COURTSHIP BEHAVIOR
What are the functions of sexual behavior?
Hypothesis #1
Reproductive Synergism: hypothesis that reproductive behaviors evolved to coordinate hormonal, gonadal, and behavioral events.
evidence to support: reproduction is carefully regulated with successive phases dependent upon preceding events
reproduction only occurs when participants send and receive the appropriate signals
coordinates maturation and release of each individual's gametes
Hypothesis #2
Reproductive Isolationism: hypothesis that reproductive behaviors evolved to keep species from interbreeding
species-typical behaviors evolved to keep species isolated and maintain species boundaries
when inter-species mating does occur viable off-spring are not produced, or non-fertile off-spring result
Current trend is to support Reproductive Synergism hypothesis.
In general
the male produces the courtship stimulus (song, visual display, etc) then the sensory receptors in the female detect the display according to pitch. location, and pattern, these induce a patterned motor response typical of courtship (male and female produce different but complementary courtship behaviors).
Why has courtship evolved?
1) Intra-sexual selection (competition between males) where the hardiest males have survived to mate and produce offspring.
Trait examples: antlers, larynx, teeth, song, male body size and muscles, scent/scent marking, aggression, courtship display
2) Inter-sexual selection (male behavior that attracts females) most selective females have off-spring that survive.
Trait examples: bright plumage, song
SEXUAL DIMORPHISMS:
male needs brain areas necessary for producing/generating the response/behavior; the motoneurons and muscles to produce the behavior; activation of the behavior by hormones.
female needs the brain areas to detect the male's behavior, receptors for detection, and in some cases activation of the appropriate behavior &/or sensitivity for the signal produced by the male.
There are 3 ways that hormones affect sex differences in courtship behavior
1) Activation of systems to produce and receive signals (e.g., electric fish)
2) Masculinization of musculature to organize neural systems (target-derived trophic effect e.g., frog)
3) Organize brain and activate neural system (e.g., song bird)
Courtship in the Weakly Electric Fish
"The night of spawning is an electrical extravaganza, males will fight for many nights [to establish dominance] females defends spawning territories (floating plants) and the dominant male will spawn only with the dominant female."
Males fight for privilege of fertilizing eggs of dominant female
Females spawn in response to electric organ discharge of males and males fertilize eggs as she produces low amplitude chirps, the male rubs through plants fertilizing eggs.
Electric Discharges produced by modified muscle cells called electrocytes
Electric signals received by specialized receptors on fishes body called "knollenorgen" (knob or tuber-shaped organ)
EOD=electric organ discharge
Courtship:
FIRST - Find potential mate
-electric discharge frequency is sex-related
SECOND - Display EOD and induce female to oviposit
EOD must be typical of male
either testosterone or DHT will broaden EOD of adult female or juveniles so that it resembles the male (castration of male has opposite effect)
Female's knollenorgen receptors are also responsive to T or DHT as is the EOD -> activational effect, not organizational effect.
Electroreceptors are selective for certain frequencies - female's frequency is higher than male's
EOD is controlled by circulating hormones
Receptor selection frequency & EOD are sexually dimorphic
1. Testosterone or DHT will broaden EOD of females making it more like that of the male. Castration of male fish has the opposite effect.
2. Testosterone or DHT to male lowers electroreceptor frequency sensitivity (even without input from EOD).
EOD are detected at 70-100 cm "active space" - no directional information other than relative intensity on 2 sides of the body.
1) EOD used to locate conspecific of other sex (low rates of continuous discharge in all individuals)
spontaneous EOD conveys information about age & sex -> Males: low frequency; Females: high frequency; juveniles in between
rhythm can also be sex-specific
2) Used to attract mate during spawning and to stimulate spawning by female
The specialized receptors for the EOD are called electroreceptors or knollenorgen. The EOD stimulates sensory cells within the knollenorgen (modified hair cells) that stimulate the sensory nerve.
The electroreceptors are tuned to specific characteristics of electrical stimuli
1) detects own EOD to orient and navigate in the murky water of its habitat
2) detects EOD of other sex
Hormones tune the EOD (activational and transitory) -> both male and female hormones contribute
1) T an d DHT broaden the EOD of females or juveniles to that of the male -> prolong EOD pulse duration and decrease rate of pulses
2) Castration shortens EOD pulse and increases frequency
3) OVX decreases rate/ estrogen increases rate of EOD pulses
FROG SONG IN XENOPUS
Male frogs call during courtship and as an aggressive/territorial behavior
The song convey information
1) amplitude or loudness tells about the size of the animal
2) frequency tells about size and age (low freq -> older animal)
3) length of time/duration of calling tells about the health (Investment) and location of the animal
Overall temporal pattern conveys information about the species calling
The female hears the call (and estrogen produced by the female makes her more sensitive to the male's call) and moves toward the male. When she gets near him she wiggles around in the mud.
The male sees the wiggling female, locates her and attempts to mate by clasping. An unreceptive female (or other male) will "tick" and the male will release her.
Laryngeal muscles contract and relax the vocal organ - the larynx
The motorneurons innervating these muscles have been traced within the laryngeal nerve to cell bodies in the hindbrain. From there, Kelley was able to determine the other areas of the brain important for song in the frog.
Male and female xenopus differ on 2 aspects:
1) the female vocal organ is not capable of generating the mate call because her muscles cannot contract and relax fast enough. The male larynx contains more muscle fibers capable of contracting and relaxing at very rapid rate (100/sec) The female has fewer fibers and they are slower (40 contractions per sec)
2) the female brain lacks certain connections that prevent her from generating the mate call pattern. In addition, the auditory region contains estrogen receptors and the perception of mate calling is affected by estrogen in the female
Androgens act in the male during development to produce male larynx musculature and a male brain. Same mechanism as SNB in spinal cord. The temporal pattern of contractions is produced by the brain and dependent on organizational effects of hormones on the brain.
1) sex differences in peripheral vocal organ which is permanently masculinized or feminized during development
2) neural pathways also are sexually dimorphic
3) activating effects of T necessary for male specific vocal behavior and female receptive behavior in the adult.
Courtship in the SongBird
Male bird song is a sexually dimorphic behavior characterized by the male bird leaning a species-specific song/dialect
In the male song bird, song has two functions. It is a territorial defense (dominance indicator) and it serves to attract females.
The process by which male song birds learn to sing and develop local song dialects begins during the organizational period during neural development in late embryonic/early post-hatching development. During this period, hormones prepare the male brain for song behavior and inducing sexual dimorphism's in the song control system.
In seasonal breeders, song is also seasonal and serves to signal reproductive fitness. Hormones restrict song production to the time of year when the testes are active.
Many species of birds sing, but most of the work has been done on the canary and the zebra finch. They are alike in some ways, and different in some of the exact hormone-behavior relations.
Canary - Fernando Nottebohm
Nottebohm began the study of songbird behavior as an ethologist studying sexual dimorphisms in behavior, who became a neuroscientist as he followed his research topic from the observance of the behavior to the description of the underlying neural systems that mediate the phenomena.
The canary is a seasonal breeder who learns a new song every breeding season, with approximately a 40% increase in repertoire each season. Some elements of the old song are retained, but most of the song is new.
Sounds are produced by the syrinx during expiration. The expiratory muscles contract the abdominal air sacs which then functions as bellows. In the canary, the syrinx consists of two roughly symmetrical and functionally equivalent halves. The syringeal muscles modulate the tension of membranes within the syrinx to modulate the frequency and amplitude of the sounds produced. Each syringeal half is innervated by the tracheosyringeal (ts) branch of the ipsilateral hypoglossus nerve.
**SHOW PICTURE OF SYRINX AND INNERVATION/MUSCULATURE**
During song learning, a bird goes though subsong (at about 40 days old) which sounds like bird-babble: low-amplitude patterns of frequency modulation
Then at 60 days old the song begins to sound like a song, but it is highly variable - called plastic song phase.
Finally the adult song is achieved - called 'crystallized' song.
During song acquisition both testosterone and auditory feedback are necessary to acquire the song. A learned motor program does not require feedback, so a bird that has been deafened will continue to sing. A bird that has been castrated to remove testosterone, however, does not sing.
How is the syrinx controlled by the brain to activate the motor program?
Song is produced by the syrinx, which is innervated by the hypoglossal nerve, unilaterally.
Left hypoglossal -> left half of the syrinx
Right hypoglossal -> right half of the syrinx.
Are both inputs to the syrinx required for song?
In an experiment to study the role of proprioception on song production, one side of the syrinx was denervated with the expectation that this operation would interfere with the production of song, yet allow the birds to breath normally. It was arbitrarily decided that only the left ts would be cut. As expected, the birds had great difficulty singing, and in fact lost their ability to sing, but could breath fine. Then in a follow up experiment, birds arbitrarily received transection of the right ts, surprisingly, with no effect. Repeating the experiments with some birds getting left ts transections and other getting right ts transections, they found that there is left hypoglossal dominance for song production in the canary. The investigators soon realized that they had discovered the first example of a consistent right/left asymmetry in neural function in a non-human species.
The song of a canary consists of complex units called "syllables", which are repeated several times to form a "phrase". Syllables in turn consist of one o more "elements" - an element is a continuous trace in a sound-spectograph. After section of the hypoglossus, elements or syllables that are affect are replaced with silent gaps. In canaries, 90% of the song elements are contributed by the left hypoglossus, and are lost after left transection.
How does this develop?
The syrinx is virtually identical on the right and left - so the asymmetry is not at the level of the syrinx, although the musculature on the left is somewhat heavier due to greater use of the muscles. When the left ts is cut during the first 2 week after hatching the normally subordinate right assumes dominant control in song control. If the left ts is cut 14-28 days after hatching, the nerve regrows and both right and left ts contribute comparable numbers of song syllables. Thus either side can develop normal song, or the two sides can collaborate. Thus the two sides are equipotent, and it is not known why one side assumes dominance.
THE SONG BIRD BRAIN
In order to identify efferent pathways controlling song the motor neurons innervating the syringeal muscles had to be found. The hypoglossal nucleus was identified by locating the cell bodies that degenerated after transection of the ts nerve. Then by lesioning the nucleus of the hypoglossus nerve, the nuclei the send projections there could be identified by using stains that visualized degenerating neurons. In this way it was shown that the HVc, RA, Area X and ICo were part of the song pathway. Lesions of these brain regions also demonstrated their role in song control.
If males and females are compared, the female has significantly less brain space devoted to song system - proportional to the behavioral dimorphism.
HVc, RA, Area X male >female This was the first description of a gross sex difference in the size of brain regions controlling a specific sexually dimorphic behavior.
The development of HVc and A in male canaries shows as interesting relation to song ontogeny. At 15 days post-hatch, the canary brain is as large as in the adult, - RA can be seen, but HVc cannot be identified. At day 30 (still before subsong development) HVc is about 20% the adult size, and RA is 30% the adult size. By 60 day, HVc and RA are about 50% adult size, achieving adult size with the development of crystallized song.
HEMISPHERIC DOMINANCE
Destruction of the left HVc or RA has a more disruptive effect on song than comparable lesions of the right RA or HVc. Left HVc - total loss of preoperative syllables and phrase structure; right HVc loss of a few syllables, phrase structure is intact.
In spite of this - there is no noticeable difference between these structures on the right vs left!
There is plasticity in the song control system --> Lesion left HVc - lose song control for the current breeding season. However, if the bird is allowed to survive to the next breeding season - it can develop a new repertoire with the onset of the next breeding season. In other words, the right HVc is able to take over and develop song control even in adulthood. The development of this song control is still under hormonal control, as it does not emerge until the onset of the next breeding season.
TESTOSTERONE and SONG
Hormone autoradiography identifies the areas in the bird brain that contain testosterone receptors. As anticipated, it was found that the motor neurons of the ts concentrated testosterone - indicating that they had receptors for testosterone or one of its metabolites. Then it was found that RA and HVc had testosterone receptors as did a nucleus called MAN. Subsequent studies showed that MAN projected to both RA and HVc and was involved in song modulation. A total of 5 brain regions in the song system were ultimately found to have androgen receptors : ICo, HVc, MAN, RA, and nXIIts.
Testosterone treatment of ADULT female canaries over a period of 4 weeks can bring them into song. This treatment results in an increase in the size of RA and HVc by 69% and 50% respectively. The song of the testosterone treated female tends to be much simpler than that of intact males, with a range of 4-11 syllable types in T-treated females as compared with 15 - 41 syllables in 1-yr old males.
If male canaries are castrated during the first month of life and brains are examined at 12 months, they do not develop adult song during that time and HVc and RA are 45% and 53% smaller than in controls.
Male and Female differences
dendritic complexity male > females
give female T -> increases dendritic branching and size of neurons (larger cell bodies) in RA and HVc
T also increases the number of spines (presumably # synapses) on a dendrite throughout the dendritic tree.
How does T produce its effect on the song system?
Not a target-derived neurotrophic effect.
Trophic effect on neurons that increases neuronal growth and synaptic connections
ALSO
Effect of T on neural differentiation - BUT with a twist!
In an attempt to determine how RA and HVc became sexually dimorphic, Nottebohm's group did a study in which they attempted to label neurons with 3H-thymidine throughout development. Since RA and HVc keep getting bigger until day 240 post-hatch, some bird were treated very late in life. To their surprise they discovered that neurons continued to be born in the adult canary!
It turns out that in the canary, neurons are continuously being born in an area called subventricular zone. You should recall that this is the area of the brain in which neurons are born during development.
In most animals that have been studied to date (including adult humans) there remains the capacity for cells to be born in the subventricular zone throughout life. Progenitor cells in the subventricular zone differentiate into neurons and glia cells. In most animals it is only the glial cells that migrate out of the ventricular zone in adulthood, the neurons if they are born at all (and that is not clear in mammals) are simply destroyed by phagocytosis.
In the canary, the differentiation and migration of neurons and glia from the subventricular zone continues to occur into adulthood!!
At first, it was thought that only the interneurons were produced in the adult birds. More recent research has demonstrated an increase in the number of neurons that project from HVc to RA in the adult. This indicates that new projection neurons are also formed in the adult bird. Glial cells, similar to radial glia that are present during mammalian development form a pathway for the neuronal migration and axon elongation.
What is the role of hormones in this scheme?
They then gave T to adult females and discovered that the number of HVc neurons was greater in females treated with testosterone. Subsequent work demonstrated that testosterone increased neuronal SURVIVAL not differentiation. Neurons continue to be born in the adult canary brain for both males and females, but in males the neurons survive and become incorporated into the song system.
They also found that the seasonal change in size of HVc and RA is due to a hormone-dependent change in the number of neurons in these brain regions.
NEW neurons are made in the bird brain each spring. The new neurons are both interneurons and projection neurons. In addition there are new connections among old projection neurons that are established each spring - allowing new songs to be built from the old and new output connections.
The size of the song control nuclei can vary, therefore with the production of T each season.
HORMONAL INFLEUNCES ON SONG IN OTHER BIRD SPECIES
The goal of interspecies comparisons is to correlate components of song system structure with vocal behavior, and to determine the role of hormones in modulating the behavior.
For example, only male zebra finches sing, female canaries sing a little but their song is not very complex, females of the white-browed chat sing duets with males - so species can vary in the sexual dimorphic nature of song behavior.
Is the song system of the brain correlated with these species differences in the sexual dimorphic nature of song behavior?
In all species in which females are normally capable of singing, we find the same network of song control nuclei as in males. Thus only zebra finch females totally lack an Area X. As males and females become more similar in their song behavior, they also become more similar in the size of song control nuclei. The same pattern is observed for the number of neurons in these regions.
The same pattern is observed for the accumulation of hormones by thewse brain regions. the more similar the sexes are in song behavior the more likely both sexes are to have neurons that accumulate steroids.
SUMMARY
Courtship is a way for individuals of a species to identify conspecifics and induce members of the other sex to engage in mating:
In dispersed species, courtship bring males and females together.
In closely related species it serves to identify members of the same species.
Courtship also serves to allow individuals to assess the reproductive fitness and/or readiness to reproduce.
In most species, males initiate courtship and engage in showy, energetic behaviors or displays. This occurs because in most species, the resource that is most critical to reproductive success is access to females.
Male courtship signals can read for indicators of vigor or longevity, as well as paternal contributions to survival of their offspring. Females maximize their reproductive success by selecting mates of high genetic quality.
Thus, the hormonal organization and activation of the brain to produce courtship behavior (in males), and the ability to detect and choose males of high quality (females) is another important role for hormones in behavior.
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