Question--Last Lecture (Chp. 6)
Two main alternative reproductive strategies in male bluegill fish: (heritable)
•
territorial male:
–
large colorful males that defends territories and solicits females to release eggs so
that he can fertilize the eggs
– territorial males will give rise to young that are large and brightly colored
•
sneaker males that becomes a female mimic:
– sneaker males “sneak” matings when the large territorial male is preoccupied
– sneaker males are younger and smaller and possess a light body coloration
– as sneaker males age they become female mimics, their body size increases and they
develop a coloration pattern with dark vertical bars (like females)
– female mimics (large drab males) look like females and they hang around in the
vicinity of real females
– female mimics are ready to release sperm when the female releases her eggs in
response to the behavior of the territorial male
Chp 7: Hormonal Influences on Courtship Behavior
Overview:
•
Courtship tends to be a sexually dimorphic response:
– in many species, courtship is initiated largely by males
– links to female preferences and male’s comparative quality
•
Ex. Production of EODs in Weakly Electric Fish:
– fish communicate via electric organ discharges (EODs)
– gonadal steroids influence the display of the EOD and of “chirping”--the male’s
courtship response
•
Ex. Production of the “mating call’ in Xenopus (clawed frog)
– the ‘mating call’ is used to attract females to a breeding area
– gonadal steroids act to organize and activate the ‘mating call’
•
Ex. Production of “song” by song birds
– males produce song to attract females for mating
– gonadal steroids act to organize and activate both learning and production of song
Courtship As a Sexually Dimorphic Response
Courtship tends to be a sexually dimorphic response.
For example:
•
In most fish species, males do all or the majority of “chirping.”
•
In frogs like Xenopus, only males can produce the “mating call.”
•
In several bird species, only males produce song.
Why are courtship responses sexually dimorphic?
•
Trivers (1985) suggests that sex differences in courtship behavior reflect
differences in the relative investment of energy and time in reproduction.
– females spend more time and energy
– males spend less time and energy
Investment of energy & time in reproduction:
Males
Energetic
investment
in production
of gametes
Number of
gametes
produced
over a
lifetime
Females
Produce sperm, which
consist of male’s
chromosomes
surrounded by a
protein coat and
flagellum
Produce eggs, which
consist of female’s
chromosomes
and yolk, a high
energy nutritive
substance
“cheap”
“expensive”
Produce large
numbers of sperm
Produce small
numbers of eggs
Ex. humans (men),
1 ejaculation
can release
100 million sperm
Ex. humans (women),
over lifetime,
see production of
a few hundred eggs
Investment of energy & time in reproduction:
Males
Care of
offspring
Less time
and energy
is devoted
in care of
young
Females
Much greater
time and energy
is devoted
to care of
young
development
in utero
(gestation)
feeding and
caring for
young once
born or
hatched
Why is courtship largely initiated by males?
female is limited
by costs of making
and rearing young
female maximizes
her reproductive
investment
by choosing to
which males will
fertilize her eggs
males must
demonstrate
their
comparative
quality
“Good” male:
• male with high
genetic quality
(good genes)
• male that cares for
young (by feeding
or protection)
To mate with females:
• winning territorial
battles
• showing specific
courtship
responses
• possessing other
traits (e.g., colorful
plumage)
Courtship in the Weakly Electric Fish
Weakly electric fish communicate and navigate by use of electrical signals.
•
electrical signals are called electric organ discharges (EODs)
•
EOD is produced by the electric organ located in the tail
– EOD is spontaneously produced (important for navigation in murky waters and for
identification of others in environment)
– EOD is also produced in response to cues that trigger mating: rain triggers the
production of “chirping” by males (courtship response)
•
EOD is perceived by specific sensory cells called electroreceptors
– electroreceptors are concentrated in the head region
– transduce electrical stimuli into chemical stimuli to activate sensory pathways in brain
Courtship in the Weakly Electric Fish
The electric organ is involved in producing EOD:
•
neurons within the hindbrain control production of spontaneous EODs
– pacemaker nucleus-->electromotor neurons in spinal cord-->electric organ
– electric organ consists of modified muscles cells called electrocytes that produce the
EOD
•
neurons in forebrain control production of EODs in response to various cues
(e.g., EODs produced by females or to activating cues like “rain”)
– prepacemaker nucleus-->pacemaker nucleus will stimulate production of EODs
The EOD varies in “form”:
•
discharge frequency: number of pulses produced per given length of time;
frequency discharge can be low or high
•
pulse duration: the waveform may be long or short
•
there are species differences and sex differences in the form of the EOD
Courtship in the Weakly Electric Fish
•
Spontaneous EODs provide information about
sex and age of individual:
•
mature males
mature males:
– low discharge frequency (50-90 Hz)
– long pulse duration
•
mature females:
– high discharge frequency (100-150 Hz)
– short pulse duration
•
juveniles:
– intermediate values for both
mature females
Courtship in the Weakly Electric Fish
Gonadal steroids influence discharge frequency and pulse duration of EOD:
•
androgens act to broaden pulse duration and lower discharge frequency
•
estrogen acts to increase frequency discharge
Female
Male
EOD of low frequency
and long duration
castrate
male
further
decrease in
frequency
and increase
in pulse duration
[Juvenile]
EOD of high frequency
and short duration
increase in
frequency
and decrease
in duration
decrease in
frequency
administer androgens
ovariectomize
female
Courtship in the Weakly Electric Fish
Gonadal steroids mediate their effects in two ways:
•
androgens alter pulse duration by acting at electric organ
– electrocytes possess androgen receptors
– androgens act at electrocytes to increase thickness of the electrocyte membrane
– a thicker membrane can store more electrical charges that can then be released for
a longer period of time
– androgens “prolong EOD waveform” (long pulse duration) by increasing the
thickness of the electrocyte membrane
•
androgens and estrogens are believed to alter discharge frequency by acting
on groups of neurons within the brain
– androgens act to decrease discharge frequency
– estrogen acts to increase discharge frequency
Courtship in the Weakly Electric Fish
Courtship response of males is called “chirping”:
•
brief and rapid increase in EOD frequency
•
important in stimulating a female to lay eggs
Ex. Observations made by Hagedorn:
– “The night of spawning is an electrical extravaganza, males will fight for many
nights for [dominance in the mating hierarchy], the females defend spawning
territories (floating plants) and the dominant male will spawn only with the
dominant female. The female hangs almost vertically in the plants, while the male
courts her with a barrage of [electrical] “chirping” (60 to 80 chirps/minute). As
the female lays her eggs, she produces low amplitude chirps, then the male rubs
through the plants fertilizing the eggs. Peripheral, subordinate females try to
sneak their eggs into the spawning territory [often by turning off their EOD as
they rush towards the plants], only to be driven away by the dominant pair.”
Vocal Courtship in Frogs
Male frogs typically produce the majority of vocalizations.
Vocal communication provides a selective advantage in these species:
•
most frogs live in a muddy and wet environment, and they are behaviorally
active at night (nocturnal)
•
as a consequence, visual cues would not be very helpful in finding a mate
•
sounds have the advantage of traveling long distances and around obstacles, and
they do not need to be in a certain orientation for effective communication to
occur
The vocalizations serve two main functions:
•
attract females for mating--production of “mate calling”
•
defend territorial boundaries (aggressive response)
Vocal Courtship in Frogs
The “call” of the frog contains important information:
•
sound amplitude (loudness) and sound frequency (pitch)
– sound amplitude and frequency changes as the frog ages
– frogs exhibit indeterminate growth--”as they get older they get bigger”
– an old frog will have a larger vocal apparatus-->he will produce a louder sound at a
lower frequency
•
duration of call (long or short): indication of health
•
overall-pattern of the call: indicates species of male calling (viability of young)
You are “it” as a male if you are large, and old and call for a long duration!
•
females prefer to mate with large, old males that call for a long period of time:
– these males have successfully survived their environment and are healthy
– consequently, these male must possess “good genes” that will increase the
likelihood that their young will survive
Vocal Courtship in Frogs
There are two types of calls that can be made:
•
“mate calling”
– this is exclusively produced by males (courtship response)
– typically, clawed frogs are dormant during the dry season, but become active when
the rainy season starts--“rain” activate courtship response
– serves to attract a female to breeding area and to arouse the female (stimulates her to
“wiggle around in the mud”)
– mate calling will lead to mating in which the male clasps the female from behind
and then fertilizes eggs released by the female
•
ticking
– can be produced by males or females
– serves to release a female when she is not receptive
– in the mud, males can also clasp other males; consequently, males also “tick” to gain
release
Vocal Courtship in Frogs
Gonadal steroids have both organizational and activational effects on vocalizations:
•
organizational effect: androgens have a masculinizing effect on laryngeal
muscles that leads to masculinization of brain nuclei (similar to SNB--target
derived neurotrophic function)
– males have laryngeal muscles (that control the larynx) with many muscle fibers that
can contract and relax at a fast rate (100 contractions/sec)
– in contrast, females have laryngeal muscles with fewer muscle fibers that contract
and relax more slowly (40 contractions/sec)
– as a consequence, males have more motorneurons that innervate laryngeal muscles
(motorneurons within cranial nerve nuclei--IX and X)
– in addition, there are more forebrain connections to the dorsal tegmental area of the
medulla (DTAM) that projects to cranial nerve nuclei to control vocalization
– DTAM (and its connections to cranial nerve nuclei IX and X) is believed to be
responsible for producing the “mating call”
Vocal Courtship in Frogs
Comparison between males and females:
Males
forebrain
DTAM
cranial
nerve
nuclei
IX & X
laryngeal
muscles
“mate
calling”
cranial
nerve
nuclei
IX & X
laryngeal
muscles
no
“mate
calling”
Females
forebrain
DTAM
Males have more and faster laryngeal muscles, more neurons in cranial nerve
nuclei IX and X, and more connections within the brain to mediate “mate calling.”
Receptors for gonadal steroids are present at each level within brain and within
laryngeal muscles.
Vocal Courtship in Frogs
Gonadal steroids have both organizational and activational effects on vocalizations:
•
activational effect: androgens have an activational effect on the production of
“mate calling”
normal
adult
males
castrate
will show
“mate calling”
•
will not show
“mate calling”
administer
exogenous
androgens
What would happen if you gave adult females androgens?
Vocal Courtship in Frogs
Summary:
•
giving adult females androgens would not stimulate “mate calling”--why?
– the females lack the organizational effects of androgens during development that
masculinize the laryngeal muscles first and then the brain
•
androgens act early in development to organize the laryngeal muscles and brain
in a masculine fashion
•
the organizing effects of androgens then set-the-stage for androgens to activate
the brain (permissively) to show courtship behavior and mating when the
opportunity arises
Vocal Courtship in Songbirds
Song is used for communication among birds:
•
courtship responses (attracting a mate for mating)
•
aggressive responses (protecting territorial boundaries)
Species differences in the production of song:
•
in many species, the male produces all or the majority of song
– Ex. zebra finch and canary
– clear link between male’s display of song as a courtship behavior
•
in other species, both males and females can sing
– Ex. white-browed robin chat in which both males and females routinely sing in duets,
although females have a smaller song repertoire
– Ex. bay wren in which both males and females routinely sing in duets, with no sex
difference in the size of song repertoire
Vocal Courtship in Songbirds
Distinctions can be made among seasonal and nonseasonal breeders:
•
nonseasonal breeders:
– song production and mating occur throughout the year
– food and nesting materials are available throughout the year
– gonadal steroids are involved in organizing the adult male songbird brain in a
masculine fashion and play an important but permissive role in the adult
•
seasonal breeders:
– song production and mating occur at specific times of the year
– gonadal steroids are important for “activating” the display of song behavior and mating
– gonadal steroids are also important for organizing the adult male songbird brain in a
masculine fashion
– seasonal changes in gonadal steroids and the display of song behavior and mating are
reflected in seasonal changes in brain structure and connections
Vocal Courtship in Songbirds
Song:
•
definition: series of syllables, or brief sounds, arranged in a rhythmic sequence
•
a given song can last from a few seconds to minutes
•
different species of birds produce different songs (species-specificity)
A songbird must “learn” how to sing.
•
There are 3 stages to song learning and song production:
– acquisition phase (sensorimotor learning) and a production phase (motor response)
– subsong: considered “bird-babble”--male produce crude sounds that are highly
variably in structure (canary--40 days of age)--acquisition
– plastic song: bird starts to produce more polished sounds that begin to resemble a song
(canary--60 days of age)--acquisition
– crystallized song: well-defined song that is invariant in structure, can see clearly
defined notes and motifs (canary--240 days of age--8 months)--production
Vocal Courtship in Songbirds
Song learning and production require 2 main factors:
•
ability to hear (hearing songs of others and own song)
•
presence of gonadal steroids
Hearing:
•
if a bird is deafened (cannot hear) while he is acquiring song (during subsong or
plastic song), he will not be able to produce normal song
•
if a bird is deafened after he has acquired crystallized song, then he will be able to
produce normal song--this ability depends on how he learns
– age-limited learner: male goes through 3 stages of song learning and production and then
song stabilizes; deafening after production of crystallized song has no major effect
– open-ended learner: males goes through 3 stages of song learning during first breeding
season, and then repeats each phase during subsequent breeding seasons (learning new
song syllables); deafening after production of crystallized song has no effect during
current breeding season but will drastically reduce ability during subsequent seasons
Vocal Courtship in Songbirds
Gonadal steroids:
•
gonadal steroids play a role in the both the organization and activation of song
behavior
Activational effects:
•
gonadal steroids increase the production of song behavior (performance)
•
both metabolites of testosterone (estrogen and DHT) are necessary for full response
•
Ex. adult male zebra finch
adult male
zebra finch
increase in song
production
castrate
replace
testosterone
reduction in
rate of song
production
Vocal Courtship in Songbirds
Activational effects:
•
gonadal steroids also play a role in the acquisition of song behavior
•
testosterone is important for acquisition of crystallized song
•
estrogen (from nontesticular sources) is believed to be important for acquisition of
subsong and plastic song
•
Ex. swamp sparrow: males must hear song between 20-60 days after hatching, they
will produce subsong (8 mo), plastic song (10 mo), & crystallized song (12 mo)
young male
swamp sparrows
(3 weeks)
castrate
plus expose
them to song
[low T, high E]
crystallized
song
administer
exogenous
testosterone
males produce
subsong &
plastic song, but
not crystallized
song
Vocal Courtship in Songbirds
Organizational Effects:
•
gonadal steroids play a role in organizing the male brain to produce song as an adult
in response to elevated levels of these hormones
•
several brain areas involved in either sensorimotor learning or the production of song
are masculinized in the male:
– MAN - magnocellular nucleus of the anterior neostriatum
– HVc - “high vocal center”, AKA hyperstriatum ventrale, pars caudalis
– RA - robust nucleus of the aarchstriatum
– area X
•
the process of masculinization is dependent upon estrogen (aromatization of
testosterone to estrogen)
Vocal Courtship in Songbirds
Neurocircuitry:
•
Neurocircuit involved in the production of learned song:
HVc
RA
nXIIts
muscles
controlling
syrinx
production
of sounds
nXIIts: tracheosyringealis portion of the hypoglossal nucleus
syrinx: vocal production organ in birds
Vocal Courtship in Songbirds
Neurocircuitry:
•
Neurocircuit involved in the acquisition of song
– area X and MAN are important for learning song
– hearing is important for learning song
HVc
RA
nXIIts
muscles
controlling
syrinx
MAN
auditory
input
area X
thalamus
production
of sounds
Vocal Courtship in Songbirds
Neurocircuitry:
•
HVc is important for the production of learned song
– lesion HVc will inhibit production of learned song (simple sounds remain)
– lesions of RA or nXIIt will inhibit production of all sounds
•
Area X and MAN are important for acquiring or learning song
– if these areas are lesioned before crystallized song has been acquired, no crystallized song
will occur
– if these areas are lesioned after crystallized song has been acquired, crystallized song will
occur; note that this would be true only during the current breeding season of seasonal
breeders
Vocal Courtship in Songbirds
Gonadal steroids affect this neurocircuitry in distinct ways:
•
HVc, RA, MAN and area X are larger in males than in females
•
HVc, RA and MAN all concentrate gonadal steroids
– gonadal steroids act directly upon neurons within these three areas
•
area X does not appear to concentrate gonadal steroids
– it appears that neuronal input into area X from HVc is involved in masculinizing area X
– survival or increased production of neurons in HVc leads to increased synaptic contact
between neurons in these two areas
– neuron--neuron interactions provide a trophic effect (increasing cell survival)
Vocal Courtship in Songbirds
Seasonal changes in gonadal steroids and the display of song behavior and mating are
reflected in seasonal changes in brain structure and connections.
Ex. male canary:
•
in this species, the male produces all or the majority of song
•
male is an “open-ended learner”:
– male goes through song learning and production each year
– male learns new songs (e.g., adds song syllables to repertoire)
•
seasonal variations in levels of testosterone and its metabolites:
– during nonbreeding season, levels of testosterone are generally low; transient rises and
falls in steroid levels are associated with increases in cell death followed by increases in
neuronal recruitment within the brain; these changes reflect loss of some song syllables
and the addition of others
– during breeding season, levels of testosterone rise to peak values; high levels of
testosterone are important for the production of crystallized song at high rates
Vocal Courtship in Songbirds
April
A
June
M
J
J
A
S
breeding season
•
males produce
crystallized song
males engage in
mating
N
D
J
F
M
nonbreeding season
High T
levels
•
O
Low T
levels
•
•
song production decreases
form of song changes:
– crystallized song changes to subsong or
plastic song
•
song learning occurs:
– loss of song syllables
– addition of new song syllables
Vocal Courtship in Songbirds
How are seasonal changes in song production and learning mirrored by changes
occurring within the brain?
Study: Kirn et al. (1994)
•
followed changes in the number of neurons within HVc during each month of one
entire year (and after the first breeding season) in adult male canaries:
– addition of neurons to HVc : administered tritiated thymidine into HVc of male birds
during the beginning of each month and killed the birds 27 days later
– death of neurons within HVc: identifying pycnotic profiles (dying neurons)
•
discussed the relationship of these changes to seasonal changes that occur in learning
new song syllables and in the levels of gonadal steroids
Vocal Courtship in Songbirds
Neurocircuitry:
•
Neurocircuit involved in the production of learned song:
HVc
RA
nXIIts
muscles
controlling
syrinx
production
of sounds
nXIIts: tracheosyringealis portion of the hypoglossal nucleus
syrinx: vocal production organ in birds
•
•
increase in number of tritiated
thymidine labeled cells in HVc
(neuronal recruitment)
increase in new song syllables
Rise in T
April
A
Rise in T
June nonbreeding season
M
J
J
A
S
O
N
D
J
breeding season
High T
levels
•
no change in
neuronal
recruitment or
cell death
Low T
levels
Low T
levels
•
increase in pycnotic
cells in HVc (cell
death)
F
M
Vocal Courtship in Songbirds
•
Gonadal
steroids
several
processes
could
affect
leading
neuroblast
to
“neurogenesis”
“neuronal recruitment” in HVc:
– increased
neurogenesis
(more
immature
neuron
neurons are born)
– increased migration
– increased differentiation
migrate to
new location
– increased survival
•
“differentiation”
A subsequent study suggests that
gonadal steroids do not increase
mature
neuron
cell division (neurogenesis) but
rather cell survival.
survive
Vocal Courtship in Songbirds
Changes that occur in HVc leads to changes in other birdsong control regions.
HVc
•
RA
nXIIts
muscles
controlling
syrinx
production
of sounds
Following a period of cell death, as new neurons are added to HVc, we see
corresponding changes in the volume of RA:
– increase in number of synapses
– increase in dendritic length of neurons
– increase in the size of neurons
•
gonadal steroid receptors are present in both HVc and RA; the effects of
testosterone (and/or its metabolites) on size of RA presumably reflects both
direct actions on RA neurons and indirect actions via connections with HVc
Vocal Courtship in Songbirds
Gonadal steroid-mediated plasticity can also be seen in the adult female canary.
adult female
canaries
administer
exogenous
androgens
•
•
activation of song behavior
increase in size of HVc
– (90% of male)
– more neurons
•
increase in size of RA
– (50% of male)
– larger neurons with longer
dendrites and more synapses
•
Complete masculinization of brain and song behavior is thought to be dependent
upon gonadal steroids present during development and in the adult:
– although exogenous androgens can activate song behavior in adult female canaries, the
song that is produced by females is simpler in form
– neuroanatomical changes that occur with androgen treatment in adult females do not reach
the levels observed in normal adult males
Vocal Courtship in Songbirds
Bottom line for role of gonadal steroids in song behavior by male songbirds:
•
aromatization of testosterone to estrogen is important for masculinization of the
songbird brain
– HVc, RA, area X and MAN are larger in males than females
•
estrogen is also important for acquisition of song (subsong and plastic song)
•
testosterone is important for the crystallization of song, and for the activation of
singing (courtship behavior)
– these events occur seasonally in seasonal breeders
•
testosterone (and/or its metabolites) is important for the addition of neurons in HVc,
and for the formation of new connections with RA
– these neuroanatomical changes are believed to reflect alterations in the bird’s song
repertoire
– these changes can be seen yearly in males that are seasonal breeders
Vocal Courtship in Songbirds
Comparative studies of sex differences in song behavior:
•
degree of sex differences in song behavior are mirrored by differences in brain
Zebra finch
Bay Wren
only males sing
males and females
both sing
(possess similar
song repertoires)
volume of HVc:
males > females
volume of HVc:
males = females
number of steroidaccumulating cells:
males > females
number of steroidaccumulating cells:
males = females