The Mating Mind: How Sexual Choice Shaped the Evolution of Human Nature (25 page)

On its own, the idea of ornamental evolution through sensory biases has about the same number of strengths and weaknesses as the runaway brain theory and the healthy brain theory do. We probably need to combine all three perspectives to understand human evolution. I would not have spent a whole chapter on the runaway process if I did not think it was important in explaining the capricious divergence of courtship behavior between different ape and hominid species. I would not have spent a chapter on

fitness indicators if I did not think that the pressure to advertise good genes was important in mental evolution. And I would not have discussed sensory biases, pleasure, and entertainment if I did not think that the psychological quirks of our ancestors had influenced our psychological capacities through the sexual choices they made.

Later, when I come to discuss particular human abilities like language and creativity, I shall draw on all three viewpoints. Biologists sometimes compare runaway theory, indicator theory, and sensory bias theory as if they were competing models of sexual selection. Such debates helped revive sexual selection theory, but I think that each of the theories now has enough support for them to be considered as overlapping sexual selection processes, not competing models. They all really happen in nature.

Runaway happens because sexual preferences really do become genetically correlated with the sexual ornaments they favor. It helps to explain human mental traits that are extreme, unusual, attractive, and useless for survival, and why such traits evolved in our lineage and not in other ape species. Runaway is endemic to sexual selection, always happening, or just finished, or just about to happen. It explains much of sexual selection's power, speed, and unpredictability.

Sexual ornaments really do evolve higher costs and higher condition-dependence in order to work better as fitness indicators. Indicator theory explains why some sexual ornaments stick around for many generations rather than disappearing as transient runaway effects. It gives sexual selection much of its direction, explaining why individuals usually prefer large tails to small, loud calls to whispers, good territories to bad, winners to losers, health to sickness, and intelligence to stupidity.

Sensory biases really do influence in which direction runaway is most likely to go, and which indicators are most likely to evolve. Sexual selection for pleasure and entertainment explains why so many sexual ornaments like the human mind are pleasing and entertaining. It draws attention to the role of sensation, perception, cognition, and emotion in sexual choice.

How Ornaments and Indicators Interact

Any particular trait that evolved through sexual selection was probably influenced by some combination of runaway processes, pressures to advertise fitness, and psychological preferences. Most sexually selected traits probably work as both ornaments and indicators. Some elements of their design evolved to provide hardto-fake information about fitness; others evolved just because they happened to be exciting and entertaining. To understand the human mind as a set of sexually selected traits, we have to envision how ornamental and indicator functions can exist side by side in the same trait.

An indicator must accurately indicate a particular quantity. But this requirement does not determine every aspect of an indicator's design: there are always many design elements that are free to vary in ornamental ways. Almost all car speedometers can successfully indicate the car's speed, but there are hundreds of different speedometer designs used in different makes and models of car. All wristwatches indicate the time, but different watch designs may vary in every possible detail according to the aesthetic tastes of manufacturers and consumers. As long as speed, time, or some other indicated quantity is more or less intelligible, the indicator's design is free to vary according to aesthetic whimsy, exploring the fringes of ornamental style.

Actually, the handicap principle makes sexually selected traits a bit more constrained than watch designs. The Rolex Corporation has no incentive to mislead its customers about the time. Animals do have incentives to mislead potential mates about their fitness. Coins make a better analogy for sexually selected traits than do watch-faces. Numismatists are familiar with the two criteria of successful coins: they are hard to counterfeit (a requirement that increases with their monetary value), and they are attractive to the eye and the hand. Coins indicate value just as watches indicate time. But with coins there is a much greater incentive for fakery.

Counterfeiting has been a concern ever since 560 B.C., when King Croesus of Lydia invented true official coinage

(government-issued cast disks of standard weight, composition, and guaranteed value). To guard against counterfeiting, authorities produce coins according to the handicap principle.

They endow coins with features that would be prohibitively
expensive for a counterfeiter with low capital to imitate. In the

ancient era, it was usually sufficient to produce coins with hard-tomake iron coining dies. By the 17th century, authorities had to invest in expensive rolling mills, sizing dies, and blanking presses to deter counterfeiting. The modern principles of coinage-accuracy of dimension, perfect reproduction of design, standard weight of an easily tested alloy—all evolved to make coins accurate indicators of monetary value.

And yet there has been enormous scope for coins to vary in ornamental ways. This ornamental elbow room is what gives

numismatics its interest, just as sexual selection gives

biodiversity its fascination. Ancient Greek coins, though
commonly made of precious-metal alloys to a common basic

design, were ornamented in different ways depending on the

city-state of origin: owls for Athens, bees for Ephesus, the griffin
for Abdera, the eagle of Zeus for Olympia, the lion of Leontini,

the minotaur of Knossos, the quince of Melos, the silver-

miner's pick at Damastium, the grapes of Naxos. The
requirement that the famous Sicilian decadrachm of 480 B.C.

must properly indicate its value did not determine its beautiful

ornamentation, with triumphal chariots above a fleeing lion
(symbolizing the recently conquered Carthage) on one side,

and, on the other side, Arethusa. (Arethusa was a water nymph who escaped unwanted sexual attention from the river-god Alpheios by asking Artemis to transform her into a freshwater spring—an evolutionary counterproductive way to exercise female mate choice.) Within a few years of the invention of

coinage, Greek city-states were not just worrying about overcoming counterfeiting; they were competing to make coins

beautiful. While there were just a few principles to guarantee a coin's value, there were an infinite number of ways to ornament it with a pleasing design.

The principles of coinage, like those of sexual selection, are not

just economic but aesthetic. While the economic principles of value-indication tend to produce similarities between coins, the aesthetic principles are more creatively protean, producing endless diversity. To understand the features of any given coin, it is not enough to appreciate the general requirements of money (durability, divisibility, portability), or the particular anti-counterfeiting principles of coinage (standard size, weight, composition, and design). One must also appreciate the aesthetic imperatives, from the universal sensory demands of the human hand and eye, to the historically contingent symbolism of a particular culture. Likewise for a sexually selected trait—one must understand how certain features indicate an animal's fitness, and how other features evolved as aesthetically pleasing ornaments, just because they happened to excite the senses and brains of the opposite sex. As anti-counterfeiting principles rarely suffice to explain every detail of a coin, in almost no case of a sexually selected trait does the handicap principle alone suffice to explain every detail. There is always some aesthetic slack.

In sexual selection, traits that began as indicators tend to grow more complexly ornamental because the sensory preferences of the opposite sex partially impose their own aesthetic agenda on the indicator. Conversely, traits that originate as pure runaway ornaments tend to acquire value as fitness indicators because aesthetically impressive ornaments tend to be costly and difficult to produce. Almost all sexually selected traits that last more than a few hundred generations probably function both as indicators and as ornaments. They may have originated mainly as one or the other, but soon imposed sufficient costs that they indicated fitness accurately, and soon acquired enough aesthetic complexity that they stimulated the senses of the opposite sex in ways that could not be reduced to indicating fitness.

The messy overlap between indicators and ornaments does not mean that we can afford to get messy about sexual selection theory. Zahavi's handicap principle is quite distinct from Fisher's runaway process. But they frequently work together,
so
we should not worry too much about trying to categorize every sexual trait

as either an indicator or an ornament. Instead, we should use different models of sexual selection as lenses to view a given trait from different angles and different distances, to answer

different evolutionary questions. The fitness-indicator
principles are good at explaining why animals of a given species have such a strong consensus about what they like in a sexual trait: why all peahens like the peacocks to have large, symmetric, bright, many-eyed tails. The fitness-indicator perspective explains the perfectionism and conservatism of sexual tastes within each species. It also explains why large, long-lived animals have not degenerated to extinction under the pressure of harmful mutations. On the other hand, the ornamental principles are good at explaining why animals of different species develop such different tastes: the tails that attract peahens, for example, are not turn-ons for female turkeys or female albatrosses. The ornamental perspective explains the protean divergence of sexual tastes across species over macro-evolutionary time. It also explains why sexually reproducing life on our planet has split apart into millions of different species.

The ornamental view is especially important for appreciating the role of evolutionary contingency in shaping sexual traits, just as it is in appreciating the role of historical contingency in shaping coins. Once King Croesus invented official coinage, we could have predicted that most city-states of the ancient Mediterranean world would adopt coins, would make them hard to counterfeit, and would ornament them with some pleasing designs. However, we could not have predicted that the coin-engraver's art would reach its peak in 5th-century B.C. Syracuse, on the island of Sicily. It could have happened at some other time in Carthage, Crete, or Athens, but it didn't.

Likewise for the products of sexual selection. We can see that, once sexually reproducing animals evolved the capacity for mate choice, every animal species would then evolve some sort of fitness indicator; and that some indicators might be costly, exaggerated body parts, and others would be costly, ritualized courtship behaviors. But we could not have predicted that courtship

behavior would reach an especially high degree of sophistication exactly 535 million years after the Cambrian explosion (when multicellular animals proliferated) in our particular species of bipedal ape. Nor could we have predicted that the courtship behavior would take the precise form of interactive conversations using arbitrary acoustic signals (words) arranged in three-second bursts (sentences) according to recursive syntactic rules. Perhaps it could have happened in an octopus, a dinosaur, or a dolphin. Perhaps it was likely that it would happen sometime, in some species of large-brained social animal. Rewind the tape of evolution, and the human mind would probably not have evolved, because sexual selection would have taken a different contingent route in our lineage of primates. But I suspect that in any replay of evolution on Earth, sexual selection would sooner or later have discovered that intelligent minds similar to ours make good courtship ornaments and good fitness indicators.

Sexual Selection, Natural Selection, and Innovations

The interaction of the three major sexual selection processes can explain sexual ornaments. Less often appreciated is how they can interact with natural selection for survival to produce evolutionary innovations. To understand any specific innovation such as the human mind, it may help us to look at what role sexual choice might play in the evolution of innovations in general.

The history of life on Earth is marked by major evolutionary innovations such as the evolution of DNA, chromosomes, cell nuclei, multicellular bodies, and brains. Classic examples of moderately important innovations include legs, eyes, feathers, eggs, placentas, and flowers. Much more frequent are the minor innovations that distinguish one species from another. These micro-innovations are often no more significant than a different mating call or an unusually shaped penis.

The major innovations give their lineages such an advantage in exploring new niches that they result in a burst of biodiversity

called an "adaptive radiation." The first species that suckled its young with milk ended up being the ancestor of all 4,000 species

of mammal. The first ape that walked upright became the ancestor of a dozen or so species of hominid, including us. Every major group of organisms (such as a kingdom or phylum) has a major innovation at its root. Every medium-sized group (such as a class or order) has a moderately important innovation at its root. Every species is distinguished by some micro-innovation. The tree of life is a tree of evolutionary innovations.