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ULTIMATE MECHANISMS OF SONG LEARNING
S. Nowicki Æ W.A. Searcy Æ S. Peters
Brain development, song learning and mate choice in birds: a review
and experimental test of the ‘‘nutritional stress hypothesis’’
Received: 9 November 2001 / Revised: 3 April 2002 / Accepted: 5 September 2002 / Published online: 19 October 2002
Springer-Verlag 2002
Abstract The nutritional stress hypothesis explains how
learned features of song, such as complexity and local
dialect structure, can serve as indicators of male quality
of interest to females in mate choice. The link between
song and quality comes about because the brain struc-
tures underlying song learning largely develop during
the first few months post-hatching. During this same
period, songbirds are likely to be subject to nutritional
and other stresses. Only individuals faring well in the
face of stress are able to invest the resources in brain
development necessary to optimize song learning.
Learned features of song thus become reliable indicators
of male quality, with reliability maintained by the de-
velopmental costs of song. We review the background
and assumptions of the nutritional stress hypothesis, and
present new experimental data demons trating an effect
of nestl ing nutrition on nestling growth, brain develop-
ment, and song learning, providing support for a key
prediction of the hypothesis.
Keywords Indicator mechanism Æ Neural develop-
ment Æ Nutritional stress Æ Sexual selection Æ Song
learning
Abbreviations HVc high vocal center nucleus (formerly
nucleus hyperstriatum ventralis, pars caudalis) Æ
RA robust nucleus of the archistriatum Æ SCC
spectro-gram cross-correlation
Introduction
The development of song in male oscine birds is sup-
ported by an extraordinary set of brain mechanisms
specialized for the memorization of external song models
and for the translation of these auditory memories into
motor output. The endpoint is an equally remarkable
acoustic display, which functions, in part, in attracting
females and stimulating their courtship (Searcy and
Andersson 1986; Catchpole and Slater 1995). In the
context of mate choice, female birds show preferences
based on a variety of song features (Searcy and Yasuk-
awa 1996), some of which are the direct product of song
development. Two of the commonest preferences are for
complexity of song repertoires and for fidelity to the local
dialect, features that reflect, respectively, the quantity
and quality of learning in males. The existence of such
preference raises the question of why females should care
about male song learning. Stated another way: how do
females benefit from choosing a male that has been, by
some measure, successful in song development?
For a signaling system to be maintained by na tural
selection, both the signaler and receiver must benefit on
average from the interaction. In the case of a mating
signal such as birdsong, signalers (males) and receivers
(females) have conflicting evolutionary interests. Males,
on the one hand, are selected to produce signals that
manipulate females to the male’s advantage, which is
likely to mean that males will exaggerate their own
quality when possible. Females, on the other hand, are
selected to respond only to signals containing reliable
information that is of value to them (Dawkin s and
Krebs 1978). Theory suggests that in such cases signal-
ing systems will only be stable if the signals carry some
cost that enforces their accuracy, or ‘‘honesty’’ (Zahavi
1975; Grafen 1990a). Only if song features are costly can
they be reliable signals of something females want to
know, such as mal e quality. This leads us to rephrase the
question as follows: in what way could superior per-
formance in song development be costly?
J Comp Physiol A (2002) 188: 1003–1014
DOI 10.1007/s00359-002-0361-3
S. Nowicki (&) Æ S. Peters
Evolution, Ecology and Organismal Biology Group,
Department of Biology, Duke University,
Durham, NC 27708, USA
E-mail: snowicki@duke.edu
Tel.: +1-919-6846950
Fax: +1-919-6607293
W.A. Searcy
Department of Biology, University of Miami,
Coral Gables, FL 33124, USA
One potential answer to this question, the ‘‘nutritional
stress hypothesis’’ (Nowicki et al. 1998), explicitly links
the selective factors responsible for the evolution of song
preferences in females to the brain mechanisms that un-
derlie song development and production in males. Spe-
cifically, the hypothesis proposes that learned features of
song can serve as reliable indicators of male quality be-
cause the brain structures underlying song learning and
production develop during a period early in life when
young birds are very likely to experience developmental
stress resulting from undernutri tion. Individuals may
differ both in the magnitude of the stress they experience
and in their developmental response to a given level of
stress. Variation in brain development, the hypothesis
argues, will translate into variation in song learning
abilities among males. Better brains enable young song-
birds to learn better or more, but are more costly to build
(Catchpole 1996). Thus, the cost of song is a develop-
mental one – by choosing males based on song features
that reflect the outcome of song learning, females really
are choosing males that fared better in the face of nu-
tritional (and other) stresses experienced early in life.
Such males are likely to be phenotypically or genotypi-
cally superior, or both. In either case, females gain reli-
able information about male quality based on song.
This paper is divided into four main sections. In the
first, we briefly review current thinking about signal re-
liability and mate choice, to provide background on the
evolutionary context from which our ideas emerge.
Second, we review what is known about female prefer-
ences for male song, in order to establish which prefer-
ences can be accounted for by cu rrent theory and which
cannot. Third, we review the nutritional stress hypot h-
esis in detail, outlining previously published evidence in
support of the argument. In the fourth section, we pre-
sent new experimental data testing a key prediction of
the hypothesis: that a limited period of nutritional stress
experienced early in life will adversely affect brain
development and song learning abilities.
Indicator mechanisms and the evolution
of female preferences
An indicator is a trait that provides an index of indi-
vidual condition or viability (Andersson 1994). Any trait
that is a reliable indicator in one sex may be used by the
opposite sex to identify superior mates, and in many
cases the exaggeration of signals and ornaments associ-
ated with mating behavior is thought to be the result of
sexual sele ction acting on such indicator traits (An-
dersson 1994). The interests of signaler and receiver in
mate choice are rarely identical, however. Signalers may
benefit from dishonesty (Dawkins and Krebs 1978), i.e.,
from producing a signal that indicates a higher quality
than they actually possess. As a consequence, receivers
should be selected to respond to a signal only if the
reliability of that trait is somehow ensured (Grafen
1990a, 1990b). Theoretical modeling predicts in such
situations that indicators will be reliable only if they are
costly to produce (Zahavi 1975; Enquist 1985; Grafen
1990a; Johnstone and Grafen 1993). Signals used in
mate choice are expected generally to be indicators of
signaler quality whose reliability is maintained by pro-
duction costs, which may include the time and energy
expended during signaling, as well as costs associated
with developing the display (Vehrencamp 2000).
Female choice for male traits that serve as indicators
can evolve through either direct or indirect selection
(Kirkpatrick and Ryan 1991). Direct selection means
that females benefit from a preference by an increase in
their own survival or fecundity, for example through
obtaining a better territory or more parental care from
the male. Indirect selection means that females benefit
from their preference by an increase, not in their own
fitness, but in the fitness of their offspring. Offspring
fitness is enhanced, under indirect selection models, be-
cause the preferred males pass to their offspring superior
genes for viability or attractiveness. Clearly, the ex-
pression of an indicator trait can be influenced by both
environmental and genetic factors, and thus indicators
can potentially signal either phenotypic or genotypi c
quality. Population genetics models suggest that female
choice can evolve if females obtain only direct benefits
by mating with phenotypically superior males (Grafen
1990b; Hoelzer 1989; Heywood 1989; Price et al. 1993),
as well as if they obtain indirect benefits by mating with
genotypically superior males (Andersson 1986; Pomi-
ankowski 1987; Iwasa et al. 1991).
Work on plumage color provides an exam ple of how
the expression of indicator traits can be influenced by
both environmental and genetic factors, and thus of how
indicators can signal phenotypic quality, genotypic
quality, or both to potential mates. Hill (1990, 1991) has
shown that female house finches (Carpodacus mexicanus)
prefer to mate with males having bright red plumage
over duller males. Plumage brightness is strongly influ-
enced by the amount and type of carotenoids present in
the diet at the time of the post-winter molt, as well as by
general nutritional status, making red feather color a
reliable indicator of male nutritional status (Hill 1992,
2000). Brighter males provide better pare ntal care, which
is a direct benefit to the females that choose them as
mates (Hill 1991). Brighter males also have a higher
overwinter survival, suggesting that brightness is an in-
dicator of viability. Brightness of fathers is positively
correlated with brightness of sons, consistent with the
idea that females also obtain indirect benefits for their
offspring by mating with brighter males (Hill 1991).
Thus, females benefit directly and perhaps indirectly by
preferring to mate with males having brighter red
plumage, so selection is expected to favor the evolution
of this female preference.
Features of birdsong that influence female choice
Empirical studies have identified a wide array of song
features that affect female preferences in one species of
1004
songbird or another. Across all species, however, three
broad categories of features have the most consistent
effects: song output, song complexity, and local song
structure (Searcy and Nowicki 2000).
Song output
In severa l species of songbirds, females prefer high song
output in males, where output is measured in terms of
the length of songs or the rate at which they are sung. In
European starlings (Sturnus vulgaris), for example,
males singing long song bouts pair earlier and obtain
more mates in the field, and they are preferred by fe-
males in laboratory experiments (Eens et al. 1991). A
correlation between male song rate and success in mate
attraction has also been demonstrated for the pied fly-
catcher Ficedula hypoleuca (Gottlander 198 7; Alatalo
et al. 1990). Male blue tits (Parus caeruleus) singing long
songs are more successful in obtaining extra-pair fertil-
izations and are less likely to lose paternity to other
males (Kempenaers et al. 1997). In laboratory tests,
female zebra finches (Taenopygia guttata) prefer to
associate with males singing at higher rates (Collins et al.
1994) and female white-throated sparrows (Zonotrichia
albicollis) perform more courtship display in response to
longer songs (Wasserman and Cigliano 1991).
Song complexity
Female songbirds prefer more complex song repertoires
in a number of species. Repertoire complexity is mea-
sured as either the number of song types or, in the case
of species having more variable or continuous songs, as
the number of syllable types the male is able to sing.
Captive females perform more courtship displays in re-
sponse to larger song type repertoires in song sparrows
Melospiza melodia (Searcy and Marler 1981; Searcy
1984) and great tits Parus major (Baker et al. 1986) and
in response to larger syllable repertoires in sedge war-
blers Acrocephalus schoenobanus (Catchpole et al. 1984)
and great reed warblers A. arundinaceus (Catchpole et al.
1986). In the field, males with larg e repertoires attract
mates earlier in sedge warblers (Buchanan and Catch-
pole 1997; Catchpole 1980), attract more mates in red-
winged blackbirds Agelaius phoeniceus (Yasukawa et al.
1980) and great reed warblers (Hasselquist 1998), and
obtain more extra-pair fertilizations in great reed war-
blers (Hasselquist et al. 1996).
Local song structure
Song in songbirds typically varies geographically. In
some species, such as white-crowned sparrows Zonotri-
chia leucophrys (Marler and Tamura 1962) and corn
buntings Miliaria calandra (McGre gor 1980), extensive
variation occurs over quite small distances with distinct
boundaries between ‘‘dialect’’ regions. In other species,
such as song sparrows (Searcy et al. 1997, 2002), varia-
tion is more gradual, with differences only apparent over
broad geographic ranges. Irrespective of how songs vary
geographically, females generally prefer songs sung by
males from their own local population over songs re-
corded elsewhere, even when they are unfamiliar with
the particular songs heard in both cases. This prefere n-
tial response to local over foreign songs has been dem-
onstrated in white-crowned sparrows (Baker and
Cunningham 1985), song sparrows (Searcy et al. 1997,
2002), brown-headed cowbirds Molothrus ater (King
et al. 1980), yellowhammers Emberiza citrinella (Baker
et al. 1987), and red-winged blackbirds (Searcy 1990),
among a number of other species (Searcy 1992).
Are song features reliable indicators?
Of these three categories of preferences, the prefere nce
for high song output seems easiest to explain evolutio-
narily. Singing incurs costs in both time and energy re-
gardless of what is sung, so high song output can serve
as a reliable indicator of a male’s condition; males in
better condition can afford to devote more time and
energy to singing than can males in poorer condition.
Male condition, in turn, may correlate with direct ben-
efits a female obtains by nesting on a territory with su-
perior resources or from having more parental care
contributed by her mate. By choosing males in better
condition, females also may obtain indirect benefits in
the form of ‘‘good genes’’ for foraging ability or general
viability.
The link between male quality and either song com-
plexity or fidelity to a local dialect is much less clear.
Empirical evidence indicates that such a link must exist,
however, at lea st for song complexity. In a sample of
male song sparrows from an island population, variation
in repertoire size accounted for a staggering 50% of the
variation in lifetime reproductive succe ss, with repertoire
size significantly correlated with both years of territory
tenure and annual reproductive success (Hiebert et al.
1989). These relationships are not explained by reper-
toire size increasing with age; male song sparrows re-
corded in successive years show no change in the number
of song types they produce (Searcy et al. 1985). Instead,
the implication is that males with larger repertoires are
of higher phenotypic quality at any given age. Strong
correlations between repertoire size and fitness measures
also have been found in great reed warblers (Hasselquist
et al. 1996; Hasselquist 1998) and great tits (McGregor
et al. 1981; Lambrechts and Dhondt 1986). Song rep-
ertoire size thus appears to be an indicator of male
quality. The problem with this conclusion, however, is
that singing multiple song or syllable types seems to
entail no additional time or energy costs over producing
single types so it is not clear how the reliability of this
indicator is enforced. If anything, singing different
song types may decrease exhaustion to the extent that
1005
different types use different patterns of neuromuscular
activity (Lambrechts and Dhondt 1988).
The ability to produce songs with an acoustic struc-
ture appropriate for a given locality also seemingly re-
quires little in the way of additional costs, making the
production of local song an equally dubious candidate
as a reliable indicator trait. A long-standing alternative
hypothesis for the evolution of local song preferences is
that females benefit by mating with locally born males
by obtaining locally adapted genes to pass on to their
offspring (Nottebohm 1969, 1972; Baker and Cunning-
ham 1985). Local genetic adaptation, however, has
never been demonstrated for birds on the small geo-
graphic scales at which song variation often occurs.
Moreover, females in some species seem to prefer local
song even when males learn the details of song after
dispersal so that song does not reveal natal origin (Baker
et al. 1981; Baptista and Morton 1988). In song spar-
rows, females discriminate against foreign songs over
relatively short distances, but the distances that song
sparrows disperse are even shorter, making it unlikely
that females ever encounter foreign males whose songs
are discriminably different from local ones (Searcy et al.
2002). The genetic adaptation hypothesis thus also
seems doubtful as an explanation for the evolution of
female preferences for local song, and we are again left
with the question of how local song structure could
signal some aspect of male quality that is of interest to
females.
The nutritional stress hypothesis
According to the nutritional stress hypothesis, the reli-
ability of song as an indicator of male quality is main-
tained by developmental costs associated with song
learning and production. The acquisition and produc-
tion of song are mediated by a well-described series of
brain nuclei, collectively referred to as the ‘‘song system’’
(for review see Mooney 1999). Song system nuclei and
the connections between them develop late relative to
other parts of the nervous system (Alverez-Buylla et al.
1994; DeVoogd 1994). In the zebra finch, where the
process has been best studied, much of this development
occurs in the period 10–50 days post-hatching (e.g.,
Bottjer et al. 1985; Konishi and Akutagawa 1985;
Nordeen and Nordeen 1988; Johnson and Bottjer 1992;
Mooney and Rao 1994; see Nowicki et al. 1998 for re-
view). For example, area X of the avian striatum (area
X), a nucle us known to be important during song
learning, increases in size between 20 and 55 days, while
the high vocal center (HVc) and robust nucleus of the
archistriatum (RA), areas important for both learning
and production, increase in size betwe en 10 and 50 days
(Bottjer et al. 1985; Konishi and Akutagawa 1985;
Nordeen and Nordeen 1988). Song memorization in
zebra finches occurs at about the same time, from 25 to
65 days post-hatch (Slater et al. 1988). Functional con-
nections between song system nuclei also continue to
form during this period of post-hatch development. For
example, the projection from HVc to RA, a pathway
critical for both song learning an d production, forms
between 15 and 30 days of age in zebra finches, but the
projecting neurons stop at the border of RA until 30 to
35 days when they rapidly invade the nucleus (Mooney
and Rao 1994).
Zebra finches, the species most commonly used in
studies of the song system, reach sexual maturity and
complete song development within 90 days of hatching,
much sooner than is typical for songbirds. Thus,
although the timing of many post-hatch developmental
events (such as appearance of feathers, body size in-
crease, and time to fledging) are comparable to other
species, some events in neural development may be
compressed in zebra finches relative to other songbirds.
The comparatively few studies done on other species,
however, support the general conclusion that significant
events in the development of the song system occur after
hatching, during the period when young birds are likely
to experience nutritional stress in the field. In canaries
(Serinus canaria), RA doubles in size between days 30
and 60, while HVc grows at an even faster rate during
this interval (Nottebohm et al. 1986). Nottebohm et al.
(1986) observed continued HVc growth for up to
7 months, but later work by Alvarez-Buylla et al. (1992)
suggests that HVc growth in canaries is complete by
4 months post-hatch. A single study by Nordeen et al.
(1989) has examined song system development in swamp
sparrows (Melospiza georgiana), a more typical songbird
and the subject of our first nutritional stress manipula-
tion experiment (see below). Nordeen et al. (1989) found
the timing of song system development in swamp spar-
rows to be remarkably similar to that observed in zebra
finches, with the majority of growth of HVc, RA and
Area X completed by 61 days post-hatch.
These major events in the development of the song
system coincide with a period early in life when birds are
very likely to experience nutritional stress (Nowicki et al.
1998). Being altricial, young songbirds are completely
dependent on their parents for food between hatching
and fledging, and this dependence may continue for
some time after leaving the nest. Growth is extremely
rapid at this time, with nestlings reaching an average of
90% of their adult weight within 10 days (Ricklefs
1968), and energy requirements are correspondingly
high (Ricklefs 1974). Both growth rates and survival
rates are related to food abundance and level of provi-
sioning by parents, and starvation is common (Ricklefs
1983; O’Connor 1984). The potential for nutritional
stress may be even greater during the first few weeks of
independence, after parents stop feeding their fledglings.
Yellow-eyed juncos (Junco phaeonotus), for example,
become independent at about 5 weeks post-hatching, at
which time their foraging skills are still poor (Sullivan
1988). During the next 2 weeks the young juncos must
forage more than 90% of daylight hours in order to
maintain a positive energy balance; nonetheless about
40% of young die during this brief interval (Weathers
1006
and Sullivan 1989). Similar patterns of post-fledging
mortality have been observed in many songbirds, with
survival tied to the ability to obtain adequate nutrition
during this period as well as to energy stores accumu-
lated earlier when the young still received parental care
(Lack 1966; Ringsby et al. 1998).
The effects of early nutritional stress on brain devel-
opment are not well studied in birds, but significant
deleterious effects have been described in mammals
(Dobbing 1981; Smart 1986; Levitsky and Strupp 1995).
Particularly relevant are studies of the mammalian hip-
pocampus, which like the song system is closely tied to
specific behavioral abilities, in this case involving spatial
learning and memory (Jacobs 1995). In rats, poor nu-
trition early in life causes permanent reductions in cell
size, cell number, and dendritic branching in the hip-
pocampus (Levitsky and Strupp 1995; Castro and Rudy
1987). These anatomical effects are associated with
physiological abnormalities and with reduced perfor-
mance of adults on spatial memory tasks (Jordan et al.
1981; Goodlet et al. 1986). Development may be more
buffered against nutritional deprivation in birds than in
mammals (Schew and Ricklefs 1998), but the vertebrate
brain in general is susceptible to the effects of stress
(Dobbing 1981) and the avian brain in specific may be
particularly vulnerable to undernutrition because of its
relatively rapid development (Schew and Ricklefs 1998) .
The key question, which we have begun to address ex-
perimentally (see below), is whether a limited period of
stress incurred early on will have effects that last through
development and into adulthood. This question is es-
pecially relevant in the case of song learning, where
growth (or regrowth) of the song system, and memori-
zation and motor development of song, all may continue
beyond the period when nutritional stress is most likely
to be experienced. Lasting effects of early stress on
neural development are known to occur in mammals
(Dobbing 1981), and can be expected in general when-
ever there are critical periods in development.
Stressors other than undernutrition also may affect
the development of the song system. Parasites attack
young birds of most species, with a variety of detri-
mental effects (Loye and Zuk 1991; Clayton and Moore
1997). In some respects, the effects are parallel to those
of undernutrition, in that parasites can potentially drain
away resources from the host and cause the host to
mount energetically costly defenses (Sheldon and Ver-
hulst 1996). Indeed, in a recent study of sedge warblers,
Buchanan et al. (1999) found a negative relationship
between parasite load and aspects of song, including
repertoire size, consistent with the hypothesis that par-
asite-induced stress lowers condition in males which in
turn affects their singing behavior. von Schantz et al.
(1999) suggest that oxidative stress may be a critical
common denominator linking the expression of sexu al
ornaments to an individual’s condition. Oxidative stress
is damage on a cellular level that results from the pro-
duction of free radicals and reactive metabolites by
activated immune and detoxification systems; such stress
has been shown to have an adverse affect on neurogen-
esis in vertebrates (e.g., Saito et al. 1997). Thus, a variety
of other stressors may act synergistically with under-
nutrition to degrade song system development and song
learning.
If early nutritional stress does have a negative effect
on the development of the song system, then both song
learning and the songs subsequently produced by birds
as adul ts would in turn be adversely affected. This
conclusion seems likely given what is known of the re-
lationship between structure and the function of song
system nuclei, especially HVc and RA, which have been
most studied in this regard (Brenowitz and Kroodsma
1996). The sizes of both these nuclei are known to cor-
relate with adult song repertoire size across species
(DeVoogd et al. 1993; Sze
´
kely et al. 1996), between
populations of a single species (Canady et al. 1984), and
among individuals (Airey et al. 2000). Differences in the
size of song nuclei between birds with different reper-
toire sizes reflect differences not only in number of
neurons but also in the size of individual neurons
(Brenowitz and Kroodsma 1996).
The structure of the song system also is likely to be
important in determining the accuracy with which local
song structure is copied during song development,
though here the evidence is scantier. In canaries and
song sparrows, RA and HVc vary in size seasonally, and
the strongest behavior al correlate of this variation is
song stereotypy: song tends to be stereotyped when
brain nuclei are large and variable when nuclei are small
(Nottebohm 1981; Nottebohm et al. 1986; Smith et al.
1997). In song sparrows these seasonal changes can be
observed down to the level of the smallest subunits of
song (notes), whose form is more stereotypic in the
spring when HVc and RA are large, than in the fall when
these nuclei are smaller (Smith et al. 1997). These results
suggest that structural differences in song system nuclei
may influence the ability of males to adhere to the kinds
of small structural differences typical of geographic
differences in song. If so, then female preferences for
local song dialects may be explained in the same terms as
preferences for larger repertoires, both features serving
as honest signals of male quality.
Neither the size of song system nuclei nor the other
structural measurements that have been made, such as
synaptic density, necessarily reflect all the relevant neu-
ral underpinnings of song learning and production
(Bolhuis and Macphail 2001; Gil and Gahr 2002).
Nevertheless, these measurements can provide useful
yardsticks of the quality of neural development. The
important point is that variation in the development of
the song system is likely to result in variation among
individuals in thei r learning abilities.
A key prediction of the nutritional stress hypothesis is
that variation in the growth or condition of individuals
as nestlings or young fledglings should be reflected in
their subsequent adult song production, in features that
are used by females in mate choice. Doutrelant et al.
(2000) provided a first field test of this prediction by
1007
examining the relationship between song repertoire size
and adult tarsus length in blue tits. In this species, tarsus
length has been shown to reflect the level of nutrition
received early in life and also to correlate with juvenile
survival (Merila
¨
and Wiggins 1995). Thus, tarsus length
can be used as a convenient proxy for the relative con-
dition of individuals as nestlings or young fledglings.
Doutrelant et al. (2000) found a positive correlation
between repertoire size and tarsus length, consistent with
idea that repertoire size reflects early nutrition.
Using data from a long-term study of great reed
warblers (Bensch et al. 1998; Hasselquist 1998), Nowicki
et al. (2000) offered a more direct field test of the pre-
diction that variation in the condition of nestling males
should be reflected in their adult song behavior. Syllable
repertoire size is known to influence female mate choice
in great reed warblers (Catchpole et al. 1986; Hasselquist
1998) and also to correlate with potential benefits fe-
males receive based on that choice (Hasselquist et al.
1996; Hasselquist 1998), suggesting this feature of song
as a likely indicator of male quality in this species.
Nowicki and his colleagues used two measures as esti-
mates of nestling growth and developmental condition,
body mass and the length of the innermost primary wing
feather, and asked how well these measures predict the
size of individual male’s song repertoires as adults in
their first year.
Each nestling could be measured only once because
of the increased risk of predation associated with dis-
turbing nests. Single point measurements of body mass
are notoriously inaccurate measures of nestling growth,
however, largely because wei ght gain in songbirds is
non-linear (Ricklefs 1984). In spite of this limitation,
Nowicki et al. (2000) found a positive relationship be-
tween nestling body mass and first-year repertoire size,
with the regression closely approaching significance.
Feather growth rate is more linear than weight gain, so
single point measurements are a more accurate measure
of growth and development than single point body mass
measurements (Ricklefs 1984; Quinney et al. 1986).
Feather growth also has been shown to reflect nutri-
tional condition during nestling de velopment in a
number of species (Price 1985; Quinney et al. 1986).
Nowicki and his colleagues found a statistically signifi-
cant positive relationship between adult repertoire size
and nestling feather length (Fig. 1). This relationship
suggests that a female great reed warbler choosing a
male with a large song repertoire obtains a mate that
fared well in post-hatch development, as predicted by
the nutritional stress hypothesis.
An experimental test of the nutritional stress hypothesis
Observing a correlation between nestling growth and
adult song behavior in the field shows that a relationship
between nestling condition and adult song can occur
within the naturally occurring range of variation for
both variables. To demonstrate a causal relationship
between nutritional stress and song, however, an ex-
periment is required, one that is more practical in the
laboratory than in the field. As a first experimental test
of the nutritional stress hypothesis, we compared brain
development and song development in two groups of
swamp sparrows hand-reared in the laboratory: a con-
trol group raised with unlimited food and an experi-
mental group exposed to a period of nutritional stress at
approximately the same time as such stress wou ld be
incurred in the field.
Materials and methods
We collected nestling swamp sparrows at 3–7 days post-hatch, and
assigned them either to the control group (n=9) or to the experi-
mental group (n=7). All subjects were housed in a single, large
sound isolation room and raised under identical conditions except
for their feeding regimes. Siblings were kept together until 20 days,
first in their nests and then in large cages. After 20 days, individuals
were housed singly in cages. We tutored all birds with the same set
of recorded swamp sparrow songs (16 song types from 10 males;
see for example Fig. 2), beginning at about 20 days and continuing
for 12 weeks, a period that brackets the memorization phase of
learning in this species (Marler and Peters 1988). We chose training
songs that were quite distinct from each other to ensure we could
unambiguously identify which songs had served as models for
learning.
From the time they were collected to when individuals were
feeding completely independently (about 28 days of age), we hand-
fed the birds a standard hand-rearing diet (see Marler and Peters
1988) by syringe, keeping track of the volume to the nearest 0.1 ml
that each individual ate at each feeding. Birds in the control group
were fed until sated. We then fed each bird in the experimental
group 70% of the volume received on average by the controls for
that feeding. Birds in both groups remained healthy throughout,
although the difference in amount of food received had a pro-
nounced effect on individual growth rates, as measured by daily
Fig. 1 Relationship between nestling primary feather growth and
1st-year repertoire size of male great reed warblers. Because
individuals were not all measured at exactly the same time relative
to hatching, feather length measurements were adjusted to account
for the time offset from a standard measurement time, based on a
regression of feather growth over time measured for all male chicks
hatched in the population between 1987 and 1999. n=38,
r
2
=0.127, P=0.028. Reprinted from Nowicki et al. (2000)
1008
weights (Fig. 3). Beginning at 14 days of age, birds were provided
with a variety of foods (such as seed and mealworms) so that they
could learn to feed themselves; from this point on, the disparity in
weight between the two groups diminished and the mean weights of
the two groups ceased to differ statistically by 21 days of age. We
limited the stress that was experienced by the experimental group to
a short period because this timing corresponds to when such stress
is most likely to occur in the field. The nutritional stress hypothesis
specifically predicts that even such a limited exposure will have
lasting effects on brain development, song learning and adult song
production.
All birds were recorded in individual sound isolation chambers.
To document song development, we began recording a subset of
the birds (four control, four experimental) on a weekly basis be-
ginning at about 250 days of age. All birds were recorded inten-
sively at about 1 year of age to document their crystallized song
repertoires. One bird in the experimental group only sang spo-
radically. Because we did not record a sufficient number of songs
from this individual, we did not include him in our behavioral
analyses. Spectrograms of adult songs were compared to tutor
models to determine which songs had been copied from which
models. We used as a quantitative measure of copy accuracy the
average pairwise spectrographic cross-correlation (SCC) value
calculated for ten different renditions of each copy syllable against
the training song syllable that had served as a model (Signal v 3.0
sound analysis software, Engineering Design, Belmont, MA; sam-
ple rate=25 kpts/s, 128-pt FFT; see Clark et al. 1987 for more
background on SCC).
At approximately 14 months of age, all birds were perfused and
their brains removed using standard methods (e.g., Kirn et al. 1989;
Burek et al. 1995). To determine the relative volume of brain nuclei,
40-lm brain sections were cut on a freezing microtome, mounted,
and then stained with cresyl violet, again using standard tech-
niques. The Nissl-defined borders of the nuclei HVc and RA were
drawn from alternate sections with the aid of a camera lucida; the
outline of the telencephalon was drawn from these same sections
using a Bausch and Lomb slide projector set to 10· magnification.
Areas were measured from these drawings using NIH Image or
Scion Image software. We calculated volumes by multiplying the
area of each section by 80 lm (e.g., 2 lm·40 lm, because only
every second section was measured) and summing the results.
Results
The most striking difference in the adult song behavior
of the two treatment groups is that the experimental
birds produced significantly less accurate copies of the
model songs from which they learned, as measured by
SCC (Fig. 4). The two groups did not differ in song
complexity, as measured by song repertoire size (exper-
imental=2.2±0.8 versus control=2.1±0.3; mean±
SE). Swamp sparrows, however, have small song rep-
ertoires with little variation among males in a popula-
tion (a range of two to four song types; see for example
Fig. 2), so it is not surprising that we did not find an
effect on repertoire size in this species. The groups did
differ in the timing of song development, with the ex-
perimental group beginning to sing subsong earlier
(270±10 versus 293±6 days old, Mann-Whitney
U=12, P=0.032) and remaining in the subsong and
Fig. 2 Sonograms of a typical swamp sparrow male’s song
repertoire. Each song type is a trill of repeated ‘‘syllables,’’ which
are in turn are composed of a series of two or more distinctive note
types
Fig. 3 Weight gain in control (filled circles) and experimental (open
circles) swamp sparrows. The means±SE shown for days 4–8 are
based on nest averages because birds within nests were not yet
individually marked during this period; means and standard errors
from days 9–28 are based on individual measurements. The weight
loss in both groups beginning at 9 days is typical for individuals
after fledging (Ricklefs 1983)
Fig. 4 Effect of early nutritional stress in young swamp sparrows
on copy quality of learned song notes, as measured by spectrogram
cross-correlation (SCC) of individuals’ learned notes to the tutor
models from which these notes were copied (Mann-Whitney
U=47, P=0.018, n=9 control, 6 experimental). One experimental
bird was incompletely recorded and thus not used in the behavioral
analysis, as explained in the text
1009
early plastic stages longer (subsong: 22±6 versus
9±4 days, Mann-Whitney U=12, P=0.030; early
plastic song: 29±4 versus 18±4 days, Mann-Whitney
U=12, P=0.030). Both groups crystallized their songs
at approximately the same age, however (339±8 versus
347±9 days).
We also found a significant effect of early nutritional
stress on adult brain structure: the volumes of both HVc
and RA were significantly smaller in nutritionally-
stressed birds than in controls (Fig. 5A, B). These dif-
ferences in the size of song system nuclei reflect an
overall difference in the size of the telencephalon, which
was significantly smaller for the stressed group
(Fig. 5C). To determine whether song system nuclei
were affected disproportionately by stress, beyond the
overall effect on brain size we observed, we compared
the ratios of nuclear volumes to telecephalon volume
between the two groups. The HVc/telencephalon ratios
did not differ between the two groups (experimental=
1.6·10
–3
±0.1·10
–3
versus control=1.8·10
–3
±0.2·10
–3
;
mean±SE), but the RA/telencephalon ratio was signif-
icantly smaller for the experimental group (0.56·10
–3
±
0.04·10
–3
versus 0.70·10
–3
±0.04·10
–3
; Mann-Whitney
U=47.0, P=0.028).
Discussion
Our results demonstrate that even a relatively brief pe-
riod of undernutrition experienced early in life can affect
the outcome of song learning (Fig. 4), directly support-
ing a key prediction of the nutritional stress hypothesis.
More specifically, the effect we observed is consistent
with the idea that not only repertoire size (i.e., the
quantity of what is learned) but also the ability to copy
precisely local song material (i.e., the quality of what is
learned) can serve as an indicator of male developmental
condition in some cases. We do not know yet how
variation in the quality of song learning might influence
mate choice in female swamp sparrows, but two lines of
evidence suggest it would have a strong effect . First,
swamp sparrows are particularly sensitive to the acou stic
fine structure of the notes that comprise their songs, as
adult males responding to perceptual tests (Nelson and
Marler 1989), as young birds in learning experiments
(Marler and Peters 1989), and most importantly as adult
females responding in a copulation solicitation assay
(Balaban 1988). Second , we recently have demonstrated
that in song sparrows, closely related congeners of
swamp sparrows, females respond preferentially to ac-
curate copies of song, across a range of copy accuracy
similar to that we observe d in swamp sparrows (Nowicki
et al. 2002).
Our results further show that developmental stress
experienced early in life can have a lasting effect on
brain structure (Fig. 5), thus providing critical evi-
dence that the link between our nutritional manipu-
lation and the effect on song learning we observ ed
does indeed involve brain development. The effect of
stress on brain development is not limited to the song
system, as shown by a significant difference in the
overall size of the telencephalon between experimental
and control birds. However, it is not necessary that
stress specifically affects development of the song
system for song learning to serve as an indicator of
male quality. As long as variation in brain develop-
ment correlates with phenotypic or genetic factors that
will benefit the female or her offspring, selection
should favor a preference for song features that reflect
such variation.
Fig. 5A–C Effects of early nutritional stress on volume of brain
areas in adults. A High vocal center nucleus (HVc): Mann-Whitney
U=47.0, P=0.028; B Robust nucleus of the archistriatum (RA):
Mann-Whitney U=50.0, P=0.011; C Telencephalon: Mann-
Whitney U=47.0, P=0.028. n=8 control, 7 experimental birds
in all cases. Volume data were averaged across left and right
hemispheres for each individual in the analysis. One control bird
was not included in the neuroanatomical analysis because it was
poorly perfused
1010
At least one region of the song system, nucleus RA,
appears to be affected disproportionately by early stress.
This finding is significant in light of data from both
microstimulation and chronic recording studies that
suggest RA may be responsible for specifying the
acoustic fine-structure of individual note or syllable
types, while HVc and other areas upstream in the song
system are responsible for the temporal patterning of
those elements (Vu et al. 1994; Yu and Margoliash
1996). Thus, the observed effects of stress on the quality
of learned song notes (Fig. 4) occurred on the level of
song organization thought to be controlled by RA,
strengthening our interpretation that the effect of de-
velopmental stress on learning is causally related to
variation in brain development. If it proves to be the
case across different species that RA is generally more
vulnerable to the effects of early stress, then this obser-
vation also suggests that a male’s ability to learn and
reproduce specific phonological features accurately may
be an especially reliable indicator of early development,
and thus of particular interest to females in the context
of mate choice.
Conclusions
Data from both the laboratory and the field are begin-
ning to provide empirical support for the nutritional
stress hypothesis. The condition of young blue tits and
great reed warblers in the field has been shown to cor-
relate with the size of their adult song repertoires, a
feature of song known to be subject to sexual selection
by female choice (Doutrelant et al. 2000; Nowicki et al.
2000). In the laboratory, we have be en able to demon-
strate a causal effect of early nutritional stress on brain
development and song learning in swamp sparrows. We
did not observe an effect on repertoire size in this spe-
cies. Instead we observed an effect on learning accuracy
that may be related to an individual’s ability to copy
precisely features of a local dialect. We know that fe-
males of many species generally prefer males singing
their local dialect; we suggest this preference reflects fe-
male choice for an accurate indicator of male quality,
the same as preferences for larger song repertoires.
We are now rep eating our early nutrition experiment
using song sparrows, a species that has considerably
greater variance among males in measures of repe rtoire
size (Sea rcy 1984) and that also is sensitive to geographic
variation in song structure (Searcy et al. 2002). We ex-
pect this work will enable us to look more carefully at
how early developmental stress affects both these song
features, and to ask how both these effects may influence
female choice separately or together. It also is necessary
to look in more detail at the brain, to determine if fea-
tures of the song system other than nucleus size, such as
cell size or density, synaptic density or neurophysiolog-
ical properties, are sensitive to the effects of early stress.
Finally, we are interested in knowing which aspects of
male phenotype other than the song system are affected
by developmental stress, including other aspects of brain
function, as this information may lead to insight into
specific mechanisms through which females benefit by
their choice of males based on song.
Signal reliability is a general problem in the context
of mate choice. Why should a male signal his quality
honestly when he would benefit from exaggerating it?
The broad outline of the mechanism by which reliability
is maintained has been apparent for some time: indica-
tors can be honest when they are costly, because the cost
to high quality males will be relatively lower than for
low quality males. But this general mechanism begs the
question of what the costs are and how and when they
affect the signal. The nutritional stress hypothesis helps
to answer this question for one mating signal, bird song,
for which the costs have been particularly enigmatic. To
the extent that this hypothesis continues to receive em-
pirical support, bird song may transform from an enig-
matic example of a sexually selected trait to a
particularly informative model system, given the wealth
of detailed information available about the neural
mechanisms responsible for the development and pro-
duction of this trait.
Acknowledgements We thank Martin Beebee, Staffan Bensch,
Dennis Hasselquist, Melissa Hughes, Peter Narins, Jeff Podos,
Torbjo
¨
rn von Schantz, R. Haven Wiley and an anonymous re-
viewer for helpful discussions of this material and the manuscript,
and Bill Hoese and Rich Mooney for help with our neuroana-
tomical work. Supported by the National Science Foundation
through grants IBN-9408360 to S.N. and IBN-9523635 to W.A.S.
All work reported herein complies with the ‘‘Principles of Animal
Care,’’ publication No. 86-23 revised 1985, of the National Insti-
tutes of Health and with local and U.S. federal laws, and was ap-
proved by the Duke University Animal Care and Use Committee.
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