Creature Feature: Spotted Hyena

| Content warning: This post talks about sex and genitalia in detail.  It’s part of biology, but if the birds and the bees isn’t for you, skip this one.|

Have you ever wondered – perhaps drunkenly, or in the shower – what it would be like if men had to give birth to babies? (If you hadn’t before, this lede has now undoubtedly made you wonder…) While this would make for a horrifying reality in human males (as parodied by SNL here), besides being physically impossible, a similar feat is the norm for female spotted hyenas (Crocuta crocuta). How, you may wonder, if they’re female? Well, spotted hyena females have a pseudo penis instead of a vaginal canal. And just like female mammals of any other species, they have to copulate, urinate, and give birth through this pseudo penis. Talk about a difficult life!

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Male and female hyena cubs. Could you have told the males apart from the females without these labels? (Figure from Cunha et al. 2014,  Differentiation)

Let’s back up a bit. Spotted hyenas are the lurching, hunch-backed scavengers of the African savannah, made notorious by Disney’s The Lion King. These predators have an ambiguous look that makes them hard to categorize: are their closest relatives dogs? Cats? Bears? Recent phylogenetic analyses classified hyenas in the suborder Feliformia, grouping them with cats, rather than Caniformia (Tree of Life, 2000). As hinted in The Lion King, hyenas can often have antagonistic relationships with other predators in the savannah, including lions (Kay Holekamp, pers. comm.). By ganging up as a group, they can “raid” lion kills to steal the carcass away from the lionesses (see video below). This strong social intelligence has been studied in captivity – in fact, much recent research about hyenas came out of a colony kept at the Berkeley Field Station here in California, where researchers found that hyenas can outperform chimpanzees in social cooperation tasks, without training (Drea & Carter 2009). That’s at least one fact that The Lion King got wrong: hyenas are not just dull-witted minions!


Hyenas gang up on lions and raid their kill. [Source: EarthTouch News Network]

Captive hyenas demonstrate their prowess with problem-solving tasks. Here, the hyenas must open a “puzzle box” to get access to food. [Source: Animal Behavior and Cognition Lab] (*not to be confused with the synonymous lab at UC Davis, here)


Given their social intelligence, hyenas have a particular social structure: matriarchal societies. This means that females are the queen bosses of the clan. This is different from say, lions, where the males are dominant in the pride, and compete over access to females and resources. In hyena societies, females are dominant, and are highly aggressive towards males, who are often at the bottom of the pecking order for access to food and other resources. The dynamics of a social order maintained by aggressive females may be one of the reasons hyenas have such a weird reproductive system: it is argued that the “masculinization” of their bodies and behavior allows females to reap benefits that usually go to males.

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Spotted hyena society is characterized by strong female bonds, matriarchies, and males at the bottom of the so-called “pecking” order [Photo taken by Oliver Höner, Source]
So, why does a female hyena have junk that looks like a male’s? To explain this, we need a quick primer on normal mammalian reproductive development. Back to Physiology 101! “Normal” reproductive development (in rodent models, at least), starts with a gene hard-coded on the Y chromosome (which only males have) that codes for testes. Without this gene, ovaries will develop. So, XX individuals will develop ovaries because they don’t have the gene, and XY individuals will develop testes since they do. Testes and ovaries (the gonads), produce sperm and eggs, respectively, but also produce sex hormones, like testosterone and estrogen. The male baby’s newly-formed testes will start producing testosterone in the womb, while the female’s ovaries will stay quiet. This testosterone goes on to stimulate the growth of the penis and scrotum (affectionately, the ball sac).  Without testosterone, the baby’s tissues develop into the female external parts.

sex_determination
This schematic depicts conventional mammalian reproductive organ development and in utero responses to hormones, which determine how different doodads develop in male vs. female embryos. However, spotted hyena sexual development does not follow this pattern!

Given this developmental pathway, scientists hypothesized that somehow female hyenas must be producing testosterone while in the womb, just like other male mammal babies do. However, researchers found that baby hyena testes produce testosterone, while baby hyena ovaries do not (Brown et al 2006 ). So, hyena sexual development seemed to be the same as every other mammal. Since the female babies weren’t producing testosterone themselves, the next guess was that their mothers (already “male”-like) were producing the hormone which would then be delivered to developing embryos. Studies found high levels of androsteionione – a hormone that acts similarly to testosterone – in the hyena placenta. This seemed like the end of the story, but elegant experiments on the captive Berkeley hyenas demonstrated that this wasn’t the whole picture. Dr. Christine Drea and colleagues gave hyenas anti-androgens – drugs that would stop the effects of testosterone or hormones like it – to see what would happen to the female babies that grew up. They hoped to produce a “normal” female hyena – with normal holes and parts just like a lioness or other female mammal. Instead, the females still had their weird pseudo-penis – testosterone wasn’t necessary! This suggests that hyena genitals are dependent on genes encoding them, not just the hormones they are exposed to. Interestingly, however, females that got the anti-androgen drug actually had an easier time giving birth through their pseudo-penis. Many first-time hyena moms lose their first baby because their genital tract has to tear open – yikes! – which means the birthing process takes a long time and the baby often dies in the process. This suggests that females pay a fitness cost for having the aggressive, “male” advantage – they are less successful in birthing babies (Drea et al 1998; Drea et al 2002; Glickman et al 2006).

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First-time hyena mothers pay a fitness cost when delivering their cubs because their penis-shaped reproductive tract literally has to tear open during the birthing process. Now that’s what you call a labor of love. [Source]
Overall, the hyena exemplifies why it is important for scientists to study other animals than the typical lab rats, mice, and monkeys. By discovering more of the physiological diversity in other species, we can better understand mechanisms in our own bodies, which might help diagnose and cure human disease. Besides, hyenas would make sex-ed class way more exciting, and they can teach us something new too!

[By: Victoria Farrar]


References:

Browne P, et al (2006) Endocrine differentiation of fetal ovaries and testes of the spotted hyena (Crocuta crocuta): timing of androgenindependent versus androgen-driven genital development.  Reproduction 132, 649-659

Drea CM, Carter AN.(2009) Cooperative problem solving in a social carnivore. Animal Behaviour, 78 (4): 967 DOI: 10.1016/j.anbehav.2009.06.030

Drea CM, et al (2002) Exposure to naturally circulating androgens during foetal life incurs direct reproductive costs in female spotted hyenas, but is prerequisite for male mating. Proc Biol Sci 269, 1981-1987

Drea, CM et al. (1998) Androgens and masculinization of genitalia in the spotted hyaena (Crocuta crocuta). 2. Effects of prenatal anti-androgens. J. Reprod. Fertil. 113, 117–127

Glickman SE, et al (2006) Mammalian sexual differentiation: lessons from the spotted hyena. Trends in Ecology and Metabolism, 17(9).

Tree of Life Web Project. 2000. Carnivora. Dogs, cats, bears, raccoons, weasels, mongooses, hyenas, seals, walruses, etc.. Version 01 January 2000 (temporary). http://tolweb.org/Carnivora/15971/2000.01.01 in The Tree of Life Web Project, http://tolweb.org/

Main featured image source:  http://www.freestockphotos.biz/stockphoto/17760

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