Biological Exuberance: Animal Homosexuality and Natural Diversity

maturational; that is, it happens automatically to all individuals when they reach a certain age or size or else occurs spontaneously at different times for each individual. In other species, sex change appears to be triggered by factors in the social environment of the fish, such as the size, sex, or number of neighboring fish. In female-to-male fish species, many different gender profiles are found. In some cases, all fish are born female, and males result only from sex change (such a system is called monandric). In other cases, both genetic males (born male) and sex-changed males are found (this arrangement is called diandric). In these fishes, genetic males are sometimes referred to as primary males while sex-changed males are called secondary males. Often these two types of males differ in their coloration, behavior, and social organization so that transsexual males form a distinct and clearly visible “gender” in the population.

Homosexuality as a “masculine” activity: a male Bighorn ram mounts another ram. Males who mimic females in this species (behavioral transvestites) do not generally permit other males to mount them, unlike nontransvestite rams.

Things get even more complicated in some species. Among secondary males, some change sex before they mature as females (prematurational secondary males), while others change sex only after they live part of their adult life as females (post-maturational secondary males). Many species also have two distinct color phases: fish often begin life with a dull color and drab patterning, then change into the more brilliant hues typically associated with tropical fish as they get older. Which individuals change color, when they change, and their gender at the time of the color change can yield further variations. Many species of parrot fishes, for example, have multiple “genders” or categories of individuals based on these distinctions. In fact, in some families of fishes, transsexuality is so much the norm that biologists have coined a term to refer to those “unusual” species that don’t change sex—gonochoristic animals are those with two distinct sexes in which males always remain male and females always remain female.

As an example of how elaborate transsexuality can become in coral-reef fish, consider the striped parrot fish, a medium-sized species native to Caribbean and Atlantic waters from Bermuda to Brazil (the name refers to the fact that its teeth are fused together like a parrot’s beak).⁵⁷ Striped parrot fish, like many sex- changing fishes, have both males that were born as males and males that were born as females. In fact, more than half of all males in this species used to be females. Moreover, all female striped parrot fish eventually change their sex, becoming male once they reach a certain size; the sex change can take as little as ten days to be completed. Sex-changed males have fully functional testes that used to be fully functional ovaries when the fish was female; they are able to mate and fertilize eggs the same way that genetic males do. Striped parrot fish have one of the most complex polygendered societies in the animal kingdom. There are five distinct genders, distinguished by biological sex, genetic origin, and color phase. Biological sex refers to whether the fish has ovaries (= female) or testes (= male). Genetic origin refers to whether the fish was born that sex or has changed from another sex (= transsexual). Color phase refers to the two types of coloration that striped parrot fish exhibit: initial-phase fish (so named because all fish start out with this coloration) are a drabber brown or bluish gray, while terminal-phase fish are a brilliant blue-green and orange. These three categories intersect to create the following five genders (percentages refer to what proportion of the total population, at any given time, belongs to each gender): (1) genetic females: born female, each of these initial-phase fish will eventually become a male and change color (45 percent); (2) initial-phase transsexual males: born female, these fish become male before they change into their bright colors and are fairly rare (1 percent); (3) terminal-phase transsexual males: born female, these fish become male at the same time they changed color, usually at a later age than genetic males (27 percent); (4) initial-phase genetic males: born male, most of these will change color as they get older (but won’t change sex) (14 percent); and (5) terminal-phase genetic males: born male, these fish start out as initial-phase males and change color (but not sex) at a younger age than transsexual males (13 percent).

Along with its numerous genders and fluid changes between them, striped parrot fish society is characterized by a number of intricate systems of social organization and mating patterns, each found in a particular geographic area. One system, known as group spawning or explosive breeding assemblages, is common in Jamaican striped parrot fish. Large groups of up to 20 initial-phase males and females gather to spawn together, swimming in dramatic formations that rapidly change direction. Often, terminal-phase males try to disrupt this mating activity. Another system is found in the waters off Panama and is known as haremic because the basic breeding group consists of one terminal-phase male and several females. These individuals are known as territorials since they live in permanent locations that they defend against intruders. Other fish in the same area, however, associate with each other in different kinds of groups: “stationaries” are celibate (nonbreeding) fish in both initial and terminal phases, while “foragers” gather together to feed in large groups of up to 500 fish. Some of these foraging groups are composed of females and initial-phase genetic males, while others are made up only of terminal-phase males; half of all the females, and all the males, in such groups are nonbreeders. Finally, striped parrot fish in the waters off Puerto Rico and the Virgin Islands associate together in “leks,” clusters of small, temporary territories that both initial-phase and terminal-phase males defend and use to attract females for spawning.

Further variations in transsexuality are found in other species. The paketi or spotty, a New Zealand fish, combines transsexuality with transvestism (some females become males before changing color, thus “masquerading” as females), while the humbug damselfish combines transsexuality with same-sex pairings and associations. An even more complex gender system, involving hermaphroditism, transsexuality, transvestism, and apparent homosexual activities, exists in the lantern bass and other fishes. In addition to nontranssexual males and females, some individuals are hermaphrodites (both male and female at the same time) and others are secondary (transsexual) males, while in a few cases individuals exhibit courtship and mating patterns typical of the opposite sex (directed toward individuals of the same sex). All female Red Sea anemonefish start out as males; once they change sex, however, they become dominant to males and tend “harems” of up to nine males, all but one of whom are nonbreeders. Finally, although most transsexual fishes are one-way sex changers, in a few species sex change actually occurs in both directions. In the coral goby, for instance, some individuals go from male to female, others from female to male, and some even undergo multiple sequential changes, “back and forth” from male to female to male, or female to male to female.⁵⁸

As these examples show, not only are transgendered and genderless biologies a fact of life for many animals, they have developed into incredibly sophisticated and complex systems of social organization and behavioral patterning in many species. For those of us used to thinking in terms of two unchanging and wholly separate sexes, this is extraordinary news indeed. Likewise, animal homosexuality itself is a rich and multifaceted phenomenon that is at least as complex and varied as heterosexuality Animals of the same sex court each other with an assortment of special—and in some cases, unique—behavior patterns. They are both affectionate and sexual toward one another, utilizing multiple forms of touch and sexual technique, ranging from kissing and grooming to cunnilingus and anal intercourse. And they form pair-bonds of several different types and durations and even raise young in an assortment of same-sex family configurations. If, as scientist J. B. S. Haldane stated, the natural world is queerer than we can ever know, then it is also true that the lives of “queer” animals are far more diverse than we could ever have imagined. In the next chapter, we’ll take a look at how these different forms of sexual and gender expression in animals compare to similar phenomena in people.

Chapter 2

Humanistic Animals, Animalistic Humans

Titus and Ahab—male Gorillas—often courted and had sex with one another in the mountains of Rwanda, while Marchessa sought out her own sex during her pregnancy. In Florida, Bottlenose Dolphins Frank, Floyd, and Algie participated in homosexual activity with each other, as did Gabe and Moe-Miller,