For mammals that returned to the water, tucking everything back up inside seems only sensible; a dangling scrotum isn’t hydrodynamic and would be an easy snack for fish attacking from below. I say snack, but the world record-holders, right whales, have testicles that tip the scales at more than 1,000 pounds apiece. The trickier question, which may well be essential for understanding its function, is why did the scrotal sac lose its magic for terrestrial hedgehogs, rhinos, and scaly anteaters?
The scientific search to explain the scrotum's raison d'être began in England in the 1890s at Cambridge University. Joseph Griffiths, using terriers as his unfortunate subjects, pushed their testicles back into their abdomens and sutured them there. As little as a week later, he found that the testes had degenerated, the tubules where sperm production occurs had constricted, and sperm were virtually absent. He put this down to the higher temperature of the abdomen, and the cooling hypothesis was born.
In the 1920s, a time when Darwin's ideas were rapidly spreading, Carl Moore at the University of Chicago argued that after mammals had transitioned from cold- to warm-blooded, keeping the body in the mid-to-high 90 degrees must have severely hampered sperm production, and the first males to cool things off with a scrotum became the more successful breeders.
Heat disrupts sperm production so effectively that biology textbooks and medical tracts alike give cooling as the reason for the scrotum. The problem is many biologists who seriously think about animal evolution are unhappy with this. Opponents say that testicles function optimally at cooler temperatures because they evolved this trait after their exile.
If mammals became warm-blooded 220 million or so years ago, it would mean mammals carried their gonads internally for more than 100 million years before the scrotum made its bow. The two events were hardly tightly coupled.
The hypothesis' biggest problem, though, is all the sacless branches on the family tree. Regardless of their testicular arrangements, all mammals have elevated core temperatures. If numerous mammals lack a scrotum, there is nothing fundamentally incompatible with making sperm at high temperatures. Elephants have a higher core temperature than gorillas and most marsupials. And beyond mammals it gets worse: Birds, the only other warm-blooded animals, have internal testes despite having core temperatures that in some species run to 108 degrees.
Any argument for why cooling would be better for sperm has to say exactly why. The idea that a little less heat might keep sperm DNA from mutating has been proposed, and recently it's been suggested that keeping sperm cool may allow the warmth of a vagina to act as an extra activating signal. But these ideas still fail to surmount the main objections to the cooling hypothesis.
Michael Bedford of Cornell Medical College is no fan of the cooling hypothesis applied to testicles, but he does wonder whether having a cooled epididymis, the tube where sperm sit after leaving their testicular birthplace, might be important. (Sperm are impotent on exiting the testes and need a few final modifications while in the epididymis.) Bedford has noted that some animals with abdominal testes have extended their epididymis to just below the skin, and that some furry scrotums have a bald patch for heat loss directly above this storage tube. But if having a cool epididymis is the main goal, why throw the testicles out with it?
Another proposal for how the scrotum generates better sperm is that the scrotal sac serves as a school of hard knocks. Scott Freeman of the University of Washington hypothesized that the scrotum's poor blood supply keeps the testicles in an oxygen-starved environment and so toughens up the sperm. Deprived of oxygen, sperm might react like "muscle cells to aerobic training," increasing the number and size of mitochondria they contain and therefore becoming better prepared for the herculean task of ascending a cervix, uterus, and fallopian tube.
The main problem with the training hypothesis is that it was primarily concerned with the testicles’ lousy blood supply rather than their expulsion¾surely it would have been easier to evolve poor gonadal vasculature while keeping them in the body?
The alternative to scrotums benefiting sperm is that in some other way, despite their fragility, they actually benefit their owner. Such a notion was first presented in 1952 by a Swiss zoologist named Adolf Portmann after he'd presented the first major attack on the cooling hypothesis. What he proposed instead was the display hypothesis. Portmann argued that by placing the gonads on the outside, the male was giving a clear indication of his "reproductive pole," a sexual signal important in intergender communication. Portmann’s best evidence was a few Old World monkeys who have brightly colored scrota.
This theory is not widely accepted because such conspicuous displays are rare (many scrotums are barely visible) and bright coloration seems to have evolved long after the original scrotum. Some have suggested it’s not surprising that in its 100 million-year existence, the scrotum has been co-opted as a sexual attractant by a handful of groups.
I was just about to discard the display hypothesis when two things happened. First, a colleague returned from her honeymoon in Tanzania excitedly showing anyone who'd look photos of a scrotum. The scrotum belonged, don't worry, to one of Portmann's Old World monkeys, a vervet monkey, and it was screamingly, beguilingly bright blue.*
OK, it's just one monkey, I thought, but then I met Richard Dawkins. I had three minutes with the esteemed evolutionary biologist at a book signing, so I asked him for his opinions on the scrotum. After expressing severe doubt about the cooling hypothesis, he said he wondered whether it might have something to do with evolutionary biology's handicap principle.