BN Exam 3: Female Reproductive Behaviour, Parental Behaviour, Social Behaviour

Female reproductive behavior (definition)

All behaviors necessary and sufficient to achieve fertilization of female gametes by sperm

6 components of female reproductive behavior

1. Courtship 2. Mating 3. Ovulation 4. Pregnancy 5. Parturition 6. Lactation (first 3 = sex behavior; last 3 = parental behavior)

Estrus

Period during which female mammals will permit copulation; females seek out males, work for access to males, and spend time near males

Anestrus

Reproductive condition of a female mammal that is not in estrus (not in mating condition)

Behavioral estrus

When females will permit copulation ('in heat'); coincides with the transition from vaginal proestrus into vaginal estrus

Vaginal estrus

The condition directly following vaginal proestrus, characterized by cornified epithelial cells

Why research on female sexual behavior got a slow start

Female sexual behavior is cyclical and less overt (more complex to study); historical lack of interest; and ovariectomy is a harder surgery than castration

Dr. George Papanicolaou

Showed vaginal cytology closely correlates with ovarian function (first in guinea pigs); noticed abnormal cervical cells, leading to the Pap test for cervical cancer

Rat estrous cycle stages (order)

Diestrus 1 (metestrus) -> Diestrus 2 -> Proestrus -> Estrus; lasts about 4-5 days

Rat estrous cycle hormones

Estradiol rises during diestrus 2 and peaks in proestrus; LH surge and progesterone surge follow in proestrus; ovulation ~10-12 h after the LH surge

Vaginal cytology: proestrus

Nucleated epithelial cells (this is when behavioral estrus begins)

Vaginal cytology: estrus

Cornified epithelial cells

Vaginal cytology: metestrus (diestrus 1)

Cornified epithelial cells decrease and leukocytes appear

Vaginal cytology: diestrus

Many leukocytes

Rat ovarian changes across the cycle

Diestrus: follicles develop and make estrogen; proestrus: oocytes mature and meiotic division creates the secondary oocyte; estrus: follicle ruptures releasing eggs (ovulation); leftover follicle cells form the corpus luteum (progesterone + estrogen); if no pregnancy, the corpus luteum degenerates

What triggers pseudopregnancy in rats?

Sufficient vaginal stimulation (intromissions) during mating, even without fertilization

Pseudopregnancy

Physiological state resembling pregnancy without an embryo; corpora lutea stay large ~14 days (vs. most of pregnancy if fertilized) maintaining progesterone; readies the reproductive system in case fertilization occurred; seen in dogs, rodents, others

Lordosis

Female rodent mating posture: arched back with raised rump and deflected tail, allowing intromission; 'not so passive'

Female rat initiation behaviors

Hopping and darting (hop near the male then away) and ear wiggling; she pauses these after an intromission

Dogs: cycle and receptive behaviors

Cycle ~8-9 months; behavioral estrus ~10 days; points hindquarters toward male, deflects tail, allows vulvar licking and mounting

Dogs: anestrus behaviors

Will not permit mounting; avoidance: sits down, moves away, growls, snaps, or bites

Chimpanzee vs humans/bonobos/orangutans/gorillas sexual behavior

Chimps: highly stereotyped, copulate only during behavioral estrus. Humans/bonobos/orangutans/gorillas: less stereotyped, sexual activity not limited to a particular time

3 components of female sexual behavior (FSB)

Attractivity, proceptivity, receptivity; estrogens affect all three

Attractivity

Stimulus value of a female to a particular male; a hypothetical construct inferred from a conspecific's behavior. It is whether she is attractive to males, NOT who she is attracted to

Proceptivity

Extent to which females initiate copulation; both overt behavior and underlying motivational state (appetitive sexual behavior, sexual motivation/libido)

Receptivity

Female responses necessary and sufficient for fertile copulation; responsiveness to another's sexual initiation (consummatory phase)

Estrogen and attractivity (rhesus data)

Male mounting rate was highest around the female's estradiol peak

Estrogen and proceptivity (rhesus bar-press data)

Females pressed a bar 250 times for access to a male; access time was fastest (lowest) around ovulation when estrogen is highest

Estrogen and receptivity (rhesus ejaculation data)

Number of male ejaculations was highest and time to ejaculation was lowest around the female's estradiol peak

Lap dancer tip study

Tips highest around ovulation (~$335/shift), lower in luteal phase (~$260), lowest at menstruation (~$185); no variation in women on hormonal contraceptives; could reflect attractivity and/or proceptivity

Women's face preferences across the cycle

Early studies: women in the follicular phase prefer more masculine faces. Caveat: large later studies found NO cycle shift

How is attractivity measured?

Often through preference tests (e.g., a male choosing between chambers with different females)

Male acceptance ratio

Proportion of female solicitations that result in male mounting; males more likely to mount an ovariectomized female after estradiol injection

Ovariectomy vs ovariectomy + estrogen on attractivity

Ovariectomy reduces attractivity; adding estrogen restores/increases it (e.g., dogs)

4 factors that influence attractivity

Physiological (estrogen), morphological (perigenital swelling), chemical cues, and behavior

Perigenital swelling

Morphological attractivity cue: estrous female primates' perigenital skin swells; olive baboon males (even subordinates) look at and approach swollen females more

Main sources of chemosensory attractivity cues

Urinary and vaginal secretions of females in estrus; males sniff/lick genitalia before copulation

Vomeronasal organ (VNO)

Chemosensory organ (Jacobson's organ) used by many ungulates, carnivores, and rodents to process pheromone cues

Flehmen response

Lip-curl behavior (e.g., horses, zebras, tigers) that draws chemical cues toward the VNO

Does the human VNO work?

Long thought reduced/absent in higher primates; some recent cadaver studies found VNO-like cells connected to capillaries, suggesting possible function (unresolved)

Red-sided garter snakes: chemical cues

Females make methyl ketones (attractive; estrogen needed for production); males make squalene; VNO activation leads to chin-rubbing, alignment, intromission; a male who achieves intromission releases a signal that stops other males' courtship

Behavioral attractivity factor

Males attend more to females that actively solicit (presentation behaviors); in rats mounting almost always follows female solicitation, so male behavior is gated by female signals

Male-side factors that make attractivity non-uniform

Individual male preferences (e.g., OVX+E dogs: some females favored), prior experience, and novelty

Coolidge effect

New or unfamiliar females temporarily increase attractivity/renew male sexual behavior

3 ways proceptivity is measured

1. Affiliative behaviors (getting close to males) 2. Number of solicitations before intromission 3. Alternating approach and withdrawal

Affiliative behavior example (proceptivity)

In rhesus monkeys, 80% of proximal male-female social interactions before mating were initiated by females

Solicitations (proceptivity)

Seen in many species incl. birds, fish, reptiles; can include vocalizations, head bobbing, fin flaring; diverse, species-specific, measurable index of sexual motivation

Alternating approach and withdrawal

Proceptive measure in rodents, ungulates, canines, primates (e.g., rat hopping/darting); may include female anogenital sniffing or mounting

Male attractiveness and proceptivity

Females are less likely to show proceptive behavior toward castrated males

Ovariectomy, estradiol, and proceptivity

Estradiol increases proceptivity even in the absence of male interest; solicitation by presentation peaks midcycle (highest estrogen) in lab, zoo, and wild studies

Receptivity measure: rats

Lordosis quotient

Receptivity measure: dogs

Rejection coefficient

Receptivity measure: primates

Acceptance ratio

General way receptivity is quantified

Ratio of successful copulations (female acceptances) to male mating attempts

Female ringdoves and receptivity

Female initiates her own receptivity: male signals -> female cooing -> hormonal changes. Hearing her own nest coos stimulates follicle development and estrogen; devocalized females show no ovarian development to male stimulation (behavior -> hormones)

Ovariectomy and mating posture: non-primates vs primates

Non-primates: mating posture disappears in most OVX females; female cooperation required and tied to fertility. Many primates (incl. humans): constant receptivity, can copulate at any cycle stage or without ovarian steroids

Social factors x endocrine state (rhesus)

When female monkeys are tested in groups (risk of aggression from other females), copulation is more tightly coupled to endocrine state than in pair tests

Pacing: seminatural vs standard lab tests

In seminatural burrow settings females retreat after each intromission (~3 min apart); in standard non-paced tests intromissions are ~1 min apart

Return latencies in paced mating

Females return to the male most slowly after ejaculation, then intromissions, fastest after mounts

Why pacing matters

Slower paced intromissions -> prolactin release -> corpora lutea support (progesterone) -> implantation of the blastocyst; optimizes reproduction

Vaginal code

Females have a preferred timing pattern of vaginal-cervical stimulation (VCS) that is rewarding and shapes future mate choice

Evidence for the vaginal code

1. Artificial VCS at the preferred interval produces conditioned place preference 2. After paced mating with a scented male, females solicit more toward males with that scent

Female- vs partner-initiated sex across the menstrual cycle

Female-initiated sex varies across the cycle (peaks near ovulation); partner-initiated sex is flat. Caveat: correlational, cycle phase often estimated from cycle day

Diaries of erotic thoughts

Women's erotic thoughts and autosexual activity peak around ovulation (correlational)

Burleson et al., 2002

Solo sexual activity peaks around ovulation in women without a live-in partner (gay or straight); with a live-in partner the pattern flattens (partner availability shapes cycle effects)

Estrogen in postmenopausal women

Estrogen replacement can increase sexual desire (modest; partly via improved lubrication/comfort)

Estrogen in naturally cycling women

Positively associated with sexual desire and attraction to men other than one's primary partner

Hormonal contraceptives and sexual motivation

Many studies show reduced sexual motivation, but effects are highly variable

Follicular phase

From menstruation to ovulation; estrogen rising and follicles forming

Luteal phase

From ovulation to menstruation; corpus luteum forms and progesterone is high

Menstruation vs proestrus bleeding

Menstruation: steroid DEPRIVATION (E and P at baseline, endometrium sloughs). Proestrus bleeding (dogs): steroid STIMULATION (estrogen causes rapid uterine growth that tears vessels)

Negative to positive feedback

Estrogen normally inhibits GnRH/LH (negative feedback); sustained high estradiol flips this to positive feedback -> LH surge -> ovulation

Kisspeptin neurons: location

AVPV in rodents; mainly the infundibular nucleus in humans (POA/hypothalamus)

Kisspeptin neurons: what they do

Express estrogen receptors, receive SCN (circadian) input, activated during the GnRH/LH surge; integrate estrogen + circadian info to time the surge and ovulation

Reproductive cycle type: short-lived prey

Spontaneous, short cycles (e.g., rats/mice) that minimize time spent non-pregnant

Reproductive cycle type: solitary carnivores

Induced ovulation (ovulate in response to mating/male cues), useful when mates are rarely encountered

Induced ovulation in prairie voles (sequence)

Male present -> anogenital investigation + male urine -> VNO -> accessory olfactory bulb -> GnRH release -> LH (maybe FSH) ~1 h later -> estrogen and estrus behavior within 24 h -> ovulation ~12 h after copulation. Solitary females don't cycle

Releaser pheromone

Elicits an immediate, specific behavior (e.g., boar androstenone triggers standing posture in estrous sows)

Signaler pheromone

Provides information about an individual (dominance, recent food, mother-offspring recognition)

Modulator pheromone

Alters mood, emotion, or attention; proposed mainly for humans (e.g., androstadienone)

Primer pheromone

Slower, longer-lasting endocrine changes (e.g., Whitten effect)

Lee-Boot effect

Female mice housed in groups (no male) go into anestrus; pheromone in urine lowers LH, suppressing cycles

Whitten effect

Male mouse urine induces and synchronizes estrus in grouped females within ~48-72 h via GnRH release

Bruce effect

Recently mated female exposed to a new male (not the sire) fails to implant (pregnancy block); not seen with castrated or juvenile males

Vandenbergh effect (earlier puberty)

Juvenile female mice exposed to male urine reach puberty earlier (GnRH release)

Vandenbergh effect (later puberty)

Juvenile female mice exposed to urine of mature (grouped) females reach puberty later

Menstrual synchrony (McClintock effect): original claim

Dorm roommates/close friends' cycles moved closer together after ~7-8 months of cohabitation; axillary compounds study: follicular-phase sweat shortened, ovulatory-phase sweat lengthened recipients' cycles

Menstrual synchrony: later studies

Larger studies (e.g., Yang & Schank, 2006) found no more synchrony than chance

Stress and the menstrual cycle

HPA axis suppresses GnRH -> irregular cycles; high-stress jobs ~2x risk of short cycles; high stress ~2x dysmenorrhea risk; incarceration linked to amenorrhea/irregularity

Nutrition and the menstrual cycle

Undernutrition and chronic overnutrition both impair ovarian function; energy signals like leptin act via kisspeptin/GnRH

Sickness behavior

Infection-induced lethargy, hypersomnia, malaise, anorexia, social withdrawal, anhedonia, less goal-directed behavior

LPS and IL-1beta as tools

LPS (Gram-negative bacterial membrane, acts via TLR4) and IL-1beta (pro-inflammatory cytokine) mimic immune activation without replicating infection

IL-1beta effects on sex behavior

Reduced attractivity of FEMALES (males spent less time with them) but not of males; also reduced female proceptivity and receptivity

Genital sensory mapping (Komisaruk et al., 2011)

Self-stimulation of clitoris, vagina, cervix, and nipple activated genital region of primary somatosensory cortex (medial paracentral lobule); distinct but overlapping areas; nipple also activated genital cortex

Brain regions active at orgasm (Wise et al., 2017)

PVN of hypothalamus (oxytocin), periaqueductal gray, hippocampus, amygdala, nucleus accumbens, insula, cingulate cortex, cerebellum

Imagined stimulation (Wise et al., 2016)

Imagined genital/nipple touch activated the same paracentral lobule; imagined erotic (dildo) also activated hippocampus, amygdala, insula, NAcc, mPFC; imagined non-erotic (speculum) gave minimal activation

Hormones and orgasm study results

Adrenaline and noradrenaline rise at arousal/orgasm; prolactin rises markedly after orgasm and stays high; gonadal hormones and cortisol largely unchanged

Prolactin and post-orgasmic satiety

Prolactin rises after orgasm in men and women; ~400% greater after intercourse than masturbation (Brody & Kruger, 2006); proposed satiety index; may reduce drive by inhibiting dopamine

Parental behavior

Behaviors toward one's offspring that contribute directly to survival of fertilized eggs or offspring that have left the female's body

Maternal behavior

Parental behavior performed by the mother or another female