The Private Bits of Gregarious Carnivores

Female spotted hyenas give birth through the tip of a penis-like clitoris. That sounds unpleasant, right? It’s also quite damaging. First-time birth through this “peniform” clitoris is long and difficult and results in the clitoral opening tearing when the relatively large, open-eyed pup (with teeth and claws) is born. Quite often, the first birth through this pseudopenis also results in the the death of the pup. So, uh, why is it there?

Hyena Baby: Arno and Louise Wildlife via Flickr

Spotted hyenas aren’t the only mammals with masculinized female genitalia.  Female moles, civets and even some “less thoroughly investigated” primates have masculinized genitalia for at least some part of their lives. Some insects do too. Female spotted hyenas, though, have the most masculinzed genitalia of mammals. Externally, the outer labia are fused and form a kind of fake scrotum. The clitoris is enlarged and can become erect like a regular penis. The female urinates, copulates and gives birth through this. Delivery is difficult:

Clitoral delivery involves an unusual right-angled trajectory through the pelvic region. Consequently, the birth canal of a normal spotted hyena is both longer and more circuitous than that of similar sized mammals. These structural constraints clearly contribute to the complicated and protracted labour in this species and probably account for some cases of maternal death associated with parturition. (2)

Copulation, on the other hand, is simply awkward and requires not insignificant forbearance on the part of the female.

Internally, everything is what you would expect based on your average female carnivore. Essentially, the genitalia just looks and seems masculine externally. Again, why? According to Davis and Story (1949):

Nearly every investigator who has studied the female genitalia of the spotted hyena has made a more or less careful comparison and homologization of its parts with the external genitalia of the male. Impressed by the astonishingly close correspondence he was able to demonstrate, each has then proceeded to “explain” it. The interpretations follow fairly closely the changing vogues of research in experimental biology, and the final result is more than a little reminiscent of the fable of the blind men and the elephant. (1)

The interpretations Davis and Story recount are previous researchers calling it “arrested development”, trying to compare it with antlers in female reindeer, reducing it to a “freak of nature” kind of hermaphroditism and, finally, relating it to possibly too much “androgenic substance” (hormones like testosterone) and also maybe too little estrogenic substance (like estrogen).

This last idea, related to androgen exposure, has been the prevailing theory for a while: the development of sexual structures runs on a generically feminine program unless androgens are present. In developing males, these androgens would come from the fetal testes and would set in motion the whole male program.  During the late stages of a spotted hyena pregnancy, levels of androgens increase, getting close to levels found in males. So, female as well as male hyenas are exposed to androgens during development.

There are some theories as to why this would be so. First, it is important to consider that social dominance is important in hyena society. They are “gregarious carnivores” who live in clans of various sizes (from 6 to 90 individuals). They mostly scavenge food or work together to take down larger prey. Eating is a very competitive activity. A kill goes quickly and who gets to eat first is directly related to the dominance hierarchy. An individual’s place in this hierarchy is related to parentage – children of a highly ranked female will themselves have high rank. This is true of both males and females. However, males leave the clan after weaning and enter new clans at the lowest possible rung of the dominance ladder. Females in these clans are, therefore, always dominant to males.

Spotted Hyena: Arno and Louise Wildlife via Flickr

Some theories as to why androgens are so high during development are related to the need for aggression.  Androgens are closely associated with aggression which is thought to aid individuals at kill sites and in the “competitive nursing” of newborns who sometimes kill their siblings. The young of highly ranked females are given priority at kill sites – and are often able to be weaned earlier because of it. All this is thought to lead to better survival – along with some interesting female genitalia as a byproduct. The benefits of the increased androgens may very well outweigh the downsides (protracted labor and loss of first-born pups) and this will allow the trait to be passed on. So, the development of masculinized external genitalia in female spotted hyenas, then, was postulated to be a byproduct – a side-effect – of high levels of androgens present during fetal development

This sounds perfectly reasonable, except that when researchers experimentally treated hyenas with anti-androgens – chemicals that blocked the effects of the androgens present, they found that much of the masculine appearance of the female genitalia remained. The female’s penis-like clitoris was a bit shorter and rounder and the clitoral opening was more flexible. But it was still there. (Incidentally, in females, the cost of clitoral delivery – tearing of the opening and infant death – disappeared after treatment with anti-androgens.  On the other hand, males exposed to anti-androgens – who also ended up with somewhat shorter, rounder-ended penises – during eight years of study, were unable to impregnate a single female.)

It seems, then, that there may be another reason for the masculinization – one that is more directly adaptive for the female. One theory is that having a “penis” may have allowed females to take part in the hyena greeting ceremony which involves sniffing of privates and the display of erections to show submission. This theory reminds me of those boxy business suits women wore the ’80s – as though being vaguely man-shaped made access to the greeting ceremony a little easier.

Another theory is that it allows more female control over mating. And this brings us to fossas.

Fossa: San Diego Shooter via Flickr

Female fossas also have masculine-looking external genitalia. However, they only have it temporarily – from about 12 months of age, right about when a fossa leaves her mother, until about 3 or 4 years of age, when she reaches sexual maturity. During this time, a female fossa’s genitals will appear masculine – complete with spikes and an orange discharge. In fossas there are no especially high aggression levels nor are there especially high levels of androgens. Also, unlike hyenas, fossas are solitary. So, theories that masculinization is related to social needs like female dominance or participation in greeting ceremonies do not fit with the fossa’s lifestyle. The time period in which her genitalia appears masculine coincides with the life stage in which a female fossa is both on her own and not quite ready for intercourse. Masculinization could signal to males that she is not a potential mate or it could simply make penetration too much of a hassle. In any case, it is believed to prevent, to some degree, sexual harassment from males which can otherwise lead to injuries or fatalities.

It is, of course, not necessary that the development of similar traits in two separate species have the same or even similar explanations. Many large animals have large brains because they are large, while humans developed large brains for entirely different reasons. However, the ability to wield more control over mating may have benefited the hyena – particularly the hyena female – greatly.

Although they tend to get a bad rap, hyenas live in social units not unlike many primate groups. Social relationships are valued and individuals recognize each other and form affiliations. Female control over mating may have made it necessary for males to establish a relationship with them before mating can occur.  And this may also explain male submission to females and the relative lack of aggression between males. Clearly the whole issue hasn’t been resolved yet, though. While some masculinization occurs without help from androgens and may be the result of direct adapation, androgens do exhibit some affects on genitalia, and account for much of the reproductive “disadvantages” associated with masculinized genitalia. It’s still an open and very, very interesting question.

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Again, I would suggest visiting zooborns: hyenas and fossas.

1. Davis D, Story HE. Female External Genitalia of the Spotted Hyena. Chicago, Chicago Natural History Museum 1949 31(33) http://biodiversitylibrary.org/page/2761806

2. Drea, C., Place, N., Weldele, M., Coscia, E., Licht, P., & Glickman, S. (2002). Exposure to naturally circulating androgens during foetal life incurs direct reproductive costs in female spotted hyenas, but is prerequisite for male mating Proceedings of the Royal Society B: Biological Sciences, 269 (1504), 1981-1987 DOI: 10.1098/rspb.2002.2109

3. Hawkins, C. (2002). Transient Masculinization in the Fossa, Cryptoprocta ferox (Carnivora, Viverridae) Biology of Reproduction, 66 (3), 610-615 DOI: 10.1095/biolreprod66.3.610

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