True Hermaphrodites

Underwater Curacao

Note: This post is first of a series on sexual development and sex differences.

The following was partly motivated by what I observed underwater in Curacao. But motivated as well by my ex-mother-in-law. The subject of interest in both cases was a fish, called the “hamlet”. There are about 10 species of hamlets, all belonging to the genus Hypoplectrus, which, in turn, belong to the family of fishes that includes groupers and sea basses, called Serranidae. I have never heard an explanation for the common name, hamlet, of these fishes; But I’m pretty sure it doesn’t refer to Shakespeare’s famous protagonist.

I first learned of hamlets, while at U.C. Berkeley, from the eminent ethologist and ichthyologist, George Barlow. He was among the first to recognize their unusual mode of reproduction, called egg trading. To trade eggs, of course, both individuals must be able to make eggs. But eggs alone are insufficient for sexual reproduction. At some point sperm must enter the equation. Fortunately, for the egg traders, they can supply the sperm as well, for they are true hermaphrodites, replete with both functional ovaries and testes, ergo, functional eggs and sperm. Hamlet sex is unusually reciprocal. Some background is required here.

Hamlets live at quite low densities, for reasons we can ignore here. They spend their lives hunting near the bottom of the reefs in well demarcated territories. Near dusk, every day of the year, their hostility toward others of their kind temporarily abates and they seek out a neighbor, often the same neighbor. The rendezvous spot is also the same, day in and day out. This is where the egg trading occurs. Their courtship is brief, as befits old acquaintances. For the sexual act itself, the two hamlets briefly wrap their tails around each other’s abdomen, at which point one releases eggs and the other releases sperm. They then separate and sink toward the bottom. But soon they rise again together and repeat the mutual wrapping, but this time the roles are reversed, egg and sperm-wise.

The cycle is repeated several times before the egg supplies are mutually exhausted. (Sperm which is much cheaper to produce, is virtually inexhaustible.). Twenty-four hours later, their eggs replenished, they reconvene at the same spot, to do some more “trading”. And so on.

Hermaphroditism

In Curacao, it occurred to me that though I had used the term thousands of times in my research and after, I really didn’t know the derivation of the word, hermaphrodite, its etymology. As a Greek word, I figured it had to derive from Greek mythology. Fortunately, I had on my Kindle, Ovid’s “Metamorphoses”, the idiosyncratic and relentlessly entertaining, retelling of tales from Greek mythology. Ovid was an envelope pusher and famously pissed off Augustus Caesar, to the point that he was ultimately exiled to a Black Sea port in present day Romania, where he spent his last years.

It is amazing how much of Greek mythology that has reached us today has arrived through the filter of this Roman Poet. The Tale of Hermaphroditus is one example. (But keep in mind that Ovid felt no obligation as to fidelity to original sources. For the Metamorphosis, He viewed Greek mythology as a raw material for his creative imagination.)

On all accounts, Hermaphroditus was the son of two gods, Hermes (whom the Romans called Mercury) and Aphrodite (whom the Romans called Venus). Hermaphrodite is a combination of the names of the two Greek Gods, Hermes and Aphrodite. Hermaphroditus was born a typical male, as typical as a male can be when both your parents are gods. Physically, all we known from Ovid, is that he was extremely comely. Too comely for his own good as it turned out. While bathing nude in a pool of crystalline water, he attracted the attention of the nymph (naiad to be exact), Salmacis. She was an atypical nymph. Most obviously, she rejected the ways of Artemis. This is important, because all nymphs were part of that God’s entourage. That was the whole point of being a nymph.

Unlike Artemis, Salmacis was vane and lazy; she flat out refused to hunt. Most relevant for Hermaphroditus she rejected the vow of virginity. In fact, according to Ovid, she was something of a nymphomaniac, though I don’t believe the source of that term.  When she spied the naked Hermaphroditus, she forced herself upon him sexually and refused to let go. (Remember, this is myth logic. And I have no problem adopting myth logic, especially Greek myth logic. But what transpires next is problematic even from a mythical logic perspective.) Salmacis did not succeed in raping Hermaphroditus, which would strain even mythic credulity, but she did succeed in her plea to the Gods that she be united with Hermaphroditus forever. This request, from a notorious ne’er-do-well, was inexplicably granted. As a result, Hermaphroditus, from then on, possessed both male and female attributes, most obviously a penis and breasts. Hence, forever after, hermaphrodites combine male and female elements.

In his account, Ovid, to my mind, violates mythological logic. First and foremost, the Gods to which Salmacis pleaded, included the parents of Hermaphroditus himself, Hermes and Aphrodite. Both were not just Gods, but Olympian Gods, the highest echelon of Godness. There were only twelve, if you count Dionysus. Why on earth, or in this case, Mount Olympus (think heaven), would these Olympian gods grant her wish. It couldn’t have been on the recommendation of Artemis, another Olympian. Nor does it seem mythologically logical that Hermes or Aphrodite would want to saddle their son, for eternity, with this vane and lazy nymphomaniac. I wish that, at the very least, Ovid had blamed it on Zeus, a serial philanderer and rapist (both god and human), who despite his obvious faults, was the Chief of the Olympian gods. He is also the only Olympian god that could have possibly sympathized with Salmacis.

But Hermaphroditus is/ was a god for god’s sake; why couldn’t he have dealt with Salmacis all by himself. As a nymph, Salmacis was also a divinity, but a minor one, not a god born of two Olympian gods, not a god, certainly, of Hermaphroditus’s stature. It makes no sense that she could have done a full body merge, Zeuss or no Zeuss, unless Hermaphroditus himself was tempted at the prospect.

A simpler explanation for the hermaphroditism of Hermaphroditus, one that is more consistent with mythological logic, is that for whatever reason he was born that way. Since Hermaphroditus is the prototype for human hermaphroditism, it’s worth exploring what hermaphroditism means in human discourse and how it differs from the hermaphroditism of hamlets, other fishes, and a whole lot of other animals.

Until recently, the criteria for hermaphroditism in humans were, except in a few rare cases, quite superficial. Most concern what are known as secondary sexual characteristics, those traits most influenced by gonadal hormones. This superficiality was recognized by the American Medical Society, which now discourages the use of the term, as well as “intersex” and “pseudohermaphrodite”. All have been subsumed under the label “disorders of sexual development” (DSD), though this term itself has become controversial among those advocating for more tolerance of the sexually atypical. Disorders of sexual development come in varying degrees, depending on the developmental cause.

The least fundamental, biologically, result from abnormally high testosterone levels in females or abnormally low testosterone levels in males. One example of the former is called congenital adrenal hyperplasia. As the name implies this disorder is rooted in the adrenal glands, the main source of cortisol. The synthesis of cortisol shares steps with sex hormone—including—testosterone synthesis. Competition for the precursor chemicals for both can result in low cortisol levels and high testosterone levels.  Affected females are outwardly masculinized in obvious ways, sometimes behaviorally. Conversely, several developmental disorders can result in abnormally low testosterone levels in young males, or in androgen insensitivity of the target tissues. In either case, the penis and testicles are markedly reduced, enough to cause misdiagnosis of sex at birth.

More fundamental causes of disorders of sexual development result from sex chromosome abnormalities. Sometimes XX individuals develop male gonads and produce sperm. Alternatively, some XY individuals are (gonadal) biological females, though often outwardly atypical.

But the closest humans approach hamlet level hermaphroditism are rare cases of individuals with both ovarian and testicular tissue, sometimes called ovotestes. Unlike hamlets, however, such individuals do not produce both eggs and sperm. Most produce neither, a few can generate viable eggs.

In summary, there are no true human hermaphrodites. In fact, there is no truly hermaphroditic mammal or bird. I have long been interested in finding the answer as to why this is the case. The question naturally arises because sexual development across these all vertebrates is remarkably conserved, from brain to gonad, hormones included. But I’ll save my take on that subject for another day. In the next post in this series, I will explore other forms of true hermaphroditism in fishes. First though, back to my ex-mother-in-law.

The Barbados Affair

I tried to minimize my exposure to the in-laws during my marriage, so I had to be coerced to spend a week with them and my then wife in Barbados. I only assented after a promise that I could dive every day. Unfortunately, Barbados is a pretty crappy place to dive, certainly by Caribbean standards. Nonetheless, those dives were welcome reprieves from socializing. Moreover, I did see two frogfish, an exciting experience for any diver. I also observed hamlets on every dive, though not their mating.

At one dinner, under the influence of a couple of shots of the local (Mount Gay) rum, I overcame my usual reticence to talk to my in-laws about my research or anything remotely related to it, and relayed the hamlet story in what I thought was an entertaining and compelling way. They seemed interested, enthralled, in fact. But later that night I found out otherwise. The corridors of this small hotel had remarkable acoustics; while walking to deliver a book from my wife to the mother-in-law, I heard the latter loudly exclaim to the father-in-law, from the floor above, something to the effect of “I hope you didn’t believe a word of what he said about the fish”. Most people, though surprised when the hamlet story is told, react with a sense of delight at the wonders of nature. But this woman was so complacently parochial that my hamlet story offended her sensibilities; she couldn’t accept such exotic information. I had to be making it up.

I aborted the book delivery and retreated to the sanctuary of the room I shared with my then wife. I relayed what I heard, expecting an expression of sympathetic outrage but was instead emphatically instructed not to bring it up the next day. I said, I had no intention to do so; that was her job. She demurred. Our relationship, already on a downward trajectory, hit a markedly slope steepening inflection point then and there.