Spotted Hyena Research Paper

Amongst social mammals, spotted hyaenas (crocuta crocuta) display a number of unusual traits, including high maternal investment, strong sibling rivalry that may lead to siblicide, female dominance, and masculinization of female genitalia. (1) This paper will concentrate on the masculinization of female genitalia but will also touch on the other traits listed.

Taxonomic Hierarchy

Kingdom: Animalia

Phylum: Chordata

Class: Mammalia

Infraclass: Eutheria

Order: Carnivora (cats, dogs, bears, raccoons, weasels, civets, mongooses, hyenas)

Suborder: Feliformia (cat-like carnivores)

Family: Hyaenidae (hyenas)

Genus: Crocuta

Species: Crocuta crocuta (Erxleben, 1777) - spotted hyena

The Spotted Hyaena

In the barren landscape sub-Saharan Africa, one

of Africa’s most underestimated predators have risen to greatness. Spotted hyaenas are extraordinary survivors with bone crushing jaws and cast iron stomach which can digest even rotting meat. Unlike popular belief, spotted hyaenas hunt more than they scavenge. Although spotted hyaenas resemble primitive dogs, hyaenas and dogs last shared a common ancestor 43 million years ago.(2) Crocuta crocuta have dark, thick muzzles, sharp teeth and powerful jaws for breaking bones. Large rounded ears and eyes with a short erectile mane on their neck is displayed. They’re fur is yellowish-brown with darker oval spots and they have a bushy tail. Spotted hyaenas usually weigh between 110 to 176 pounds depending on the sex. Female spotted Hyaenas are remarkable amongst mammals, (Image:spotted hyena:wikipedia) they are larger, stronger and fiercer than male hyaenas. They have the most male like sexual organ than any female mammal. (3)
The Pseudo-penis
Female spotted hyaena’s have evolved to acquire a peniform clitoris. The image below compares a spotted hyaena male penis (left) to female pseudo-penis (right.) (1-11)The female clitoris exhibits and extreme example of clitoromegaly, an abnormal enlargement of the clitoris. Clitoromegaly is rarely observed in mammals, usually being displayed in binturongs (Arctictis binturong), fossas (Cryptoprocta ferox) and ring-tailed lemurs (Lemura catta). Crocuta crocuta’s clitoris can range upto 90% of a males penis.(3) Therefore it may be difficult to distinguish female from male spotted hyaena’s. However there are a few clear distinguishes in phallic morphology. The peniform clitoris is long and thin, consisting of two visible structures, the glans and the shaft. The peniform clitoris glans is dissimilar to males as it (image: spotted hyena; wikipedia) has a small opening at the narrow tip. The shaft contains the urogenital canal, which enlarges and becomes more elastic because other than urination the pseudo-penis is used for copulation and giving birth through. (4-6) Which is facilitated by a pair of robust retractor muscles that enable the female to retract the phallus upon itself, forming a hole which permits the male to achieve intromission. During a females first birthing, the urogenital cannot stretch sufficiently to allow 1.5 kg fetus through, therefore the urogenital canal has to tear in order for the cub to emerge.(4) During a female spotted hyaenas first birthing there is a 60% chance for stillbirths to occur due to suffocation in the urogenital canal. In place of an external vagina, the female spotted hyaena has a pseudo-scrotum due to the fusion of labia, which contains connective tissues and fat. When erectile, the pseudo-penis can range up to 7 inches long. (5)
Reproduction
Female spotted hyaenas sexually mature at approximately three years of age, with males sexually maturing at two years of age. Mating is not seasonal amongst spotted hyaenas. After mating, gestation occurs for about 110 days, with liters consisting of 1-3 cubs, most commonly twins are born. (1-3) Due to the pseudo-penis, the number of cubs are limited as giving birth is a highly risky procedure that may result (Image: spotted hyena: wikipedia) in the death of the mother due to the rupture of the pseudo-penis or the death of the cub due to suffocation as it travels down the pseudo-penis. When a successful birthing occurs, it takes weeks for the pseudo-penis to heal. (2-4) The cubs take over a year to produce a strong jaw therefore is fully dependent on the mother for over a year. The breeding cycle occurs during a 12 month period, the lactation; 6 months or more and anoestrus from three to four weeks. (5) Mating in spotted hyaenas can be a highly time consuming event due to the female pseudo-penis, therefore cubs do mock mating allowing practice of form. Having a pseudo-penis gives females complete control of mating. (6) In order for sexual interaction to occur, female must permit penetration and volunteer to retract pseudo-penis up into itself, allowing an entrance for the male. Which infers that it is completely impossible for a male to force sexual penetration onto a female. (7)
Hyaena ecology and social organization
The female hyenas govern the clans, lead by all powerful matriarchs. Neighboring clans are sworn enemies and territorial trespassers are often viciously attacked. Territories are marked by distinctive scented pastes produced by glands beneath their tails. (9) Hyenas are popularly known to be scavengers but they are more predators than scavengers. Although the pseudo-penis may physically seem to be a disadvantage to female spotted hyaenas, it has its advantages when it comes to the social organization of spotted hyaenas. A popular social greeting amongst spotted hyenas is lifting its legs when approach in order to recognize the hyenas scent produced by bi-lobed sebaceous glands. (8) When a cub is introduced to the clan, it lifts its leg in a typical hyena greeting, allowing her clan mates to identify her distinctive scent. The clan will recognize the cub by this smell, and the cub in turn must learn to recognize theirs. Its an important learning curve since each hyena has its own rank and the cub needs to recognize who’s who as it fins its place in the clan. Although if the cubs were born from the matriarch, it gets more than just milk from its mother, as cubs it gets its mother superior status. (1-3) As the matriarch, she ranks the highest in the clan and enjoys the support and protection from all of the clans dominant females. Next would be next female in line if anything were to happen to the current matriarch. Followed by other high ranking females. The females are ranked by their aggression, the higher the rank the more aggressive the female is. Low ranking females cubs inherits its mothers rank as well. Low ranking hyaenas are often bullied by the clan. The low ranking mother will care for its cub but won’t dare to defend him from the more dominant females or their cubs. After the lowest rank possible among female spotted hyaena comes the male. (8) The top male rank would be the male who is chosen by the matriarch to copulate with, and this is usually an outsider or immigrant from a different clan. This allows genetic variability within the clan and therefore a greater chance for survival. Adult males in a clan are immigrants from other clans who joined current clan to find a mate. They forfeited the rank they inherited from their mothers when they left their own clan, falling instantly to the bottom of the hyena hierarchy. The number of clan members could be unto 90 individuals. Presenting an erect penis or pseudo-penis for inspection is a important social interaction between spotted hyenas. (9) High-ranking females rarely allow for inspection to occur and immigrant males almost always allow it as a sign of submission. Sexually mature males are usually immigrant males. Between the age of 2-6, reproductively mature males leave their mother clan in search for a mate. Females are 25% bigger than the males. Males have to be extremely submissive in order for sex to occur. (8)
Evolution of Spotted Hyaena
The height go the Hyaenid diversity occurred in the late Miocene, 24 different species roamed Africa and Eurasia .

Spotted hyenas are members of the family Hyaenidae, a lineage of carnivores that split from ancestral viverrids 25-30 million years ago. (2) Hyaenid is succeeded by four species, the smaller carnivore family existing today from the discovered 69 fossilized species. The four species left in the family are; striped hyenas (Hyaena hyaena), brown hyaenas (Parahyaena brunnea), spotted hyenas (Crocuta crocuta) and a small termite-eating outlier, the aardwolf (Proteles cristatus). (8) Amongst these species, only female Spotted Hyaenas display masculinization of genitalia. Closest living members of Hyaenas currently are civets and mongooses. It is quite remarkable, the evolution of modern hyaenas compared to its ancestors and relatives. The rise of Hyeanidea dates back 18-17 million years ago. The first known hyena, Protictitherium gaillardi resembled a civet rather than a large primitve dog. Protictitherium g is thought to have spent most of its times in trees due to its retractable claws. It is thought to have eaten birds, smaller mammals and insects. Various species of Protictitherium survived over millions of years and only died out between 5.3-4.2 million years ago. Other Hyaenids spent more of their time on the ground such as the first known European hyaenas, Plioviverrops orbignyi which resembled a mongoose and was specialized in eating insects. Its claws could

not retract therefore it most likely spent more time on the ground then in trees. This species survived till the end of Miocene. Preceding that Plioviverrops genus evolved to be bigger hyaenas and change in teeth occurred as there were more grassland with definite seasons then warm forests. (7) Running hyaenas” evolved 15 million years ago, who ran down their prey and looked similar to small wolves. 10 - 12 million years ago “bone-crushing” hyenas evolved. The spotted hyenas diverged from the striped and brown hyena approximately 10 million years ago.
Evolution of pseudo-penis
There have been few studies on the pseudo-penis of female spotted hyenas and even fewer on the evolution of hyena genitalia.

In order to understand the the reason behind the evolution of the pseudo-penis, the general “hyperaggresiveness” and complete dominance of female spotted hyenas must be understood as the masculinization of genitalia in Crocuta crocuta is in my understanding correlated with the masculinity of the female itself. (9) One theory suggest that female dominance in Spotted hyena clans could be due to the selection of aggressive females who successfully competed with males over the kills, ensuring there would be enough milk for the cubs who are dependent on their mothers for over a year. (4)Another theory suggests that aggressive female spotted hyaenas were selected because the cubs jaws are not fully developed for over a year since birth, so it is completely dependent on the mother for food. This aggressiveness has been hypothesized due to increased hormones such as testosterone. In turn the development of a pseudo-penis in females is theorized to be a by product of hormones due to hyperaggrresiveness. (4,5) However when proper studies were done, blood samples taken from Serengeti population (2) Hormones: testosterone (T), 5a-dihydrotestostrone (DHT), androstenedione (AE). Significantly lower (T) and DHT observed in females. (AE) little difference in female and postdispersal males but significantly lower in predispersal males. (9) Data shows hormones are

not a factor for “hyperaggresiveness.” Therefore the reason to female aggressiveness over male spotted hyaenas are inconclusive. It appears that the pseudo-penis in a female fetus is displayed before differentiation of the fetal and ovary and adrenal gland, and is thought to be androgen dependent. To test this, pregnant spotted hyenas were treated with an androgen receptor blocker alone (cryproterone or flutamid) or combination with an inhibitor of 5a-reductase (finasteride + flutamide). Even though these were applied well before sexual differentiation, female cubs continued to display peniform penis’, though then pseudo-penis were reduced. The pseudo-penis was broader and shorter and the urogenital meatus had greater elasticity. The males penis were reduced as well in this experiment. (4,5) Clitoromegaly is exhibited in humans as well due deficiency of placental aromatase. Studies done indicated that aromatase activity was low in female spotted hyaenas and perhaps was the reason to masculine genitalia. When aromatase inhibitions were tested in a pregnant spotted hyaena, that encompassed 60 day gestation, the results were curious. A single female cub was born and its glans were blunted and urethral meatus displaces with part opening on the ventral surface of the glans. An apparent case of clitoral hypospadias. Therefore genital masculinization may be due to androgens, estrogens, and peptide hormones being used at different stages of sexual differentiation and development in preparing genital tissues. Experimental studies so far have not provided the reasons to the occurrence of a pseudo-penis in female spotted hyenas. (5)
Conclusion
I chose to research topic; pseudo-penis of a female spotted hyena due to its uniqueness. Every little physical research has occurred to understand the peniform clitoris of crocuta crocuta. However I continued my research as my interest peaked when learned of the complete female dominance in spotted hyaena clans. My research in both cases lacked resolution. There were simply hypothesizes on the formation of the pseudo-penis due to excess or reduction of specific hormone production during sexual differentiation. I assumed that the reason to aggressiveness in female hyenas and their complete dominance over males correlated with their formation of a pseudo-penis, however my research was inconclusive. It has been popularly told that their “hyperaggresiveness” is due to increase of androgen and testosterone production in a mother (female spotted) when developing of a fetus, however research says otherwise. Perhaps genetic makeup of spotted hyaenas should be studied as well as hormone production.