question--last lecture (chp. 6) two main alternative reproductive strategies in male bluegill fish:...

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 BehaviorOverview:

• 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 most fish species, males do all or the majority of “chirping.”

• In frogs like Xenopus, only males can produce the “mating call.” 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:

Energeticinvestment

in productionof gametes

Produce sperm, whichconsist of male’s

chromosomessurrounded by aprotein coat and

flagellum

Produce eggs, whichconsist of female’s

chromosomes and yolk, a high energy nutritive

substance

Males Females

“cheap” “expensive”

Number ofgametesproduced

over alifetime

Produce largenumbers of sperm

Produce smallnumbers of eggs

Ex. humans (men),1 ejaculationcan release

100 million sperm

Ex. humans (women),over lifetime,

see production ofa few hundred eggs

Investment of energy & time in reproduction:

Care of offspring

Less timeand energyis devotedin care of

young

Much greatertime and energy

is devotedto care of

young

Males Females

developmentin utero

(gestation)

feeding andcaring for

young onceborn orhatched

Why is courtship largely initiated by males?

female is limitedby costs of makingand rearing young

female maximizesher reproductive

investmentby choosing to

which males willfertilize her eggs

males mustdemonstrate

theircomparative

quality

To mate with females:• winning territorial

battles• showing specific

courtship responses• possessing other

traits (e.g., colorful plumage)

“Good” male:

• male with high genetic quality (good genes)

• male that cares for young (by feeding or protection)

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


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


• Spontaneous EODs provide information about

sex and age of individual:

• 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 males

mature females


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

Male Female

EOD of low frequency and long duration

EOD of high frequencyand short duration

castratemale

increase infrequency

and decreasein duration

ovariectomizefemale

decrease infrequency

furtherdecrease infrequency

and increasein pulse duration

[Juvenile]

administer androgens


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 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)


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


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


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”


Comparison between males and females:

forebrain DTAM

cranialnervenuclei

IX & X

Males

laryngealmuscles

“matecalling”

forebrain DTAM

Females

laryngealmuscles

no“mate

calling”

cranialnervenuclei

IX & X

Males have more and faster laryngeal muscles, more neurons in cranial nervenuclei 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 withinlaryngeal muscles.


Gonadal steroids have both organizational and activational effects on vocalizations:

• activational effect: androgens have an activational effect on the production of

“mate calling”

normaladultmales

castratewill not show“mate calling”

administerexogenousandrogens

will show “mate calling”

• What would happen if you gave adult females androgens?

Vocal Courtship in FrogsSummary:

• 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 SongbirdsSong 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 SongbirdsSong:

• 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 SongbirdsSong 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 SongbirdsGonadal 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 malezebra finch

castratereduction in rate of song production

replace testosterone

increase in song production

Vocal Courtship in SongbirdsActivational 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 maleswamp sparrows

(3 weeks)

castrateplus expose them to song

[low T, high E]

males produce subsong &

plastic song, but not crystallized

song

administer exogenous

testosterone

crystallized song

Vocal Courtship in SongbirdsOrganizational 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 SongbirdsNeurocircuitry:

• Neurocircuit involved in the production of learned song:

HVc RA nXIItsmuscles

controllingsyrinx

productionof sounds

nXIIts: tracheosyringealis portion of the hypoglossal nucleussyrinx: vocal production organ in birds


• Neurocircuit involved in the acquisition of song

– area X and MAN are important for learning song

– hearing is important for learning song


controllingsyrinx

productionof sounds

auditoryinput area X thalamus

MAN


• 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 SongbirdsGonadal 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)


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


• males produce crystallized song

• males engage in mating

A M J J A S O N D J F M

April June

breeding season nonbreeding season

High T

levels

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


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


• Neurocircuit involved in the production of learned song:


controllingsyrinx

productionof sounds

nXIIts: tracheosyringealis portion of the hypoglossal nucleussyrinx: vocal production organ in birds

• no change in neuronal recruitment or cell death

A M J J A S O N D J F M

April June

breeding season

nonbreeding season

Low T

levels

High T

levels

Low T

levels

Rise in T

• increase in pycnotic cells in HVc (cell death)

• increase in number of tritiated thymidine labeled cells in HVc (neuronal recruitment)

• increase in new song syllables

Rise in T


• Gonadal steroids could affect

several processes leading to

“neuronal recruitment” in HVc:

– increased neurogenesis (more

neurons are born)

– increased migration

– increased differentiation

– increased survival

• A subsequent study suggests that

gonadal steroids do not increase

cell division (neurogenesis) but

rather cell survival.

neuroblast

immatureneuron

migrate tonew location

matureneuron

survive

“neurogenesis”

“differentiation”


Changes that occur in HVc leads to changes in other birdsong control regions.


controllingsyrinx

productionof 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


Gonadal steroid-mediated plasticity can also be seen in the adult female canary.

adult femalecanaries

administerexogenousandrogens

• 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


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


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 femalesboth sing

(possess similarsong repertoires)

volume of HVc:males > females

volume of HVc:males = females

number of steroid-accumulating cells:

males > females

number of steroid-accumulating cells:

males = females

question--last lecture (chp. 6) two main alternative reproductive strategies in male bluegill fish:...

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