Booknotes: The Mating Mind

First, some context: we are only here because our genes enjoyed an unbroken series of successful sexual relationships in every single generation since the first evolution of animals with eyes and brains, almost half a billion years ago. Let that sink in.

This book concerns itself primarily with sexual selection, equally valued by Darwin but less popular than his other child, natural selection. The core idea is very simple: for a gene to survive as long as possible, it must be able to withstand the dangers of its environment, but it must also be able to reproduce. Natural selection filters out those who cannot do the first, but sexual selection takes care of the second. It’s an incredibly powerful paradigm, because it dramatically shifts the frame of survival, multiplying the short span of a lifetime by a long chain of generations. Once you grasp its importance, sexual selection starts to pop up everywhere - which companies make it beyond the reign of one great CEO, how a virus can survive longer than its host, and why religions depend on fertility doctrine more than solid theology.

I’ll start by breaking down some of the key ideas (fitness indicators, ornamentation, runaway theory), before delving into Miller’s applications of mating theory to explain language, beauty, and morality. Finally, I’ll leave a few Tweetable quotes at the end so you can show off how learned you are to all your potential mates.

Fleshing out sexual selection

An animal with a stellar production orientation (obsession with food and survival) will survive excellently for a lifetime. But, over the course of two lifetimes, it will lose out to the competitor that adopted a marketing orientation by trying to please the opposite sex and profited genetically by reproducing. No matter how good something is at survival, if it doesn’t reproduce, its genes only last one generation. Natural and sexual selection are, in effect, two filters that mutations of DNA must pass through, lest they be eternally erased from the collective book of life.

Biologists refer to this quality - how much of the future gene pool a current gene will eventually fill - as fitness. It reframes the goal as longevity, not of a lifespan, but of a gene. A useful analogy is Dawkins’s cultural analogy - the meme. And to follow the simplified Internet definition of a meme (usually a humorous video or image), the memes that survive the longest, regardless of who posted or upvoted them, are considered the most fit. This means that it survives both filters: someone likes the meme = natural selection, and someone shares the meme = sexual selection. Fitness is everything. Remember, in evolution, all that matters is survival.

How does a gene ensure its survival beyond the lifetime of its host? By signaling to potential mates that it has everything it needs to be a fit gene, if the potential mate would just allow that gene to exist in its offspring. This signalling process is accomplished with fitness indicators.

Fitness Indicators

These are the advertisements of the genetic world. And they comprise a bulk of animal behavior, which makes us walking, talking advertisements for our genes. Courtship rituals (for birds or for humans) are just ways to put all these indicators on display.

The development of fitness indicators is an incredibly interesting but strange process, though. In the beginning, animals with fitness indicators that match the preference of the opposite sex survive. Those with great survival skills but no matching indicators die off. Then, those with poor preferences produce offspring that die off. Eventually, the surviving line is one with great survival skills and matching indicators. Sometimes, though, the link between the two becomes longer and less direct. Usually, the potential mates don’t even know why they cared about a specific quality in the first place - it’s just considered an attractive quality. This is because those who find a “good” quality attractive are more likely to start a successful chain of descendants, regardless of whether or not they understand why it is “good.” This can lead to weird places, because thousands of iterations can sometimes produce fitness indicators that are like greedy tabloids - all advertisements and very little good content. But we’ll get to the weird parts in a bit.

So how does the fitness indicator change over time? Above all else, it will skew through a sensory bias. If an indicator can’t be perceived by the opposite sex, it can’t serve its role as an indicator. Therefore, the best indicators develop to match the sensory sensitivity of the opposite sex (which in turn, develop to better evaluate the fitness indicators).

Beyond showiness, a fruitful fitness indicator should also be an honest signal. And a good measure of this is cost.

Sexual ornamentation

Consider the peacock tail, which requires a lot of energy to grow, to preen, and to carry around. Unhealthy, unfit peacocks can’t afford big, bright tails. The ornament’s cost guarantees the ornamented individual’s fitness, and this is why costly ornaments evolve. We call these indicators ornamentation because the indicator itself has little practical value in itself, beyond its (still-valuable) signalling ability.

The handicap principle suggests that prodigious waste is a necessary feature of sexual ornaments and courtship, in order to create reliable fitness indicators. In nature, showy waste is the only guarantee of truth in advertising, but the wastefulness of courtship is what makes it romantic.

Human fitness indicators

Do not think that this is a phenomenon limited to peacocks. I used the word “romantic” in the last paragraph on purpose, because romance is inherently human, and fitness indicators are everywhere in the human world.

And, like any ornamentation, that romance is usually wasteful, or at least costly. This is why romantic gifts are those that are most useless to the woman and most expensive to the man (think flowers and jewelry). Or consider blood drives, which usually give donors buttons saying something like “I gave blood today.” This essentially proclaims “I am altruistic, not anemic, and HIV-negative.” Of course, this does not mean that all kind gestures are part of a sex-crazed mission to reproduce, but it could potentially explain how certain behaviors came to be and why our preferences point the way they do.

It is certainly a great explanation for why social hierarchies exist, and why we continually compete to raise our relative position in the hierarchy (i.e. status). Take the example of sports, an activity that has confused game theorists for decades, because the rules do not specify what the winner actually wins. Through the lens of sexual selection, though, the sporting arena is a great way to signal superior (relative) fitness to potential mates. This is why we consider winners attractive, and losers less so. Some even posit that hunting originated as a fitness indicator of males, since the act originally provided so little survival benefit at such great cost.

A note on gender

Here is where I will put my disclaimers, especially given the relatively recent (considering the timeline of human history) change in attitude towards gender among humans. We live in a world where gender constraints are fading and morphing, and how we treat male and female is undoubtedly unique among the species of our planet.

Sexual selection is a tool to understand the 8.7 million species of Earth, and how they have evolved to their current state. The same goes for humans, which is to say that this selection process, no matter how gendered, is not meant to offer imperatives and injunctions on how humans should behave. However, it may shed light on how humans came to exist in their current state, why we act the way we do in certain situations, and where some deep-seated patterns find their origins.

However, sexual selection is almost always gendered, and typically, compete to mate with as many females as possible, and females try to be as choosy as possible in order to only reproduce with the best males. The basis for this can be explained by Triver's supply-and-demand model:

DNA is balanced so that an embryo can carry maximum nutrients, which means that eggs cost more for females to make than sperm costs for males. Therefore, females make fewer eggs than males make sperm. But since each offspring requires only one of each, the rarer type of DNA packet, the egg, becomes the limiting resource. Practically, females only need to copulate once every three years. Males vary much more in the number of children they produce, and this makes sexual reproduction a higher-risk, higher-stakes game for them. Thus, it makes sense that males should compete more intensely to fertilize eggs than females do to acquire sperm, and that females should be choosier than males. Males thus compete for quantity of females, and females compete for quality of males.


The beauty of sexual selection through mate choice is that it is a fickle, unpredictable, diversifying process. It never happens the same way twice. As long as there is some level of polygamy, there is no specific direction to sexual selection, in stark comparison to the filter of natural selection. It drives divergent rather than convergent evolution. And this means that it takes species that make their livings in nearly identical ways and gives them radically different sexual ornaments.

This process is taken to extremes when you add in runaway theory, proposed by Ronald Fisher. To gender the selection process, one can see how persistent female choice leads to exaggerated male features over the course of generations. Since sexual ornaments get their value from their relative standing to the ornaments of other males, they must continually grow more and more in the direction of the stated preference. Meanwhile, the females must improve their sensory abilities to keep up with the changing ornaments. This leads to offshoots of specific ornaments in a specific and often unique direction.

The only limit is extinction: if the courtship trait becomes so costly that it imperils the survival of too many individuals, the species may simply die out. It is the danger inherent to any arms race, like a pathological competition between two millionaires trying to one-up each other’s philanthropic efforts, and losing sight of the original goal of generosity (and incidentally, leading to the neglect of the most cost-effective, low-publicity programs). Some believe this is why the Irish elk went extinct. At some point, females began favoring larger antlers, so those with the largest antlers reproduced more, and dominated the gene pool. Eventually, though, the elk would grow antlers so large - over six feet wide - that they would prove burdensome for survival. WIth too little time for the females to try to change their preference, the species was eliminated altogether.

Runaway theory is a great way to explain 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.

This could even explain how a species could split apart into new species, entirely as the result of divergent sexual preferences. Suppose you take a dozen species of ape that lived in social groups in Africa about ten million years ago. Think of these species as nearby clusters in the space of all possible sexual ornaments and courtship behaviors. Now turn runaway sexual selection loose in each species. One species might develop a runaway preference for large muscles, and turn into gorillas. Another species might develop a runaway preference for constant sex, and turn into bonobos. A third species might develop a runaway preference for creative intelligence, and turn into us.

Quick recap

We’ve covered a lot of ground, so here’s a short review. in the animal kingdom, males typically compete to inseminate females. They do this by intimidating other males with weaponry, and by attracting females with costly and wasteful ornaments. Females exercise sexual choice, picking the stronger and more attractive males over the weaker and plainer. Over generations, male weaponry evolves to be more intimidating and male ornamentation evolves to be more impressive. There are two results. First, within each sexual species, males diverge from the female norm. Mature males become more strongly differentiated, compared with females, compared with young animals, and compared with their own ancestors. The other result is very fast divergence between species. The weaponry and ornamentation of one species can go off in a very different direction from the weaponry and ornamentation of a closely related species.

Theories on human behavior

I will preface this bit by saying that it consists of several theories put forth to attempt to describe human behaviors and structures with the lens of sexual selection. The author put them forth only after acknowledging that there is not (and likely can never be) enough evidence to truly confirm them. However, I hope that they provide you, as they did to me, with some food for thought and, at the very least, a novel perspective on aspects of being human that are largely unexamined in our day-today.


It is undeniably strange that ordinary people routinely transmit their thoughts to us through invisible waves that influence our behavior. But how to explain the apparently altruistic act of speaking? Language is often analyzed as a system designed for efficient information transmission. However, a sexual selection model, which would work reasonably well in analyzing many details of peacock courtship displays, may apply here as well.

Without contraception, it takes an average couple about three months of regular sex before a pregnancy occurs. If we assume two hours of talk per day in the early stages of sexual relationship, and three words spoken per second (an average rate), each member of a couple would have uttered about a million words before they conceived any offspring.

Both individuals must clear the million-word hurdle before they contribute to the next generation. When language first evolved, it may have been a ten-word hurdle, or a thousand-word hurdle. But at each step, both individuals were trying to extract, by using the language available to them, as much information as they could. The more talking they did, the more of their minds they revealed. The more verbal courtship revealed, the greater effect sexual selection could have. Language thus lets us learn about potential mates much more efficiently and interactively than any other species. Couples in long-term relationships tend to have vocabularies of similar sizes, and the strength of this assortative mating for vocabulary size is higher than for most other traits, suggesting the matching process is rather successful.

Men traditionally have been more outspoken, occupying more public positions that give them a voice. To say this is due to patriarchy is to beg the question of the behavior’s origin. If men control society, why don’t they just shut up and enjoy their supposed prerogatives? Instead, what if this behavior comes from an evolutionary history of sexual selection in which the male motivation to talk was vital to their reproduction.

Scientific implications

This poses some concerns for those of us who value rational thinking. If language is primarily about social communication and ornamentation, then it is inherently unscientific because it favors entertaining speech, some degree of showing off, and prioritizes the status of the speaker over the transmission of information. How to reconcile this with arenas where the transmission of information is actually the priority? Rational thinking may be useful, in the natural selection sense, but flowery talking is crucial, in the sexual selection sense. There seems to be a trade-off between reliable individual cognition and social communication—we can be mute realists or chatty fabulists, but not both.

However, one can also see obvious patterns in the world of academia, which is largely (but not exclusively) built on the currency of status. And like other status-oriented structures, is science just another avenue of human courtship? Scientists are required to provide intellectual displays to young single people (through undergraduate teaching, graduate advising, and colloquium-giving), but are discouraged from enjoying any sexual benefits from these displays, keeping them in a state of perpetual quasi-courtship until retirement.

Science is not asexual or passionless. But neither is it a result of some crudely sublimated sex drive. Rather, it is one of our most sophisticated arenas for human courtship, which is the most complex and conscious form of mating that has ever evolved on our planet.

Aesthetic taste

Sexual selection may explain why we find some things more beautiful than others, but it cannot explain any of the aesthetic criteria we use to make such judgments, because any standard of beauty can evolve through runaway. We must bear in mind that humans are much better at producing and judging art than any artificial intelligence program or primate. It is also significant that, upon seeing a beautiful work of art, we naturally lean towards respecting the artist.

Throughout most of human history, the perceived beauty of an object has depended very much on its cost. That cost could be measured in time, energy, skill, or money. A common reaction to abstract expressionist painting is to dismiss it by saying “My child could have done that,” “Any idiot could have done that,” or “Even a monkey could have done that.” Instead of condescending at such comments, we should ask what sort of aesthetic instincts they reveal. To say “My child could have done that” could mean “I cannot discern here any signs of learned skill that would distinguish an adult expert from an immature novice.” The “Any idiot” comment could mean “I cannot judge the artist’s general intelligence level from this work.” The “Even a monkey” comment could mean “The work does not even include any evidence of cognitive or behavioral abilities unique to our species of primate.”

Kohn suggested that the normal, pragmatic hand-axes may have been fashioned by females, while the very large, very small, and very symmetrical ones were produced by males as sexual displays. This divergent behavior could have sown seeds for foundational technology (which, I presume, would have been recognized and largely capitalized on by the more pragmatic women of the time).

Likewise, the cultural theorist Walter Benjamin pointed out that, before photography, accurate visual representations required enormous skill to draw or paint, so were considered beautiful indicators of painterly genius. But after the advent of photography, painters could no longer hope to compete in the business of visual realism. In response, painters invented new genres based on new, non-representational aesthetics: impressionism, cubism, expressionism, surrealism, abstraction. Signs of handmade authenticity became more important than representational skill.

Therefore, for one to succeed at making “good” art, one must only make something which appears to be very, very time-consuming or costly to make. Truly then, anyone can be an artist.

Moral societies

Ecologists have long understood that the typical interaction between any two individuals or species is neither competition nor cooperation, but neutralism. Neutralism means apathy. Being nasty has costs, and being nice has costs, and animals evolve to avoid costs whenever possible. This is why watching wild animals interact is usually like watching preoccupied commuters trying to get to work without bumping into one another. We started in the middle, already sitting on the ethical fence, neutral and apathetic.

David Buss’s study of global sexual preferences, however, found that “kindness” was the single most important feature desired in a sexual partner by both men and women in every one of the 37 cultures he studied. It ranked above intelligence, above beauty, and above status. Somewhere along the line, we diverged from neutrality to kindness.

We, as humans, have the capacity for moral behavior and moral judgments today because our ancestors favored sexual partners who were kind, generous, helpful, and fair.

This is why our status-oriented hierarchies are also laced with reciprocity. The importance of both was perhaps one of the greatest insights of Karl Marx, who understood that a society could be based on status signals without reciprocity (a simple dominance hierarchy), or on reciprocity without status signals (an egalitarian utopia). Somewhere in the middle, though, is a healthy balance that leads to an enduring society (remember, all that matters is survival).

Take the Yanomamo tribe of the Amazon: the males stand facing each other and take turns at bashing their opponent’s head with a very long stick until one contestant gives up, faints, or drops dead. The survivors mate, the losers are not so fortunate. Or, imagine a group where elites signal their power by piling up their year’s agricultural surplus in the plaza and burning it up in front of their subordinates. Elsewhere, elites engage in status displays by staging elaborate feasts and handing out gifts to their subjects. After several generations of intense warfare, which type of display behavior is likely to survive in the population? One might expect that the “feasters” would be much more successful at attracting supporters than the “burners.”

None of this means that moral instincts are subverted manifestations of a deep-rooted sex-drive. Rather, instincts for generosity just happen to have many of the showy, fashion-conscious features common to other products of sexual selection. These achievements are not side-effects of having big brains that can learn everything, but of having minds full of courtship adaptations that can be retrained and redirected to invent new ideas even when we are not in love.

The big one, and a conclusion

I cannot end this without making mention of one of Miller’s largest claims: perhaps, in an effort to signal fit genes, our ancestors at some point developed larger and larger brains. These were useful as fitness indicators but also as fitness evaluators. As the males competed to come up with more creative and sometimes humorous speech, females benefited from higher cognition to better judge the males. Eventually, this led to our massive brains (relative to the rest of the animal kingdom), which had as unintentional side effects the ability to understand gravity, paint the Mona Lisa, and build an atomic bomb.

However, this is one theory that I will not try to summarize or explain, because it is such an extraordinary claim that I think the reader would be better served to go straight to Miller’s book. I hope, though, that the search for extraordinary evidence (or at least reasoning) is enough to pique the curiosity of the reader enough to dedicate a few hours to try to learn more sexual selection and its many facets.

And now, as promised, a few Tweetable bits and hopefully thought-provoking ideas:

“Sexual selection works, I think, as evolution’s venture capitalist. It can favor innovations just because they look sexy, long before they show any profitability in the struggle for survival. It can protect the early stages of innovations by giving them a reproductive advantage that can compensate for their survival costs.”

"Teaching ability would have been favored by both survival selection and sexual selection."

"Among competent professionals in any field, there appears to be a fairly constant probability of success in any given endeavor. Simonton’s showed that excellent composers do not produce a higher proportion of excellent music than good composers—they simply produce a higher total number of works."

“Suppose you take a dozen species of ape that lived in social groups in Africa about ten million years ago. Think of these species as nearby clusters in the space of all possible sexual ornaments and courtship behaviors. Now turn runaway sexual selection loose in each species. One species might develop a runaway preference for large muscles, and turn into gorillas. Another species might develop a runaway preference for constant sex, and turn into bonobos. A third species might develop a runaway preference for creative intelligence, and turn into us.”

"Even male chimpanzees hold each other’s penises for comfort when they are frightened."

“For male genes, copulation is the gateway to immortality. This is why males risk their lives for copulation opportunities—and why a male praying mantis continues copulating even after a female has eaten his head.”

“During human evolution there may have been a three-way arms race: females developed better tests for male sympathy, male psychopaths developed better ways to fake sympathy, and male non-psychopaths developed sympathy-displays that were harder and harder to fake.”