Biological Exuberance: Animal Homosexuality and Natural Diversity

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.