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Evolution's Rainbow

The University of California Press

Chapter One

As further evidence of the difficulties with sexual selection theory, let's consider how real-life female choice differs from female choice in Darwin's sexual selection theory. Darwin focuses on mating only. A female is supposed to select males according to their attractiveness and prowess. Males are supposed to compete among themselves for mating opportunities and to advertise their good looks to females. This peculiar emphasis on the mating act alone is simply not supported by actual female choices, which are more concerned with the totality of reproduction, including the growth and protection of the young.

"Darwinian fitness" is a technical term that refers to production of the young who will partake in the next generation's reproduction; in mathematical terms, fitness is the product of fertility and probability of survival. Evolution depends on this overall measure of reproductive success. Mating is one component of fitness, but a preoccupation with "mating success" has led to an emphasis on mating to the exclusion of other components of fitness. In reality, female choice considers the overall production of offspring, keeping mating inperspective. Darwin is incorrect in almost all details concerning female choice, although he must be credited with recognizing that female choice among animals exists in the first place.

What, then, are the preferences of female animals, and how do females vary in their preferences? What do females want from a male, how many times do females want to mate, how many males do females want to mate with, how does a female find Mr. Right, and how do females decide how many eggs to produce?

Deadbeats Need Not Apply

Is a male's true mettle tested in combat with other males? Does the best male surface as the winner and assume dominance over a hierarchy of wannabes? Shouldn't a female yearn to shack up with a proven winner? Shouldn't a female respect the winner of male-male competition as the best father for her baby, a stud with the best genes? Does mating with him guarantee the best and brightest child?

Let's see what female gobies think about male dominance. Sand gobies (Pomatoschistus minutus) are small fish (5 to 6 centimeters) common along European coasts. To see what a female goby wants in a male goby, specimens were collected from a shallow sandy bay near the Klubban Biological Station in Sweden and housed in seawater tanks for observation. After the experiment, they were released back to the sea.

Sand gobies live for one or two years and experience one breeding season. Both males and females reproduce often during the breeding season, which is two months long (May and June). Males build nests under empty mussel shells by covering the shells with sand and excavating a cavity underneath. They attract females with a courtship display that includes showing their colorful fins. During spawning, a female attaches her eggs to the nest in a single layer.

In an experiment, two goby males were allowed to compete for a clay pottery fragment to use as a nest in order to determine the dominant male. The winner was usually slightly larger than the loser, although only by 3 millimeters. They were then placed in chambers at opposite ends of a tank. The tank was divided into thirds using transparent partitions. The middle chamber was left empty. The winner and loser were given new pottery fragments and allowed to build nests by themselves.

Next, a female was introduced into the middle chamber. The female could choose which of the males she preferred, indicated by the side of the chamber where she spent her time. After the female's preference was determined, she was placed with one of the males, either the one she preferred or not, by flipping a coin, and then the time needed for spawning to occur was noted. Another female was placed with the remaining male, and the time they took to spawn was also noted. Thus both males were able to spawn.

Finally, after spawning, the females were removed, as were the partitions separating the males, leaving two males, each with a nest containing eggs, at opposite ends of the tank. A small crab was introduced, which is an egg predator. Observers counted the number of eggs lost to the predator in order to determine how good the males were at protecting the eggs.

The results are striking. Whether a male was dominant in competition for nests did not correlate with whether he was a good father in protecting the eggs. Also, female preference didn't correlate with dominance in male-male competition. The females didn't care if the male they preferred won his fight with another male. The females did care whether the male would protect the eggs. Somehow females were able to predict who would or wouldn't be a good father, and decidedly preferred mating with males who later turned out to be good egg protectors. A female could somehow look a male in the eye and tell if he was a deadbeat.

Now, let's take a look at the peacock wrasse (Symphodus tinca) that lives off the coast of Corsica in the Mediterranean in a shallow rocky habitat. The female peacock wrasses have a choice of whether to lay eggs in a male's nest or to broadcast their eggs over the sea floor. Which they do depends on how they assess the offer of male parental care.

Large controller males construct guarded areas of a meter in diameter and place pieces of algae in the middle, to which the eggs attach. Nest construction takes one or two days, followed by two or three days during which females visit the nests and deposit about fifty eggs at a time, leading to as many as fifty thousand eggs in a nest. Thereafter, the male may guard the egg mass until hatching, which varies from twelve days in the cold water of mid April to six days in the warm water of mid June.

Smaller males take on two roles. They may be "followers," who swim at a distance behind gravid females and fertilize eggs broadcast on the open sea floor. Or they may hang out as end-runners around the territories of controllers and fertilize eggs laid in the territory. During the first half of the reproductive season, however, small males are absent. The small males arrive only for the second half, presumably when the ability of the large male to shoo them away is constrained by the need to guard the eggs that have already been deposited.

Males defending eggs lose weight and appear to have a higher mortality during this period, so they abandon nests that haven't accumulated enough eggs to be worth their while. Abandoned eggs are hung out to dry, so to speak. Because abandoned eggs are concentrated in one spot, they quickly attract predators. Thus the best chance of an egg surviving is to be laid in a nest that is not abandoned, the next best chance is for an egg to be broadcast on the sea floor, and the worst is to be laid in a nest that is subsequently abandoned.

The males stay with only 20 percent of the nests early in the season, remain with 85 percent of the nests at midseason, and drop off to 20 percent again by the end of the season. Thus laying eggs in a male's nest is a good bet only in midseason. Indeed, only 15 percent of the females lay their eggs in nests at the beginning of the season, rising to 85 percent at midseason, and falling back to 15 percent as the season ends.

What does a female peacock wrasse want of a male? A male who isn't a deadbeat, who won't abandon her eggs. And she can tell. The investigators write, "If a female chooses to lay her eggs outside a nest, she tends to do so only after visiting several nests."

Inviting Female Commitment

How does a guy convince his gal that he isn't a deadbeat? Fish offer some advice on this ancient question too. Females know that males abandon nests that don't accumulate enough eggs to be worthwhile from the male standpoint. From a female's standpoint, adding eggs to an egg mass that's already large makes sense, because the male guarding it is more likely to stick around than if it was a small egg mass. So, how does an egg deposit get started? A female has to take a chance on a male or go it alone.

Various male fish have structures on their body that resemble eggs, a common example being the fantail darter (Etheostoma flabellare). These small fish are found in freshwater streams in North America, including central Kentucky. During the spring, males excavate nests beneath flat rocks, defend small territories, and mate with various females who deposit eggs in their nests. Males then guard the eggs until hatching.

Each of the seven to eight dorsal spines on the male's front fin is tipped with a fleshy knob. These knobs are smaller than the size of real eggs but, on the largest males, approach the size of actual eggs. Deceit theorists have suggested that a female is fooled by these structures into believing that a male is already tending eggs, so that adding her own to the collection is safe. This hypothesized deceit is called "egg mimicry."

Two facts compromise this interpretation: females also have these fleshy knobs, and the knobs on males are smaller than real eggs. Why do females have these knobs if their only function is for males to deceive females? Why would these fish, who are visual predators, be fooled by fleshy knobs that are smaller than real eggs?

Experiments suggest that the females prefer to lay eggs in the nests of males with fleshy knobs rather than the nests of males whose knobs have been snipped off with scissors. Although the study was preliminary, we can still ask what such a result would mean. Were the females fooled? The alternative is that the fleshy knobs are symbols of eggs, not mimics of eggs. When a male swims close to the underside of a rock, he might be showing where the eggs should be placed.

Female fish want male fish to live up to their promise of guarding the eggs. The male must communicate that he is serious about his willingness to provide for the young. The invitation to lay eggs in his nest must somehow show he knows how to handle this responsibility. The female carefully assesses the credibility of the promise; she seems unlikely to be deceived by a trick such as egg mimicry.

How Much Sex Is Enough?

Newspapers are filled with advertisements for new toys and chemicals to help people have sex more often. Well, how often is enough? Birds illustrate how females may take the lead in determining how often matings happen and when.

Female alpine accentors (Prunella collaris) from the central Pyrenees of France like sex. These females don't worry about male harassment. If anything, it's the reverse-females harassing poor males into sex all the time. What do these horny females want? They want the same thing female sand gobies and female peacock wrasses want: males who do their share of the housework.

Alpine accentors go in for eightsomes, as many as four males and four females. A female is fertile for about two weeks, from about a week before her first egg until the last egg is laid. After the eggs hatch, the males may help feed the young.

Fertile females actively solicit copulation. A female approaches a male, crouches with her breast touching the ground, lifts her tail to expose a bright red, swollen cloaca, quivers her tail from side to side, and shivers her wings. Just to be sure he's awake, she often jumps in front of him and presents her cloaca directly in his face. Hard to miss. A female solicits in this way once every 8.5 minutes. A full 93 percent of all solicitations are initiated by the female approaching the male, the other 7 percent by him approaching her.

The males in the group form a dominance hierarchy. The alpha male follows behind any fertile female, limiting but not entirely preventing lower-ranking males from approaching her. Moreover, the males play hard to get, ignoring 68 percent of the solicitations. Still, they do a lot of mating anyway. In fact, a female copulates 250 times per clutch of eggs, although a single insemination provides enough sperm to fertilize all the eggs. So much for believing that the sole purpose of copulation is to conceive!

What's going on here? An alpha male doesn't stick around to help at the nest unless he's sufficiently occupied at home. He can easily visit nearby nests, so to keep him at home, the female invests more time in mating with him than with the lower-ranking males. The lower-ranking males don't have as many opportunities to shop around outside the nest, but if they are to remain as helpers at the nest, they require some minimum share of the action. Therefore, a female actively displays to the subordinate males as well, making sure that they have some share of the copulations and therefore of the paternity.

Alpine accentors provide an example of females preferring the alpha male, because most of the copulations are with him and are initiated by the female. This preference might seem to suggest that the alpha male offers some benefit to the female, such as his "great genes," and that female preference for alpha males is an endorsement of their superior quality. The data show, however, that the quality of the chicks sired by an alpha male is no better than that of chicks sired by the subordinate males, judging by the weight of the chicks at the time they leave the nest. In fact, the only reason the female appears to prefer to copulate more with the alpha male is that the greater availability to him of opportunities outside the nest makes it more of a challenge to keep him at the nest. From the female perspective, copulation provides the shared paternity needed as a "staying incentive," which is allocated to males of various dominance status according to what is required to keep them involved at the nest.

Do monogamous females mate only during the brief period when the eggs are ready for fertilization? Or do monogamous females like fun too? In fact, monogamous females may be even more sexually active than females in other types of families. In birds such as the mallard duck and common guillemot, mating starts before the female is ready to produce eggs, and before the male is ready to produce sperm. Why should all this mating occur when it is apparently not needed? The obvious answer, one might have thought, is that mating maintains the bond between male and female. Regular mating keeps the pair in touch with one another, so to speak. By mating, they enjoy sexual pleasure with one another. One might theorize that the pleasure of mating evolved in such species in order to provide an ongoing motivation for the members of the pair to stay together.

But in the minds of deceit theorists, "excess" mating between members of a pair has nothing to do with building relationships; rather, it represents females using sexuality to manipulate males into giving them free food-a dinner date followed by sex. According to one model for the evolution of "female sexuality" in monogamous birds, males keep buying dinner because they can't "risk leaving." As a result, "females benefit from the presence of males in such a way that males get nothing in return."

For the record, biology provides no evidence whatsoever that the function of sexuality in monogamous relationships is deceit. Instead, theories of male/female cooperation should have been considered as a rationale for sexuality in the monogamous family.

When Females Look Like Males

What does female-to-male cross-dressing tell us about the role of female choice? Reports on feminine males are marked by deceit rhetoric and sensationalism. Reports of masculine females are scanty, suggesting underreporting. What emerges is that some females signal receptiveness with colors that coincidentally resemble male colors, whereas other females modify their attractiveness to males to control how often males solicit them.

At the northwestern tip of the Iberian peninsula lies the seaport city of A Coruna, Spain, where Bocage's wall lizard (Podarcis bocagei) lives. This lizard is the only vertebrate animal species so far in which females have been reported to imitate males, but the case isn't convincing. Males have an intense green color on their back. Female wall lizards are usually brown, but when they have fertilized eggs already in their oviducts or have recently laid an egg, they turn green to signal that they won't accept courtship. Is being green masculine and therefore romantically unappealing to other males, as some scientists have speculated? Whereas feminine males are cast as deceivers, masculine females are cast as unattractive. Or could green simply be a gender-neutral signal telling males not to bother courting?

The green color seems to be a gender-neutral signal rather than a masculine presentation that males find unattractive, because males do occasionally try to mate with green females and are rebuffed. These males are presumably learning what green means. If males found green females unattractive, they wouldn't court them to begin with.

(Continues...)

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Excerpted from Evolution's Rainbow by Joan Roughgarden Copyright © 2004 by Joan Roughgarden. Excerpted by permission.
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