I don’t find this theory plausible. Sunfish, which prey on tiny shrimp in the water during the day, have great eyesight. As predators, they estimate size and distance very well, constantly using these abilities to decide which prey to catch and which to ignore. Lots of visual cues distinguish a medium male from a female, including simply size and shape. A fish that can detect the difference between a 1- and 2-millimeter shrimp 1 meter away can surely detect 2 centimeters of difference between two fish right next to him. In addition, the large male has lots of time to check out a medium male as they turn together in courtship for up to ten minutes. During this time, the large male can see that the medium male isn’t laying eggs.
If the large male were being deceived, he should occasionally break off the three-way mating ceremony. For a large male and a female to swim in formation with the medium male squeezed in between, precision is needed. If the large male were being deceived, he would maneuver to exclude the medium male once the medium male was discovered to be producing sperm rather than eggs, just as the large male actively chases off small males. Furthermore, when two actual females are in the territory with a large male, the three don’t swim together in a three-way mating ceremony. If the large male believed the medium male was a female, then he shouldn’t carry on a three-way mating ceremony with him.
The explanation for why the large male doesn’t chase off the medium male once the deceit is discovered is supposed to be his worry about losing fertilizations while the female is actively laying eggs. But the large male does chase small males in spite of this same cost. To counter this, it’s further argued that the medium male’s female coloration suppresses the large male’s tendency toward aggression.
All in all, this theory is another instance of biologists explaining away something surprising by assuming the animals are somehow incapacitated. The large male should chase away the medium male, shouldn’t he? And if the large male doesn’t—well then, for some reason he just can’t. A large male is too dumb to tell a medium male from a female. A large male can’t turn his aggressiveness on when he needs it.
COMMON UNGENDERED SIGNAL
An alternative theory is that the medium male is helping the large male, that they are working together as a team.9 How? One possibility is that the two males together are more successful at attracting a female than one male is by himself. Females prefer to lay eggs in territories in the midst of many males because collectively many males protect against predators better than an isolated male does. Therefore, a territorial male might enhance his chances of attracting a female if he teamed up with a medium male. Teaming up with a medium male might seem more appealing from his point of view than teaming up with another large male because the medium male, with smaller gonads, produces fewer sperm than a large male would. By teaming up with a medium male, he obtains a helper at the least cost.
According to this theory, the fertilizations obtained by the medium male are not stolen from the large male, but actually offered to him by the large male as an incentive to stay, a transaction based on reproductive opportunity. The courtship that precedes the medium male joining the large male’s territory amounts to a job interview. Medium males have female color patterns, this theory claims, to act as a white flag, an invitation to cease hostility and aggression. The medium male resembles a female by coincidence, because both are sending the same signal, flying a white flag. By this account, the medium male is a bona fide male known to all as male, even though he happens to be flying the same colors as a female.
Although this theory does seem plausible to me, I’m still suspicious. It seems a bit too male-centered, suggesting that the more males the better—more males mean more protection, more aggregate masculinity means more attractiveness.
Well, maybe. But what about the function of female and medium male coloration? Are these only ungendered white flags? Or does the medium male really intend to be a feminine male, and is the large male specifically employing a feminine male as a helper, rather than a smaller version of himself?
MALE FEMININITY
I suggest a third interpretation, that females view a large territorial male as dangerous, to be approached with caution. A female might wonder if she will suffer domestic violence from this male who’s trying to look big and powerful. She sees the large male chase neighbors and small males. All she sees is violence. Where’s the evidence that this good-looking guy with a great territory is safe to be with? Conversely, how is a large male to say that he’s gentle after all—that all the tough stuff is reserved for male colleagues?
Perhaps the courtship between the large male and the medium male offers the female a chance to see how the large male behaves with a feminine-looking fish who is slightly smaller than she is. She can watch how the large male does his courtship turning with the medium male. She can watch whether the large male is aggressive toward the medium male. Of course, a large male who is kind to a medium male is not guaranteed to be kind to her too, but at least watching how the large male behaves with the medium male supplies evidence, which is better than just going on a hunch.
Furthermore, once the medium male is sandwiched between the large male and the female during their combined courtship turns, he may somehow facilitate the mating process by synchronizing the release of egg and sperm. The medium male may protect the female from spawning harassment through his position between her and the large male. Also, the medium male may have developed a relationship with the females while schooling with them, and thus be able to vouch that the large male is safe.
In my interpretation, the medium male’s femininity as such has a genuine, nondeceptive role. I suggest that the feminine male is a “marriage broker” who helps initiate mating, and perhaps a “relationship counselor” who facilitates the mating process once the female has entered the large male’s territory. This service is purchased by the large male from the small male with the currency of access to reproductive opportunity.
Thus, the second and third theories both view the medium male as working in tandem with the large male, rather than as stealing from him, and extend the concept of a helper. Sharing fertilization represents an incentive to stay, not theft. To coin some new biology jargon, we might say that a medium male is a prezygotic helper, in contrast to the postzygotic helper, who assists in caring for offspring that have already been born. Nothing prevents animals from cooperating in bringing about a mating, as well as in caring for young after a mating—the animal counterparts of a dating service selling prezygotic help, and a pediatric clinic selling postzygotic help (see the discussion of ruffs in chapter 7).
In view of the roles played by the three male genders, let’s agree to call the large male a “controller,” the small male an “end-runner,” and the medium male a “cooperator.”
THREE MALE, ONE FEMALE-OTHER CASES
The services of the third male gender, typically the intermediate body size type, are purchased by controller males with the currency of access to reproductive opportunity. The services that are most valuable to the controller vary with the circumstances.
The wrasses of Europe are as interesting as those on coral reefs. These species don’t do any sex changing, but they do have multiple male genders. The two-male species have a controller morph that is colorful, territorial, and guards eggs, plus an end-runner morph that is smaller and plain-colored. The three-male species add a medium-sized male, offering a useful comparison to the North American sunfish.
Take the spotted European wrasse (Symphodus ocellatus), which lives in the shallow water of the Mediterranean along rocky shores. Biologists have observed these wrasses while scuba diving in Revellata Bay, west of Calvi on Corsica.10 These rather small fish live for up to three years, breed during the summer, and have a maximum length of 8 centimeters. Of the three morphs, the medium male is again the most interesting. This medium male does not look or act like a feminine male. It’s a bit bigger than a female, has its own distinctive coloration, and can be aggressive. Nonetheless, the medium male is enticed by the large male into his territory and fertilizes some of the eggs laid in the territory. Why? The large male has apparently hired the medium male as a security guard. The medium male chases away small males that the large male would otherwise have to chase away