Evolution's Rainbow. Joan Roughgarden

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      The small unchanged and large sex-changed males are hostile to each other. The large sex-changed males chase the small unchanged males away from the territory or from females they control. The small unchanged males are more numerous than the large sex-changed males and may form coalitions to mate with females that a large sex-changed male is trying to control. The small unchanged males mate by darting in and fertilizing the eggs that a large sex-changed male was intending to fertilize. Some small unchanged males keep the large sex-changed male busy while others are mating.

      Different ecological circumstances favor unchanged and sex-changed males. The wrasses live both on coral reefs and in the seagrass beds nearby. In seagrass, females nestled among grass blades can’t be guarded very well, and the balance of hostilities tips in favor of the small unchanged males. This situation leads to only two genders, unchanged males and females. On the coral reef, clear water and an open habitat structure permit the large sex-changed males to control the females, and the balance tips in their favor.³ This situation encourages the presence of all three genders. Simple population density also shifts the gender ratios. At high densities females are difficult to guard and small unchanged males predominate, whereas at low densities a large sex-changed male can control a “harem.”⁴ Whether females prefer either type of male isn’t known.

      The sex changes are triggered by changes in social organization. Another type of wrasse is the cleaner wrasse, named for its occupation of gleaning ectoparasites from other fish. When a large sex-changed male is removed from his harem, the largest female changes sex and takes over. Within a few hours, she adopts male behavior, including courtship and spawning with the remaining females. Within ten days, this new male is producing active sperm. Meanwhile the other females in the harem remain unchanged.⁵ I haven’t been able to find out whether any female can turn into a male if she is the biggest female when the existing male dies, or whether females divide into two groups—those who remain female no matter what and those who change sex when circumstances are right.

      Does this animal society seem oh-so-bizarre? It isn’t. Aspects of this system appear again and again among vertebrates, especially the themes of male control of females or their eggs, multiple male genders, hostility among some of the male genders, flexible sexual identity, and social organization that changes with ecological context. Still, if you think the coral reef fish scene is bizarre, you’re not alone—so did the biologists who first witnessed it. We’re only just realizing that the concepts of gender and sexuality we grew up with are seriously flawed.

      MALES CHANGING TO FEMALE

      Sex changes from male to female also occur. A group of damselfish are called clown fish because their bold white strips remind one of the white makeup used by clowns. These fish live among the tentacles of sea anemones, which have cells in their tentacles that sting any animal who touches them. To survive in this lethal home, a clown fish secretes a mucus that inhibits the anemone from discharging its stinging cells. Although living within the anemone’s tentacles provides safety for the clown fish, the size of its house is limited by how big its sea anemone grows. An anemone has space for only one pair of adult clown fish and a few juveniles.

      The female is larger than the male. If she is removed, the remaining male turns into a female, and one of the juveniles matures into a male.⁶ The pair is monogamous. Female egg production increases with body size. A monogamous male finds no advantage in being large because he’s not controlling a harem of females. The advantage for males of remaining small and for females of becoming large may account for the developmental progression from male to female.⁷

      MALE AND FEMALE SIMULTANEOUSLY

      Hamlets, which are small coral reef basses, don’t have to worry about choosing their sex: they are both sexes at the same time. However, they cross-fertilize and must mate with a partner to reproduce. These simultaneous hermaphrodites change between male and female roles several times as they mate. One individual releases a few eggs and the other fertilizes them with sperm. Then the other releases some eggs, which the first fertilizes with sperm, and so on, back and forth.⁸

      No one has offered any suggestions about why hamlets are simultaneous hermaphrodites. Deep-sea fish also tend toward simultaneous hermaphrodism, which for these species is viewed as an adaptation to extremely low population density.⁹ Hamlets don’t have a strange appearance, nor do any other hermaphroditic fish. Hermaphroditic fish look like, well, just fish. Hamlets are not particularly rare, nor are they derived from ancestors who were rare or lived in the deep sea. So just why hamlets are simultaneously hermaphroditic remains mysterious.

      MALE AND FEMALE CRISSCROSSING

      Changing sex once may seem a big deal, but some fish do it several times during their life span. An individual may change from an unsexed juvenile to a female, then to a male, and then back to a female. Or it may change from a juvenile to a male, then to a female, and then back to a male. In certain species, sexual identity can be changed as easily as a new coat.

      Sex crisscrossing was first discovered in a species of goby, which is the largest family of fish. Gobies are tiny and often live on coral reefs—in this case, on the Pacific island of Okinawa.¹⁰ These gobies live as monogamous pairs on branching coral, and the males care for the eggs. About 80 percent of the juveniles mature female, and the rest mature male. Some of the females later switch to male, and some of the males later switch to female. Of those that have switched once, a small fraction later switch back again—the crisscrossers.

      Why go to the expense of changing one’s sexual wardrobe? One theory envisages pair formation in gobies as resulting when two larvae drop out of the plankton together onto a piece of coral.¹¹ They awake after metamorphosis to discover that they are both the same sex. What to do? Well, one of them changes sex. Changing sex has been suggested as a better way of obtaining a heterosexual pairing than moving somewhere else to find a partner of the opposite sex when traveling around is risky. Thus this theory comes down to a choice: switch or move. This theory is rather heterosexist, though. As the hamlets show, a heterosexual pair is not necessary for reproduction, because both could be simultaneously hermaphroditic and not have to bother with crisscrossing.

      A species of goby from Lizard Island on Australia’s Great Barrier Reef has recently been discovered to crisscross, but in a way that is interestingly different from the Okinawan goby.¹² In the Australian goby, all the juveniles mature into females, with some later becoming males. The males, however, can change back into females. In fact, the meaning of male is ambiguous here. The investigators defined a male to be any fish with at least some sperm production. All males, however, contain early-stage oocytes—cells that develop into eggs—in their gonads. So all the males remain part female. The species therefore consists of two genders at any one time: all-female fish and part-male-part-female fish.

      Among flowering plants, populations with hermaphrodites and females are common,¹³ more so than populations with males and females. These mixed hermaphrodite/single-sex species contrast with most plant species, which are entirely hermaphroditic. (Perhaps as more gobies are investigated, a species will be found consisting of females and hermaphrodites, just as in plants.)

      Plants also offer the most amusing examples of crisscrossing sex changes. In a tropical ginger from China, some individuals are male in the morning, making pollen, while others are female in the morning, receiving pollen. Then they switch sexes in the afternoon. This phenomenon, called flexistyly, is known in eleven families of flowering plants.¹⁴ The ginger’s diurnal sex change is not too different from how hamlets mate, where members of a mating pair switch back and forth between male and female once a minute.

      These examples of sequential, simultaneous, and crisscrossing hermaphrodism show that male and female functions don’t need to be packaged into lifelong distinct bodies. Hermaphroditic vertebrate species are successful and common.

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