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6

Multiple-Gender Families

The social roles of multiply gendered animals are indicated by their bodies. Males or females in a species may come in two or more sizes or colors. The morphological differences are the tip of the iceberg. The two morphs approach courtship differently, have different numbers of mates, have different arrangements of between-sex and same-sex relationships, live different life spans, prefer different types of real estate for their homes, exercise different degrees of parental care, and so on. Because body shape, color, and posture—the important modes of communication in fish and lizards—are so easily visible to biologists, multigender societies are better described in these groups than in groups that communicate more by sound and scent.

Biologists have struggled with naming these within-sex polymorphisms. They may be called alternative mating strategies to emphasize the different approach of each morph to courtship. Or they may be called alternative life histories to emphasize the different life path each morph takes. Previously, I suggested that we call these different expressions of how to live “genders.” I feel this word best captures the totality of the differences between the morphs, extending from mating, through lifestyle, to length of life.

Phrases like “alternative” mating strategy or “alternative” life history are especially poor names for multiple genders because the “alternative” strategy is usually the most common strategy. Singling out a minority strategy as “normal” and labeling the rest “alternative” is simply prejudice. Societies with multiple genders are not easy to describe because we’re not prepared to find what we actually see. But let’s wade in.

TWO MALE, ONE FEMALE

The first step beyond one-male one-female two-gender societies are those with two male genders and one female gender, making three altogether. Here’s a sample.

Bullfrogs (Rana catesbeiana) have two male genders: large males who call at night, giving bullfrogs their name, and small males who are silent.¹ Both are reproductively competent, and females mate with both. Silent males turn into calling males as they grow older. Male frogs in other species² and males in many vertebrate groups also have to decide when to begin breeding—whether to wait until established enough to flaunt wealth and power, or to begin sooner with fewer resources but lots of charm. Perhaps silent males should not be considered a different gender from calling males, but rather an early developmental stage of the same gender. Compare this case with others, though, and you may agree that it makes more sense to view males who mature from a silent stage into a calling stage as changing genders.

Did you know a fish could sing? There is a fish in the bays and estuaries of the Pacific coast, including San Francisco Bay, called the plainfin midshipman (Porichthys notatus) because of its bioluminescent spots, which resemble rows of buttons on a Navy uniform. These fish are also known as the California singing fish or canary-bird fish. The species has two male genders who behave somewhat like bullfrogs. The large male gender consists of fish who defend territories and guard the eggs laid in them. To signal readiness to mate, a large male emits a low humming sound for as long as fifteen minutes, and a female may respond by entering the territory and laying eggs there. Females lay only one batch of eggs. A large male guards a big collection of eggs laid by five or six females. The small male gender consists of fish that mature at a younger age and are silent, like the silent bullfrogs. They don’t defend territories. Instead, they mate by darting in to fertilize eggs being laid in a large male’s territory.

This fish is but one of hundreds of known species where males come in two or more genders. This species is unusual because its habit of singing has allowed biologists to determine how deeply the anatomy of the two male genders differs. For biology wonks, here are the technical details: The large male gender relative to the small male gender has a relative sixfold advantage in the mass of sound-producing muscles, a three-to fivefold increase in the number and diameter of sound-producing muscle fibers, a cellular ultrastructure with enlarged zones densely filled with mitochondria, a more branched endoplastic reticulum, larger sarcomeres, and Z-lines that are twenty times wider. Motoneurons and pacemaker neurons are also three times larger, as well as sonic axons with terminal boutons two to three times larger. And so on. Even without being a biology wonk, the large male and small male genders clearly represent deeply different developmental programs, involving different expressions of entire suites of genes.³

Thus, both the bullfrog and plainfin midshipman have a calling large male gender and a silent small male gender. A bullfrog male changes from the small gender to the large gender as he ages, whereas a male plainfin midshipman is locked into one of these genders for life.

In the Pacific, coho salmon (Oncorhynchus kisutch) have two types of males. A “jack” spends two years in the ocean before returning to streams to breed, and a “hooknose” spends three years in the ocean before returning to breed. The female spends three years in the ocean too. All three types die after breeding. A jack is small and cryptically colored, and a hooknose is big, has a pronounced snout (hence its name), and is brightly colored.

The females excavate a nest in the gravel in which they lay their eggs. When they do, the closest male fertilizes the most eggs. Hooknose males are better than jacks at fighting for position near a female and wind up with the most fertilizations. The jacks obtain some fertilizations by darting in under the female while she is laying eggs. The benefit for the jack of being able to breed one year earlier and avoiding the hazard of living another year at sea compensates for its relative disadvantage in fertilizations compared with the hooknose. Jack and hooknose coho salmon appear to have equally successful strategies of life.⁴

In the Atlantic, salmon (Salmo salar) have some males that migrate from rivers to the sea as smolts and return after about five years as large anadromous males about 75 centimeters in length. Other males, called parr, don’t bother journeying to the sea. They remain in the streams and mature in about three years at near 50 centimeters. The females also migrate to the sea and return. At spawning, a large anadromous male defends access to a female, while the parr hang out downstream. When the anadromous male and female are mating, the parr dart in and obtain some fertilizations. These two male life strategies work out to have about the same overall success when survival and mating access are factored in.

Male red deer (Cervus elaphus, also called elk) who don’t have antlers probably are counterparts of the silent male frogs.⁵ Called hummels (or notts), these deer are in better physical condition than males with antlers, and may at times be more successful at mating.⁶

THREE MALE, ONE FEMALE-SUNFISH

Now to species with three male genders. The females here have one gender, making four genders in total. A good example is the sunfish, a deep-bodied fish averaging about 10 centimeters in length and exceedingly common in North American lakes. When I was in high school in New Jersey, I remember seeing sunfish underwater. Every time I went snorkeling in one of the nearby lakes, I would see them through my face mask. If I went fishing, all I would catch were sunfish. Everybody took these fish for granted and hoped to catch a perch or other rarer fish. I would never have guessed that these everyday freshwater fish from the United States and Canada would someday challenge the foundations of gender and sexuality.

One sunfish species, the bluegill sunfish (Lepomis macrochirus), has been studied in detail at Lake Opinicon, Ontario, Canada, and at Lake Cazenovia, in upstate New York.⁷ Spawning males consist of three distinct size/color classes, and together with females, fall into four morphological categories, corresponding to four distinct genders:

1 Large males are about 17 centimeters long and eight years old. Their gonads constitute 1 percent of body weight, and they have a light body color with a yellow-orange breast.

2 Medium males are about 10 centimeters long and four years old. Their gonads are 3 percent of body weight, and they have a dark body color marked with dark vertical bars.

3 Small males are about 7 centimeters long and three years old. Their gonads are 5 percent of body weight, and they have a uniformly light body color with neither a yellow-orange breast nor dark vertical bars. The testes may occupy most of the body cavity, crowding the stomach and displacing the intestines.

4 Females are about 12 centimeters long and six years old, making them larger than the medium males by about 2 centimeters and older by about two years. At breeding, females bulge somewhat with eggs. Females have a dark body color with vertical bars, like the medium males. The medium males somewhat resemble small young females because of the similarity of color pattern.

The yearly spawning episode lasts only one day. In preparation, large males aggressively stake out territories next to one another in aggregations of a hundred or more, called leks, along the bottom of the lake at a depth of 1 meter. Large males are called on to defend their space against neighbors about once every three minutes. Large males make nests for eggs in their territories by scooping out a depression in the mud with their tails. Females aggregate at the locales with many males and do not visit isolated or peripheral nests. Females prefer nests belonging to large aggregations because the presence of many males affords more protection from egg predators.

The large males are not Mr. Nice Guys. Their acts of aggression include biting, opercular spreading, lateral displays, tail beating, and chasing. Although primarily directed at intruding males, aggression sometimes is directed at a female in the territory—domestic violence, sunfish style. The male apparently tries to control the speed and timing at which a female lays eggs. Females simply leave if harassed too much in this way.

The females arrive in a school, and one by one they enter the territories of the large males. When a female arrives, a large male begins to swim in tight circles, with the female following. Every few seconds as the pair turns, the female rotates on her side, presses her genital pore against that of the large male, and releases eggs that the large male fertilizes. The egg release is visible as a horizontal dipping motion.

A female may spawn in many nests. A large male accumulates up to thirty thousand eggs from various females during the one-day spawning episode. A female lays about twelve eggs at a time with her dipping motion, so this total egg accumulation involves some female laying in the nest about once every thirty seconds. The scene is fast. Still, large males somehow find the time to enter the nests of neighbors, and about 9 percent of the fertilizations in a nest are by a neighboring large male.

Meanwhile, the small males are active. They stay at the borders between territories of large males and in the periphery, often close to rocks or in vegetation. Eggs remain viable in lake water for about an hour and sperm for only a minute. When the female releases eggs, the small males dart in quickly to release sperm over the eggs and carry out their own fertilizations. The large males try to repel the small males from their territories, but the small males are more numerous than the large males—about seven to one in shallow-water colonies. Chasing all these small males, as well as neighboring large males and the occasional predator, takes a large male away from fertilizing the eggs being laid in his territory. In these circumstances, the females spawn readily with small males while the large male is busy with all his chasing.

There are more small males in shallow-water colonies than deep ones because there is more vegetation for cover. It is important to hide because predators—large-mouth bass, small-mouth bass, and pike—lurk in the lake. Thus the ratio of small to large males depends on the surrounding environmental context. All in all, the small males seem to be the gender counterpart of silent bullfrogs, silent singing fish, jack and parr salmon, and antlerless male deer.

The medium males—the third male gender—are really surprising. No one knows where the medium males live most of the time, but they may school with the females. A medium male approaches the territory of a large male from above in the water and descends without aggression or hesitation into the large male’s territory. The two males then begin a courtship turning that continues for as long as ten minutes. In the end, the medium male joins the large male, sharing the territory that the large male originally made and defends.

Although the medium male sometimes joins the large male before a female has arrived, more often the medium male joins after a female is already present. The large male makes little if any attempt to drive away the medium male, in contrast to the way the large male drives away small males that dart into the territory. When a female and two males are present, the three of them jointly carry out the courtship turning and mating. Typically, the medium male, who is smaller than the female, is sandwiched between the large male and the female while the turning takes place. As the female releases eggs, both males fertilize them.

Occasionally, two females may be within a large male’s territory at the same time. Although the large male mates with both females, the three do not participate in any common ritual similar to the three-way interaction of the female with a large and a medium male.

After the day’s excitement is over, each large male remains in his territory for eight to ten days to guard the eggs. The large male repels nest predators. During this period he never leaves the nest to forage and loses body weight.

In all, 85 percent of spawning males are either small or medium, with the remaining 15 percent large males. Though in the minority, large males take part in most of the matings. Among the large males, the reproductive skew is high and only some of the large males apparently survive the mutual aggression that is necessary to acquire a successful territory. The small and medium males obtain about 14 percent of the spawnings. Overall, 85 percent of the territories in which spawning occurs consist of one male with one female, 11 percent of two or more males and one female—usually a large male accompanied by a medium male—and 4 percent of one male and two females.

Developmentally, the small and medium males are one genotype, and the large males another. Individuals of the small male genotype transition from the small male gender into the medium male gender as they age, whereas individuals of the large male genotype are not reproductively active until they have attained the size and age of the large male gender.

Explaining the medium male gender has caused big-time confusion among biologists. Three theories have emerged.

DECEIT

The most popular theory is that by sharing some female coloration and participating in courtship turning, a medium male deceives a large male into thinking he’s a female.⁸ This female-disguised male then steals some of the fertilizations that rightfully belong to the large male.

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 himself. More interestingly, this species happens to have more females than it does males with territories. During spawning, several females arrive at one nest, and because only one female can spawn at a time while the large male is there, the others wait at the rim of the nest. But females may try to crowd in and interrupt the female who is laying eggs. In this situation, the medium male expels the excess females so the spawning can continue. The medium male then stays with the nest for three days, compared with the full week that the large male sticks around.

The spotted European wrasse has three developmental pathways. One type skips early reproduction and matures into a controller. The second starts as an end-runner and transitions into a cooperator. The third starts as a cooperator and transitions into a controller.¹¹ Thus, comparing wrasses to sunfish, the operational sex ratio may determine whether the medium male is feminine or masculine. If females are scarce, as in sun-fish, the large male will need help attracting them, and a feminine male can assist. If females are common, as in wrasses, the large male will need help keeping order at home. In this case, the controller employs a bouncer instead of a marriage broker.

Another particularly graphic case is found among the cichlids, a family of colorful perchlike fishes found in the tropical freshwaters of Africa, South and Central America, India, Sri Lanka, and Madagascar. About 1,500 species are known, or 5 percent of all vertebrate species! Most species occur in the Great Rift lakes of eastern Africa—Lake Malawi, Lake Tanganyika, and Lake Victoria. Cichlids are most closely related to the saltwater damselfishes, wrasses, and parrotfishes, among others.¹² They are the freshwater equivalent of the colorful and diverse coral reef fish.

Oreochromis mossambicus, a kind of cichlid, from the Incomati River in Mozambique were studied in an aquarium in Portugal.¹³ These fish are rather small, around 6 centimeters, and males come in three genders. The controller recruits the cooperator through a courtship that includes remarkable same-sex sexuality.

The black territory-controlling males form dense aggregations, leks, in the sand or mud during the breeding season. A male digs a pit to attract a female, and after courtship, she lays eggs there. The male then quivers and releases spawn over the eggs. The female inhales the mixture of eggs and spawn into her mouth where the actual fertilizations take place. The female then broods the eggs in her mouth, continuing brooding even after the young fry have hatched, for a total of three weeks. The young are “born” when they swim out of the female’s mouth.

The second male gender is the familiar end-runner, who darts into a controlling male’s territory during spawning and adds some of his own spawn to the mix inhaled by the female. The controlling male aggressively repels the end-runners. The third male gender is once again the most puzzling one. These males have a neutral light color and are actively courted by controller males using the full courtship repertoire used for females, including tilting, signaling the nest, circling, and quivering.

Of six hundred courtships observed, two hundred were directed to these light-colored males and the remaining four hundred to females. In three of the male-male courtships, the light-colored male placed his mouth on the genital papillae of the dark territorial male, then the territorial male quivered and released spawn, whereupon the light-colored male moved his mouth as a female does when she inhales the sperm/egg mix. The end-runners did not intrude into these male-male courtships, although they did dart into male-female courtships, indicating that everyone around knew what was going on.

In most groups of these fish, males courted females more than males. In one group, though, males courted males more than females. The authors concluded that “further experimental work is needed.” In particular, the benefits to the controller presumably provided by the third male gender need to be described.

Male genders may also range from territorial stay-at-homers to non-territorial travelers. Although many of the three-male species are organized according to the template of controller, end-runner, and cooperator, not all are. Among tree lizards (Urosaurus ornatus) living in the American Southwest,¹⁴ the males come in various colors—nine are known for the species. Some populations have only one color, others only two colors, and still others as many as five.

At one site upstream of the Verde River in Arizona, two colors each account for 45 percent of the total males. The orange-blue form is a punk rocker’s delight—an orange chin with a big blue spot in the middle, a throat fan with orange near the body and a blue band at the tip, and blue on the stomach. In contrast, the orange form is solid orange on the chin, throat fan, and stomach. The orange-blue males are the most aggressive, and their body proportions are short and stocky. They are the controllers, defending territories large enough to overlap the territories of three to four females. The orange males are end-runners, but they come in two subvarieties, nomadic and sedentary. Unlike most end-runners, these males are the same weight or heavier than the controllers, although longer and leaner. These males are not aggressive and defer to controllers when challenged.

In a typical dry year, orange males are nomadic, spending only a day or two at a site before moving on. In a rainy year, orange males settle down for the season, becoming sedentary and occupying relatively small territories, the size of a female home range. The controllers and end-runners are fixed for life, although an end-runner can transition back and forth between nomadic and sedentary styles in successive years.

In this species, the hormonal dimension of gender expression has been worked out. Progesterone determines whether a male matures into a controller or an end-runner. A single injection of progesterone given to a tiny hatchling on the day he hatches from the egg will ensure that he matures into an orange-blue controller. In contrast, males with low progesterone develop into orange end-runners.¹⁵ No intermediates occur. Presumably genes produce high or low progesterone levels on the day of hatching, thereby determining whether a male develops into a controller or an end-runner.

As the season progresses and the lizards wait for rain, the oranges listen to the lizard version of Emmylou Harris’s song “Born to Run.” How does an orange male get to feelin’ like it’s time to hit the road rather than settlin’ down for a spell? Orange males are sensitive. When conditions are dry, orange males show high levels of the hormone corticosterone, an indicator of stress. In orange males, corticosterone causes testosterone to decline. This drop in testosterone in turn causes orange males to hit the road and become nomadic.¹⁶ Meanwhile, orange-blue males are indifferent to weather conditions—they tough it out no matter what.

The tree lizards illustrate what are called the “organizing” effects of hormones (irreversible effects that occur early in development) and also the “activating” effects (reversible effects, which usually occur later in life). Progesterone on the day of hatching organizes the male body to mature into an orange-blue controller. Corticosterone from the stress of going thirsty during a drought activates the orange end-runner to turn nomadic rather than remaining sedentary.

TWO MALE, TWO FEMALE

When multiple genders occur in both males and females, we may wonder whether some gender combinations don’t mesh together especially well. Would a feminine male paired with a masculine female be just as successful as macho male with a femme female? What about other pairings too?

White-throated sparrows (Zonotrichia albicollis) of Ontario, Canada, have four genders, two male and two female:

1 A male with a white stripe is the most aggressive, calls often, and is the most territorial.

2 A male with a tan stripe is less aggressive and unable to defend a territory from the white-striped male.

3 A female with a white stripe is aggressive, calls spontaneously, and defends a territory.

4 A female with a tan stripe is the most accommodating of all. When challenged with a territorial intrusion, she continues foraging.17

So, in both males and females, the white-striped individuals are more aggressive than the tan-striped individuals. Ninety percent of the breeding pairs involve either a white-striped male with a tan-striped female or a tan-striped male with a white-striped female—attraction between opposites.

The white-striped male appears to have everything going for him. A female who chooses to pair with a tan-striped male has to settle for an inferior territory. Yet some females do prefer tan-striped males. In studies in both 1988 and 1989, more tan-striped males found mates, and found them sooner, than did the white-striped males. So why is the macho white-striped male doing so poorly at attracting mates?

A tan-striped male and a white-striped female work as a team to defend the territory. When the performance of a pair is considered, the team of the tan-striped male and white-striped female is just as effective at repelling intrusions as that of the white-striped male and tan-striped female. The aggressive potential of both teams is the same. The tan-striped males don’t acquire territories until the females arrive to help them out.

Still, why doesn’t a white-striped female pair with a white-striped male? That way she’d form a team with the most aggression of all, and together they would get the best territory of all. Well, tan-striped males provide more parental care than do white-striped males, so when nesting survival is factored in, the white-striped female is better off with a more domestic partner who leaves her to do more of the fighting. Conversely, the tan-striped females provide more parental care than their white-striped counterparts, so a team composed of a white-striped male and a tan-striped female provides the same total parental care as the other type of team.

White-throated sparrows are a neat case of gender meshing. Two kinds of teams provide the same total amount of protection and parental care, but divide the labor differently. These genders represent a genetic polymorphism, in which the body differences are not limited to colored stripes. The brain architecture of the morphs differs. Just as with the morphs of the singing fish, the plainfin midshipman, the differences among the genders extend deep into the body (see also p. 224).

THREE MALE, TWO FEMALE

So far, the most genders that have been described in one species is five: three male and two female genders. The present medal-holder—the side-blotched lizard (Uta stansburiana), from the American Southwest and West—has both males and females of multiple colors, signifying different genders in both sexes. Mortality is high, and the population turns over annually. Three male and two female color morphs occur at a grassland site in Los Baños Grandes in central California:

1 Orange-throated males are controllers. These “very aggressive, ultradominant, high-testosterone” males defend territories large enough to overlap the home ranges of several females.

2 Blue-throated males are less aggressive and juiced with less testosterone. They defend territories small enough to contain only one female, whom they “guard.”

3 Yellow-throated males don’t defend territories. Instead, they cluster around the territories of the orange males, “sneak” copulations, and masquerade as “female mimics.”

4 Orange-throated females lay many small eggs, 5.9 eggs per batch. Orange-throated females, like their male counterparts, are very territorial and, as a result, must distance themselves from one another, achieving a maximum density of only one female per 1.54 square meters.

5 Yellow-throated females lay fewer but bigger eggs, 5.6 eggs per batch. Yellow-throated females, like their male counterparts, are more tolerant of one another and can achieve a maximum density of one female per 0.8 square meter.18

Females lay up to five batches of eggs at monthly intervals during a season. The ratio of males in each gender cycles over time. In one four-year period, blue males predominated in 1991, orange in 1992, yellow in 1993–94, and blue again in 1995. The ratio of females in each morph also cycles, but over a two-year period. The total abundance also fluctuates in a two-year cycle. The female cycle synchronizes with the two-year cycle of total abundance.

Concerning the male genders, an explanation for the male cycling was proposed based on the child’s game of rock-paper-scissors: rock beats scissors, paper beats rock, and scissors beats paper, leading to a never-ending cycle of who’s winning: “Trespassing yellows can fool oranges with their female mimicry. However, trespassing yellows are hunted down by blue males and attacked. Although oranges with their high testosterone and high stamina can handily defeat blues, they are susceptible to the charms of yellows.”¹⁹ And so on, in an ecological perpetual motion machine.

Does this theory seem too cute to be true? The problem, as usual, lies with how the nonaggressive male gender is interpreted. First, all the males “sneak,” not only the yellow ones. Thus, the yellow-throated male isn’t distinguished correctly as a sneaker. More important, the yellow male isn’t a female mimic after all. What is supposedly feminine about the yellow-throated male? Early studies indicated that all females had yellow throats. Therefore, the yellow male was thought to resemble a female in throat color. Later study revealed that the orange females had been at a low point of their population cycle during the original study. Once the orange females peaked, the yellow-throated and orange-throated males both resembled corresponding morphs in the females. The loss of throat color as a criterion of femininity left only one other trait: “The most intriguing display that males make, which is restricted to yellow-throated males, is an imitation of the female rejection display. This rejection display is characteristic of post-receptive females and consists of a series of rapid head vibrations [called buzzing]. The male extends his yellow throat, assumes a humped back, and comes in and nips the dominant male on the tail. The parallel between the yellow male . . . and an actual rejection by a bona fide female is extraordinary.”²⁰

Why would performing this one behavior be sufficient to fool an orange male into thinking the yellow male is a female? The blue males aren’t fooled, why only the orange males? This question seems to bother the investigators a bit too. A revealing passage on their website entitled “Are You Blind?” states, “The orange male is somewhat blind and can’t recognize the yellow male in front of him as a male.” A blind lizard that makes its living as a visual predator catching insects? Impossible—the orange males would starve if they were blind. The possibility that the orange male knows what he’s doing and actually wants the yellow male around is never remotely considered.

As for the females, the synchrony between population size and morph ratio in the females suggests that alternating low and high crowding drives the alternating ratios of orange to yellow females. The orange female is more valuable when crowding is low and growth is at a premium. The yellow female is more useful when crowding is high and the ability to pack into a small space is at a premium.²¹ Thus the polymorphism between orange and yellow females is theorized as a polymorphism between a genotype adapted to low-density conditions and a genotype adapted to crowded conditions.

Still, the alternation of high and low crowding can’t be the whole story. Helping takes place too, not just the negative effects of crowding: “When orange females had more orange neighbors their fitness was reduced, but fitness increased with more yellow neighbors. Yellow female fitness was not affected by the density of either morph. “²² Also, one wonders how the two-year female orange/yellow cycle connects with the four-year male orange/yellow/blue cycle. All in all, this social system with multiple genders would benefit from rethinking and further study.

FEMININE MALES-THE DECEIT MYTH

From what we’ve seen, the notion of a universal male or female template is clearly false. Let’s focus specifically on the males who would seem to most clearly violate the universal male template: the feminine males. The third male gender in bluegill sunfish consists of males that look like females. Are such cross-dressing animals rare? Members of one sex often dress in the clothes of the other. Feminine males especially provoke biologists to froth at the mouth. Why would any self-respecting male want to appear feminine? Well, maybe it’s okay if the purpose is deception. Hey, it’s war out there—a guy does what he has to, even wearing a dress, in order to win.

Let’s look into cases of male-to-female cross-dressing to see if biologists have really demonstrated that the function is deception. If not—banish the thought—we might have to consider that being a feminine male might be adaptive in itself.

The pied flycatcher (Ficedula hypoleuca) is a common insectivorous European bird. Males vary in plumage from a striking black and white to brown, and the colors are inherited. Females are also brown. Some biologists have suggested that the brown males are female mimics, even though brown males have a darker tail and more white on their wings than females. So a human observer can tell the sexes apart, but the birds somehow can’t.²³ Do you think it likely that biologists are more observant than birds?

In woods near Oslo, Norway, male flycatchers who had set up territories were presented with individual caged birds to see if they could distinguish the sexes.²⁴ A territory-holding male who hadn’t already attracted a female reacted to a female by showing off the entrance to his nest hole and calling enticingly. When the same male was presented with a macho black-and-white male, he was not so hospitable, and jumped on the cage of the visitor, pecking at it, trying to attack, and not bothering with any welcoming calls. When a feminine brown male was presented, the male again showed off his nest hole and called invitingly. Is the territory-holding male making a mistake, believing the feminine brown male is a female?

Later in the season, after these territory-holding males had attracted a female, they were again presented with the feminine male. This time, about half of the territory holders did not court the feminine male visitor, but instead reacted aggressively. The investigators concluded that the territory holders had now acquired enough “experience” with females to tell the difference between a female and a feminine male, so they were no longer deceived.

But some of these very same territory-holding males had bred the preceding year. Didn’t they become “experienced” at that time? The investigators concluded that the territory-holding males forgot over the year how to tell a feminine male from a female, and needed “recent sexual experience for correct sex recognition,” which had to be “refreshed each year.” Could territory-holding male birds be this dumb?

At the beginning of the breeding season, the feminine males tend to arrive late, and they must find space for their territories amid the territories of birds that arrived earlier. The feminine males are allowed to settle closer to the macho males than the macho males can settle next to each other. If you were a macho male, wouldn’t you allow a friendly neighbor to settle closer to you than an aggressive neighbor? Not that the feminine males are necessarily wimps. When forced to compete with a macho male for a nest box in experimental aviaries, the feminine male attacked first and won, provided he fought at all. Twenty percent of the time the feminine male didn’t bother fighting and simply let the macho male have the nest box.²⁵

Males with territories who had not yet attracted a female have been observed in the wild advertising to feminine males. The territorial male shows off his nest hole, gives enticing calls, and the feminine male joins him and they enter the nest cavity together. Does it seem plausible that the feminine male has used deceit to enter the home of a territorial male “to obtain information” about his “nest site quality”? Would the feminine male be that devious?

A simpler explanation is that territorial males who have not yet attracted a female are horny and invite romance with feminine males. Once the territorial males have attracted a female, they are no longer horny and no longer interested in courting a feminine male. A simpler explanation is that no one is deceived, no one forgets from year to year, and no one requires continual updating of his limited memory. A simpler explanation is that the two male birds who retire together into the nest hole are enjoying a romance. These birds may be neighbors building a cooperative relationship based on same-sex sexual attraction.

The problem with deceit theories of animal behavior is that not only must some animals be implausibly dumb, but others must be remarkably devious—there must be great asymmetry in cognitive ability. Imagine a bird sneaking into the nest of another to spy on it. What would a bird do with what it saw? Does a bird keep a file cabinet in its head full of dirty secrets about its neighbors? I don’t think so, and scientists have not shown any such thing.

The European kestrel (Falco tinnunculus), a dramatic bird of prey, offers another instance of cross-dressing. Males two years and older are blue-gray with brick-red on the back and spots on the head. The females are mostly brown, with a barred pattern on the head. One-year-old males resemble females, so much so that observers find it difficult to tell young males from females. Biologists have therefore suggested that year-old males are female mimics who deceive older males into thinking they are females.

About thirty birds were housed in isolation at a field station in central Finland.²⁶ A bird was placed in a box with one-way glass on the sides. Birds were also placed on the sides; these birds couldn’t see the central bird because of the one-way glass, but the central bird could see them. The biologists then noted which side bird the central bird paid most attention to and tried to associate with—called the “preferred bird.”

When the central bird was a macho male and was offered a macho male on one side and a female on the other, he always preferred the female. When he was offered a feminine male on one side and a female on the other, he preferred either in a fifty-fifty ratio. The investigators claim they’ve shown that a macho male bird can’t distinguish a feminine male from a female. Clearly, though, there is another possibility: a macho male may be quite able to tell the difference between a feminine male and a female, but he doesn’t care which he sits next to.

When the central bird was a female and was offered a macho male on one side and a feminine male on the other, she always preferred the macho male. The investigators claim they’ve shown that females are better able to distinguish sexual identity than males are. The experiment doesn’t speak to whether a female can distinguish a feminine male from a female. The female wasn’t presented with a choice between a feminine male and a female; the female was offered only males.

The investigators go on to speculate that “the better sex recognition ability of females compared with males may have evolved because she is the ‘choosy’ sex. Males . . . do not need to be so good at sex recognition as females.” Deceit theory is a trap. Deceit theory forces scientists to take sides on who is smarter—in this case, claiming that females are smarter than males.

A different kind of cross-dressing is found among red-sided garter snakes (Thamnophis sirtalis parietalis).²⁷ One of seven distinct subspecies of the common garter snake, this nonpoisonous snake is predominantly black with yellow stripes and red bars, and eats invertebrates and small rodents. Females are 10 centimeters larger than males, averaging 55 and 45 centimeters, respectively.

The red-sided garter snake has made Manitoba’s interlake region world-famous for snake-watching, and the town of Inwood has even created a monument in recognition of its large population of garter snakes. Snake dens (or hibernacula) can be found in tree roots, shale cliffs, rock piles, sewers, foundations, animal burrows, rock outcrops, and sinkholes. Twenty thousand garter snakes may gather in a single den during the winter. In spring the snakes’ mass emergence creates an awesome natural spectacle. As far back as the 1880s fashionable picnics were held near Stony Mountain just to watch this phenomenon. But the snake gatherings have also provoked fear. In a labor strike, penitentiary construction workers once refused to work at Stony Mountain until the den was destroyed.

After the snakes emerge, they mate and then disperse to their summer homes in marshes and shallow lakes. Males hang around the dens longer than the females, so that the ratio of males to females near the den entrances is ten to one. Courtship takes place in small groups called “mating balls,” in which one animal is courted by several others. These “suitors” align their bodies with the courted individual and vigorously work to position their tails base to base with the tail of the courted individual, resulting in a ball of writhing snakes.

Females have special lipid perfumes in their skin that turn males on. In 1985 some male garter snakes were found with female perfumes in their skin. Of two hundred mating balls, about 15 percent consisted of a male, presumably with female perfumes in his skin, surrounded by courting males. The males with female perfumes were called—you guessed it—female mimics. The feminine males who joined female-centered mating balls in progress were thought to be distracting the males already there, thus giving themselves greater access to the female.

As with the other claims of female mimicry, the story had internal contradictions. In choice experiments, the males preferred a female to a feminine male, showing that males could tell the difference—they were not deceived. Moreover, in 2000 it was found that all male garter snakes have female perfumes when they emerge from the den in the spring and that all males court these perfumed males in addition to females. At this point, the investigators floated four deceit-based theories to explain why all males have female perfumes on emergence: (1) a perfumed male may confuse the other males while carrying out his own mating; (2) the perfumed male may avoid wasting energy in courting before he has fully awakened from hibernation; (3) a perfumed male may induce the other males to waste time and energy courting him while he gets ready to start his own courting; and (4) a perfumed male may distract other males from the females so he has more to himself when he does get going.

The investigators discarded what seems like an obvious hypothesis. Imagine you’re a male garter snake just waking up in the spring. You’re chilly and covered with cold dirt and mud. You see a spot of blue sky through the ceiling. You crawl out and are greeted by the smiling faces of ten horny males hoping you’re a female. You’re not. But they’re hot and fast, and you’re cold and slow. Wouldn’t it be nice to roll around in the sun—why not use some perfume to signal your intentions? And if you’re one of the ten males watching this face poke up through the ground, and you see he’s not the female you were waiting for, why not welcome him into the sunlight and get acquainted? Better than attacking him, with nine of your buddies looking on ready to attack you too.

This explanation, that the female perfumes might protect a male from attack when he is emerging, was dismissed because garter snakes just aren’t “agonistic.” By nature they’re friendly. Indeed, they’d better be, with twenty thousand of them in one spot! But why are they so “notoriously amorous”? And what makes them so friendly? Group sex.

These studies are disturbing because they attempt to sensationalize at the expense of transgendered people. An article in the scientific journal Animal Behaviour begins, “Female mimicry, whereby a male takes on a female’s appearance, is a rare but widely publicized trait in human societies. Remarkably, parallels can be seen in other animal species.” Feminine males and masculine females are not rare among humans. Nor are transgendered people comparable to snakes. All male garter snakes wear female perfume and participate in same-sex copulation every year. No human society has ever enjoyed such a rite of spring! An article in another scientific journal, the Canadian Journal of Zoology, refers to female mimicry as “bizarre.”²⁸ The problem with female mimicry is not that it is bizarre; the problem is that female mimicry is a myth.

Both articles refer to feminine males in text and figure captions as “she-males.” This language, derived from pornography, is derogatory. A she-male is a woman with a penis. The transgender community has better words to describe transgendered bodies. In the biological literature expressions like “gynomorphic male” and “andromorphic female” are preferred when describing a feminine male or a masculine female.²⁹

The articles derogate not only transgendered people but also their partners. The title of one article includes the phrase “transvestite serpent,” and another claims to be about the “behavioural tactics of ‘she-males’ and the males that court them.” This writing not only stigmatizes transgendered people with certain body types, but also transfers the stigma to their friends. I hope future work on these animals is carried out with more professionalism, and that future publications on this subject receive better editorial oversight.

The examples just cited involve males whose appearance is somewhat feminine. A different kind of example, involving a male bighorn sheep that is morphologically indistinguishable from other males but quite different behaviorally (called an “effeminate male”), might also have been discussed here (see chapter 8). What seems common among all these feminine males is a lessening of hostilities. The cessation of hostility may be temporary, as in garter snakes, or last a year or so, as in young birds whose juvenile color matches the color of females, or be permanent, as in the sunfish cooperator morph whose occupation is to assist controller males in their courtship. The feminine males may exhibit a distinctly feminine signal, such as colored bars or stripes, or simply share with females the absence of the threatening colors of controller males. In either case, feminine imagery seems to be adopted by males to reduce hostility and promote friendship.

Overlooking the positive value of feminine males is part of a larger problem of overlooking cooperation among animals. Even apart from gender expressions, many forms of cooperation occur. Let’s look at a few more.

FRIENDLY FISH

Books on fish behavior are the ponderous rivals of telephone directories. Without going into extensive detail, a few more examples are worth noting to fill out some missing colors in the rainbow of fish gendering.³⁰

Some species don’t bother with a controller morph. Instead, they spawn in large groups of two genders—just male and female. Simple. In surgeonfish, thousands of individuals aggregate for one giant love feast. Other species spawn both in pairs and in groups.³¹

In the bluehead chub (Nocomis leptocephalus), males form partnerships to build nests together. Two large, individually recognizable males were observed together building five different nests in succession. Males of the northern greenside darter (Etheostoma blennioides) form partnerships to court females. Several species of temperate freshwater fish carry out joint courtship, including lake trout (Salvelinus namaycush), the yellowfin shiner (Notropis lutipinnis), and the sucker (Moxostoma carinatum). In many species of suckers, spawning appears to occur only in trios. Two male spawning partners adjoin the female on either side and press against her flanks. This formation is aided by breeding tubercles, called “pearl organs,” which roughen the body surface of males so that the three fish can hold position and not slip apart.

Males in some species, such as the Mediterranean peacock wrasse (Symphodus tinca) — “hot bed,” that is—lay eggs in a nest while the nest owner is between spawning periods. For some reason, biologists term this nest sharing “piracy,” again reflecting a preoccupation with theft. In the tesselated darter (Etheostoma olmstedi), a male who spawns in a breeding hole abandons it to find another one. Another male takes over the nest and cares for the eggs, including cleaning and guarding them.³²

Some species show cooperative brood care in extended families, just as in the extended families of birds with postzygotic helping at the nest: Lamprologus brichardi, a small fish from Lake Tanganyika, is one of six species there exercising cooperative brood care.³³ There is even cross-species brood care! All broods older than five weeks guarded by Midas cichlids (Cichlasoma citrinellum) in Central America contained young of Neetroplus nematopus in addition to their own, and conversely, some guarded broods of Neetroplus nematopus contained young of the Midas cichlid.³⁴

All in all, fish show lots of cooperation. Although not my first choice, I could live with being a fish.

BIASED VOCABULARY

Silent bullfrogs, antlerless deer, and small, medium, and large male sun-fish are happily ignorant of how they’ve been described by biologists. If they knew, they’d be mad.

The silent bullfrog has been termed a “sexual parasite” by the biologists who study it. Instead, the bullfrog who croaks all night long is the model bullfrog, what every young male frog should aspire to. Why is the noisy male so privileged? If I were a female frog, I’d certainly prefer a male who didn’t keep me awake all night. I see no reason to admire a large, noisy male bullfrog as the masculine norm for frogdom while disparaging the silent bullfrog as a parasite.

Biologists call a small male fish who darts in to fertilize eggs a “sneaker,” a medium male who resembles a small female a “female mimic,” and a large aggressive territorial male a “parental,” to place a positive spin on his egg guarding. Both the sneaker and the female mimic are “sexual parasites” of the parental male’s “investment” in nest construction and territorial defense. The sneaker and the female mimic are said to express a gene for “cuckoldry,” as though the parental male were married to a female in his territory and victimized by her unfaithfulness. In fact, a territorial male and the female who is temporarily in his territory have not pair-bonded. Scientists thus sneak gender stereotypes into the primary scientific literature and corrupt its objectivity. Are these descriptions only harmless words?

No. The words affect the view of nature that emerges from biology. Animals are not warrior robots—wind them up and all they do is lie, cheat, steal, and fight. The biology I know reveals sophisticated relationships among animals, relationships that involve honesty and cooperation as much as or more than deceit and competition.

Scientists are open about their predilection for seeing deceit everywhere. They write, “Natural selection favors those individuals that are able to increase their own fitness by manipulating the behavior of others,” and “Cooperation might be seen as the opposite of competition . . . it is instead another form of selfish behavior.”³⁵ These attitudes spin how animal behavior is interpreted and predetermine what data are taken.

The expression “female mimicry” prevents the study of gender variation. The words suggest a male deceptively impersonating a female. In biology, mimicry usually refers to such cases as an edible fly that looks like an inedible bee. “Looks like” here means “exactly like,” not “approximately like.” A fly that mimics a bee almost totally resembles a bee. A good magnifying glass and technical knowledge are needed to tell them apart. A bird flying quickly over the ground can’t spot the difference.³⁶ So-called female mimics don’t exactly resemble females, and all the players have a long time to examine each other. I doubt that female mimicry exists anywhere outside the imagination of biologists.

Thus biologists project scripts of their own prejudices and experiences with male-male competition onto animal bodies and use insulting language about animals. Far from being a sexual parasite, why not see the silent male bullfrog as nature’s antidote to excess macho, preventing the controller from grabbing unlimited power? Far from being a cuckolder, why not picture the feminine male sunfish as nature’s peacemaker? Biologists need to develop positive narratives about the diversity they’re seeing. Then a new suite of hypotheses will emerge for testing, taking the place of the shallow, pejorative, and far-fetched ideas that deceit theory requires.

TRANSGENDER SPECIES

Some species have an appearance or behavior that invites the term “transgender.” These species contain polymorphisms of feminine males, masculine females, masculine males, and feminine females all together, and/or gender-crossing behavior. One study offers comparative data on transgender morphology from museum specimens.

Hummingbirds, the world’s tiniest birds, feed on nectar from flowers and on insects. Their name comes from the buzzing sound their wings make as they hover while feeding at a flower. About 340 species exist worldwide. Hummingbirds typically live three to five years. The smallest is the bee hummingbird of Cuba—a bird only 2.25 inches long.

Hummingbirds also have the smallest eggs of all birds—half the size of a jellybean. A female builds the nest and broods the young alone. Males only fertilize. A typical nest is tiny—about the size of a bubblegum ball. A female incubates two eggs for two to three weeks and feeds them for three more weeks. Because females do all the work, males would seem to be in great excess, allowing females to choose among them. Indeed, the males of many hummingbird species are spectacularly colored, which Darwin would argue is what female hummingbirds find handsome. Recently, though, hummingbirds have begun to emerge as the best documented example of transgender expression in birds.

Male sunangel hummingbirds (Heliangelus) of the Andes, from Venezuela through Colombia, Ecuador, Peru, to Bolivia, have colorful feathers on their throats called a gorget. The name comes from a biblike collar of metal armor used in fencing to avoid being pierced in the throat by a sword. In birds, a gorget is a broad band of distinctive color on the throat and upper chest.

Museum specimens revealed that eight of nine sunangel hummingbird species have some percentage of masculine females with gorgets just like those of males. A few instances of males with female coloration were also detected.³⁷ The investigation of masculine females and feminine males has now been extended to forty-two species of hummingbirds from five genera, yielding the first statistical information about transgender expression in birds.³⁸ Of the forty-two species, seven had both masculine females and feminine males, nine had masculine females and no feminine males, two had feminine males and no masculine females, and twenty-four had neither masculine females nor feminine males. Pooling the species with either masculine females, feminine males, or both, yields data on the total variation of gender expression in both sexes. The appearance of a bird’s gorget was divided into four classes, from most femalelike to most malelike. Fifty-two percent of the adult females (288 of 548) were masculine, including 34 percent who were very masculine. In contrast, only 2 percent of the adult males (18 of 745) were feminine.

Not only the total gender variation but also its distribution varied between the sexes. The distribution of masculinity among females was gradual. That is, most of the females were feminine, and the percentage dropped off gradually from most feminine to most masculine. In contrast, the distribution of femininity among males was bimodal. The great majority were masculine, with no intermediates and a small second peak at the most feminine category. Thus the sexes are not symmetric in either the total amount or the distribution of transgender expression.

What does this variation in gender expression mean? Hard to say. The strength of this study on hummingbird museum specimens is its breadth of coverage. The study’s weakness is the absence of field data on how the genders behave. Still, clues are provided by other traits besides the gorget.

Male hummingbirds tend to have shorter bills than females.³⁹ In hummingbirds, bill length is important in indicating the type of flower that is visited—short bills for short, squat flowers, long bills for long, tubular flowers. Overall, short flowers and short-flower users are more abundant than long flowers and long-flower users. Hence, short-billed birds wind up having to defend their flowers and are aggressively territorial compared to long-billed birds, who don’t defend flowers. With its relatively short bill, then, a male typically also has a showy gorget and territorial behavior.

Masculine females have a shorter bill than feminine females, and presumably defend territories containing flowers. It is possible that a male might prefer to mate with a female whose offspring are guaranteed access to resources in the territory she defends. In fact, studies have recently shown that males prefer ornamented (masculine) females in seven bird species, including an auklet, pigeon, swallow, bluethroat, tit, and two finches.⁴⁰ Thus one guess is that masculine female hummingbirds represent a gender of female controllers maintained in part by male choice.

The feminine males have longer bills than masculine males, even longer than feminine females. Hence feminine males must be using different flowers than the masculine males. The feminine males also have smaller testes than the masculine males, indicating a lower allocation of energy to sperm production. Perhaps the feminine males are pair-bonded to masculine females, as another case of gender meshing. Alternatively, they may have a role in facilitating courtship. Also, mating in some of the species takes place in leks, suggesting a comparison to the feminine male sunfish and ruffs found in leks. Perhaps the feminine males have a role in facilitating courtship at the leks. In any case, the data on museum specimens show that transgender expression is widespread in hummingbirds, inviting follow-up fieldwork.

For a case of transgendered behavior, let us turn to the opposite extreme in data collection, a single individual in the field. Hooded warblers (Wilsonia cirtina) live in woods of the mid-Atlantic United States. They are named for the black plumage that adult males have on their heads—a hood. Some females also have these black hoods, and can’t be distinguished from males by birdwatchers.⁴¹ Early on, variation in female plumage color was thought to represent age, but later work showed that the color is permanent, suggesting a genetic polymorphism for color. About 5 percent of the females very closely resemble males.

Of particular interest is one transgendered black-hooded warbler that was discovered in Maryland.⁴² The bird was originally assumed to be a masculine female, but was later discovered to be gonadally male. Black-hooded warblers are monogamous, and the transgendered bird behaved as the female member of a monogamous pair, consistently showing female-typical behavior throughout two years, including nest building, incubating and brooding young, and not singing or engaging in territorial defense. The bodily appearance of the transgendered bird was typical of males, the behavior typical of females. This bird pair-bonded to a male who was also typically male in both appearance and behavior.⁴³ In this case, a male-bodied bird behaved in all respects like a female, except for laying eggs. Gender identity in this individual hooded warbler evidently crossed over from that typical of the sexed body.

In conclusion, families with multiple genders can be explained using the concepts developed for two-gender families. The idea of helping at the nest in return for reproductive access that was devised for social insects and applied to extended families of birds and mammals also works for how multiple genders are integrated into a social system. Extending kin selection theory now leads to a theory for a labor market that trades access to reproductive opportunity for service, with genetic relationship merely affecting the worth of a unit of reproductive access. The different genders represent different sectors within this economy. While some sectors, like the end-runners, clearly compete with the controllers, others (like the cooperators) are service providers working under contract. Understanding this complex and interesting social dynamic, an animal political economy, I believe is the next step for evolutionary social theory. The part of Darwin’s theory of sexual selection that predicts universal male and female templates may be false, but an evolutionary approach to social behavior is alive and well.