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Chapter 6: Diversity of Hormone-Behavior Relations in Reproductive Behavior red-sided garter snakes and parthenogenetic whiptail lizards Chapter 7: Hormonal Influences on Courtship Behaviors weakly electric fish, clawed frogs, and songbirds

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overview
Chapter 6: Diversity of Hormone-Behavior Relations in Reproductive Behavior

red-sided garter snakes and parthenogenetic whiptail lizards

Chapter 7: Hormonal Influences on Courtship Behaviors

weakly electric fish, clawed frogs, and songbirds

Chapter 8: Hormone-Behavior Relations in the Regulation of Parental Behavior

rat (as a model system)--species comparisons

ring dove

Chapter 9: Hormones and Aggressive Behavior

rat and other rodents (as a model system)--species comparisons

Chapter 10: Neuroendocrinology of the Stress Response

effects of acute and chronic stress--metabolism, cardiovascular regulation, digestion, growth, reproduction, immune system, analgesia, learning and memory

Overview
chp 6 diversity of hormone behavior relations
Overview:

variations in reproductive strategies:

different modes of reproduction

different reproductive patterns: associated versus dissociated

why?

1) function of sex behavior, 2) distinction between natural selection and sexual selection, and 3) nature of constraints on reproduction

additional issues of mate compatability, alternative life-history strategies

different cues may activate and/or coordinate sex behavior in different species:chemical signals, environmental signals, social stimuli

red-sided garter snake--example of a dissociated reproductive pattern

parthenogenetic whiptail lizard--example of an associated reproductive pattern

steroid-mediated activation of female-like and male-like pseudosexual behavior

Chp 6: Diversity of Hormone-Behavior Relations
different modes of reproduction
placement of testes and ovaries:

gonochoristic: separate male and female individuals; males have testes and produce sperm, females have ovaries and produce eggs

hermaphroditic: individuals have both ovaries and testes

parthenogenetic: all individuals have ovaries

development of fetus:

viviparity: young develop within the body and are born live; there is an exchange of nutrients and waste products between mother and fetus

oviparity: refers to the laying of eggs, from just a few eggs to thousands of eggs; eggs may have a protective shell covering; young develop apart from the mother

fertilization:

internal

external

Different Modes of Reproduction
reproductive patterns
Two distinct associated reproductive patterns:

associated reproductive pattern

mating behavior occurs when gonadal activity takes place

gonadal activity: development of eggs and sperm and increased sex steroid hormone secretion

Ex: rats, hamsters, primates, whiptail lizards

dissociated reproductive pattern

mating behavior and gonadal activity occur at different times

Ex: red-sided garter snake

Reproductive Patterns
why do such differences exist in reproductive strategies
What is the function of sex behavior?

reproduction can be viewed as the single most important element in an individual’s life--it is the means by which we pass on our genes to future generations

sex behavior tends to be highly ritualized, stereotyped and characteristic of a species; as a consequence, sex behavior can be viewed as either synergizing or isolating reproductive activities

reproductive synergism: sex behavior evolved to coordinate hormonal, gonadal, and behavioral events (Ex. estrogen and progesterone in coupling behavioral estrus with ovulation in the female rat)

reproductive isolation: sex behavior evolved to prevent interbreeding or to maintain species boundaries (mating usually does occur within a species)

Why do such differences exist in reproductive strategies?
why do such differences exist in reproductive strategies1
Role of evolutionary forces:

evolutionary forces can interact often in opposing ways to lead to the development of specific traits--such as behaviors shown during courtship or other features like the coloration of males

two primary forces driving the evolution of various traits:

natural selection: development of traits that are adaptational responses to changes in the environment; animals that “survive” possess traits that are adaptive to their environment

sexual selection: development of traits that arise from interactions among individuals that compete for mating opportunities

Why do such differences exist in reproductive strategies?
why do such differences exist in reproductive strategies2
Ex. Development of feathers that cover a bird--”plumage”

how does natural selection and sexual selection affect development of a bird’s plumage?

Why do such differences exist in reproductive strategies?

bird’s

plumage

natural selection

sexual selection

drab

plumage

showy

plumage

bird would be harder

to see and less likely

to be killed by predation

female birds often choose

to mate with males the

have a showier plumage

“adaptive to be drab”

“drab may be lonely”

why do such differences exist in reproductive strategies3
Reproductive constraints:

environmental constraints:

environmental conditions that influence when reproductive activity occurs--availability of food, nesting materials, or predation

events are often “signaled” by changes in day length (photoperiod), but they can also occur in response to changes in temperature or moisture (rain)

represents the phenomenon of “seasonal breeding”

developmental and physiological constraints:

reproductive processes are time-dependent events; for example, development of mature sperm in most species takes at least 6 weeks; similar time constraint also exists in females with development of eggs (length of the ovarian cycle)

during a given season, there may not be enough time for gametes (sperm and eggs) to mature, adults to mate and for the young to develop before adverse environmental conditions occur

Why do such differences exist in reproductive strategies?
why do such differences exist in reproductive strategies4
Reproductive constraints:

(developmental and physiological constraints)

scenario #1: in some species, sex behavior occurs immediately following a period of hibernation; because cold temperatures inhibit the production of gametes and gonadal steroids, sperm are produced during the summer, and are stored during the winter and available for mating in the spring following hibernation (ex., red-sided garter snake)

scenario #2: in other species, see phenomenon of embryonic diapause--implantation of the embryo is delayed; in this scenario, gametes have matured, mating has taken place and an egg has been fertilized, but implantation of the embryo and development of the embryo in utero has been delayed; embryonic diapause can last for as little as one week to as long as several years; at the end of diapause, the embryo implants and normal development resumes (ex., some species of bears, kangaroos)

Why do such differences exist in reproductive strategies?
why do such differences exist in reproductive strategies5
Reproductive constraints:

evolutionary constraints:

concept #1: evolutionary history, or phylogeny, of a species can predispose the evolution of certain “traits” but not others

closely related species that live in different environments can have similar modes of reproduction

concept #2: different species that face similar environmental demands may develop similarities in certain “traits” (phenomenon of natural selection)

distantly related species living in a similar environment can develop similar modes of reproduction

Why do such differences exist in reproductive strategies?
why do such differences exist in reproductive strategies6
Diversity in hormone-behavior relations--importance of mate compatibility

in some species, choosing a mate can affect reproductive success

Ex. female canvasback duck

Why do such differences exist in reproductive strategies?

female

canvasback

duck

randomly paired

with male

selects own

mate

will lay eggs

will not lay eggs

“reproductive success”

“reproductive failure”

why do such differences exist in reproductive strategies7
Diversity in hormone-behavior relations--alternative life-history strategies

definition: individuals within a given population can adopt different morphologies, physiologies and behaviors

Ex. bluegill sunfish: (3 types of males)

territorial male: large colorful male that defends territories and solicits females to release eggs so that he can fertilize the eggs

sneaker males: small males that “sneak” matings; when the large territorial male is preoccuied, a sneaker male can rush in and release sperm to fertilize eggs

female mimics: large drab males that look like females; these female mimics hang around a territorial male that is courting a female; when the female releases her eggs, the female mimic can rush in and relese sperm to fertilize eggs

alternative life-history strategies are heritable: sneakers grow up into female mimics, while territorial males produce young that are large and brightly colored

androgen concentrations vary: territorial males > sneaker or female-mimics

Why do such differences exist in reproductive strategies?
why do such differences exist in reproductive strategies8
Diversity in hormone-behavior relations--cues that activate/coordinate behavior

previously we considered the following relationship:

increases in gonadal steroids (and gamete production)-->increases in the display of sex behavior (associated reproductive pattern)

however, other “cues” or factors may be important in “activating” or “coordinating” the display of sex behavior

chemical signals

environmental signals

social stimuli (social systems)

Why do such differences exist in reproductive strategies?
why do such differences exist in reproductive strategies9
Diversity in hormone-behavior relations--cues that activate/coordinate behavior

Chemical signals:

hormones: providing “internal communication” within an individual

pheromones: providing “external communication between individuals

this distinction is becoming “blurred”: 1) hormones can act as pheromones (Ex. goldfish), and 2) hormones do stimulate the production of pheromones

female pheromones can stimulate male sex behavior

male pheromones can also stimulate sex behavior in females:

Ex. male pig: he will breathe into a female pig’s face (air current will carry a male pheromone--”sex attractant” to female); if female is receptive, then the sex attractant will cause her to stand immobile, arching her back in lordosis and allowing the boar to mount

profitable science--companies manufacture an aerosol preparation containing androgen metabolites called “Boar Mate” used to immobilize sows for artificial insemination

Why do such differences exist in reproductive strategies?
why do such differences exist in reproductive strategies10
Diversity in hormone-behavior relations--cues that activate/coordinate behavior

Environmental signals:

Ex. Desert-dwelling zebra finch

considered an “opportunistic breeder”--engages in mating behavior when the opportunity presents itself (right time=rain fall)

desert-dwelling zebra finch lives in deserts of western Australia, in which rain occurs only once in a 3-year period

throughout each year, the male and female zebra finches possess high levels of gonadal steroids and mature gametes

however, mating occurs only when rain falls-- 10 minutes after the start of rain, mating takes place, within 4 hours nests are built, within one week eggs are laid

rain is the cue activating mating behavior; gonadal steroids (androgens, estrogen, progesterone) play a permissive role by preparing the individual for reproduction once rain has fallen

Why do such differences exist in reproductive strategies?
why do such differences exist in reproductive strategies11
Diversity in hormone-behavior relations--cues that activate/coordinate behavior

Social stimuli:

the social system of a number of species of birds are associated with different endocrine profiles and different male-female and male-young interactions

monogamous species: one male bird pairs with one female

polygamous species: one male pairs with two or more females

levels of parental care: to what extent does the male help in raising the young?

levels of aggression: degree of male-male interaction (low--moderate--high)

levels of testosterone: low--high, transient--prolonged

Why do such differences exist in reproductive strategies?
why do such differences exist in reproductive strategies12
Diversity in hormone-behavior relations--cues that activate/coordinate behavior

Social stimuli:

basic relationships--focusing on the male:

polygamous species--high degree of male-male interactions--low degree of parental care--high levels of testosterone that are prolonged

monogamous species--low degree of male-male interactions--high degree of parental care--low levels of testosterone that are transient

key point: different social systems are associated with different degrees of behavior (male-male interactions and male-young interactions) and with different patterns of testosterone secretion

Why do such differences exist in reproductive strategies?
associated and dissociated reproductive patterns
Dissociated reproductive pattern: Ex. red-sided garter snake

courtship and copulatory behaviors are not dependent on a rise in gonadal steroids, nor on the presence of high levels of gonadal steroids

sex behavior and gonadal activity are dissociated

gonadal steroids are thought to “prime” the nervous system to respond to other cues that activate mating behavior

Associated reproductive pattern: Ex. parthenogenetic whiptail lizard

increases in estrogen (occur with follicular development) activate the display of female-like pseudosexual behavior and stimulate ovulation

subsequent increases in progesterone activate the display of male-like pseudosexual behavior

sex behavior and gonadal activity are associated

gonadal steroids are thought to “activate” the nervous system to activate behavior

Associated and Dissociated Reproductive Patterns
dissociated reproductive pattern
Red-sided garter snake:

found in northern US and Canada

hibernate 9 months out of the year, emerging from hibernation late Spring

males emerge ‘en masse’, while the females emerge singly

as each female emerges from hibernation, a group of males will surround the female forming a “mating ball”

female secretes an attractant pheromone on her skin that stimulates “chin-rubbing” from males

chin rubbing is the male’s courtship response and involves the male moving up and down the back of the female rapidly and repeatedly with his chin while flicking his tongue on the female’s back (contacts pheromone)

eventually one male in the “mating ball” will copulate with the female--the male will align himself along the female and will intromit a hemipenis into the female’s cloaca

Dissociated Reproductive Pattern
dissociated reproductive pattern1
Red-sided garter snake:

note: male lizards and snakes have 2 penises; when they mate they use only one, hence the term--hemipenis

note: cloaca is a Latin term for “sewer”; it refers to the fact that all vertebrates but mammals have a single urogenital opening once mating takes place, the female becomes unreceptive

once mating has occurred, the female becomes unreceptive and leaves the area; she will gestate and the young will be born at the end of the summer

males will engage in sex behavior for about 3-4 weeks following emergence from hibernation

following courtship and copulation, both males and females will shift their behavioral responses exclusively to feeding

Dissociated Reproductive Pattern
dissociated reproductive pattern2
How does the behavior of male and female garter snakes reflect changes in development of the gonads and secretion of gonadal steroids?

at emergence from hibernation, the level of gonadal steroids are low, the size of gonads are small, and the formation of mature gametes is low (true for males and females)

at emergence, both males and females readily show sex behavior

thus, sex behavior can occur independent of a rise or high levels of gonadal steroids; evenmore striking evidence--(males) you can remove the pituitary, testes, and adrenal glands in the fall before hibernation, the male snakes still show normal sex behavior in spring

in males, sperm used to impregnate females was produced previous summer; during the summer, there is an increase in androgen levels and production of mature sperm--events that occur during the feeding cycle; sperm are then stored through winter months and used for mating in the spring

in females, mating stimulates a neuroendocrine reflex that will stimulate ovarian growth and ovulation (6 weeks later); sperm received at the time of mating will fertilize the eggs; these events also occur during the feeding cycle

Dissociated Reproductive Pattern
dissociated reproductive pattern3
Red-sided garter snake:

If gonadal steroids are not important for activating sex behavior, what stimuli are?

critical stimulus for stimulating male courtship and mating: period of low-temperature dormancy followed by increasing temperatures

critical stimulus for terminating male courtship and mating: a shift from mating to feeding

What role do gonadal steroids play in reproductive processes of this species?

gonadal steroids arenotimportant in activating sex behavior in males or females

gonadal steroids are important in spermatogenesis (males) and ovulation (females)

gonadal steroids also play an important role in “priming” the nervous system to respond to cues that will activate sex behavior--increases in gonadal steroids must occur at some point during the year (usually occurs during summer with feeding)

if you castrate the male and follow his behavior for several years, you will see a steady decline in his courtship behavior; administration of testosterone can reverse effect

exact mechanism? unclear

Dissociated Reproductive Pattern
associated reproductive pattern
Whiptail Lizards:

gonochoristic species--C. inornatus

male and female members

males show male-typical sex behavior, while females show female-typical sex behaviors

[Figure 6.12] male-typical sex behavior: male will approach and investigate the female, and if she is receptive, he will mount her; this often involves the male gripping a portion of the skin on her back or next; the male will begin to maneuver his tail beneath the female’s tail, attempting to appose their cloacal regions; this involves shifting his jaw grip from the female’s nect to her pelvic region--posture called the “doughnut”; during mating, the male will insert one of two hemipenes into the female’s cloaca and maintain that posture for 5 to 10 minutes, after which the male dismounts and then leaves

parthenogenetic species--C. uniparens

consists entirely of females

parthenogenetic females show bothmale-like pseudosexual behavior and female-like pseudosexual behavior

Associated Reproductive Pattern
associated reproductive pattern1
Parthenogenetic Whiptail Lizards:

the whiptail lizards are seasonal breeders

3-4 ovarian cycles per season, each lasting approximately 3-4 weeks

as follicles develop, there is a rise in estrogen that has 2 effects: 1) to activatefemale-like pseudosexual behavior--female will be receptive to mounting from other females, and 2) peak of estrogen is associated with ovulation

the rise in estrogen is followed by rise in progesterone which has the opposite behavioral effect--to activate male-like pseudosexual behavior--female mounts other receptive females and engages in male-like behaviors (like the doughnut); this occurs even though the parthenogen has no hemipenis and intromission does not take place

after ovulation, the ova (typically 1-3 eggs) will pass into the oviduct where shell deposition occurs; shelled eggs are usually laid 7 to 10 days after ovulation

Associated Reproductive Pattern
associated reproductive pattern2
Parthenogenetic Whiptail Lizards:

What role do gonadal steroids play in reproductive processes of this species?

gonadal steroids are important in activating pseudosexual behavior

estrogen activates female-like pseudosexual behavior, in addition to stimulating ovulation

progesterone activates male-like pseudosexual behavior

ovariectomy leads to a loss of female-like and male-like pseudosexual behaviors, and the administration of estrogen restores activation of female-like pseudosexual behavior, while the administration of progesterone restores activation of male-like pseudosexual behavior

Why should these parthenogens engage in pseudosexual behavior?

the behavior is not necessary for reproduction as these individuals reproduce by parthenogenesis (“virgin birth”)--eggs are not fertilized by sperm

pseudosexual behavior increases reproductive success--parthenogens are more likely to lay eggs and will lay more clutches if they engage in this behavior

Associated Reproductive Pattern
associated reproductive pattern3
Parthenogenetic Whiptail Lizards:

Conservation of neural structures mediating male and female sex behavior:

Gonochoristic species:

MPOA is larger in males than females-->importance of MPOA for male sex behavior

VMH is larger in females than males-->importance of VMH for female sex behavior

Parthenogenetic species:

the brain of the parthenogens looks like the brains of females in the gonochoristic species: small MPOA and a large VMH--somewhat surprising finding!

in ovariectomized females, estrogen implants into the VMH can activate sexual receptivity

in ovariectomized females, progesterone implants into the MPOA can activate mounting behavior

in the parthenogen, the MPOA is not masculinized in size but in function and can respond to the progesterone surge to activate male-like pseudosexual behavior

Associated Reproductive Pattern
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