The Evolution of Ape Ejaculate.

There have long been attempts by evolutionary biologists and evolutionary psychologists to understand just what effect different mating systems have on evolution. Certainly, mating systems in which a male is able to sire many offspring with many different females will cause natural selection to favor different traits than one in which a male is limited to one female. Additionally, a mating system that causes some types of competition to become more extreme can greatly reduce other types of competition. Gorillas, for example, are polygamous, with one male controlling a harem of females to which he has exclusive access. In a situation such as this, there is extreme competition for gaining control of such a harem, but little competition for mating once dominance is established. As a result, there is selective pressure for gorilla males to beat back other males and become dominant, and the results are obvious: gorillas exhibit the greatest sexual dimorphism of any living primate, with males almost twice as large as females. Selection favors the big and brawny types who can successfully fight off their rivals. But there is another form of competition, one in which gorillas aren’t subjected much to – competition between sperm to be the first to reach the egg. There are any number of ways in which sperm from different males can compete, the most obvious of which is through simple quantity. But since male gorillas can be pretty well assured that the females in their harem will mate only with themselves, their sperm has no competition, and it shows when it comes to quantity: male gorillas have the smallest testes to body weight ratio of the great apes. That’s right, the burly boys of the ape world aren’t really packing that much down below, but I still wouldn’t poke fun at them.

You can see how mating systems affect evolution throughout the primate world of which we are a part. Chimpanzees, whose females are very promiscuous, tend to have little sexual dimorphism but a very large testes to body weight ratio. For them, the selective pressure is more heavily focused on post-copulatory sperm competition rather than simple fighting ability. Gibbons, on the other hand, are strictly monogamous. They have little sexual dimorphism and a small testes to body weight ratio. For them, there isn’t much competition to fight off rival males or to thwart rival sperm. We humans seem to be somewhat in the middle, with a moderate amount of sexual dimorphism and a moderate testes to body weight ratio, indicating that during our evolutionary past, we weren’t nearly as monogamous as we’d like to think. But at least we weren’t as slutty as the chimpanzees. (Our lack of total monogamy is corroborated by additional evidence from our genome, some of which Carl Zimmer talks about here.)

Now a new piece of the puzzle has been tossed into the mix, thanks to some new research appearing in Nature Genetics by Steve Dorus and coworkers. The new study, titled “Rate of molecular evolution of the seminal protein gene SEMG2 correlates with levels of female promiscuity” (subscription required), focuses on another facet of sperm competition other than simple quantity. In this case, post-copulatory semen coagulation.

The gene that the authors looked at codes for the protein semenogelin, which undergoes covalent cross-linking to form a seminal coagulum after ejaculation. A protease later breaks up the coagulum and releases the sperm. It’s been proposed that this process of forming a coagulum and later releasing the sperm aids in getting sperm to where they need to go, and, more importantly for our discussion, preventing a rival’s sperm from getting there first. For one thing, the semen coagulum can block other semen from getting to its destination, in some cases forming a “plug” which blocks access altogether. A previous study showed that there is a strong correlation between the thickness of the coagulum and the promiscuity of females. Species in which females mate with multiple males have thicker or more plug-like coagula.

Dorus and coworkers decided to look at the evolution of semenogelin in humans and several related species, and attempted to see if there was a correlation between evolutionary rate and mating system. What they found was that in species in which females mate with multiple males, semenogelin has been evolving faster than in those who are monogamous or polygynous. The results are shown in graph A of the following figure, and they look quite similar to the correlation between female promiscuity and testes size shown in graph B.

On the Y-axis, the lower-case Greek letter ‘omega’ represents the ratio of nonsynonymous to synonymous mutations. A ratio above 1 indicates positive Darwinian selection, whereas a number less than 1 represents purifying selection, and a ratio of exactly 1 represents neutral evolution. We can see that there appears to have been substantial positive selection in chimpanzees (who also have the highest slut factor), somewhat less but still decidedly positive for macaques, and around one or less for the rest of us prudes. We humans, yet again, fall somewhere in the middle.

These results suggest that post-copulatory sperm competition drives the evolution of semenogelin. To complement this study, we’ll need to see what biochemical properties of the protein have presumably been selected for in chimpanzees, for example, and how they give sperm a tail up on the competition. For now we don’t know much other than the fact that semenogelin has undergone positive selection, and that it’s highest in polyandrous species. It’s interesting to note that the protease that liquefies the coagulum, kallikrein 3, did not show any signs of positive selection. That would indicate that it’s some property of coagulum formation, rather than liquefaction, that allows some sperm to do better than others. There’s bound to be lots more fascinating research in this area, thanks to those intrepid scientists who study monkey splooge.

Update: It’s been brought to my attention that people may lose their appetite from reading this topic, and that they should be forewarned. Since I am a caring person, here goes: Don’t read this post before mealtime.