Lecture 4 Sexual mimicry in Nature and the strange case of the hyena Flashcards
occurence of sexual mimicry male - female, female - male
rare for males to mimic females.
PLANET EARTH THING THO
Some male cuttlefish are too small to fight for a mate, so have to come up with a sneaky plan if they are to get their way with the girls. Approaching a cuttlefish couple a smaller male assumes the role of a female, tucking up his tentacles and changing colour in an attempt to fool the large male who stands guard over the female. The large male thinks his luck is in with two females after his attention and is completed fooled by the small newcomer. As long as he avoids being grabbed in the mating embrace the cross-dresser is safe. Surreptitiously the female who’s not too picky, mates with the smaller, sneaky male right in front of the large male. The eggs she now lays will contain a mixture of sperm from both fathers, giving her eggs the best possible chance of success.
what is cliteromegaly?
Mimicry of primary sexual characteristics (penis and scrotum) by females.
Development of penis-like structure from the clitoris (the female homologue of the penis).
animals that exhibit cliteromegaly
moles, spotted hyenas, lemurs, bonobo, spider monkeys.
how does the false penis in spotted hyenas occur?
false penis from the clitorus, and false scrotum from the vuvla (filled with fatty tissue).
what are the consequences for the spotted hyena?
Females mate and give birth through the “peniform” clitoris.
In pre-pubertal females, the urinogenital sinus is only slightly larger than the penis.
At puberty it enlarges and retractor muscles develop
super hard to mate, Male has to flip the semi-erect penis against the abdomen of the female as he searches for the clitoral opening.
social aspects of sexual mimicry?
Genital sniffing and inspection is part of social greeting display. Hyenas have ferocious teeth, so a good deal of trust is required. Females re-enforce their position in hyena society by developing the most delicate appendages.
What are the theories for sexual mimicry?
Competition aggression hypothesis:
Intense competition for food – selection for increased female size and aggression in order to survive.
This hypothesis requires that female rank, body size, aggression and reproductive success are closely linked and that variance in reproductive success is greater in females than males.
spotted hyenas ecology?
Female rank is inherited – from their mothers
Females dominate males at the kill and in social encounters.
Females 10% larger. Other hyenids (striped, brown, aardwolf) have normal anatomy and lack dimorphism
High ranker produce more offspring, breed earlier, neonates survive better.
Spotted hyenas are the only true carnivores of the group.
Female status is a key predictor of offspring survival.
the only hyenas to show dimorphism.
describe spotted hyenas offspring
Neonates are very aggressive.
Born with fully functional teeth
Twins are often produced
Fighting commences within 1-5 minutes of birth
Often one of the cubs dies
Survival is in favour of females – ie the male cub often killed.
Juvenile females show male-like play patterns
describe problems at birth for the spotted hyenas.
In a normal mammal of this size, distance from cervix to external vagina is about 30 cm.
In hyenas, the distance is ca 60 cm.
Umbilical cord is only 12-18 cm long
Cord breaks before birth
In primiparous females, the neonate can lodge in clitoris.
Birth can only occur after urinary meatus has torn. A large proportion of first cubs die of anoxia.
Female cubs are larger than male cubs at birth and in adult hood.
9-18% of females die at the attempt of first birth.
how is the spotted hyena placenta different?
The hyena placenta converts ovarian androstenedione to testosterone.
During pregnancy, ovary produces
High levels of androstenedione
(AD; weak androgen).
Normal mammal placenta convert to oestrogen via aromatase.
Early studies suggested that hyena placenta is deficient in aromatase.
In hyenas, placental 17β
hydroxysteroid dehydrogenase is
high, and converts AD to testosterone.
sex steroids in spotted hyenas?
Measures of umbilical cord steroid levels shows females exposed to similar “T” concentrations than males
Neonatal androgen blockers (AB) do not prevent peniform clitoris from forming
But, such clitorises are thicker and cannot be stretched as far in AB-treated females.
Males are unable to mate as adults – so neonatal androgens are essential. Penis is too small to penetrate the female clitoris.
what happens when females are treated with androgen blockers?
for females:
reduces the length of clitorus, and increases circumference (more male like).
For males:
reduces length of penis, increases circumference.
neonatal mortality rates in primiparous females:
- Controls: 12 pregnancies, 20 cubs, 11 stillborn
- Blocker treated: 4 pregnancies, 7 cubs, 0 mortality
therefore neonatal mortality rates may be related to the steroid dependent development of the clitoral structures.
primiparous?
bearing young for the first time
female and males mounting behaviour?
Fenstemaker et al 1999 Nature Neuroscience Vol 2, p 943.
females mount less frequently and wrongly orientated.
hyenas and sexual dimorphic brains?
Male hyenas have sexually dimorphic brains - Fenstemaker et al 1999 Nature Neuroscience Vol 2, p 943.
volume - male dimorphic SDN (sexually dimorphic nuclei) of
hypothalamus is larger
than females by factor of 2.
Cell numbers are also higher.
This is not as much as in some mammals, but it is still dimorphic
Thus, the hypothalamus may be partially masculinised.
summary
Neonatal androgen exposure partially masculinises the female
Dimorphism of body size and aggression favours the female
Androgen blockers do not reverse the phenotype - can change external genitalia in males/females but didn’t eliminate the external clitorus.
Male brains still dimorphic, despite similar T levels in neonatal males in females.
Dimorphism therefore probably a consequence of both steroid and non-steroid factors.
advantages of a partially androgenised status?
Large females are dominant and become
alpha lineages in hyena society.
natural selection therefore operates to give reproductive
advantage to larger dominant females. alpha females higher reproductive success (2x)
Masculinisation of behaviour confers an advantage in the ferociously competitive
hyena society
Hyenas have a mutation of the aromatase gene, but clearly sexual differentiation can proceed in its absence. This mutation is associated with the aggressive female
phenotype.
one hypothesis:
Perhaps masculinisation of the female genitalia is a secondary consequence of selection for early exposure to testosterone.
What is the adaptive significance of high female androgens?
- Measure faecal steroid concentrations
- Associate with social rank
- Assess behaviour of offspring
take faeces, extract steroid metabolites, can measure faecal androgen concentration. associate to social rank.
rank in pregnan females hyenas in 2nd half of gestation is strongly associated with concentration of faecal androgen.
more testosterone, which likely crosses planetal barrier, higher rank.
Dominant females produce
higher levels of androgens in pregnancy.
play/aggression of cubs?
Cubs exposed to high uterine androgen levels in second half of gestation (when behavioural imprint likely) are more aggressive.
- look at mounting behaviour per hour, all combos of FF/FM/MM.
- compare to faecal androgen levels in 2nd half of pregnartcy.
- correlation between the two for females, not for males.
maternal androgens and sexual mimicry?
Link between maternal androgens and offspring behaviour
Rank determines success, selection drives maternal androgen
Not so clear for sexual mimicry
Androgen blockers do not reverse the phenotype
Suggests that primary mechanisms are involved
sexual dimorphism in mammals hypothesis
Development of external genitalia in female eutherian mammals is the default state
Occurs in absence of the potent virilising androgen (5α dihydrotestosterone; DHT)
Does masculinization of female require an alternative source of androgen?
read -
Mammalian sexual differentiation: lessons from the spotted hyena Stephen E. Glickman, Gerald R. Cunha, Christine M. Drea, Alan J. Conley and Ned J. Place
Endocrine reviews 2006
elephants sexual mimicry?
large external clitorus in female,
elephants have intra-abdominal testis. nearest relatives are sea cows/manatees?
The male and female have an identical anogenital distance, with the prepuce and the vulva being situated on the ventral aspect of the abdomen, just behind the umbilicus, and opening anteriorly. The male has no scrotum, and the female has a hypertrophied clitoris that resembles the male’s penis, except that it is not canalized by the urethra (like in hyena) and cannot be extruded.
In order for a male elephant to copulate successfully (like hyena), female cooperation is essential. The upturned tip of the penis has to engage with the vagina, which the female must retract caudally, presumably using the well-developed levator clitoris muscles that arise from the pelvis and insert via a common tendon near the tip of the clitoris. It would be anatomically impossible for a male elephant to rape a female.
The social structure is matriarchal, centered around an elderly female and her related offspring, to form a tight-knit stable family group. The males leave or are driven out from the family group at puberty and have few social bonds, pursuing a solitary existence or occasionally forming short-lived bachelor groups.
Nearest relatives are marine sea-cows (Manatees)
Like marine mammals, they grow throughout life
Testis are intra-abdominal
The trunk acts as a snorkel for aquatic life
Little opportunity in marine mammals for evolution of overt sexually dimorphic structures
summary of hyenas/elephant on slides.
Summary of ancestry, reproductive
anatomy and behavior of the spotted hyena, elephant
The spotted hyena
Carnivore with, during some periods, intense competition for limited food resource
Body size: female slightly larger than male
Extreme male mimicry by female, including a penile clitoris and pseudoscrotum
Matriarchal social structure, with sexually differentiated roles in the mating system
Adult females socially dominant to adult immigrant males
Mating impossible without cooperation of female
The elephant
Eutherian herbivore with aquatic ancestry
Male much larger than female
Some male mimicry by female
a. Identical male and female anogenital distance
b. Female has enlarged clitoris
Male has no scrotum and intra-abdominal testes
Matriarchal social structure
Mating impossible without cooperation of the female
european moles and sexual mimicry?
no explination.
European moles are very hard to sex (identify).
Testis are intra-abdominal
Females possess bilateral ovotestes
Ovarian tissue of normal histological appearance and develops in spring
Also a histologically defined interstitial testicular region which develops in the autumn
females have enlarged peniform clitoris in the female. quite similar.
mole ovotestes?
Jimenez et al: Fertile females of the mole Talpa occidentalis are phenotypic intersexes with ovotestes: Development 118, 1303-1311 (1993)
- during early development, male gonad develops tubes.
- sertoli cells support germ cells. clumped together, germ in centre.
- in females cells all spread around, follicle cells, germ cells, thecal cells.
- NO IDEA, Seminiferous
tubules @ Sertoli cells and ovarian follicles? - testosterone production in females in springtime/breeding season low.
- females in autumn out of breeding season high testosterone.
- males reverse.
- during breeding season, testosterone low in females, follicular structures responsible for prod of eggs dominate.
- out of breeding, testosterone high, dominated by male like structures, get testosterone driven phenotype.
Ovarian follicles are limited to a distinct pole in the gonad
Ovarian interstitial tissue gland (OIG) is found on opposite pole
Follicular pole enlarges at sexual maturity and beginning of each subsequent breeding season (spring) while
interstitial tissue regresses
This situation is reversed at the end of the breeding season.
Sexual mimicry is quite widespread in the mole family in both New (north america) and Old-World (eurasia) moles
BUT in New World moles, there is little evidence for ovo-testes formation and ovaries are of normal appearance
Another source of testosterone – or steroid-independent primary genetic mechanism?
flat lizards mimicry?
Whiting M J et al. Proc. R. Soc. B 2009;276:1585-1591
reviews?
Steve Glickman PDF
