HB Lecture 4

Define sexual mimicry.

Resemblance of one sex of a species to the other sex (e.g. one sex copying the other's appearance or genital anatomy).

Which structure is the female homologue of the penis?

Clitoris

Sexual mimicry of primary sexual characteristics by females involves mimicry of which two structures?

Penis and scrotum

Which hyenid is the only one to show female sexual mimicry?

Spotted hyena (Crocuta crocuta); other hyenids have normal anatomy and lack this dimorphism

Who first noted sexual mimicry in hyenas?

Aristotle

Spotted hyena external genitalia: the false penis is the {{c1::clitoris}} and the false scrotum is made from {{c2::fused labia filled with fatty tissue}}.

c1: clitoris; c2: fused labia filled with fatty tissue

Name the three functions served by the female spotted hyena's clitoral (urogenital) canal.

Urination, copulation (intromission) and parturition

Compared with the female's, the male spotted hyena phallus is {{c1::longer}}, {{c2::thinner}} and more {{c3::angular}}.

c1: longer; c2: thinner; c3: angular

What do erections in juvenile spotted hyenas of both sexes signal?

Social excitement (not sexual arousal)

Why is mating in spotted hyenas difficult for the male?

He must flip the semi-erect penis against the female's abdomen while searching for the opening of her flaccid clitoris

What is an absolute requirement for successful mating in spotted hyenas?

Female co-operation

During parturition in a spotted hyena, what must happen to the clitoris?

It has to rupture

Where are the retractor muscles of the female spotted hyena's clitoris positioned?

Dorsal

Distance from cervix to external opening: about {{c1::30 cm}} in a normal mammal of similar size vs about {{c2::60 cm}} in the spotted hyena.

c1: 30 cm; c2: 60 cm

Spotted hyena pup birth weight range?

1.1-1.6 kg

Spotted hyena umbilical cord length, and the consequence?

12-18 cm; the cord breaks before birth

Define dystocia.

Long and difficult parturition (especially seen in primiparous hyena females)

Define primiparous.

Giving birth for the first time

Which birth complication occurs when a hyena pup becomes trapped in the clitoris?

Pup lodges in the peniform clitoris

What is the approximate neonatal mortality of spotted hyenas in captivity?

About 60%

What percentage of female spotted hyenas die during their first birth attempt?

9-18%

Approximate reduction in biological fitness caused by the cost of birth through a masculinised clitoris?

About 25%

Name the three theories for sexual mimicry given in the lecture.

Social dominance; sperm fitness and selection; competition aggression hypothesis

Social dominance theory: what behaviour is it based on?

Genital sniffing and inspection as part of social greeting display

Social dominance theory: why is a good deal of trust needed between hyenas?

Hyenas have ferocious teeth

Social dominance theory: females are proposed to reinforce their position by developing what?

The most delicate appendages (genitalia) used in greeting

Name one proposed benefit of mimicry in social dominance theory (lecture marks both with a question mark).

Protection from male infanticide of the female's young, or deterring aggression

Main problem with the social dominance theory?

It is doubtful that it compensates for the high reproductive cost of masculinised external genitalia

Sperm selection theory: female spotted hyenas are highly promiscuous and {{c1::polyandrous}}; about {{c2::one third}} of twin litters have different sires.

c1: polyandrous; c2: one third

Sperm selection theory: which male hyenas reproduce?

Mating is not dominated by alphas; low-ranked males reproduce too

Sperm selection theory: which structure is proposed to promote sperm selection?

The long and complex genitourinary sinus

Name the two problems with the sperm selection theory.

Testes are relatively small (unlike most polyandrous species); oestrous cycles lack the synchronisation typical of species with active sperm selection

Competition aggression hypothesis: intense competition for what selects for increased female size and aggression?

Food

Competition aggression hypothesis requires variance in reproductive success to be greater in which sex?

Females

How is female rank determined in spotted hyenas?

Inherited from their mothers

Polygynous species tend to have {{c1::big males}} (e.g. lions); polyandrous species tend to have {{c2::big females}} (e.g. hyenas).

c1: big males; c2: big females

Female spotted hyenas are philopatric. Define philopatric.

They do not wander (they stay in their natal area)

Which behaviours show masculinisation of the female spotted hyena?

More aggressive than males, dominate males at kills and social encounters, territorial marking and defence

Compared with other carnivores, spotted hyena milk has the {{c1::highest protein content}} of any carnivore and is exceeded only by the {{c2::sea otter}} in fat content.

c1: highest protein content; c2: sea otter

Maternal energetic investment in gestation and cub rearing in spotted hyenas ranks where among mammalian carnivores?

Highest

Main problem with the competition aggression hypothesis from fetal development?

The pseudopenis starts developing before the foetus is exposed to maternal androgens

Competition aggression hypothesis: what do large size and aggression give the mother?

Enhanced status and priority access to food and other resources to support lactation and parental care

Which steroid does the ovary produce at high levels during hyena pregnancy, and is it a strong or weak androgen?

Androstenedione (AD); weak androgen

Normal mammalian placenta converts androstenedione into oestrogen using which enzyme?

Aromatase

In hyena placenta, which enzyme is high and converts androstenedione to testosterone?

17beta-hydroxysteroid dehydrogenase

Hyena in utero environment is unusually what?

Androgenic

Umbilical cord steroid measures show female hyena fetuses are exposed to what relative to males?

Similar testosterone concentrations

What caveat applies to antiandrogen (AA) experiments in hyenas?

The AA is a derivative of cyproterone acetate, so blockade is only partial

In antiandrogen-treated female hyenas, clitoris dimensions change how?

Clitoris is shorter and thicker (still develops)

In antiandrogen-treated male hyenas, what happens to the penis and internal anatomy?

Penis is shorter and thicker; internal anatomy is reconfigured

Antiandrogen-treated males are unable to mate. Why?

Penises are too short for intromission, so androgen exposure is essential for fertility

Effect of antiandrogen treatment on neonatal mortality in primiparous females?

Improves survival (controls: stillborn cubs; blocker-treated: lower mortality)

What does hSDN stand for, and where is it?

Hyena sexually dimorphic nucleus; in the hypothalamus

hSDN in male vs female hyenas: volume is larger in males by a factor of {{c1::2}}; neuron numbers are {{c2::higher}} in males.

c1: 2; c2: higher

How does the dimorphism of the hyena hSDN compare with most mammals?

Smaller, but still dimorphic, suggesting partial masculinisation of the hypothalamus

Why do wild-hyena studies measure faecal androgens?

Blood cannot be sampled in the wild

Relationship between maternal rank and faecal androgens in pregnant hyenas (2nd half of gestation)?

Higher-ranked (dominant) females have higher androgen levels

Cubs exposed to high uterine androgens in the second half of gestation are more what?

Aggressive

Hyena neonates are born with what dental feature, and how soon does fighting start?

Fully functional teeth; fighting begins within minutes of birth

In twin hyena litters, which cub is more often killed?

The male cub (survival favours females)

Hyenas have a mutation in which gene, and with which phenotype is it associated?

Aromatase gene; the aggressive female phenotype

Effects of high rank in female hyenas?

More offspring, earlier breeding, better neonatal survival

Which androgen is potent in virilising genitalia and is absent in hyena female mimicry?

Dihydrotestosterone (DHT)

Which mammal group shares the elephant's nearest living relatives?

Sea cows and manatees

Male elephants have no scrotum and testes located where?

Intra-abdominal

Elephant female clitoris is hypertrophied but differs from a penis how?

It is not canalised by the urethra and cannot be extruded

Elephant social structure?

Matriarchal (elderly female with related offspring); males leave or are driven out at puberty

European mole female gonad type?

Ovotestis

European mole ovotestis: ovarian follicles are limited to a {{c1::distinct pole}}; ovarian interstitial tissue gland (OIG) lies on the {{c2::opposite pole}}.

c1: distinct pole; c2: opposite pole

European mole female: follicular pole enlarges when?

At sexual maturity and at the start of each breeding season (spring), while interstitial tissue regresses; reversed at end of breeding season

Mole testosterone: males peak in the {{c1::breeding}} season; females peak in the {{c2::non-breeding}} season.

c1: breeding; c2: non-breeding

Female Talpa occidentalis gonad: which testicular structure is present?

Testicular cords (seminiferous tubules with Sertoli cells) alongside ovarian follicles

New World moles: evidence for ovotestes?

Little evidence; ovaries appear normal, suggesting another testosterone source or a steroid-independent genetic mechanism

In flat lizards (P. broadleyi), what is a she-male?

A male that mimics female appearance

Sertoli cells function?

"Nurse" cells for spermatogenesis

Leydig cells function?

Testosterone-producing cells in the testis

Granulosa cells function?

Follicle production and germ cell maturation

Thecal cells function?

Androgen production in the ovary

[APPLICATION] A female mammal's placenta converts abundant ovarian androstenedione mostly into testosterone, not oestrogen. Which enzyme is high, and what is the fetal outcome?

High placental 17beta-hydroxysteroid dehydrogenase; the fetus is exposed to an unusually androgenic environment, as in spotted hyenas

[APPLICATION] A first-time captive hyena mother has a prolonged labour; the cub's head is in the stretched clitoral opening and the cord has already snapped. Name the condition and one anatomical cause.

Dystocia; a long (about 60 cm) birth canal through a clitoris that must rupture, with a short cord

[APPLICATION] Pregnant hyenas are given antiandrogens. Predict their daughters' external genitalia and neonatal survival.

Clitoris still develops (shorter and thicker); neonatal survival improves

[APPLICATION] The sons of antiandrogen-treated hyenas fail to produce offspring despite normal social behaviour. Explain.

Penises are too short to achieve intromission; androgen exposure is essential for fertility

[APPLICATION] A field researcher cannot draw blood from wild pregnant hyenas but wants to test links between rank and cub behaviour. What sample and what prediction?

Faecal androgens in the second half of gestation; higher rank gives higher androgens, so more aggressive cubs

[APPLICATION] A species shows greater variance in reproductive success in males than in females. Does the competition aggression hypothesis fit?

No; it requires greater variance in females (as in polyandrous hyenas); male variance suggests polygynous big-male species such as lions

[APPLICATION] An autumn-captured mole looks female but histology shows ovarian follicles at one pole and testicular cords at the other. Name the gonad and expected plasma testosterone trend.

Ovotestis; female testosterone is raised in the non-breeding season

[APPLICATION] Dissection of a female hyena shows a female brain nucleus about half the volume of the male's. Interpret.

Hypothalamic sexually dimorphic nucleus is larger in males by about 2x, so the brain is still dimorphic and only partially masculinised

[APPLICATION] A species shows polyandry with large testes and synchronised oestrus. How does hyena data compare with this sperm selection pattern?

Hyenas have relatively small testes and unsynchronised oestrus, which weakens the sperm selection theory

[APPLICATION] Two hyenas meet; one lowers its head and presents its erect clitoris for inspection. Which theory does this behaviour support?

Social dominance (genital inspection as greeting display built on trust)

[APPLICATION] A female hyena's mounting of another female is improperly oriented for intromission. What does this suggest about her brain?

It is still sexually dimorphic despite high fetal testosterone

[APPLICATION] A zoologist notes that a female mammal and a male have identical anogenital distance, the male lacks a scrotum, and mating fails without female co-operation. Which species fits?

Elephant

[APPLICATION] A hyena mother is alpha lineage. Predict her offspring's survival and breeding relative to a low-ranked mother.

Higher: more offspring, earlier breeding, better neonatal survival