Field and laboratory observations indicate that
males readily approach single females, whereas females are
M. E. Hauber et al.
more discriminating in their spatial approaches (Zann 1996;
Campbell and Hauber 2009b). This is in concordance with
general predictions of intersexual differences in the thresholds
of mate-discrimination, as females bear a greater reproductive
cost of erroneous mate-choice than do males, even in biparental
species (Hauber and Lacey 2005). Choosing a suitable social
partner and, eventually, a mate is essential in Zebra Finches in
general, and for females in particular, because the pair-bond is
lasting; separation apparently occurs only with the death of
one partner (Zann 1996), and new research has confirmed
that extra-pair fertilisations are rare in natural populations
(Birkhead 2010; Griffith et al. 2010). Additionally, in the wild,
the probability of offspring survival to sexual maturity is
estimated to be as low as one in four (Zann 1996) and so a
female’s choice of a mate, who is to provide parental care and
genetic contributions to her offspring, has a critical impact on her
own reproductive success, through both the physical condition
and the genetic quality of the male.
Zebra Finches are not territorial and males sing to females at
close range, within loose breeding colonies and large flocks (Zann
1996). Song is thus typically accompanied by other sensory and
social cues, including colour of plumage and bill, body size and
courtship dance. Several male morphological traits serve as visual
cues for female Zebra Finches, signalling information that is
relevant to mate-choice. Immelmann (1959), working on captive
birds, initially identified bill-colour, eye-stripes, and tail-bands in
male Zebra Finches as visual conspecific recognition signals
for females. Since then, studies that tapped into the natural
variation of vocal and visual sexual cues, and the experimental
alteration of these traits, repeatedly demonstrated that hearing
male vocalisations and perceiving other sensory cues, including
colour of plumage and bill, interact to influence female attraction
to potential mates (Campbell and Hauber 2009c, 2010b). The
relative salience and role of these cues in female choice within
natural populations, however, remain unclear, as does their
developmental trajectory, with Richard Zann’s own last study
on wild-caught birds demonstrating opposing effects of
nutritional constraint during development in reducing the
complexity of song displays, but not the accuracy of song
copying, of male Zebra Finches (Zann and Cash 2008).
Although multimodal sensory cues are clearly involved
in female mate-choice, including the synergistic effects of
vision and hearing (Campbell and Hauber 2010a), many
laboratory studies have shown that song alone can direct
the choice behaviour of a female and predict which males are
attractive (Miller 1979a, 1979b; Clayton 1990; Riebel et al. 2002;
Tomaszycki and Adkins-Regan 2005; Holveck and Riebel
2007; Vignal et al. 2008; Campbell and Hauber 2009a; Vyas
et al. 2009). Next, we discuss the role of male song in female mateselection and how song preferences of females are related to
pairing, mating and reproductive behaviours.
Female behaviours that predict mate-preference
To understand the role of male song in mate-choice by females, it
is critical to describe and quantify female displays of social
discrimination, sexual preferences, male attraction and mating
decisions. Mate-choice-related behaviours in female Zebra
Finches can be broadly grouped into three major classes. First,
Male song and female preference in the Zebra Finch
females may display preference for particular songs or categories
of songs (e.g. conspecific songs over heterospecific songs,
familiar songs of the father over unfamiliar conspecific songs).
This has been shown experimentally through spatial proximity to
the source of song (Miller 1979b) or by active elicitation of song
playback by females (Braaten and Reynolds 1999; Riebel 2009),
or both. In these experimental paradigms, female Zebra Finches
may approach or stay close to speakers that are playing particular
songs more so than speakers playing other songs (Miller 1979b;
Campbell et al. 2009a; Campbell and Hauber 2010b). Females
may also hop on perches or peck keys that elicit the playback
of particular songs more than they hop on perches or peck
keys that elicit playback of other songs (Braaten and Reynolds
1999; Riebel 2000). These behaviours are typically interpreted
in experimental reports as indicating attraction, although
spatial proximity or key-pecking may or may not indicate
sexual attraction and mate-choice (ten Cate and Mug 1984; see
below). For example, spatial approach and elicitation of playback
preferences can occur towards the songs of males that are
unsuitable mates (e.g. fathers; Miller 1979b; Riebel 2000).
Furthermore, both adult males and pre-reproductive juveniles
show these types of song preferences (Braaten and Reynolds
1999). Therefore, female mate-choice may not be the only
context that attracts Zebra Finches to particular songs.
Nevertheless, in many cases, spatial proximity to and
elicitation of playback of specific songs are clearly related to
female sexual attraction. For example, female Zebra Finches
show spatial proximity preferences for conspecific songs
over heterospecific songs (Clayton and Prove 1989; Braaten
and Reynolds 1999; Lauay et al. 2004; Campbell et al. 2009a)
and for the songs of their own mates (Miller 1979b; Clayton
1988; Woolley and Doupe 2008). The avoidance of the costs of
hybridisation (Hauber et al. 2001) and delays in re-establishing
the pair-bond (Adkins-Regan and Tomaszycki 2007) is adaptive
in systems with social monogamy, such as that of the
Zebra Finch. Experimental work with playback of song or
mate-choice has also shown that spatial proximity preferences
of females towards particular classes of stimuli are consistent
across trials and over time (Forstmeier and Birkhead 2004;
Campbell et al. 2009a), and predict the rate of copulation
solicitation displays (Witte 2006; Holveck and Riebel 2007)
and pair-formation (Clayton 1990; Tomaszycki and AdkinsRegan 2005; Campbell and Hauber 2010a). Therefore, spatial
proximity and song-elicitation behaviours appear to indicate
reliably sexual attraction in domesticated stocks of female
Zebra Finches, although not consistently so in wild-caught
stocks (Rutstein et al. 2007).
A second and more clearly identifiable class of female
attraction behaviours to specific male songs is the production
of social and sexual displays by females. These include ritualised
hops on perches, tail-quivering (i.e. copulation solicitation
displays; Morris 1954), body shakes, bill-wipes and the
production of calls (Zann 1996). With the exception of calls,
these behaviours typically do not occur in the absence of hearing
male song (Zann 1996; Rutstein et al. 2007), and can be elicited by
song alone (Clayton and Prove 1989; Campbell and Hauber
2009a; Vyas et al. 2009). Although there is increasing use
of multiple attraction behaviours in assessing preferences
(Campbell and Hauber 2009a, 2010b), the interpretation of
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behavioural responses by females could benefit from more
detailed and multivariate analyses. Measuring additional
features such as displacement behaviours (e.g. preening or
feeding) could enhance understanding of, potentially, not just
the absence of a preference, but an aversion to the male stimuli
presented.
A third, and most committed, class of mate-choice
behaviours for female Zebra Finches is pair-bonding and
breeding. Stages of pair-bonding can be measured by observing
clumping (sitting close together), allopreening, and nestbuilding. Successful breeding progresses from a female laying
eggs, followed by both sexes incubating the eggs and
ultimately, provisioning the hatchlings. Although studies
measuring breeding-related behaviours require the use of live
males, the role of male song per se in eliciting and maintaining
female pair-bonding and mating behaviour can be studied using
experimental manipulations. Examples of such manipulations
with live stimuli include surgically muting the male to prevent
him from singing (Tomaszycki and Adkins-Regan 2006), raising
juveniles in isolation from adult males to cause males to
produce less-attractive, isolate songs (Lauay et al. 2004), and
cross-fostering juveniles to broods of other species of finches to
produce heterospecific-like songs (Woolley et al. 2010). Female
nest-building, breeding-like hormonal states, and egg laying
can be induced by playback of song alone, although combining
playbacks with exposure to finch-like models of males or video
playback of behaving males enhances female responsiveness
(Tchernichovski et al. 1998; Campbell and Hauber 2010a).
The Zebra Finch has served as a prominent model system
for the behavioural and developmental basis of mate-choice
in vertebrates (Zann 1996), and several recent studies have
examined in more detail the relationships between the
characteristics of male songs and the adaptive consequences of
female-choice (Forstmeier and Birkhead 2004; Holveck and
Riebel 2007, 2010). One clear conclusion is that mate-choice
is performed by both sexes, and involves more than just the
discrimination of male song by females. This is likely because
male choice for fecund and responsive females, and the resulting
mutual mate-choice, benefits both sexes during their long-term
social and genetic partnership (Wynn and Price 1993; Griffith
et al. 2010; Holveck and Riebel 2010). We next discuss the
aspects of song that appear to be attractive to females, some of the
evolutionary explanations for why these features may be
attractive, and several potential proximate mechanisms of how
these features have an impact on the ontogeny and mechanisms
of neural processes underlying female mate-choice.
Aspects of song that attract females
Familiarity
Female Zebra Finches prefer to hear familiar songs; they show
preferential spatial proximity and peck at keys more often to hear
songs that they have heard before. The two clearest examples of
this effect are preferences for the songs of fathers and mates.
Father-song preferences have been found using several methods
of assessing female discrimination, including spatial proximity
and playback elicitation (Miller 1979b; Clayton 1988, 1990;
Riebel 2000; Riebel et al. 2002). Miller (1979b) found that
exposure to fathers up until only 35 days of age was sufficient
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to acquire a memory of, and preference for, father song up to
several months into adulthood, suggesting that early exposure is
sufficient for long-term storage of acoustic memories. Social
interactions between fathers and daughters are likely to be
involved in the development of these preferences, but are not
required; females that are exposed to male songs, but not live
fathers, during development also show preferences for those same
songs as adults (Riebel 2000). Therefore, familiarity with a song
that was experienced during a critical stage of development, rather
than the association of a song with the father, may cue a female’s
recognition of her father’s song (Riebel 2003). The relevance of
this effect for the dynamics of families and mating has yet to be
tested in the wild, given that Zebra Finches disperse from their
natal colonies after independence (Zann 1996).
The preferences of a female for hearing her mate’s songs have
also been demonstrated using spatial proximity measures
(Immelmann 1959; Miller 1979b; Clayton 1988; Woolley and
Doupe 2008). Miller (1979a) showed that nearly all mated
females preferred to perch near a speaker playing the songs of
their mates, and some even preferred the songs of their prior
mates after separation and forced re-pairing with a different
mate, again suggesting learned long-term memory for a
specific class of songs. The behavioural preferences of females
for the song of their fathers and their mates imply attraction to
familiar songs in social contexts that can be either sexual or nonsexual. Further understanding of the relative role of familiarity
in female song-preference could examine the interplay between
experience and male quality (as discussed below). For example,
would females raised with exposure to low-quality song, upon
reaching maturity, select low-quality songs that share acoustic
features with the father’s songs over high-quality but unfamiliar
songs?
Kin identity
As described above, male Zebra Finches learn to mimic the songs
of their tutors, typically those of their fathers (Forstmeier et al.
2009), and female Zebra Finches show behavioural preferences
that are consistent with long-term memory of the familiar songs
of their fathers and male siblings (Miller 1979a; Riebel and
Smallegange 2003). Therefore, song also has the potential to
be used for kin-recognition (Burley et al. 1990; Zann 1997). Such
familiar-vocalisation based kin-recognition was demonstrated in
cooperatively breeding birds (Sharp et al. 2005), and could also be
reliable for kin-recognition in a colonial, highly social system,
such as that of Zebra Finches, if young male siblings were to learn
songs exclusively from their genetic and social fathers in the
wild as predictably as they do in captivity (Slater and Mann 1990;
Zann 1996).
In contrast, the potential for familiarity-independent kinrecognition using song is weakened by recent investigations
into the genetic basis of Zebra Finch vocalisations.
Specifically, studies on the heritability of some song features,
including length and repertoire size, showed heritability to be low
when using an experiment-wide partial cross-fostering paradigm
that disassociated genetic influences from parental effects into
eggs and during early development (Forstmeier et al. 2009).
The results imply that unfamiliar songs are less likely to carry
predictably kin-relevant information. However, other song
M. E. Hauber et al.
features may be influenced by more heritable aspects of
morphology that are also known to influence acoustic
features of vocal displays, including body size and billshape, through their impacts on frequency, tonality (timbre)
and rate of production of syllables of male songs (Forstmeier
et al. 2009).
Overall, it appears that irrespective of the relative salience
of non-heritable versus heritable components of song features,
female preference for kin vocalisations is extensively based on
familiarity with the individual singing that song. Accordingly,
adult females did not show consistent preferences in an operant
task for the songs of their unfamiliar brothers despite the
acoustical similarity of these songs to the familiar songs of
their fathers (Riebel and Smallegange 2003; but see Miller
1979a). It is unlikely that the lack of such an effect was a
result of small samples sizes in this recent study, because the
same sample of female subjects was observed to display
consistent preferences for familiar songs of relatives over
unfamiliar songs of unrelated individuals in the same operant
choice paradigm (Riebel et al. 2002). Further research is needed
to confirm the degree to which specific characteristics of male
songs can be and are used for recognising genetic relatedness
in Zebra Finches in the wild, perhaps in the context to avoid
costly inbreeding (Fetherston and Burley 1990) with unfamiliar
relatives following natal dispersal (Zann 1996).
Species identity
To understand the role of song features other than familiarity
in female preferences, it is necessary to decouple familiarity
from other aspects of songs. Song-playback experiments
using only unfamiliar (never before heard) stimuli have shown
that female Zebra Finches are more attracted to conspecific
songs than to heterospecific songs (ten Cate and Mug 1984;
Clayton and Prove 1989; Clayton 1990; Braaten and Reynolds
1999; Riebel 2000; Brazas and Shimizu 2002; Lauay et al. 2004;
Campbell and Hauber 2009a, 2010a). Clayton (1990) also
demonstrated that females show preferences for the unfamiliar
songs of their own subspecies (T. g. castanotis from mainland
Australia v. T. g. guttata from the Lesser Sunda Islands). The
physiological bases of conspecific song-preferences in female
Zebra Finches are still unknown. Studies that investigate species
differences in peripheral and central song processing and
perception in female Zebra Finches are needed to understand
the proximate mechanisms of behaviours that imply memory
and recognition of vocal signals of species-identity (Hauber
et al. 2007a, 2007b).
Several isolation-rearing and cross-fostering studies have
addressed how developmental experience influences
behavioural aspects of female conspecific song preferences. In
isolation-rearing studies, females are raised without exposure to
adult males (Hauber et al. 2007a). In cross-fostering studies,
females are raised by adults of another species (usually Bengalese
Munias; Campbell and Hauber 2009a; Woolley et al. 2010) or
subspecies (Clayton 1987). The intent of both types of
manipulations is to determine whether female song preferences
are learned and, if so, to describe the effects of early auditory and
social experience on song preferences and, presumably, matechoice.
Male song and female preference in the Zebra Finch
Females show behavioural discrimination between
conspecific songs and songs of other species of bird that are
phylogenetically and geographically distant from Zebra Finches;
for example, females raised in isolation from singing males
preferentially listen to playbacks of Zebra Finch songs over
songs of Common Starlings (Sturnus vulgaris) and Common
Canaries (Serinus canaria) (Braaten and Reynolds 1999; Lauay
et al. 2004). This preference for conspecific song is shown by
both sexes of juvenile and adult Zebra Finches (Braaten and
Reynolds 1999; Campbell and Hauber 2010b), suggesting that
the developmental origin of own-species song-preferences is a
more general phenomenon and not limited to female matechoice. Recent work has demonstrated that preferences of
socially raised females for conspecific songs over songs of
heterospecific African, Asian, and Australian estrildid finches
do not depend on phylogenetic distance or geographical
sympatry (Campbell et al. 2009a). Future work, however, should
assess the strength of such conspecific song-preferences in the
wild, as well as identifying the potential role of phylogeny and
sympatry in preferences of females (and males) reared in isolation
for conspecific songs over heterospecific songs (Campbell and
Hauber 2009b).
Females that are cross-fostered show a developmental duality
in species recognition: there is evidence of both an own-species
bias and the role of early experience (Campbell and Hauber
2009a). For example, females that have been raised by
Bengalese Munias are more likely to spend time perching near
male Bengalese Munias than are females that have been raised by
Zebra Finches, but overall spatial proximity and sexual display
preferences are shown for male Zebra Finches (ten Cate and Mug
1984). When spatial proximity preferences for only the songs of
different species were quantified for females that had been raised
by Zebra Finches or Bengalese Munias, females that were raised
by Zebra Finches preferred Zebra Finch song while the crossfostered females did not discriminate among the songs of
three different species (Campbell and Hauber 2009a). Yet,
intraspecifically, females that are raised by adults of another
subspecies show preferences for the foster-subspecies songs as
adult Zebra Finches (Clayton 1990). These studies indicate that
the social experiences of juveniles guide adult song preferences
and that a juvenile’s experience with parental adults can be
considered to be a form of sexual imprinting (ten Cate et al.
2006). The adaptive significance of sexual imprinting in directing
female attraction to paternal-like songs is that it serves as a
mechanism for matching a female with a conspecific male for
mating (Irwin and Price 1999).
The neurophysiological mechanisms of sexual imprinting on
paternal songs are unknown in females. Further, the neural
pathways that are involved in attending to, and that are shaped
by, the perception of salient sexual signals during imprinting need
to be identified. Another important topic for exploration is the
neural basis of how auditory cues of species identity direct female
attraction and sexual display behaviours to conspecific song.
Subsequently, as with all model species, it also needs to be
explored how the neural circuits that mediate song-processing
and sexual attraction differ between Zebra Finches and other
acoustically oriented species. Such neurophysiological work has
only just begun to be conducted (e.g. Woolley et al. 2010 on
comparing neuronal information coding in male Zebra Finches
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and Bengalese Munias). Important clues and future discoveries
may come from understanding what acoustic aspects of
conspecific songs serve as behavioural cues for female
attraction (discussed in the next section below).
Song-type
The Zebra Finch song is not territorial in function and has been
considered traditionally to serve in attracting and stimulating
females (Morris 1954). However, the male sings two different
song-types: directed and undirected songs. The production of
either type is determined by immediate social cues, including
proximity to female and male conspecifics (reviewed in Zann
1996). The presence of a female for example, elicits directed song
that is typically sung at a faster rate, with more introductory
elements and song phrases per bout, and is characteristically
accompanied by the male courtship dance (Williams 2004). The
undirected song, in contrast, is typically performed by a male in
isolation or without a specifically intended receiver, although it
too may serve as a general display to attract females and to
advertise quality for potential extra-pair copulations (Dunn and
Zann 1996; Holveck and Riebel 2010).
Numerous experiments have assessed female choice for
conspecific males based on song (most recently extensively
reviewed by Riebel 2009) and it appears that the directed song
is what listening females approach preferentially (Woolley and
Doupe 2008). This preference for an individual male’s directed
song is strengthened by mating experience, with the strongest
preference shown for the directed song of the female’s mate.
This is consistent with the roles that directed song play in
courtship and individual recognition of mates (Woolley and
Doupe 2008). Once a pair-bond is formed, however, continued
production of attractive songs (e.g. high rate, large repertoire
of vocalisations; see below) is not required for pair-bond
maintenance in Zebra Finches, as shown by the continued
paired status between females and surgically muted or songaltered males (Tomaszycki and Adkins-Regan 2006).
Song-rate and repertoire size
Features of the normal male song that appear to be particularly
attractive to females are high rates of song output (ten Cate and
Mug 1984; Collins et al. 1994) and high numbers of different
syllables, also known as repertoire size (Clayton and Prove 1989;
Holveck and Riebel 2007; Vyas et al. 2009). Playback of male
Zebra Finch songs with more and different syllables, whether
comprised of elements sung by the same male or combined from
the songs of different males, are more attractive than repeated
playback of the same syllables (Collins 1999). The length of
syllables has also been found to be attractive to females, but this
feature of song is often confounded with the presence of more
song-elements in motifs (reviewed in Riebel 2009). Vyas et al.
(2009) specifically tested whether females showed preferences,
as indicated by more body shakes and calling, for complex songs
or long simple songs (those that were long in duration but had
relatively few song-elements) over shorter simple songs, and
found that complex songs were preferred.
For females raised hearing normal adult vocalisations, songs
produced by socially tutored males are preferred over the more
poorly structured, less consistent, and higher pitched isolate songs
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of males that have not been tutored (Lauay et al. 2004). Females
are also sensitive to whether males sing acoustically intact songs;
surgically altered males that sing abnormal songs are less
attractive as indicated by female spatial proximity and pairbond formation (Tomaszycki and Adkins-Regan 2005).
Hearing male song during development is critical not only for
the development of preferences for complex over simple songs or
conspecific over heterospecific songs (Campbell and Hauber
2009a), but also for the development of consistent preference
behaviours for the songs of the same individual males (Riebel
2009). This has been reported in both females (Riebel et al. 2002)
and males (Pytte and Suthers 1999).
Female attraction to males that sing a more structured song
composed of a larger repertoire of syllables may be adaptive, by
directing females to males whose progeny are also likely to
perform attractive songs. This is because the neural circuitry
that controls song learning by, and vocal performance of, males
(Airey et al. 2000) and the amount of paternal care contributing
to predictable variation in neural, morphological and vocal
traits, or both, may have considerably heritable components
(Freeman-Gallant and Rothstein 1999). Future work aimed at
estimating the true heritability of the genomic, anatomical,
physiological and social basis of song behaviour will require
cross-fostering paradigms aimed at estimating the contributions
of shared genes (Forstmeier et al. 2009) from shared ontogenies
(Ward et al. 2001).
There is also conflicting evidence on the role of the condition
and social context of male chicks during early development
on imitative learning and the structure of song in adulthood
(Buchanan et al. 2004; Gil et al. 2006; Zann and Cash 2008).
Male Zebra Finches that sing frequently must also maintain
increased rates of oxygen and energy consumption to keep up
this singing behaviour. Specifically, males must manage
physiologically demanding rapid shifts during singing between
the many vocal and silent intervals characteristic of Zebra Finch
songs. This in turn, may modulate the overall cost of fast,
transition-rich, song-production typical in this species (Franz
and Goller 2003), and thus serve as both honest indicator and
a constraint on the evolution of costly song display behaviour in
male Zebra Finches.
Attributes of song, such as the number of elements per motif
and rates of singing, are also correlated with morphological
measures of male sexual displays (Holveck and Riebel 2007)
and with general learning ability, as assayed using a laboratory
test of foraging problem-solving (Boogert et al. 2008).
Furthermore, increased developmental stress is correlated with
male songs that have fewer song-elements and are less attractive
to females in adulthood (Spencer et al. 2005). Therefore, highquality songs, in terms of acoustic repertoire and rate of output,
signal a high-quality male. As discussed above, females that are
attracted to these types of songs may benefit from selecting
reliably high-quality mates regarding both genetic (Forstmeier
et al. 2009) and parental contributions (Freeman-Gallant and
Rothstein 1999). Further interpretation of female preferences and
the role of the developmental environment might require
investigations of whether exposure to typical high-quality male
song while being reared in a nutritionally poor environment, and
vice versa, might influence song preferences in adulthood.
Correspondingly, recent studies have suggested that females
M. E. Hauber et al.
may modulate their mate-choice criteria regarding male quality
in response to their own perceived quality (e.g. through selfreferenced phenotype matching; Hauber and Sherman 2001). For
example, poor-condition females may benefit from being less
choosy overall to avoid a prolonged search for a mate (Burley and
Foster 2006). Alternatively, females in poor condition may even
benefit from choosing males of low rather than high quality if less
time and effort are required to compete for a high-quality male
who may, in turn, opt to pair with a different, higher quality female
(Holveck and Riebel 2010). Assortative mating by quality is
consistent with the patterns of mutual mate-choice by both sexes
reported in captive Zebra Finches (Wynn and Price 1993). These
recent studies on assortative mating based on self-perceived
quality also call for a new way of theorising about how song
may function in female mate-choice and raises several questions
about how males and females pair in nature. For example, what
range of quality is there among the potential breeders in wild
Zebra Finch colonies, given the role of predation and other
ecological constraints acting on reducing initial recruitment
into the breeder pool? Also, do low-quality birds attempt to
pair and breed or trade-off to increase condition until they
reach a threshold at which pair-bonding and breeding are
likely to succeed? If assortative and mutual-quality matching
occurs in wild Zebra Finches, then the role of directional selection
on male sexual signals, including song, in female mate-choice
will have to be re-thought.
Proximate mechanisms of female attraction to song
Hormones
There is likely to be a dynamic interplay between behavioural
interactions and hormone levels influencing selectivity in social
species. For example, there is increasing evidence of behavioural
and physiological feedback following manipulations of
male traits relevant for female mate-preferences in Zebra
Finches (Pariser et al. 2010), as well as in other species of bird
(Rubenstein and Hauber 2008; Safran et al. 2008). For example,
sex steroid hormones modulate female Zebra Finch reproductive
behaviours, and may have an impact on female perception,
discrimination and attraction to song (Adkins-Regan 2009).
Yet, the activational role of oestrogen in female attraction to
song requires further scrutiny. Historically, females, in which
displays of sexual attraction, such as tail-quivers, are measured,
have been treated with oestradiol before playbacks, suggesting
that higher oestradiol levels promote sexual receptivity and
display rate (e.g. Clayton and Prove 1989). Recent work
using acute inhibition of oestrogen production in the auditory
forebrain confirms a short time-scale at which oestrogen can act
on neuronal and behavioural responses to male song (RemageHealey et al. 2010) Specifically, Vyas et al. (2008, 2009) found
that females preferred complex songs when they were treated
with oestradiol, but not when they had naturally low circulating
levels of oestradiol that were induced by isolating females
from exposure to males. Taken together, the results of these
studies suggest that higher oestrogen levels may modulate female
responses to specific aspects of sexual attractiveness of male song.
Accordingly, new data on the effects of oestrogen manipulations
on gene expression and on the electrophysiological responses of
neurons that are important for song processing (Tremere et al.
Male song and female preference in the Zebra Finch
2009) are consistent with the hypothesis that oestrogen
significantly modulates perception of song in the female Zebra
Finch brain (see below).
Neural responses to song
Regions of the Zebra Finch brain that are important for perception
of song have been intensively studied in males and, more recently,
in females (Zeigler and Marler 2008; London and Clayton 2010).
For example, the firing rates of neurons in the primary auditory
forebrain region field L in female Zebra Finches are higher in
response to conspecific song than to synthetic sounds that are
matched in duty cycle to overall sound production, and in
frequency and power spectra to conspecific song (Hauber et al.
2007b). The ontogeny of such conspecific song selectivity
in females does not require exposure to male songs during
development (Hauber et al. 2007a). Overall, these results
parallel the patterns shown in the spike-rates of male field L
neurons (Grace et al. 2003) and imaging data, using auditory
event-related potential (ERP) or functional magnetic resonance
imaging (fMRI), in response to male songs in female auditory
forebrain regions (Maul et al. 2010). The species specificity and
experience dependence of physiological sensitivity of female
auditory neurons to conspecific versus heterospecific song remain
to be described, but, in males, the firing rates of single field L
neurons are similar in response to Zebra Finch and Bengalese
Munia songs (Woolley et al. 2010). Future research may
profitably test the synergistic contributions of early and
breeding experience and the role of endocrine modulation for
determining the neural processing of song by females, especially
in response to natural variation of the environmental cues that
promote the onset of breeding in wild populations of Zebra
Finches, as opposed to controlled laboratory conditions and
captive-bred stocks.
Genomic responses in several secondary auditory forebrain
regions of female Zebra Finches consistently show greater
sensitivity to conspecific over heterospecific songs, and to
familiar over unfamiliar songs. For example, immediate early
gene (IEG) expression in the caudomedial nidopallium (NCM), is
higher following playback of conspecific song than following
playback of heterospecific song in normal raised Zebra Finches
(Bailey et al. 2002). IEG expression in this brain region is also
higher following playback of familiar songs compared with
unfamiliar songs in females (Terpstra et al. 2006; Woolley and
Doupe 2008). The fine-scale neuroanatomical architecture of the
NCM in female Zebra Finches also varies with experience; NCM
neurons from females with early exposure to normal male song
show higher density of dendritic spines compared with those from
females without developmental exposure to song (Lauay et al.
2005). The expression of IEGs in the NCM has also been shown to
be greater in normally raised females that heard playbacks of
social Zebra Finch songs than in females that heard isolate songs
(Tomaszycki et al. 2006).
These neurobiological studies parallel the results of
behavioural experiments describing the ontogenetic duality of
species recognition in female Zebra Finches (discussed above)
demonstrating that genetic species identity, familiarity, early
experience and the quality of male song may potentially
combine and contribute to various extents in shaping the song
Emu
215
preferences of female Zebra Finches. Nonetheless, it remains to
be tested whether repeated playbacks of the same syllables cause
neural habituation in the auditory nuclei of females, in parallel
with the reduced behavioural preferences for less variable songs
(Collins 1999). Progress is ongoing, however, as Tremere et al.
(2009) recently found that acute, direct administration of
oestradiol into NCM resulted in greatly increased firing rates
of single neurons responding to song, thus providing a potential
link between hormonal state and the neural processing of specific
acoustic features of male song in the female brain.
Advancing the role of the Zebra Finch as a model species
The Zebra Finch has been a model species for diverse, insightful,
surprising, technologically advancing, and controversial studies
on the ultimate and proximate bases of reproductive vocal
behaviour (Zann 1996; Zeigler and Marler 2008). There is a
continuing need to follow the tradition of Richard Zann to
test critical theory with observations and experiments in wild
populations of Zebra Finches or, lacking experimental feasibility,
strive for more specific comparisons between data collected
from both wild-caught and domesticated strains of Zebra
Finches (Rutstein et al. 2007). This research will also benefit
from the application of rapidly advancing genomic and imaging
technologies in the study of Zebra Finches in captivity as a model
species (Boumans et al. 2007; Voss et al. 2007; Campbell et al.
2009b; Warren et al. 2010). The Zebra Finch is well positioned to
maintain this driving role for research in the near future, as its full
genome is only the second avian species genome to be sequenced
(Hauber et al. 2008; Balakrishnan et al. 2010). More discoveries
are surely to be gained from the ongoing advances of imagingbased and other in vivo and chronic neurobiological dataacquisition methods (Fee and Leonardo 2001; Maul et al.
2010). The research investment made to date combined with
new technological advances will ensure that the Zebra Finch
remains an important and productive model system for future
work, including studies of the function and the theory of acoustic
communication, species recognition and reproductive behaviours
highlighted here.
Acknowledgements
This article is dedicated to Richard Zann’s memorable visit and departmental
seminar at the School of Biological Sciences of the University of Auckland
in late 2008 when M. E. Hauber and D. L. M. Campbell were based in
New Zealand. We thank the referees and editors for their comments on draft
manuscripts. For funding, we thank the Searle Scholars Fund, the US National
Science Foundation and National Institutes of Health (to S. M. N. Woolley),
and the Provost’s Office of Hunter College and the Research Foundation of the
City University of New York (to M. E. Hauber).
References
Adkins-Regan, E. (1999). Testosterone increases singing and aggression
but not male-typical sexual partner preference in early estrogen treated
female zebra finches. Hormones and Behavior 35, 63–70. doi:10.1006/
hbeh.1998.1497
Adkins-Regan, E. (2009). Hormones and sexual differentiation of avian social
behavior. Developmental Neuroscience 31, 342–350. doi:10.1159/
000216545
Adkins-Regan, E., and Tomaszycki, M. L. (2007). Monogamy on the fast
track. Biology Letters 3, 617–619. doi:10.1098/rsbl.2007.0388
216
Emu
Adkins-Regan, E., Mansukhani, V., Seiwert, C., and Thompson, R. (1994).
Sexual differentiation of brain and behavior in the zebra finch: critical
periods for effects of early estrogen treatment. Journal of Neurobiology
25, 865–877. doi:10.1002/neu.480250710
Adret, P. (2004). Vocal imitation in blindfolded zebra finches (Taeniopygia
guttata) is facilitated in the presence of a non-singing conspecific female.
Journal of Ethology 22, 29–35. doi:10.1007/s10164-003-0094-y
Agate, R. J., Grisham, W., Wade, J., Mann, S., Wingfield, J., Schanen, C.,
Palotie, A., and Arnold, A. P. (2003). Neural, not gonadal, origin of brain
sex differences in a gynandromorphic finch. Proceedings of the National
Academy of Sciences of the United States of America 100, 4873–4878.
doi:10.1073/pnas.0636925100
Airey, D. C., Castillo-Juarez, H., Casella, G., Pollak, E. J., and DeVoogd, T. J.
(2000). Variation in the volume of zebra finch song control nuclei is
heritable: developmental and evolutionary implications. Proceedings
of the Royal Society of London. Series B. Biological Sciences 267,
2099–2104. doi:10.1098/rspb.2000.1255
Bailey, D. J., Rosebush, J. C., and Wade, J. (2002). The hippocampus and
caudomedial neostriatum show selective responsiveness to conspecific
song in the female zebra finch. Journal of Neurobiology 52, 43–51.
doi:10.1002/neu.10070
Balakrishnan, C. N., Edwards, S. V., and Clayton, D. F. (2010). The Zebra
Finch genome and avian genomics in the wild. Emu 110, 233–241.
doi:10.1071/MU09087
Birkhead, T. R. (2010). Post-copulatory sexual selection and the Zebra Finch.
Emu 110, 189–198. doi:10.1071/MU09086
Bolhuis, J. J., Van Mil, D. P., and Houx, B. B. (1999). Song learning with
audiovisual compound stimuli in zebra finches. Animal Behaviour 58,
1285–1292. doi:10.1006/anbe.1999.1266
Boogert, N. J., Giraldeau, L.-A., and Lefebvre, L. (2008). Song complexity
correlates with learning ability in zebra finch males. Animal Behaviour
76, 1735–1741. doi:10.1016/j.anbehav.2008.08.009
Boumans, T., Theunissen, F. E., Poirier, C., and van der Linden, A. (2007).
Neural representation of spectral and temporal features of song in the
auditory forebrain of zebra finches as revealed by functional MRI.
European Journal of Neuroscience 26, 2613–2626. doi:10.1111/
j.1460-9568.2007.05865.x
Braaten, R. F., and Reynolds, K. (1999). Auditory preference for conspecific
song in isolation-reared zebra finches. Animal Behaviour 58, 105–111.
doi:10.1006/anbe.1999.1134
Brazas, M., and Shimizu, T. (2002). The effect of auditory cues on visual
choice behavior in the female zebra finch (Taeniopygia guttata
castanotis). Animal Cognition 5, 91–95.
Brumm, H., and Slater, P. J. B. (2006). Animals can vary signal amplitude with
receiver distance: evidence from zebra finch song. Animal Behaviour
72, 699–705. doi:10.1016/j.anbehav.2006.01.020
Buchanan, K. L., Leitner, S., Spencer, K. A., Goldsmith, A. R., and Catchpole,
C. K. (2004). Developmental stress selectively affects the song control
nucleus HVC in the zebra finch brain. Proceedings of the Royal Society of
London. Series B. Biological Sciences 271, 2381–2386. doi:10.1098/
rspb.2004.2874
Burley, N. T., and Foster, V. S. (2006). Variation in female choice of mates:
condition influences selectivity. Animal Behaviour 72, 713–719.
doi:10.1016/j.anbehav.2006.01.017
Burley, N. T., Minor, C., and Strachan, C. (1990). Social preference of zebra
finch for siblings, cousins, and non-kin. Animal Behaviour 39, 775–784.
doi:10.1016/S0003-3472(05)80389-6
Campbell, D. L. M., and Hauber, M. E. (2009a). Cross-fostering diminishes
song discrimination in zebra finches (Taeniopygia guttata). Animal
Cognition 12, 481–490. doi:10.1007/s10071-008-0209-5
Campbell, D. L. M., and Hauber, M. E. (2009b). Spatial and behavioural
measures of social discrimination by captive male zebra finches:
implications of sexual and species differences for recognition research.
Behavioural Processes 80, 90–98. doi:10.1016/j.beproc.2008.10.007
M. E. Hauber et al.
Campbell, D. L. M., and Hauber, M. E. (2009c). Disassociation of visual and
acoustic conspecific cues decreases discrimination by female zebra
finches (Taeniopygia guttata). Journal of Comparative Psychology
123, 310–315. doi:10.1037/a0015837
Campbell, D. L. M., and Hauber, M. E. (2010a). Behavioural correlates
of female zebra finches (Taeniopygia guttata) responses to multimodal
species recognition cues. Ethology Ecology and Evolution 22,
167–181.
Campbell, D. L. M., and Hauber, M. E. (2010b). Conspecific-only experience
during development reduces the strength of heterospecific song
discrimination in zebra finches (Taeniopygia guttata): a behavioural
test of the optimal acceptance threshold hypothesis. Journal of
Ornithology 151, 379–389. doi:10.1007/s10336-009-0466-3
Campbell, D. L. M., Shaw, R. C., and Hauber, M. E. (2009a). The strength of
species recognition in captive female zebra finches (Taeniopygia guttata):
a comparison across estrildid heterospecifics. Ethology 115, 23–32.
doi:10.1111/j.1439-0310.2008.01584.x
Campbell, D. L. M., Weiner, S. A., Starks, P. T. B., and Hauber, M. E. (2009b).
Context and control: behavioural ecology experiments in the laboratory.
Annales Zoologici Fennici 46, 112–123.
Clayton, N. S. (1987). Mate choice in male zebra finches: some effects of
cross-fostering. Animal Behaviour 35, 596–597. doi:10.1016/S00033472(87)80286-5
Clayton, N. S. (1988). Song learning and mate choice in estrildid finches raised
by two species. Animal Behaviour 36, 1589–1600. doi:10.1016/S00033472(88)80101-5
Clayton, N. S. (1989). The effects of cross-fostering on selective song
learning in estrildid finches. Behaviour 109, 163–174. doi:10.1163/
156853989X00204
Clayton, N. S. (1990). Subspecies recognition and song learning in zebra
finches. Animal Behaviour 40, 1009–1017. doi:10.1016/S0003-3472(05)
80169-1
Clayton, N. S., and Prove, E. (1989). Song discrimination in female
zebra finches and Bengalese finches. Animal Behaviour 38, 352–354.
doi:10.1016/S0003-3472(89)80096-X
Collins, S. A. (1999). Is female preference for repertoires due to sensory bias?
Proceedings of the Royal Society of London. Series B. Biological Sciences
266, 2309–2314. doi:10.1098/rspb.1999.0924
Collins, S. A., Hubbard, C., and Houtman, A. M. (1994). Female mate
choice in the zebra finch: the effect of male beak color and male song.
Behavioral Ecology and Sociobiology 35, 21–25. doi:10.1007/
BF00167055
Dunn, A. M., and Zann, R. A. (1996). Undirected song in wild zebra finch
flocks: contexts and effects of mate removal. Ethology 102, 529–539.
doi:10.1111/j.1439-0310.1996.tb01145.x
Eales, L. A. (1985). Song learning in zebra finches: some effects of song model
availability on what is learnt and when. Animal Behaviour 33, 1293–1300.
doi:10.1016/S0003-3472(85)80189-5
Eales, L. A. (1989). The influences of visual and vocal interaction on song
learning in zebra finches. Animal Behaviour 37, 507–508. doi:10.1016/
0003-3472(89)90097-3
Fee, M. S., and Leonardo, A. (2001). Miniature motorized microdrive and
commutator system for chronic neural recording in small animals. Journal
of Neuroscience Methods 112, 83–94. doi:10.1016/S0165-0270(01)
00426-5
Fehér, O., Wang, H., Mitra, P. P., and Tchernichovski, O. (2009). De novo
establishment of wild-type song culture in the zebra finch. Nature 459,
564–568. doi:10.1038/nature07994
Fetherston, I. A., and Burley, N. T. (1990). Do zebra finches prefer to mate
with close relatives? Behavioral Ecology and Sociobiology 27, 411–414.
doi:10.1007/BF00164067
Forstmeier, W., and Birkhead, T. R. (2004). Repeatability of mate choice in the
zebra finch: consistency within and among females. Animal Behaviour
68, 1017–1028. doi:10.1016/j.anbehav.2004.02.007
Male song and female preference in the Zebra Finch
Forstmeier, W., Burger, C., Temnow, K., and Deregnaucourt, S. (2009). The
genetic basis of zebra finch vocalizations. Evolution 63, 2114–2130.
doi:10.1111/j.1558-5646.2009.00688.x
Franz, M., and Goller, F. (2003). Respiratory patterns and oxygen
consumption in singing zebra finches. Journal of Experimental Biology
206, 967–978. doi:10.1242/jeb.00196
Freeman-Gallant, C. R., and Rothstein, M. D. (1999). Apparent heritability of
parental care in Savannah Sparrows. Auk 116, 1132–1136.
Gil, D., Naguib, M., Riebel, K., Rutstein, A., and Gahr, M. (2006). Early
condition, song learning and the volume of brain song nuclei in the zebra
finch (Taeniopygia guttata). Journal of Neurobiology 66, 1602–1612.
doi:10.1002/neu.20312
Grace, J. A., Amin, N. A., Singh, N. C., and Theunissen, F. E. (2003).
Selectivity for conspecific song in the zebra finch auditory forebrain.
Journal of Neurophysiology 89, 472–487. doi:10.1152/jn.00088.2002
Griffith, S. C., Holleley, C. E., Mariette, M. M., Pryke, S. R., and Svedin, N.
(2010). Low level of extrapair parentage in wild zebra finches. Animal
Behaviour 79, 261–264. doi:10.1016/j.anbehav.2009.11.031
Hauber, M. E., and Lacey, E. A. (2005). Bateman’s principle in cooperatively
breeding vertebrates: the effects of non-breeding alloparents on variability
of female and male reproductive success. Integrative and Comparative
Biology 45, 903–914. doi:10.1093/icb/45.5.903
Hauber, M. E., and Sherman, P. W. (2001). Self-referent phenotype matching:
theoretical possibilities and empirical tests. Trends in Neurosciences
24(10), 609–616. doi:10.1016/S0166-2236(00)01916-0
Hauber, M. E., Russo, S. A., and Sherman, P. W. (2001). A password for
species recognition in a brood parasitic bird. Proceedings of the Royal
Society of London. Series B. Biological Sciences 268, 1041–1048.
doi:10.1098/rspb.2001.1617
Hauber, M. E., Woolley, S. M. N., and Theunissen, F. E. (2007a). Experiencedependence of neural responses to social versus isolate conspecific
songs in the forebrain of female Zebra Finches. Journal of Ornithology
148(Suppl. 2), 231–239. doi:10.1007/s10336-007-0234-1
Hauber, M. E., Cassey, P., Woolley, S. M. N., and Theunissen, F. E. (2007b).
Neurophysiological response selectivity for conspecific songs over
synthetic sounds in the auditory forebrain of non-singing female
songbirds. Journal of Comparative Physiology A: Neuroethology,
Sensory, Neural, and Behavioral Physiology 193, 765–774.
doi:10.1007/s00359-007-0231-0
Hauber, M. E., Sewell, M. A., and Zuk, M. (2008). Gender genomics and
equality. Heredity 101, 395. doi:10.1038/hdy.2008.83
Helekar, S. A., Marsh, S., Viswanath, N. S., and Rosenfield, D. B. (2000).
Acoustic pattern variations in the female-directed birdsong of a colony
of laboratory-bred zebra finches. Behavioural Processes 49, 99–110.
doi:10.1016/S0376-6357(00)00081-4
Holveck, M. J., and Riebel, K. (2007). Preferred songs predict preferred males:
consistency and repeatability of zebra finch females across three test
contexts. Animal Behaviour 74, 297–309. doi:10.1016/j.anbehav.2006.
08.016
Holveck, M. J., and Riebel, K. (2010). Low-quality females prefer low-quality
males when choosing a mate. Proceedings of the Royal Society of London.
Series B. Biological Sciences 277, 153–160. doi:10.1098/rspb.2009.1222
Immelmann, K. (1959). Experimentelle Untersuchungen über die biologische
Bedeutung artspezifischer Merkmale beim Zebrafinken (Taeniopygia
guttata Gould). Zoologische Jahrbucher. Abteilung fur Systematik,
Ökologie und Geographie der Tiere 86, 437–592.
Immelmann, K. (1969). Song development in the zebra finch and other
estrilid finches. In ‘Bird Vocalizations’. (Ed. R. A. Hinde.) pp. 61–77.
(Cambridge University Press: Cambridge.)
Irwin, D. E., and Price, T. (1999). Sexual imprinting, learning and speciation.
Heredity 82, 347–354. doi:10.1038/sj.hdy.6885270
Lauay, C., Gerlach, N. M., Adkins-Regan, E., and Devoogd, T. J. (2004).
Female zebra finches require early song exposure to prefer high-quality
song as adults. Animal Behaviour 68, 1249–1255. doi:10.1016/
j.anbehav.2003.12.025
Emu
217
Lauay, C., Komorowski, R. W., Beaudin, A. E., and DeVoogd, T. J. (2005).
Adult female and male zebra finches show distinct patterns of spine deficits
in an auditory area and in the song system when reared without exposure to
normal adult song. Journal of Comparative Neurology 487, 119–126.
doi:10.1002/cne.20591
London, S. E., and Clayton, D. F. (2010). The neurobiology of Zebra Finch
song: insights from gene expression studies. Emu 110, 219–232.
doi:10.1071/MU09079
Maul, K. K., Voss, H. U., Parra, L. C., Salgado-Commissariat, D., Ballon, D.,
Tchernichovski, O., and Helekar, S. A. (2010). The development
of stimulus-specific auditory responses requires song exposure in
male but not female zebra finches. Developmental Neurobiology 70,
28–40.
Miller, D. B. (1979a). The acoustic basis of mate recognition by female
zebra finches (Taeniopygia guttata). Animal Behaviour 27, 376–380.
doi:10.1016/0003-3472(79)90172-6
Miller, D. B. (1979b). Long-term recognition of father’s song by female zebra
finches. Nature 280, 389–391. doi:10.1038/280389a0
Morris, D. (1954). The reproductive behaviour of the zebra finch
(Poephila guttata), with special reference to pseudofemale behaviour
and displacement activities. Behaviour 6, 271–322. doi:10.1163/
156853954X00130
Morrison, R. G., and Nottebohm, F. (1993). Role of a telencephalic nucleus in
the delayed song learning of socially isolated zebra finches. Journal of
Neurobiology 24, 1045–1064. doi:10.1002/neu.480240805
Pariser, E. C., Mariette, M. M., and Griffith, S. C. (2010). Artificial ornaments
manipulate intrinsic male quality in wild-caught zebra finches
(Taeniopygia guttata). Behavioral Ecology 21, 264–269. doi:10.1093/
beheco/arp185
Pytte, C. L., and Suthers, R. A. (1999). A bird’s own song contributes to
conspecific song perception. Neuroreport 10, 1773–1778. doi:10.1097/
00001756-199906030-00027
Remage-Healey, K., Coleman, M. J., Oyama, R. K., and Schlinger, B. A.
(2010). Brain estrogens rapidly strengthen auditory encoding and guide
song preference in a songbird. Proceedings of the National Academy of
Sciences of the United States of America 107, 3852–3857. doi:10.1073/
pnas.0906572107
Riebel, K. (2000). Early exposure to song leads to repeatable preferences for
male song in female zebra finches. Proceedings of the Royal Society of
London. Series B. Biological Sciences 267, 2553–2558. doi:10.1098/
rspb.2000.1320
Riebel, K. (2003). Developmental influences on auditory perception in
female zebra finches: is there a sensitive phase for song preference
learning? Animal Biology 53, 73–87. doi:10.1163/157075603769700304
Riebel, K. (2009). Song and female mate choice in zebra finches: a review.
Advances in the Study of Behavior 40, 197–238. doi:10.1016/S0065-3454
(09)40006-8
Riebel, K., and Smallegange, I. M. (2003). Does zebra finch (Taeniopygia
guttata) preference for the (familiar) father’s song generalize to the songs
of unfamiliar brothers? Journal of Comparative Psychology 117, 61–66.
doi:10.1037/0735-7036.117.1.61
Riebel, K., Smallegange, I. M., Terpstra, N. J., and Bolhuis, J. J. (2002).
Sexual equality in zebra finch song preference: evidence for a dissociation
between song recognition and production learning. Proceedings of the
Royal Society of London. Series B. Biological Sciences 269, 729–733.
doi:10.1098/rspb.2001.1930
Rubenstein, D. R., and Hauber, M. E. (2008). Dynamic feedback between
phenotype and physiology in sexually selected traits. Trends in Ecology &
Evolution 23, 655–658. doi:10.1016/j.tree.2008.07.010
Rutstein, A. N., Brazill-Boast, J., and Griffith, S. C. (2007). Evaluating mate
choice in the zebra finch. Animal Behaviour 74, 1277–1284. doi:10.1016/
j.anbehav.2007.02.022
Safran, R. J., Adelman, J. S., McGraw, K. J., and Hau, M. (2008). Sexual signal
exaggeration affects physiological state in male barn swallows. Current
Biology 18, R461–R462. doi:10.1016/j.cub.2008.03.031
218
Emu
M. E. Hauber et al.
Sharp, S. P., McGowan, A., Wood, M. J., and Hatchwell, B. J. (2005). Learned
kin recognition cues in a social bird. Nature 434, 1127–1130. doi:10.1038/
nature03522
Simpson, H. B., and Vicario, D. S. (1991). Early estrogen treatment alone
causes female zebra finches to produce learned, male-like vocalizations.
Journal of Neurobiology 22, 755–776. doi:10.1002/neu.480220710
Slater, P. J. B., and Mann, N. I. (1990). Do male zebra finches learn their
fathers’ songs? Trends in Ecology & Evolution 5, 415–417. doi:10.1016/
0169-5347(90)90027-B
Slater, P. J. B., Eales, L. A., and Clayton, N. S. (1988). Song learning in
zebra finches (Taeniopygia guttata): progress and prospects. Advances
in the Study of Behavior 18, 1–34. doi:10.1016/S0065-3454(08)60308-3
Sossinka, R., and Bohner, J. (1980). Song types in the zebra finch (Poephila
guttata castanotis). Zeitschrift für Tierpsychologie 53, 123–132.
Spencer, K. A., Wimpenny, J. H., Buchanan, K. L., Lovell, P. G., Goldsmith,
A. R., and Catchpole, C. K. (2005). Developmental stress affects the
attractiveness of male song and female choice in the zebra finch
(Taeniopygia guttata). Behavioral Ecology and Sociobiology 58,
423–428. doi:10.1007/s00265-005-0927-5
Tchernichovski, O., and Nottebohm, F. (1998). Social inhibition of song
imitation among sibling male zebra finches. Proceedings of the National
Academy of Sciences of the United States of America 95, 8951–8956.
doi:10.1073/pnas.95.15.8951
Tchernichovski, O., Schwabl, H., and Nottebohm, F. (1998). Context
determines the sex appeal of male zebra finch song. Animal Behaviour
55, 1003–1010. doi:10.1006/anbe.1997.0673
ten Cate, C., and Mug, G. (1984). The development of mate choice in
zebra finch females. Behaviour 90, 125–150. doi:10.1163/156853984
X00588
ten Cate, C., Verzijden, M. N., and Etman, E. (2006). Sexual imprinting can
induce sexual preferences for exaggerated parental traits. Current Biology
16, 1128–1132. doi:10.1016/j.cub.2006.03.068
Terpstra, N. J., Bolhuis, J. J., Riebel, K., van der Burg, J. M. M., and den BoerVisser, A. M. (2006). Localized brain activation specific to auditory
memory in a female songbird. Journal of Comparative Neurology 494,
784–791. doi:10.1002/cne.20831
Tomaszycki, M. L., and Adkins-Regan, E. (2005). Experimental alteration of
male song quality and output affects female mate choice and pair bond
formation in zebra finches. Animal Behaviour 70, 785–794. doi:10.1016/
j.anbehav.2005.01.010
Tomaszycki, M. L., and Adkins-Regan, E. (2006). Is male song quality
important in maintaining pair bonds? Behaviour 143, 549–567.
doi:10.1163/156853906776759529
Tomaszycki, M. L., Sluzas, E. M., Sundberg, K. A., Newman, S. W., and
DeVoogd, T. J. (2006). Immediate early gene responses to song in juvenile
female and male zebra finches: effects of rearing environment. Journal of
Neurobiology 66, 1175–1182. doi:10.1002/neu.20275
Tremere, L. A., Jeong, J. K., and Pinaud, R. (2009). Estradiol shapes auditory
processing in the adult brain by regulating inhibitory transmission and
plasticity-associated gene expression. Journal of Neuroscience 29,
5949–5963. doi:10.1523/JNEUROSCI.0774-09.2009
Vignal, C., Mathevon, N., and Mottin, S. (2008). Mate recognition by female
zebra finch: analysis of individuality in male call and first investigations
on female decoding process. Behavioural Processes 77, 191–198.
doi:10.1016/j.beproc.2007.09.003
Voss, H. U., Tabelow, K., Polzehl, J., Tchernichovski, O., Maul, K. K.,
Salgado-Commissariat, D., Ballon, D., and Helekar, S. A. (2007).
Functional MRI of the zebra finch brain during song stimulation
suggests a lateralized response topography. Proceedings of the
National Academy of Sciences of the United States of America 104,
10667–10672. doi:10.1073/pnas.0611515104
Vyas, A., Harding, C., McGowan, J., Snare, R., and Bogdan, D.
(2008). Noradrenergic neurotoxin, N-(2-chloroethyl)-N-ethyl-2bromobenzylamine hydrochloride (DSP-4), treatment eliminates
estrogenic effects on song responsiveness in female zebra finches
(Taeniopygia guttata). Behavioral Neuroscience 122, 1148–1157.
doi:10.1037/0735-7044.122.5.1148
Vyas, A., Harding, C., Borg, L., and Bogdan, D. (2009). Acoustic
characteristics, early experience, and endocrine status interact to
modulate female zebra finches’ behavioral responses to songs.
Hormones and Behavior 55, 50–59. doi:10.1016/j.yhbeh.2008.08.005
Ward, B. C., Nordeen, E. J., and Nordeen, K. W. (2001). Anatomical and
ontogenetic factors producing variation in HVc neuron number in zebra
finches. Brain Research 904, 318–326. doi:10.1016/S0006-8993(01)
02488-X
Warren, W. C., Clayton, D. F., Ellegren, H., Arnold, A. P., Hillier, L. W.,
Künstner, A., Searle, S., White, S., et al. (2010). The genome of a
songbird. Nature 464, 757–762. doi:10.1038/nature08819
Williams, H. (2004). Choreography of song, dance and beak movements in the
zebra finch (Taeniopygia guttata). Journal of Experimental Biology
204, 3497–3506.
Williams, H., Kilander, K., and Sotanski, M. L. (1993). Untutored song,
reproductive success and song learning. Animal Behaviour 45, 695–705.
doi:10.1006/anbe.1993.1084
Witte, K. (2006). Time spent with a male is a good indicator of mate preference
in female zebra finches. Ethology Ecology and Evolution 18, 195–204.
Woolley, S. C., and Doupe, A. J. (2008). Social context-induced song
variation affects female behavior and gene expression. PLoS Biology
6, e62. doi:10.1371/journal.pbio.0060062
Woolley, S. M. N., Hauber, M. E., and Theunissen, F. E. (2010).
Developmental experience alters information coding in auditory
midbrain and forebrain neurons. Developmental Neurobiology 70,
235–252.
Wynn, S. E., and Price, T. (1993). Male and female choice in Zebra Finches.
Auk 110, 635–638.
Zann, R. A. (1996). ‘The Zebra Finch: A Synthesis of Field and Laboratory
Studies.’ (Oxford University Press: New York.)
Zann, R. A. (1997). Vocal learning in wild and domesticated zebra finches:
signature cues for kin recognition or epiphenomena? In ‘Social Influences
on Vocal Development’. (Eds C. T. Snowdon and M. Hausberger.)
pp. 85–97. (Cambridge University Press: Cambridge, UK.)
Zann, R. A., and Cash, E. (2008). Developmental stress impairs song
complexity but learning accuracy in non-domesticated zebra finches
(Taeniopygia guttata). Behavioral Ecology and Sociobiology 62,
391–400. doi:10.1007/s00265-007-0467-2
Zeigler, H. P., and Marler, P. (Eds) (2008). ‘Neuroscience of Birdsong.’
(Cambridge University Press: New York.)
Manuscript received 24 January 2010, accepted 20 April 2010
http://www.publish.csiro.au/journals/emu