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Proximate and ultimate causes
of bird song
 Different
species of bird (and other
organisms) sing different songs.
 How?
What proximate mechanisms
control how birds learn to sing and the
mechanics of how they sing?
 Why?
What selective advantage does
singing provide?
Gene and environment
interactions

Singing mechanism (syrinx [or voicebox],
nerves, muscles) has complex
development process. Genes are heavily
involved.
 Type of song sung also affected by
environment i.e., songs heard.
Differences between individuals in song
can result from differences in genes or
environment (or some combination).
Song dialects in White-crowned
Sparrows
Song dialects in White-crowned
Sparrows
 Peter
Marler and colleagues carried out
extensive work on songs on Whitecrowned Sparrows in San Francisco Bay
area.
 Different
songs
areas have distinctly different
Song dialects in White-crowned
Sparrows
 Were
differences due to genes or
environment?
 Birds
were hatched and reared in isolation.
Males began to sing at about 150 days of
age, but did not sing full complex song of
wild birds.
Song dialects in White-crowned
Sparrows
 Do
young birds need to be hear songs to
learn them?
 Young
birds were exposed to tapes of
singing males between 10-50 days of age.
 Began
singing at about 150 days and by
age 200 days closely mimicked song they
had heard when younger.
Song dialects in White-crowned
Sparrows
 When
developing song, sparrow must be
able to hear itself sing apparently so it can
compare its song to that it heard when
younger.
 Birds
deafened after 50 days do not
develop proper song.
Song dialects in White-crowned
Sparrows


White-crowned Sparrows are also selective
about which songs they will learn.
If exposed only to songs of another species
when young WC sparrows ultimately do not
develop a proper song.
 If exposed to songs of many species as well as
its own WC Sparrow produces a normal song.
Song dialects in White-crowned
Sparrows

Marler concluded that immature WC Sparrow
brain during critical period selectively stores
information about songs of WC Sparrows and
ignores other species. Later accesses this
information to develop it own song.
Song dialects in White-crowned
Sparrows
 In
wild WC Sparrows sometimes sing nonWC songs of other species.
 Baptista
and Petrinovich hypothesized that
being exposed to living birds rather than
tapes might cause this.
Song dialects in White-crowned
Sparrows
 Hand-reared
WC Sparrows exposed to
singing Song Sparrows and Strawberry
Finches they could hear and see learned
the other species song even if they could
hear tapes of WC song.
 Social
experience thus can have a strong
effect on WC Sparrow singing behavior.
Song dialects in White-crowned
Sparrows
 In
summary, in proximate developmental
terms W-C Sparrows are influenced when
young by their social and auditory
environment and construct a memory of
the song they should sing.
 Later
they use this model to develop their
own song.
A natural experiment in call learning:
Galahs reared by Pink Cockatoos.
Birds similar in appearance, but have
different begging, contact, and alarm calls.
Galah
Mixed clutches sometimes occur when birds
share nest holes.
Pink Cockatoos rear chicks.
Pink Cockatoo
Adopted Galahs reared in Pink Cockatoo
social environment.
As adults join Pink Cockatoo flocks.

How are calls affected?
 Galah chicks give normal Galah begging
and alarm calls, but give Pink Cockatoo
contact calls.
Sonagrams
of Galah and
Pink
Cockatoo
contact calls
Contact calls used constantly in flocks.
 Galahs learn to give a call Pink
Cockatoos will respond to.
 Pink Cockatoo social environment
overrides genetic differences between
species underlying contact call.

Neural mechanisms of song

The brain obviously plays a major role in singing
and song learning.

In most species only males sing so we would
expect there to be differences in brain structure
between males and females.

Differences could be genetic or environmental
(or both).
Neural mechanisms of song

In Zebra Finches only males sing.
 What mechanism explains this difference
between the sexes?
Neural mechanisms of song

Pre-testicular cells in male embryo produce
estrogen.
 Estrogen travels to nerve cells in the brain and is
transformed into a testosterone-like hormone.
 Complex neural system (the song system) is
then stimulated to develop
Clusters of cells called song control units form in the
brain.
Nerve connections
formed between front of
brain and syrinx
(voice box).
Higher vocal complex
Caudomedial
neostriatum
Robust nucleus
of arcopallium
Area X
You don’t need to learn all these names!
(carries signals to syrinx)
Neural mechanisms of song

Neural connections formed in male zebra finch’s
brain in first 40 days after hatching.

In females, equivalent part of brain shrinks
through cell death.
Neural mechanisms of song
 Estrogen is the crucial signal molecule for brain
development in zebra finches.

Females given estrogen within 4 days of
hatching develop song system in brain.

But, females don’t sing later unless given
testosterone implants as adults.
Neural mechanisms of song

Development of male’s brain and structures
needed to produce full song follows highly
coordinated pattern.

Genes turn on and off in various parts of the
brain in a predictable coordinated fashion.
Enzyme activity in brain.
Intensity of color correlates with gene activity
Neural mechanisms of song

Scientist’s ability to monitor gene expression in the brain
is providing insight into what genes affect the brain’s
structural changes.

For example, male Zebra Finches go through a period
when they attempt to match what they are singing to
stored memories of songs.

During the process, cells in forebrain become
progressively more responsive to male’s own song
rather than to tutor songs.
Neural mechanisms of song

As finch tries to match tutor’s song, the activity
of a gene called ZENK increases in some song
control neurons including area X in bird’s
forebrain.

Listening to itself sing causes increase in gene
activity that increases protein production, which
presumably alters neural circuits in that area of
the brain.
Neural mechanisms of song

As male’s song becomes a closer match to the
tutors ZENK gene activity falls, presumably
because when bird can sing the tutor’s song no
further alterations to the brain are needed.
High activity of ZENK gene in area X (yellow area)
How avian song control system
works

Song control systems in birds includes several
clusters of neurons (called nuclei)

Nuclei are connected together by long
extensions of neurons (axons).

Some components involved in song learning,
others in song production.
How avian song control system
works

The HVC or (higher vocal center) is a dense
collection of neurons

HVC connects to the RA (robust nucleus of the
acropallium) which then connects to the syrinx or
(voice box) via nXIIts (tracheosyringeal portion
of the hypoglossal nucleus).
Higher vocal complex
Caudomedial
neostriatum
Robust nucleus
of arcopallium
Area X
You don’t need to learn all these names!
(carries signals to syrinx)
How avian song control system
works

The connection of HVC and RA to the syrinx
suggests these brain areas control singing.
Cutting connections between RA and syrinx has
severe effects on singing.

RA in male birds is also larger than in females
consistent with a role in singing.
Difference in size of one nucleus of the song system in brain. Robust
nucleus of the Arcopallium (RA) much larger in male than female.
Male Zebra Finch (left) female (right
How avian song control system
works

Other areas of brain such as LMAN appear to be more
important in song learning.

In Zebra Finches destruction of this area in brain before
bird has learnt to sing prevents it producing a proper
song as an adult, but destruction after learning song has
little effect on the song produced.

Consistent with the idea that LMAN is involved in song
learning is that in birds that don’t learn their songs that
the LMAN is missing or reduced in size
How avian song control system
works

HVC also appears to be important in song
learning.

In species in which males learn their songs, the
larger the repertoire males of a species sing the
larger the HVC is.
How avian song control system
works

But does learning a lot of songs cause the HVC
to grow or is it necessary to have a large HVC to
learn them?

How could we distinguish between these two
possibilities?
How avian song control system
works
 Raise
two groups of birds under different
conditions (in isolation or with males to
learn from) and compare their brains.
 Male
sedge warblers reared in isolation
have HVCs indistinguishable from those of
males who learned songs from tutors.
 Supports
idea that HVC needed to learn.
Neural mechanisms of song:
Conclusions

A bird’s song is product of a complex series of
systems in the brain that regulate the learning
and production of the song.

Brain develops as the result of geneenvironment interactions in which environmental
stimuli both internal (e.g. hormonal) and external
(hearing songs) cause changes in gene activity
in certain portions of the brain, which shape the
brain’s development.
Ultimate explanations for
birdsong
 Song
learning occurs in three of 21 avian
orders (Passeriformes [songbirds, e.g.
sparrows], Trochiiformes [hummingbirds],
and Psittaciformes [parrots]).
 In
other orders songs can be complex, but
are hard-wired rather than learned.
Ultimate explanations for
birdsong

Based on the phylogenetic relationships of the
groups song learning may have evolved
independently in each group or may have been
present in the groups’ common ancestor, but
been lost in ancestors of the non-learning
orders.

Both hypotheses are equally plausible as only
three independent losses of the trait would have
been required.
Ultimate explanations for
birdsong
 However,
the song control systems in the
brains of the three groups are very similar,
which suggests song learning was most
likely derived from one common ancestor
and lost independently by several groups.
Benefits of singing
 What
fitness benefit does singing provide?
 How does having a distinct song increase
fitness?
Benefits of singing
 There
is a clear benefit in conveying
information about species membership.
 By
attracting only mates of the right
species and deterring rivals of one’s own
species energy is not wasted.
Benefits of singing
 There
is considerable evidence that
singing deters rivals.
 For
example, when territorial whitecrowned sparrows are removed, but tapes
of them singing are played, intrusions by
other males are much less frequent than
when no song is played.
Benefits of singing
 There
is also a lot of evidence that
females are attracted to singing males.
 Female
white-crowned sparrows approach
closer to and trill more in response to
playbacks of their own species rather than
another species.
But why learn to sing?
 But
it’s not necessary to learn a song to
have a species-specific song.
 Many
costs to song learning: time, energy
and special neural mechanisms. Why
then do birds learn to sing?
But why learn to sing?
 Benefits
in two main categories.
 More efficient communication with other
males.
 Greater ability to attract females.
But why learn to sing?
 Being
able to learn a local song may
enable a male to use a song that is
acoustically best suited to its acoustic
environment.
 For
example, some songs will travel better
in certain habitats than in others.
But why learn to sing?

Great Tits sing distinctly different songs in
forests versus woodlands. There is greater
difference between the songs of Great Tits in
these habitats than between Great Tits in the
same habitat in different countries.

Clearly, it is advantageous to be able to sing a
song that works well in its local environment.
Improved communication with
rivals

Being able to learn new songs or fine tune a
repertoire may allow a male to communicate
more clearly with rival males.

Copying a neighbor’s songs may demonstrate
that a male recognizes another male as an
individual and may convey information about the
singer’s competitive ability. Providing clear
information may reduce conflict between males.
Improved communication with
rivals
 Song
sparrows sing many different songs
which they learn from tutors.
 They
appear to signal different levels of
aggression when singing in response to a
neighbor’s song by how closely they
match the first male’s song.
2.22
2.21
Improved communication with
rivals

Tests using tape playbacks of the idea that the
degree of matching of a rival’s song signals the
level of aggression have supported the
hypothesis.
 Male song sparrows respond most aggressively
to tapes that type match the song they just sang
[i.e. responder sings same song], less
aggressively to tapes that repertoire match [sing
a song both birds do sing] and least
aggressively to unshared songs.
Improved communication with
rivals
 If
song matching is adaptive for males
then we would expect it to occur where
males have long-term relationships.
 Confirmed
by studies of Sedge Wrens.
Improved communication with
rivals
 In
North America male Sedge Wrens are
nomadic during the breeding season and
do not develop dialects.
 In
South America males remain on
territories year round and there dialects
and song matching occur.
Female preferences
 Some
male singing is geared at attracting
females.
 Male
Cassin’s Finches provided with a
female who is removed the next day sing
much more frequently apparently in an
attempt to lure her back.
2.23
Female preferences
 Male’s
ability to learn local songs may be
attractive to female either because it
signals that a male possesses locally
adapted genes or provides information
about the male’s quality.
Female preferences
 Study
of male White-crowned Sparrows
around Tioga Pass California found males
that sang local dialect had lower levels of
blood parasites.
 Such
males fathered more offspring than
males that sang non-local dialects which
suggests females preferred them.
Female preferences
 If
a female can use learned details of a
male’s song to assess his developmental
history she might be able to identify males
with better than average genes.
Female preferences
 In
Zebra Finches males with complex
songs have larger than average HVC’s
and HVC size is affected by genes.
 Females
who choose such males thus
provide their offspring with best available
genes.
Female preferences
 Repertoire
size of males may also indicate
physiological condition and indicate a male
that can better provision his brood.
 Great
Reed Warblers that are well fed as
nestlings have larger song repertoires than
less well provisioned nestlings.
Female preferences
 The
males with diverse repertoires deliver
more food to their offspring who grow
bigger as a result, which influences the
reproductive success of the females who
chose those males.
Female preferences
 But
why should female choice favor males
who learn complex songs?
 Perhaps
quality of vocal learning may
indicate male’s quality as a mate.
Female preferences
 Song
learning occurs when males are
developing rapidly and inferior males
(either because of poor genetics or
nutrition) may have suboptimal brain
development.

Such males may not be able to learn
complex songs and females can use
singing ability as an indicator of quality.
Female preferences
 Swamp
Sparrow study by Nowicki et al.
 During
early development some nestlings
received inadequate supplies of food.
 This
short-term deprivation resulted in
inferior brain development and reduced
bird’s ability to learn complex songs.
2.2.4
Female preferences
 Nowicki
also showed in a study of Song
Sparrows that females strongly preferred
playback tapes of songs that were more
accurate copies of the tutor’s original song
and solicited more matings.
2.25