IN THE PREVIOUS chapter, we discussed the many uses of sex besides simply conception. However, we left out one big item: sex as means to create and strengthen bonds. This is such a large aspect of sex that it requires its own chapter.
As we speak exclusively about the bonding and attachment functions of sex, it is important to keep in mind that this is in addition to the functions that we have already discussed. In any given species at any given time, sex is used for some subset of these many functions. For example, two hawks might find each other while out hunting and have sex for fun and possible procreation. Then, they might go home to their spouses and have sex to strengthen their pair bond. These are overlapping, not conflicting, purposes.
SEX FOR PAIR BONDING
It was once thought that monogamy was a purely human affair and animals had sex with as many mates as they could. The reality is not that simple. In birds, more than 90 percent of species exhibit “seasonal monogamy.”1 That is to say, they hook up with a mate for one breeding season and stick with that mate for the entire year. Birds are nest builders, and most of them do this in monogamous pairs. The roles vary among species, but in general, the birds split duties, such as foraging for nest-building materials, constructing the nest, finding food and sharing with the spouse, incubating the eggs, feeding the young, chasing off predators, and so on. It is a real partnership, and both members of the pair contribute.
For most bird species, about half of “marriages” dissolve at the end of the season when they migrate. This is because flocks of birds are not stable from year to year. Birds can switch flocks, often in search of a better position in the dominance hierarchy. You see, mate selection in many bird species follows the dominance rank order very closely. The highest-ranking females pair with the highest-ranking males and so on down the line. Rank is determined differently in each species. Size, strength, plumage, and the size, quality, and position of the nest are all things that birds may use to attract mates. The most desirable females end up with the most desirable males.
I think it is safe to say that humans are no different in this regard. The phrase “way of out of his league” comes to mind. In many birds, both males and females can attempt to climb the rank ladder by jumping flocks periodically. Humans do this, too. If we consider a season-long pairing of birds to be a “marriage,” the divorce rate of 50 percent is pretty darn similar to what is seen in humans. (I mention this as a curiosity, not a mathematical correlation.)
One thing to be clear about: pair bonding in the animal world usually involves what is called economic or social monogamy, not sexual monogamy. Exclusive sexual monogamy is indeed uncommon in animals, but economic monogamy is not.2 Economic monogamy means that two animals live together for an extended period, to the exclusion of living with others, for the purpose of tending to their young—in human terms, the making of a family unit. In some cases, these pair bonds are very short-lived. They can last just minutes, as in squirrels, or they can last an entire lifetime, as with majestic bald eagles. Lifelong economic and sexual monogamy, though rare, has been described in a variety of species, including angelfish, swans, lobsters, turtledoves, and African dwarf antelopes. In gray wolves, the alpha male and alpha female form a lifelong pair and lead their pack, which is usually made up of their siblings and children, some of which will remain celibate and help raise their younger siblings or nieces and nephews.
Economic monogamy usually involves a lot of nonprocreative sex between the members of the mated pair. Why would already-paired animals continue to have sex even when they are not fertile? One reason is that sex strengthens the pair bond. Sexual activity is known to release hormones and neurotransmitters. This time, I am not just talking about those in the pleasure–reward center. Another hormone that plays a role in sexual intimacy is oxytocin. It has been known for decades that oxytocin is released during sexual activity in many animals, and the result is the promotion of pair bonding with the sexual partner.3 In other words, this hormone makes an animal feel “attached” to the one that they just had sex with. The oxytocin effect strengthens with repeated exposure and weakens over time if not reinforced through periodic “booster” doses.
Why would this have come about? If a male and female have sex and conceive a litter, in some species and environments, that litter will have a better chance of survival if the parents stick together and care for the young as a team. Pair bonding helps biological parents behave as parents and care for their children as a coordinated unit. If that litter has a better success rate, they will be more likely to grow up and pass on this pair-bonding behavior. Like other neurohormones, oxytocin can make individuals, even humans, feel certain things without really understanding why. One of those things is attachment to a sexual partner. For this reason, oxytocin has been called the “love hormone,” though this is dangerously misleading considering some of the other behaviors that oxytocin can induce, including violence.4
If this hypothesis were true, we would expect to find this oxytocin effect more often in animal species that require extensive childcare, and not in species with little or no parental investment. We expect this because economic monogamy does not offer much benefit to a species that does not parent their children anyway. Indeed, this prediction appears to be true. Many species of mammals and birds show oxytocin-related pair bonding, while it has not been observed in any reptile, fish, or amphibian species.5 These “lower” animals do have their own versions of oxytocin, and it also functions in reproduction in various ways, but it does not seem to promote monogamy. This supports the notion that this new function of oxytocin, pair bonding, evolved as a way to promote good parenting behaviors in the ancestors of birds and mammals.
We are not quite done with oxytocin. Oxytocin is also famous for being one of the hormones produced by nursing mammalian mothers, including humans.6 Without it, nursing cannot occur, even if the breasts enlarge and produce milk due to the work of estrogen and prolactin, respectively. At the same time, we already know that oxytocin promotes bonding and attachment, so, as you can probably guess, this hormone also supports the development of the bond between a mother and her nursing child.
It does not end there, either. Oxytocin causes new human mothers to become very protective of their children and mistrustful of strangers.7 Paranoid, even. That is really clever because right at the moment when we need our moms to provide us the most care and give us the most protection, they are strongly motivated to do so by their own brain chemistry. Although this protection/paranoia-inducing property of oxytocin has so far only been proven in humans, it seems likely that it is also behind the well-known protective nature of other mammal mothers toward their young.
The neurological mechanism of oxytocin’s protectiveness-promoting properties likely contributes to the seemingly contradictory functions of oxytocin. While this hormone can produce feelings of attachment and, if we can use this word, love, for members of our family unit, it also promotes intense suspicion of those outside that unit. This helps to explain why oxytocin is also linked to xenophobia, racism, paranoia, and even violence.8 In one hopeful study, oxytocin was given to people with borderline personality disorder to see if it would help promote the empathy and altruistic tendencies that they lacked. The result was the opposite. Since they had no bonds that mattered to them, they experienced only the dark side of oxytocin and they became even more antisocial.9 Oxytocin is much more complicated than the misnomer of “love hormone” would imply. While it clearly promotes attachment, it can have the opposite effect toward those that are not the object of the attachment.10
In sum, oxytocin is a hormone with physical effects, but it also changes how we feel. The same hormone is used to promote bonding between sexual partners and to release milk, and, not surprisingly, we see that mothers and babies develop a strong bond as well. This is another case of something—in this case, a neurohormone—originally performing one function and then being co-opted to perform another, related function.
In order to do its thing, oxytocin is released in response to what we see, feel, or hear. It is released during sexual activity, even at the arousal stage. It does not make us feel sexy; it gets released when we are feeling sexy. Similarly, it is released in nursing mothers upon the sensation of suckling, which then allows milk to be released. It can actually begin even before that. Many nursing mothers will inadvertently begin releasing milk when they merely hear cries from a baby—any baby. When I was a baby, my mother once had to bolt out of the supermarket because she felt a wet spot on her shirt after she walked past someone else’s crying baby. This oxytocin is powerful stuff.
This role of oxytocin in sexual activity and pair bonding has been reported in animals for some time, but the research in humans is the most telling. In a 2012 study, researchers found that some men who were given a dose of oxytocin would actually move away from women they did not know, but found attractive, in a social setting; but not all men. Only those who were in long-term relationships would move away.11 The extra dose of oxytocin suddenly reminded these men that they were already bonded with someone else and that they should keep their distance from the forbidden fruit in front of them.
One final oxytocin example: this one comes from voles, small rodents that look like very small mice. These little guys are famous for being among the most monogamous, both economically and sexually, of all mammal species—certainly the most monogamous of the rodents that we know of. Researchers did an experiment with voles in which they deprived females of their natural oxytocin and observed that the preference for their mated partner was totally lost. These females would freely mate with any male—that is, any male that had not pair bonded with someone else (the males are monogamous, too). However, if given oxytocin replacement with injections directly into the brain, the females would regain their monogamy and once again prefer only their mated partner.12
This observation with voles and the one above with the men who avoided attractive women prompted some therapists to study whether oxytocin could aid couples in marriage counseling. In one oft-cited study, it seemed to work as hoped.13 However, in another, it promoted intimate partner violence.14 Oxytocin is complicated and its therapeutic potential in relationships must be explored with great care.15 Just as in the treatment of chronic mental illness, brain chemistry is intensely complicated and often resists our ability to manipulate it pharmacologically.
Nevertheless, given the parallels in oxytocin effects between humans and other animals, humans really do seem hardwired for pair bonding, and sex promotes that type of attachment. This will come as no surprise to psychologists. But what does it really say about human monogamy and marriage? As you can probably guess, my opinion is that it tells us that we are not that different from animals in this regard, just more emotionally sophisticated. (Some of us anyway.)
The consequences of hormone-mediated attachments are not always positive. In addition to the tendency to promote distrust of nonaffiliates, hormone-mediated attachment can maintain an unhealthy pair bond. I bet most of you know a woman or man who has stayed in a relationship that everyone else knows is bad for him or her. Why do people do this? Obviously there are very complex reasons stemming from underlying psychological issues, but I am not the first to suggest that biology may also be to blame. If we know that oxytocin is hard at work promoting attachment and that sexual activity also stimulates the release of dopamine and serotonin in the pleasure centers of the brain, we end up with a powerful chemical cocktail that drives a person to stay with the “bad guy” (or girl). It is very much like being addicted to a drug, involving many of the same neurohormones and brain centers. Partly for this reason, a bad relationship can be a hard habit to break.
INFIDELITY? THE CURIOUS CASE OF THE CLIFF SWALLOWS
As I have already mentioned, many species of birds that are impressively faithful in their economic monogamy do not always employ sexual monogamy. Is this like cheating? The answer appears to be “no,” because the behavior is often not hidden, is tolerated in the marriage, and is engaged in by both parties. It is not cheating if both parties are OK with it. Even in humans, some people choose to be in open marriages or reach some sort of an understanding about extramarital sexual activities. These arrangements might not be for all of us, and some can argue about the morality or propriety of them, but they do seem to work for some people. They certainly work for most birds.
The cliff swallow is a good species with which to highlight the complexity of avian social structures and the way that economic monogamy is totally separate from sexual monogamy.16 These birds live in very large colonies that include thousands of nests that look like large tubes made of dried mud stuck to the side of a cliff. Nests are always built and tended to by bonded pairs. For a cliff swallow, part of one’s status in the colony depends on nest location. The most desirable spots are near the bottom of the cliff nearest to the “public areas” in the center, presumably because they have the easiest access to the water source for bathing and drinking and for interacting with other birds. After all, it is fashionable to be seen in the hot spots, right? The less desirable locations are on the outskirts, and the lowest-ranking birds in the colonies reside in separate sub-communities, like bird suburbia.
These birds have very active social lives. Pairs work together to build and tend to their nests, sometimes stealing materials from other nests for their own, and so on. A pair may even occasionally attempt to take over another pair’s nest in a more desirable location. However, much of the socialization revolves around sex. For example, when females leave their male partners to guard the nest while they forage for more mud, they often engage in copulation with other males while they are at it. This is called an extra-pair copulation (EPC). In other words, while they are out getting groceries, the cliff swallow wives go ahead and get a little something on the side. How do their husbands respond to this? They have sex with them the minute they return.17
Why might this be? This is sometimes characterized as “monogamy betrayal” on behalf of the female.18 In response, the males have sex as quickly as possible in an attempt to remove the enemy sperm and replace it with their own. In other words, this hurried sexual event is nothing more than a male’s attempt to protect his paternity of future children.
There are other interpretations as well, spurred by a few complicating observations.19 First, the cliff swallow pair will have sex when the female returns, whether she is currently fertile or not. Second, the sperm-replacement technique does not work in this species. (It does in some others, however.) Third, these “welcome home” copulations occur with equal frequency when the female has engaged in an EPC and when she has not. Fourth, the female does not resist the spousal copulation. Resistance to copulation is observable in cliff swallows, and it is not typically seen in these instances. Fifth, as already alluded, the EPCs are done in full view of the colony; there is no apparent effort to be clandestine with sexual activity outside the pair bond.
A simpler explanation may be that these cliff swallow pairs simply “miss” each other when one is away from the nest doing chores. I find this to be a simpler explanation because the two birds are pair bonded and we know that attachment drives individuals to be with each other socially and sexually. When members of a bonded pair are separated, they “yearn” for each other and celebrate when reunified. Sex is a product of, and reinforcement for, pair bonding in part because oxytocin, released during sex, reinforces the attachment.
Rather than an attempt to fight back against cuckoldry, these “welcome home” copulations may be just that—a way that these two pair-bonded birds greet each other after some time apart. I suspect that their concept of time is not as developed as ours, so a quick errand to get some mud might feel like weeks apart. This hypothesis still needs experimental evidence, of course, but I think it is a good place to start.
But what about the EPCs themselves? Because they are not hidden, it may be that EPCs are a normal and accepted practice in cliff swallows. Considering that they happen in broad daylight, in the most public spot of the colony, and in the full view of everyone, including spouses, this does seem like the most likely scenario. Cliff swallows are swingers. So what?
There are some interesting consequences for this. First of all, every so often, we should expect extra-pair paternity (EPP), in which the male of a mated pair spends his time and resources helping to raise another male’s offspring. Indeed, that is exactly what is seen. Using genetic testing, scientists observed that EPP existed in 24 percent of the cliff swallow nests that were tested in one study.20 That is actually somewhat lower than was expected, given how much hanky-panky is going on with these birds.
Viewing this through the cold Darwinian view of constant competition, our hearts go out to the poor cuckold, and we see him as a hapless victim. As usual, the real story is deeper than this. It turns out that when researchers tested these “poor cuckolds,” they discovered that they were the most active of the male extra-pair copulators themselves.21 In other words, “cheating” males tend to end up with cheating females.
Extramarital sex is not the only shenanigans in these cliff swallow colonies. It turns out that these birds, usually the females, will sometimes place their eggs in the nest of other pairs.22 In this scenario, these “parasitic” mothers are actually pushing their own genetic offspring on to other birds. This allows them to have even more children than normal, exploiting the parenting effort of other bird pairs. This is referred to as nest or brood parasitism. It has not yet been tested whether these egg-passing events are actually the actions of “cheating” mothers returning eggs to their true father, but that seems unlikely. Just like with the “cheaters,” the tendency toward “egg passing” was stable in an individual over her lifetime. Some birds are just inclined to put their eggs in other birds’ baskets.
For some of the researchers who have spent so much time cataloguing the interesting behavior of these swallows, these birds are nothing but a bunch of liars, cheats, thieves, and cuckolds. Others suggest a different view.23 Maybe these swallows have a system of distributed parenting and paternity. Perhaps each pair and its young are not the family unit in these birds, but maybe they are more like one big family. Maybe the “pairs” are merely the unit for raising children, not necessarily making them, because pairs have been proven to be the most effective or efficient at incubating the eggs and raising the young fledglings. Perhaps these large colonies are more like a pride of lions or a wolf pack. The difference is that instead of true group parenting, like in lions and wolves, these animals break down into pairs for the purpose of egg incubation and care of the hatchlings.
I find this alternative especially appealing considering the fact that extra-pair copulations may be a key triggering event in the evolution of colonial living in birds.24 This theory holds that at least one incentive that a male or female bird has to live in close proximity to other birds is to pursue EPCs. While the cuckold might have a reason to try to stop EPCs by his/her spouse, the cheaters themselves stand to gain substantially by sharing their genetic potential with as many as possible. Colony living makes that easier. While this inevitably sets up a “battle of the sexes” style conflict, communal paternity may be one way that birds have evolved to mitigate that struggle.
In addition, the more traditional view that EPCs are purely deceitful, parasitic, and ruthlessly competitive, requires some assumptions that I find problematic: These poor birds cannot spot their spouses cheating on them in plain sight, despite having excellent vision. They cannot stop others from placing eggs in their nest while away from the nest for mere minutes. They cannot spot a fresh, warm, foreign egg on top of their own eggs laid days before. Some of the birds are completely helpless when it comes to thwarting this deception and exploitation, while others are ingenious at executing it. In summary, you would have to believe that these birds are both fiercely competitive and very stupid. Keep in mind that these same birds have learned how to build nests on the side of a stone cliff without the use of fingers or hands. And yet they are hopelessly dim?
On the other hand, the view that cliff swallow flocks operate as one big family has some complications as well. Most importantly, it is difficult to imagine how cooperative parenting could emerge when an individual has such a powerful incentive to “cheat.” Prosocial behaviors would not be rewarded by natural selection and selfish ones would be. Remembering that selection generally operates on the level of the individual, maintaining such distributed cooperation would be hopeless when individuals have no incentive to pull their weight.
However, there is one way in which the cooperative parenting model does favor the interests of individuals and the particular genes that make it possible. This is referred to as kin selection, when the group members in question are all close relatives.25 Kin selection can operate to promote close cooperation in groups of individuals that are closely related because the genes that promote the cooperation also promote their own successful reproduction. Under the right conditions, this can be a powerful force and helps explain the social behaviors of a diverse array of animals from ant colonies and beehives to wolf packs and prides of lions. Genes that lead you to help your close relatives are self-promoting, provided that the relatives share those same genes.
Could kin selection be at work in cliff swallow colonies? Possibly. Studies have shown that they are quite inbred. Each member of the colony has a 50 percent chance of being a first- or second-degree relative to each other member.26 While this is not as closely related as members of a wolf pack or bee hive, it is at least possible that this is related enough to promote kin selection-mediated emergence of cooperation in child-rearing. I find this even more appealing when you consider that the cliff swallows do have quite a bit of competition as well. It is not all cohesion and harmony. As I mentioned before, pairs of cliff swallows attempt to evict and steal nests from better-placed rivals. Some pair bonds are dissolved because one member finds a better mate. The lower degree of relatedness than that found in some other kin-selected social groups predicts a lower degree of cooperation and a higher degree of competitiveness.
When you factor in the EPCs and the brood parasitism, a staggering 47 percent of all cliff swallow nests produce at least one fledgling per season that is not the biological offspring of one of the parents.27 Of course, this could be because of the fierce competition that goes on, but I support the opposite view: that distributed and cooperative parenting is part of the social fabric of the species, even if it is associated with some tension and healthy competition.
Another thing that would be predicted by the more “progressive” view of cliff swallow extended family life is that copulation is about much more than just paternity and conception. I have already noted that it promotes bonding between the married couples. What I failed to mention is that the mud hole also sees a lot of male-on-male action.
Because these birds have no external genitalia or sex-specific markings, researchers have a tough time quantitating the male-male sexual activity by simply watching from afar. It is easy to tell when a male bird mounts another bird because females do not seem to mount at all, but it is not easy to know for sure if the mounted bird is a female or another male. Instead, the researchers used taxidermic stuffed swallows and observed that 70 percent of the copulation events were males mounting the stuffed male rather than the stuffed female.28
More on same-sex sexuality in a moment. For now, my point in telling you this gigantic story about swallows is to highlight how issues of sex and family are complex—not just for humans, but for all animals. When it comes to observing things like sexual activity, pair bonding, fidelity, and parenting, there is usually much more to it than meets the eye. We all know that you cannot really learn much about a married couple by observing them casually at a distance for a few hours. The same is true for animal species. A scientist must keep a watchful eye and a mind open to possibilities that do not conform to the sexual norms she is accustomed to in today’s society. As with the cliff swallows, sex might be used as often to promote pair bonding and colony cohesion as it is for procreation.
Another reason that I have spent so long discussing these swallows is to introduce a theme that has come up time and time again in this book and will continue to: cooperation. Many people, even some biologists, regard natural selection as a cutthroat competition between fellow members of the same species. The many struggles of life are boiled down to the phrase “survival of the fittest.” This can be misleading, especially because we often forget that “fitness” is measured not by strength, health, or vitality, but in contribution of one’s genes to the next generation. Many animals, particularly birds and mammals, have long figured out that cooperation is just as good a path to fitness as is competition.
Cooperation is particularly beneficial for the process of natural selection when the cooperators are closely related to each other. In this case, the relatives share many genes already, including, presumably, the genes for cooperation. One can easily imagine a scenario when “cooperation genes” came into existence through mutation and were spread to offspring for a few generations. If these cooperation-prone animals then work together and breed together, they may be more likely to survive and be successful. For this to work, the communities must be relatively small, close-knit, and inbred. Over time, the cooperation genes spread and eventually take over the population as the individuals that cooperate fare better than those that do not. Importantly, even an individual that does not breed can still promote the persistence of the cooperation genes by helping out siblings, parents, and cousins. By helping your close family, you are promoting your own genetic stock.
This is not to say that within cooperating communities there is no competition. There certainly is. Each pair of cliff swallows is always vying for the best nest, and fights over nest location do occur. There are sometimes even evictions and attempted evictions as the dominance hierarchy plays out each season. After all, a little healthy competition is good for a breeding population, even when the population is marked by substantial cooperation.
In fact, there may even be extra pressure to “weed out” freeloaders in a cooperative society. In a purely competitive social structure, any lazy or otherwise suboptimal individuals would quickly perish under the weight of their own problems. In a society of shared labor, however, these pure “takers” may attempt to slide by undetected, benefiting from the cooperation of others while donating little effort in return. Thus, intra-flock competition helps keep everyone on their toes and performing at their best.
In summary, the life of the cliff swallows, with all of its egg-passing, extra-pair copulations, sex-heavy married life, and shared parenting, is best seen as a mix of cooperation and competition. It is more like a basketball team than a track-and-field event. Each member may try to “stand out,” but the good of the team comes first.
You may wonder why I have spent so long discussing this single species of bird. I have done so not because cliff swallows are special, but because they are not. We know so much about this species only because scientists have taken the time to watch them. Charles and Mary Brown have been studying one particular colony of cliff swallows for more than thirty years.29 The story seemed so simple at first, but closer inspection revealed a staggering complexity and nuance in their social dynamics. It seems rather likely to me that just about every species has similar complexity and nuance, just waiting to be discovered. I wonder how many species we have misunderstood because we have not taken the time to observe and study them carefully.
A WORD ABOUT MONOGAMY IN HUMANS
In animals, we saw that sexual monogamy is pretty rare. Instead, social/economic monogamy, without complete sexual fidelity, is quite common. Ninety percent of bird species are monogamous in this way and about half of mammals are, with most of the remainder engaging in variations of community-based family (prides, packs, and so on) that are essentially extensions of economic monogamy in terms of mutual investment in “marriage and family life.”
In my view, economic monogamy is the better parallel to human marriage than sexual monogamy. Hear me out. I am not saying that most human married couples are not faithful; I am not saying that we should not even bother trying to be faithful; and I am not saying that sexual fidelity is not an ideal that we should strive for. What I am saying is that we should be honest with ourselves about this topic. First of all, we know that many marriages do not enjoy perfect lifelong sexual monogamy. I might even say that most marriages eventually struggle with fidelity and temptation in some way. In fact, does anyone disagree that lifelong marital faithfulness requires constant effort and ever-renewing commitment? It might even be said that being faithful feels to many, at one time or another, contrary to their natural urges and appetites. Any priest/minister/counselor/friend will tell a couple intending to marry that they may have struggles ahead in this department. This is just a fact of life for us.
To admit this truth is not the same as making a biological argument for the abandonment of marriage or faithful monogamy. That is not my intention. Far from it—I am a happily married man in an arrangement that we have both decided will be sexually monogamous. Personally, I accept that I may be “going against my nature” a little bit in order to embrace monogamy. I am happy about that choice, and I make it freely. After all, there are many behaviors commonly seen in nature that human beings have decided are no longer fitting for us, such as murder and infanticide (see chapter 7 on jealousy).
Furthermore, it has long been known that restraining some of our appetites and urges can be in our best interests (see discussion of gluttony in chapter 8). In fact, in my view, knowing the biological reality that sexual monogamy can sometimes be a struggle offers a more honest and realistic path toward achieving it. It facilitates candid discussions about sexual needs, reduces pointless guilt about temptation or near misses, and allows understanding and reconciliation should these be required.
SAME-SEX SEXUAL ACTIVITY
For many biologists, homosexuality was previously seen as a conundrum. First, they did not think that animals experienced any same-sex attraction or purposefully engaged in homosexual acts. So where did it come from in humans? Second, homosexuality, in humans or other animals, seemed contrary to what natural selection would predict. It would seem that same-sex attraction would tend to reduce fertility. If a trait reduces fertility, even a little bit, it will quickly be eliminated, as the bearers of that trait would leave fewer offspring—right? For these reasons, many people considered homosexuality to be unnatural, an aberration seen only in humans and thus probably psychological, not biological. I will not go into all the harm that this kind of thinking has caused, but suffice it to say that for a long time, many people—even scientists—considered same-sex sexual activity to be unnatural.
Once again, it turns out that we were wrong. Both of these claims were completely inaccurate. First, animals most certainly do engage in same-sex sexual activity. A lot. In every species in which it has been looked for, it has been found. As of 2008, no fewer than 1,500 animal species have been observed to engage in sexual activity with members of the same sex.30
Also, it turns out that same-sex sexual activity does not seem to reduce reproductive success, either in animals or in humans. Although the data are still coming in, several possible explanations have been proposed. First, we should discuss the prevalence of same-sex sexual behavior in animals. I begin with selected examples from humans’ more distantly related creatures and build up to our close relatives. I should also say that I am well aware that applying the term “gay” to animals is not exactly accepted terminology. I do not advocate that it should be. I am just using it to lighten things up. The term “same-sex sexual activity” is pretty clunky to write and boring to read. Please forgive me the impropriety if I take a shortcut here and there.
Bedbugs have been found to engage in male-on-male sex. I am not kidding—gay bedbugs! This example is kind of a letdown because it seems to be nothing more than a case of mistaken identity. A male bedbug will usually mount and inseminate a female bug that has recently fed. Sometimes, however, he will mount and inseminate a male that has recently fed. Insemination in bedbugs means using a needle-like organ to pierce the body and inject semen directly into the abdomen, a phenomenon called traumatic insemination, which can cause injury, infection, and death.31
Not surprisingly, male bedbugs will resist being mounted, given how injurious it is. Sex injures females also, but unfortunately, that is just how it goes for bedbugs. These injuries are the cost of reproduction for female bedbugs. When a male bedbug injects another male, however, there are no winners. In fact, it was recently discovered that male bedbugs will emit an “alarm” pheromone after eating that attempts to signal to other males that they are male and that insemination would be pointless.32 That this pheromone is not 100 percent effective argues that this antirape defense could be a relatively new evolutionary innovation and the species is still growing into it.
I offer bedbugs as an example of an invertebrate (an animal with no backbone) in which homosexual activity has been described in some detail. Other invertebrates with a pension for gay sex include blowflies, wasps, fleas, silkworms, octopus, flukes, locusts, and butterflies. Until recently, most biologists chalked all of this same-sex sexual activity up to mistaken identity. That may be a likely explanation for bedbugs, given that they have poor eyesight and their sense of smell is focused pretty exclusively on the detection of blood, whether as food or in the search for a well-fed female. However, mistaken identity is a pretty poor explanation in most other species. Many invertebrates have incredibly keen eyesight and smelling. I find it exceedingly unlikely that insects that can easily tell a virgin female from a nonvirgin would be totally helpless in distinguishing males from females.
Same-sex sexual activity has also been noted in all the major divisions of vertebrates: the older ones (fish, amphibians, and reptiles) and the newer ones (birds and mammals). In chapter 4 we talked about some of the courtship behaviors of multiple-gendered male fish and the “female mimicry” of some Canadian garter snakes that trick the males into having sex with them in order to steal body warmth.
Turning our attention to birds, same-sex sexual activity has been reported anecdotally in zoos and sanctuaries since time immemorial. In the past, this forced some uncomfortable acknowledgement from biologists that same-sex sexual activity had occurred, but it was usually characterized as a strange side effect of captivity or small population size. This is sometimes called the prison phenomenon, and I think you can imagine why. To me, the fact that it was called the prison phenomenon exemplifies the prejudice that many scientists held for so long. They refused to believe what was happening right in front of their eyes. Because of this, the long-held view was that same-sex sexual behavior in animals was rare, an artifact of captivity, and occurred only when access to the opposite sex was limited or impossible.
Farmers have known better all along. While most bulls are aggressive toward other males and are usually kept in a separate paddock to avoid fights, there is occasionally a bull that prefers to mount other males. This mounting can lead to ejaculation if the mounted bull allows it, and he sometimes does. Farmers can usually get these male-preferring males to impregnate females by simply denying them access to males. (I bet no one calls that the prison phenomenon.) But even that method fails sometimes: some bulls simply will not voluntarily have sex with a female cow.33
This reminds me of what happens with human gay males. Most of them will admit to having had sex with a woman or two before coming out of the closet, while a few remain “pure.” There is even a term for this: a gold-star gay is a man that never once engaged in any sexual activity with a woman. I digress. Actually, no. This a valid comparison, is it not? Most of the gay bulls can perform with a female if they really have no other choice, and the same is usually true for gay men. For most of the last few centuries, they really did have no other choice and so most of them remained in the closet, married, and fathered children.
Anyway, seemingly without exception, all of the herd-living mammals show plenty of male-on-male mounting, penetration, and orgasm. Bison, wolves, gazelles, antelope—you name it. The kob is an animal that looks like a cross between an impala and an antelope and lives abundantly in the African savannah. It turns out that, when population size allows it, the females will form large female-only herds and engage in lots of sexual activity among themselves, including genital licking and rubbing, mounting, and general affection, such as licking-kissing and rubbing heads. They will still get pregnant by allowing an occasional male into the fun, but the male does not stick around after the sex, nor do the females seem to “enjoy” the procreative sex when it does happen.34
One of the gayest species of all is the giraffe. One study found that 94 percent of the time that a male giraffe mounted, he was mounting another male.35 Ninety-four percent! Other studies have put the estimate of same-sex mountings between 30 and 75 percent. Either way, that is a lot of same-sex sexual activity. Some biologists of the older and more conservative persuasion get rankled if we refer to these mountings as sex. They would say that this mounting behavior in giraffes and other animals is about dominance, not reproduction, and thus, it does not count as sex. Huh? Only reproductive sex actually counts as sex? Really? So then, if a woman has sex with her husband while she is on the pill, does that mean that they did not actually have sex? By this bizarre definition, two men or two women can never actually have sex, which would come as quite a surprise to the LGBT community.
Sex is sex, and the refusal to see nonprocreative sex as true sex brings us back to the deep-seated prejudice and scientific bias with which we began this discussion. The fact that male giraffes have sex with each other for reasons that are obviously not procreative is precisely the point. Sex, in animals and humans, is about more than just procreation.
In the case of these male giraffes, they mount and penetrate each other to the point of climax, meaning that, yes, they have orgasms when they do this. What I think is even more interesting is that they will do this after a battle for dominance. Not before—after.36 One giraffe has already won, and the other has yielded, and only then do they “get busy.” Scientists that want this to be purely a dominance display are really grasping at straws because the struggle for dominance is over by this time. Furthermore, the sex that the males have is not violent, and the vanquished male is not forced into submission as if it were rape. The giraffes engage in “necking,” which is just what it sounds like—mutual neck rubbing. They are affectionate and playful for a while before the dominant male mounts. That sure sounds like foreplay to me. The interesting question is, why? Why do they have sex after the dominance struggle is over?
For giraffes, scientists do not have solid answers on that yet, just descriptions of the behavior. In many other species, however, there is a much fuller understanding of the many functions and purposes of same-sex sex. Some of these are listed on the pages ahead, and maybe one of them applies to these gay giraffes.
The rampant bisexuality and homosexuality of dolphins has been well reported in the scientific literature and the popular press. In one study of 120 male bottlenose dolphins, researchers found that they not only spend almost all of their time with other male dolphins, but they also spend a lot of time having sex with them.37 In fact, dolphins often travel in groups comprised entirely of one sex. The all-male groups will engage in sexual activity quite frequently, including body contact that is genital-anal, genital-genital, and oral-genital. (They will even penetrate each other’s blowholes, giving new meaning to the term “blow job.”) This body contact between males includes orgasm/ejaculation and often involves more than two males at a time. Orgies of up to fourteen males have been reported.
While female dolphins are not as sexually active with each other, female-female sex has certainly been seen as well.38 When it comes time to actually breed, a group of males will have to work together to herd and corner a group of females. The females do not appear to go willingly, but—as is often true with animals—it is difficult to know for sure if the chasing, resistance, and forced sexual contact are truly violent or just part of the expected courtship. After all, some like it rough. One thing is certain, however. After the brief, procreative coed encounter, both the males and females are eager to get back to their sex-segregated pods and all the orgies that await them.
Rams (male sheep) turn out to be the species that has grabbed the most headlines for their gayness. This is due to the discovery of slight brain differences in the gay rams compared with the straight ones.39 This announcement was met with simultaneous applause and outrage. While some people were delighted to see hard, measurable proof that homosexuality was an innate biological feature (and thus not a choice), others feared for what might be done with this information. Would it somehow be used in the future to try to cure, abort, or breed out the gays from the human population? Some of these fears intensified when the researchers proposed to probe further so that gay rams could be identified during the process of selecting rams for breeding. They also planned an experiment to see if hormone treatment during pregnancy would alter the same-sex attraction. Much of this was exaggerated in the press, and the researchers were demonized by great mobs because of erroneous reports about what they actually intended to do.
Controversy aside, the discovery itself is fascinating. Working with a population of domestic sheep, researchers put single rams together with pairs of restrained ewes or rams and observed their mounting behaviors. They found that 7 percent to 10 percent of the rams would not mount ewes at all but would aggressively mount the restrained rams and ejaculate. Those are the “gay sheep” that you may have read about, but the study found more than that. About 20 percent of the rams would mount both ewes and rams, reaching orgasm with both. I suppose these would be bisexual rams. A whopping 15 percent would mate with neither. Can we call them asexual rams? This study has since been repeated several times, by the same group and others, with slight variations. A later study reported slight differences between gay and straight rams in their brain anatomy and sex hormone levels. The fascinating picture that emerges from the study of male sheep sexuality is that only a slim majority of rams are the expected male-attracted-only-to-females.40
Personally, I suspect that the sheep studies actually underestimate the diversity of sexual preference because they examine only anal penetration, and only from the perspective of the mounter, not the mountee. Using common gay slang, this study was only on the lookout for “tops,” the ones that enjoy doing the penetrating. But what about the “bottoms?” (Bottoms are males that prefer to be penetrated, rather than penetrate someone else.) It is conceivable that at least some of the 15 percent of the sheep that were reported as “asexual” do not mount the males or the females simply because they are just not into mounting. Maybe they prefer to be mounted? Or maybe they are not into anal or vaginal sex at all and prefer oral sex or some form of frottage? Before you scoff, remember that so, too, did most people scoff at the notion of gay animals just a few decades ago.
The example of gay rams is useful because it shows how much more diversity exists in sexual orientation than biologists previously thought. In fact, sheep sexuality bears a striking resemblance to the Kinsey scale for humans, in which strict heterosexuality and strict homosexuality are at the extremes, plenty of individuals fall in the middle somewhere, and some individuals (so-called asexuals) have almost undetectably low sex drives. More study is needed, not least of all because many studies, for some reason, have only examined males. The most important lesson to take from all of these reports of same-sex sexual activity is that it has been found where it was least expected to be—everywhere.
How was all of this gay sex missed by biologists and naturalists for so long? Prejudice seems the likely reason. I do not necessarily mean that all biologists were sexist or homophobic, although many surely have been. What I mean is that if you are not looking for something, you usually will not find it. While critiquing a field biological study published in a top journal, Bruce Bagemil stated it this way: “Every male that sniffed a female was reported as sex, while anal intercourse with orgasm between males was [reported as] only dominance, competition, or greeting.”41 In other words, biologists did not really think of two males having sex as two males having sex. It had to be something else.
To be fair, observing, cataloguing, and analyzing animal behavior is a long and arduous process, so it is very easy to overlook things that you were not looking for in the first place. It is not that these biologists were blind or sloppy. They were just testing other hypotheses. Also, while pretty much all animals engage in same-sex sexual activity, the vast majority of them do not do so at the total exclusion of opposite-sex sexual activity. For most animals, there is plenty of sex with members of both sexes.
SAME-SEX PAIR BONDING
The previous section was about animals having same-sex sex, per se. Just the sex act itself. However, it turns out that the “homosexual” nature of animals is not limited just to having sex but also includes choosing “mates” as pair bonds. Our story begins with the most prolific of all pair bonders: birds.
Albatrosses are large sea birds that have distinctive orange beaks with downward-pointing hooks at the end of them. Unlike gulls, skimmers, and egrets, they have webbed feet that look like those of ducks and pelicans. They are majestic creatures that are both beautiful and ugly at the same time. As you may remember from your high school British literature class, “The Rime of the Ancient Mariner” centers on the pointless killing of an albatross. They are nearly as famous for a groundbreaking study documenting extensive same-sex pair bonding.42
Albatrosses live in large, stable colonies or flocks but engage in some immigration between flocks to reduce inbreeding. They generally pair bond for life, following a very elaborate dance-based courtship. In fact, these long-lived birds reach sexual maturity in five years, but most will not breed or form a pair bond for another two years, sometimes longer. It takes an average of two mating seasons for an adolescent to learn the mating dance through observation, mimicry, and trial and error. Both sexes engage in the courtship behavior, which is primarily by display only and not directly competitive or hostile. Once a pair is formed, they mate for life, and they never dance again. (Some human married couples may feel that pain.)
Each breeding season, the paired albatrosses work together to build a nest, defend it, incubate an egg or two, hunt and forage, and share food with each other and the hatchlings. There are no sex or gender roles (except in the actual laying of the egg), and duties are always shared.
In the now-famous study, hundreds of Laysan albatrosses were studied over a three-year period in Oahu, Hawaii. Of the 125 nests that were built by bird pairs, thirty-nine of them were tended by a female-female pair. That is one-third of the nests, representing half of all of the pair-bonded females. (Colonies have lots of unpaired birds of both sexes that are either widows looking to pair again or those that have not yet learned the dance or attracted a mate.) It is true that there were fewer males in this particular colony (41 percent), but that does not come close to explaining the high rate of female-female pairing. This is no “prison phenomenon,” and we are not just talking about sexual acts that some stubborn biologist will insist on explaining as something else. One-half of the pair-bonded females were lesbians—they selected a fellow female bird on purpose and stuck with her for life.
These lesbian pairs were almost as successful as their heterosexual counterparts at producing offspring. This indicates that the birds were engaging in EPCs, as we saw with cliff swallows. The two females engaged in alternating maternity such that nearly every incubated egg belonged to one of the pair. (The occasional “offspring” that belonged to neither was the result of other birds putting eggs in their nest in a rarely successful but frequent attempt to distribute offspring and parasitize parenting, also as in cliff swallows.) These lesbian albatrosses are “fit” in the evolutionary sense (they leave successful offspring), and their pair bonding is just as lifelong as the opposite-sex pairs.
Prior to this study, it was assumed that a same-sex couple raising children was a rarity in nature, occurring only when the couple were siblings or otherwise closely related. Thus, the authors of this study conducted genetic tests and were surprised to see that the same-sex albatross couples had the same low incidence of relatedness that the opposite-sex pairs had. Also, the pairing of the two females occurred after the same elaborate courtship dance and prior years of trying. The pairing was not sporadic or desperate—there were still plenty of unpaired males around. These birds knew what they were doing.
It is also worth noting that these lesbian albatross pairs are just as sexually active as opposite-sex pairs are. Sure, they occasionally go off to get pregnant by males they are not bonded to, but to be fair, so do “straight” females. Why do these birds have sex with each other when the sex cannot possibly be procreative? For the same reason that opposite-sex human couples have sex even when they are practicing birth control: because they enjoy it and because they love each other. I cannot say for sure whether these albatrosses feel love for each other like we do, but we do know that they stay paired until one of them dies. This is, yet again, a demonstration that sex promotes pair bonding among animals, even when it is not procreative.
This study shocked the scientific community and was widely reported by the popular press. Gay rights groups were elated, and conservative preachers were indignant. But why all the uproar? Surely we already knew this about birds. Once again, it turned that we had seen all of this before. We just did not believe it.
In 1998, two male penguins in the Central Park Zoo in New York, Roy and Silo, courted each other, pair bonded, and built a nest together.43 They even appeared to attempt the hatching of an egg-shaped rock. They actively tried to steal eggs from other nests. I suspect they would have been successful had they been in the wild, rather than a zoo, where the population is more concentrated and food is brought right to the nest-defenders by zookeepers. Noticing that the pair was male, the handlers provided them with a fake egg that looked and felt real. They promptly began to incubate the egg—and diligently. They took turns and primped the nest in preparation for the child. Clearly stressed when the egg never hatched, Roy and Silo got their wish when the zookeepers finally provided them with a real penguin egg to care for.
These two gay penguins incubated their egg dutifully, and a healthy baby female, Tango, was hatched. In an interesting twist, the egg that was given to them was taken from a male-female pair that had failed to hatch their eggs despite two tries. This straight couple just was not attentive enough to the incubation, and, without the proper warmth, bird eggs do not develop. This is a very good parallel to the current trend of gay human couples serving as foster and adoptive parents for children whose biological parents cannot provide the care that is needed. Little Tango was raised healthy and happy by her foster fathers. In fact, this case has served as a model for gay foster parenting of penguin eggs and chicks that has been replicated at zoos around the world.
Gay bird pairings are not just an artifact of captivity. In Australian black swans, male-male pairings are almost as common as female-female pairings are in albatrosses.44 In fact, studies have revealed that the gay black swans are more reproductively successful than their straight counterparts. How can a gay male couple have more biological children than a straight couple? Well, these gay black swans occasionally let a female into their roost for the purpose of fertilizing and laying eggs. They take turns mating with her, and paternity is shared more or less equally. Then, the three of them stay together through the egg incubation and hatchling stage. That these eggs are nurtured by a threesome explains why they are more successful than “traditional” male-female couples. When it comes to defending a nest, incubating eggs, and protecting young hatchlings, three beaks are better than two, at least in black swans.
This is a good opportunity to draw the distinction between “having lots of children” and “reproductive success.” Even if he sires thousands of offspring, an animal is not reproductively successful if those offspring do not live to sexual maturity and sire offspring themselves. Parental investment has evolved in many animals, especially birds and mammals, as a strategy to have fewer offspring and to care for each of them better. In such a strategy, pair bonding is about more than just having offspring. It is also about caring for those offspring. Among birds, pairs are usually better than single parents because they are able to divide the labor. One parent can go out to find food, while the other incubates the eggs or protects the babies. The hunter-forager must find twice as much food, but she can take all the time she needs knowing that the eggs or babies are safe. For a single parent, there is just no way to hunt and incubate the eggs at the same time.
Lest you think that I am making an argument that human single parents are not as good as human coupled parents, be assured that I am not saying any such thing. In the case of humans, we have civilization, technology, currency, society, culture, and an endless list of things that make us different from animals living in the wild, especially when it comes to meeting the needs of our children. Furthermore, I was discussing birds in this example. In most mammal species, the rearing of children is not the work of either single parents or couples—communities are involved. That is the better analogy for humans—we raise our children in a community, a society working together.
If you do not believe me, consider things like day care, playdates, babysitters, and schooling. We are constantly bringing our children together with the children of others and arranging some form of cooperative care, sometimes with an economic exchange and sometimes not. It is really not so different from when a lioness leaves her cubs to be nursed by another female in the pride while she goes off to hunt for the group. The fact that black swan threesomes are more successful parents than black swan twosomes is helpful to understand the survival pressures of their particular habitat. That habitat bears no resemblance to the modern human experience, so trying to project social values in either direction is a little silly.
My point here is to say that, if “family” is defined as individuals living together and sharing a common purpose in raising offspring, birds and mammals have long known that there are many ways to make a family, something humans are only now begrudgingly figuring out.
If I wanted to be antagonistic here, I could point out that the traditional family unit of mother-father-children is the aberration, even for humans. Before the dawn of civilization, all evidence points toward communal living, not unlike the troops of chimpanzees and gorillas that we see in Africa today.45 The family unit was a large group in which children were raised together, nursed together, and learned together. In fact, in many developing countries, families still exist in multigenerational units with grandparents and cousins all living together. There is a very solid basis to say that this extended family motif may be the most “natural” arrangement for a human family. It is curious that few people would argue that we should all return to that.
Hillary Rodham Clinton took some flak from conservatives for her 1996 book It Takes a Village, which took its name from the old proverb that children are not raised by their families in isolation but within a community. Various features of the village will profoundly affect the child, regardless of the behavior or wishes of the parents, so goes the saying. Things like education, health care, public safety, mass media, and entertainment programming are just a few of the features that come to mind.
Ignoring the politics of the issues here, this is a pretty good way of thinking about how community interactions are an integral part of how humans engage in communal parenting. The actions of the community can affect the success of your children, no matter what you do. No amount of parental investment, care, and love would have prevented the early deaths of most children born in the plague-infested days of the twelfth century. Similarly, even the most negligent parents are unlikely to lose a child to polio or smallpox these days. Working together, we have taken measures to ensure the survival and success of our children.
Human society, government, schools, and other institutions are merely our ways of formalizing the incredible amount of mutual investment we all have in each other, especially in our collective children. What is good for all of us is good for each of us, and vice versa. At the level of biology, we are all interconnected as one extended family, just like those cliff swallows, albatrosses, penguins, and giraffes.
BIOLOGICAL BENEFITS OF HOMOSEXUALITY?
I have already mentioned a couple of scenarios in which homosexuality actually provided a fitness benefit. In the black swans of Australia, two pair-bonded males entice a female surrogate to make a temporary arrangement for baby-making. In penguins and many other species of birds, two males can raise youngsters with alternating paternity without having to lay the egg. Egg laying, while not as demanding as giving birth to live young, still requires a substantial investment from the energy and nutritive resources of the mother.
Those are simple examples, but more interesting ones exist as well. For example, in any social species with sex-specific dominance hierarchies, there would be a clear benefit for an individual to form a pair bond or close alliance with the highest-ranking individual that he or she can, regardless of their sex. There would be a corresponding disadvantage for any individual that would not pursue alliance with high-ranking individuals because of their sex. In matriarchal species such as elephants, bonobos, and orcas, females will aggressively pursue alliances with higher-ranking females and those alliances include sexual gratification.46 In these species, a female who will not have sex with other females will quickly drop to the bottom of the social ladder and have no chance at successful reproduction.
Another idea regarding the advantage of homosexuality is found in the world of kin selection. Kin selection means that a trait can be favored through the enhanced reproductive success of relatives, who presumably also have the underlying genes. Genes for family cohesion and cooperation could be preferentially passed on, even when only some of the family members do the reproducing. In wolf packs, for example, some members forgo their own reproduction and instead help raise their siblings’ offspring.47 This would apply quite nicely if it were found that homosexuals tend to help their families and contribute to their reproductive success.
It turns out that there is a study that has found this to be true. This work was done in one of the strangest mammals of all—humans—located in Samoa (the independent Polynesian nation, not the American territory). Canadian researchers working there found that gay men invest more time and financial resources into their nieces and nephews than straight men do.48 Thus, kin selection could help explain the prevalence of homosexuality in humans.
You are probably thinking that this is a bit of a stretch to think that “nice gay uncles” offer so much of a survival advantage to their nieces and nephews that it would overcome any lost fecundity from their refusal to mate with women. I hear you. But remember two things. First, you are probably thinking of “nice gay uncles” in the modern world, lavishing gifts and picking up the kids from soccer practice. While humans were evolving, life was a constant struggle, and most children did not survive to reproductive age. Having another adult around to help with protection, food gathering, shelter fashioning, and predator lookout would have been really handy. It could have made the difference between life and death on more than one occasion, and voilà—there is the enhanced reproductive fitness.
Besides the data from Samoa, there is plenty of anecdotal support for the helpful gay uncle hypotheses. Many gay men opt not to have children themselves and instead spoil their nieces and nephews with both time and gifts. In the prehistoric era, this might have made a real difference in their survival rate.
Another hypothesis has emerged from studying homosexuality in humans. Several studies have found that female relatives of gay men have slightly more children than female relatives of straight men.49 It is fair to say that this connection is still considered tentative, but it has been observed in a variety of ethnic groups in studies taking place in Italy, England, and Independent Samoa. So far, this increased reproductive rate has only been seen in the relatives of gay men, not lesbians. Interestingly, the increased fertility observed in the female relatives of gay men are those that are related to gay men via matrilineage.
Matrilines are lines of ancestry that follow only females and their offspring. In other words, your mother’s sisters are your matrilinear aunts. Your father’s sisters are not. Your cousins that are the children of your mom’s sisters are your matrilinear cousins, but the children of your mother’s brothers are not, nor are the children of your father’s siblings. Basically, matrilines are genetic relationships between two individuals in which the connection between them consists only of females. What the studies mentioned here have found is that the mothers, maternal aunts, maternal grandparents, and matrilineal cousins of gay men tend to have more children than those same relatives of straight men.
What does this mean? Two related hypotheses have emerged. One says that the genetic elements that are at play are expressed as homosexuality in males and hyper-heterosexuality in females. This claim seems to suggest that there are specific genes that encode sexual attraction to men, making men gay and women very straight. If you think this sounds odd, I agree with you.
A more accepted hypothesis is that, somehow, genetic elements responsible for gayness in men can lead to increased fertility in women. This makes a lot more sense to me. First of all, there is good reason to believe that sexual orientation in humans is only influenced by genetics, not strictly coded for. Other factors, including environment and even social factors in early childhood, likely play a role. Gestational hormones in utero have long been suspected, and some animal studies do support the notion that the sex steroids (testosterone, estrogen, progesterone) in utero play a role in development of sexual orientation later.50 If this is true, a connection to fertility is easier to imagine since those same hormones can affect a woman’s fertility.
There are two genetic factors that associate with matrilineal inheritance: the X chromosome and mitochondrial DNA. Since the very few mitochondrial genes seem to function only within the mitochondria itself, most believe the X chromosome is the prime place for genes that connect sexuality and fertility. Although a specific genetic element called Xq28 (named for its location on the chromosome) has been linked to male homosexuality,51 subsequent studies failed to confirm this and the jury is still out on the matter of homosexuality and the X chromosome.
Regardless of the mechanism, would a connection between gay men and fertile women make sense in terms of evolution? It could, especially if you think about those gay uncles helping to raise the extra kids that their mothers, sisters, aunts, and cousins have. Although that seems a little too neat to me, it does make some sense and merits further study.
Another possibility is that some genetic element emerged that enhances female fertility. Then, purely by accident, it also increases the likelihood of homosexuality in men. If we assume that homosexuality causes at least some reduced fertility, this is a case in which the genetic element is being pulled in two directions, something that is not altogether uncommon in nature. Adaptations are often trade-offs, and maybe this is an example of that. In the case of male homosexuality, the genetic nature of it seems to be nothing more than a predisposition, an increased likelihood. Homosexuality does run in families, but only weakly so. Female homosexuality seems even less easy to pin down genetically, but that could simply be because less research has been done on gay women.
On a personal note, I routinely bounce back and forth between caring how and why people are gay. On the one hand, who really cares? Homosexuality is clearly a natural variation that is common among animals, especially mammals. It does not hurt anyone (although sometimes gay people are hurt by others because of it), and the vast majority of gay people say that they would not change their sexual orientation even if they could.
The scientist in me, however, is not satisfied with that. Of course we care about how people become gay, just like we care about how people get green eyes. Curiosity is in our nature; it is an essential part of who we are. I am not talking about “we scientists,” but we humans. We are a curious species, always compelled to ask why things are the way they are. And that is a good thing—our endless curiosity compelled us to the moon, to the South Pole, and to the Higgs boson. Along the way, we invented radio, refrigerators, and the Internet. You know why? Because science.
The take-home point here is that sexual activity between members of the same sex is rampant throughout nature and quite pronounced in our own class, mammals, and our own order, primates. Thus, it is not surprising that it is so common throughout all populations and cultures of our species. Whatever its reproductive costs, its benefits must outweigh them, or else it would not have persisted and flourished so far and wide. These benefits are likely to be similar in humans as in other animals because—you guessed it—we are not so different.
FREUD, OEDIPUS, AND INBREEDING
Sigmund Freud claimed that all little boys subconsciously want to kill their fathers and marry their mothers and termed this the Oedipus complex, after the classic Greek tragedy of Oedipus, whose main character unknowingly does just that. This flies in the face of the universal human taboo against incest. In all cultures across the globe, marrying and sexual activity among siblings or between sons or daughters and their parents is socially forbidden, and a vanishingly small percentage of people report any inkling of sexual interest in such endeavors. So, was Freud wrong?
Sex between close familiar relations (siblings, parents/children) is very rare indeed. The taboo is relaxed, however, when the relation is more distant. Sex and marrying among first cousins is not nearly as uncommon or as frowned upon as it is among siblings. Sex among second cousins is even less so. Beyond that, no taboo exists. In fact, the current Queen of England, Elizabeth II, married her third cousin, Philip Mountbatten. They are both great-great-grandchildren of Queen Victoria. Before you Yankees are tempted to mock the monarchists across the pond, keep in mind that Eleanor Roosevelt did not have to change her last name when she married Franklin D. Roosevelt, the thirty-fourth president of the United States. FDR and his wife were both Roosevelts, fifth cousins once removed. Also, FDR’s parents were sixth cousins as well. While incest between siblings is unheard of, there is a strong tradition of “light inbreeding” throughout the aristocracy of Europe and the New World.
While it may not be widespread throughout society, marriage among cousins is at least acceptable in Western society and even more so among other world cultures. This “light inbreeding” does not seem to lead to any higher prevalence of genetic disease and was more common in preindustrial society than it is today. It was even considered preferable among the upper classes in order to keep the family wealth concentrated among a few noble lineages. Did purely social and economic forces drive that custom, or was there some biology behind it as well? Surprisingly, there are some data to indicate that humans may actually have an attractive force toward marrying their relatives. I am not talking about siblings, parents, or children, of course, but cousins.
First of all, it has long been accepted that, generally, humans tend to be most sexually attracted to members of their same race. This has been shown not just with marriage and dating choices, which could be explained by forces other than sexual attraction, but also with choices of prostitutes, erotic dancers, and pornography. I want to move very quickly past this point because it has been, and continues to be, tinged with racist indoctrination. However, I mention this because I find it interesting that the trend toward more integration and heterogeneity in the racial composition of North America and Europe has coincided with a reduction in the favored sexual attraction towards one’s own race. This can be explained any number of ways, but one possible explanation is that the increasing exposure to people of other races during childhood has allowed more diverse sexual attraction to develop. Of course, this possibility will be inextricably intertwined with other social forces, but keep it in mind over the next couple pages.
Social scientists have also found that, at least for heterosexual couples, sexual attraction seems to favor those with similar eye and hair color.52 In these studies, generally only Caucasians are examined since white folks tend to have a greater diversity of hair and eye color than other races. Of course, this correlation is not perfect, but the studies have found that people tend to be attracted to those who have the same or similar eye and hair color that they themselves have, at least more often than would be expected by chance.
This tendency for people to be more attracted to people with their same coloring has been discovered and documented enough times by different research groups that there is little disagreement in the scientific community that it is real. The question is, why would this be? Why would opposite-sex attraction tend to favor one’s own physical features?
It turns out that that question frames the issue incorrectly. Heterosexual men and women are not most attracted specifically to their own hair and eye color, but that of their parents and other family members. Because eye and hair color are genetic and thus run in families, the fact that someone may be most attracted to their own hair color is incidental; it is really the hair color of those that raised them that most correlates to their sexual attraction. This subtle distinction has been shown most clearly by studying people who were adopted at birth, who are thus more likely than those raised by their biological parents to have different eye and hair color. (And race, of course.) One study in 2003 carefully explored this phenomenon and found that the sexual attraction of white heterosexual men and women most closely correlates with the eye and hair color of the opposite-sex parent, rather than those of self or the same-sex parent.53
This brings the whole issue into focus. Heterosexual attraction is at least in part the result of environmental imprinting during childhood such that adults become attracted to the features they saw in the opposite-sex individuals with whom they were raised. Fascinatingly, this is true not only with conspicuous features like eye and hair color, but also subtle things like ear shape and size, length of fingers, and distance between the eyes.54 This makes perfect sense to me because sexual attraction can be very subtle. We cannot always pin down why we are more attracted to this person over that one. We might just say something like, “I don’t know, she just has a better face.” What we could be noticing, subconsciously of course, is that she has a general face shape most similar to the face shape of our mother and sisters. You might find that conclusion uncomfortable, but as my doctoral advisor often told me, “the data’s the data.”
The phenomenon of one’s sexual preferences matching the physical features of close opposite-sex relatives has been reported many times. So far, nothing like this has been noted among gays and lesbians, which itself is calling out to be studied. What does this all mean? For me, it reveals a biological basis for the preference toward “light inbreeding” that we see in many human societies. Who looks most like our fathers and brothers (without actually being our fathers and brothers)? Our cousins!
This idea of Oedipal imprinting recently got a huge lift from an unlikely field of research—the study of the human genome. Researchers at the University of Colorado at Boulder recently examined genome-scale differences between individuals and their spouses. To keep things simple, they established the most homogeneous population possible by sticking to a single race, Caucasians of non-Hispanic ancestry (big surprise), and they included only heterosexuals. In 825 such couples, they examined 1.7 million single-nucleotide polymorphisms (SNPs). An SNP is the tiniest possible genetic difference between two people. What the researchers found was that married couples tended to have fewer genetic differences between them than you would expect at random. In other words, if you selected a guy and a girl at random from this group of 1,650 people, they would, on average, have more genetic differences than the married couples have to each other.
This study did not probe exactly what the genetic similarities or differences were, nor did they ask how we humans can possibly know who out there is genetically similar to us and who is not. Those are both very difficult questions. Nevertheless, the results of the study are rather convincing, given the very large and homogeneous population that was studied. There seems to be something real going on here, some force that pulls together people with similar DNA. We have always known that human mating is nonrandom. People tend to marry people of their same socioeconomic status, educational level, race, ancestry, political persuasion, and geographic location. However, this new study found that, even within those specific groups, there is another level of attraction at work—we are drawn to people with similar genetic information.
It turns out that Freud was at least partially right. Subconsciously, many of us are somewhat attracted to our mothers or fathers—but not to them personally. We are attracted to the features that they have when we see them in other people. Because we will likely be attracted when we meet someone that looks or acts like our close relatives, attraction among cousins is perfectly understandable and, in fact, expected.
This creates a conundrum because this would seem to argue against a taboo against incest. Are we conditioned to avoid incest purely by social forces, or is there something biological at work? How is it that we can be attracted to the features of our parents and siblings, but not our parents and siblings themselves? Most of us are not attracted to our parents or siblings.
Where does the incest taboo come from? The answer again seems to be social imprinting during childhood. Edvard Westermarck, the so-called father of sociobiology, first initiated the study of incest avoidance in humans and animals. He began his work by studying the marriage practices of humans in many cultures around the world and found that, in addition to the already well-known close incest taboo, people tend not to marry individuals with whom they closely associated as children.55 This phenomenon became known as the Westermarck effect and is almost universal throughout human cultures and time periods. It is not just our siblings that we avoid: we humans tend not to marry anyone with whom we grew up closely. (Exceptions to the incest taboo are found among the ruling class of several ancient civilizations. This may have extended to commoners in ancient Egypt.)
Of course, spousal choice is complicated by the fact that, in many parts of the world, spouses are actually chosen by people other than the betrothed themselves. This was especially true when Westermarck was doing his work in the late nineteenth century. Further still, perceived sexual attractiveness does not always feature prominently into the decision-making process for arranged marriages, at least not ostensibly. However, given that potential brides and grooms do have some voice or veto power, there is plenty of room for the preference for avoidance of close childhood peers to express itself among the would-be spouses.
Not long after he first published his ideas, support for the Westermarck theory began to roll in from a wide variety of cultures and contexts around the globe. The strongest such support came from a now-classic study performed among residents of an Israeli kibbutz.56 The kibbutz, or collective farm, is an ideal context for studying this phenomenon because, within the large settlement, children are often reared in small communes. Within the communes, several families live together and behave as one large family even though they are not usually related to one another. The children in the commune are mostly raised together in a collective effort.
In this study, researchers examined both marriage choice and premarital sexual behaviors and found that individuals specifically had sex and/or contracted marriage with peers from outside their specific commune—in other words, those they were not raised with. The statistical analysis was convincing. Out of three thousand marriages that took place among second-generation kibbutz residents, only fourteen involved two individuals that had grown up in the same commune.57 The avoidance of childhood peers was much stronger than random chance could explain, even though there was no cultural taboo against marrying someone from the same commune. An earlier study had reported an even lower percentage of intracommune marriages, but was not as rigorous or quantitative in its approach.58 Something about the experience of growing up with someone, even a nonrelative, made desire for sex or marriage unlikely.
There have been challenges to the Westermarck-based interpretation of the data from Israeli kibbutzim.59 An alternative hypothesis is that low rates of intracommune marriages may be the result of tendencies toward the maintenance of group cohesion. Many of us have personally experienced the disruptive consequences when two people in a group of friends begin (and end) dating. The avoidance of dating and thus marriage among close childhood friends could be reflective of that, and would be a sociological phenomenon, rather than a biological one. Importantly, while the opponents of Westermarck quarrel with the mechanism of the incest taboo, they do not doubt its near universal existence in human society.
As I mentioned in chapter 1, playing and growing up with someone creates a special bond that long endures. Part of that bonding experience, it seems, is the imprinting against mate selection. As children, the people that we spend the most amount of time with are family. This is as true now as it was in our hunter-gatherer days. Thus, in order to avoid heavy inbreeding, our biology may have programmed us to be sexually averse to those that we spend a great deal of time with during childhood, when social imprinting occurs.
Humans are not alone in this. Westermarck quickly turned to other animal species and found a similar pattern.60 Many species of animals tend to avoid reproductive sex with their siblings and others with whom they were closely reared. In almost all primate species that live in packs, families, and harems, males leave the group when they begin their sexual lives. What happens after that is different among different species. In gorillas, for example, the young males will roam on their own for a while in search of a harem to take over. Most fail and die in the process, which is why harems have one male and several females.
In chimpanzees, most often it is the females that join another troop when they are old enough to roam.61 Still, those that do stay or those that are raised in captivity will not reproduce with males that they grew up with, siblings or not. In the wild, some females go even further and take short trips during their estrus period to have sex with males from other troops. Interestingly, chimps that were raised together, even siblings, will indeed have sex with each other but not reproductive sex. Both males and females know when the fertile reproductive period is and they almost always choose to out-breed at that time.
It turns out that, in her wisdom, nature does not rely on social imprinting alone to help guide us away from too-close relatives when choosing sexual partners. There are even more subtle forces at work. In 1974, Lewis Thomas first suggested that animals might be able to detect genetic features of potential mates using their sense of smell.62 He was later proven correct when it was discovered that mice can detect genetic differences in the MHC proteins using smell and will selectively breed with mice that have different forms of MHC than their own.63 Presumably, this is a means to promote genetic diversity and avoid inbreeding.
The MHC proteins play an important role in the immune system of vertebrates by helping us “mark” our own cells and proteins and protect them from self-attack. MHC proteins are present on almost every cell of our bodies and have important functions in our fight against viruses, bacteria, and other pathogens. However, they also mediate the rejection of foreign cells, hence their name: MHC stands for major histocompatibility complex. When organ and tissue donors are sought for transplants, doctors search for a “match,” which means someone with the same or very similar MHC proteins. If a transplanted organ has a different set of MHC proteins, it will be rejected by the recipient.
In our modern era of organ transplantation, we must perform an elaborate laboratory test to determine if two people have matching MHC proteins. However, nature figured out how to do this eons ago. Animals can actually detect the MHC proteins of other animals by their smell. While this was puzzling at first, with the discovery that MHC proteins play important roles in olfactory perception per se, a possible mechanism is now clear.64
The most fascinating part of this is that animals will use the olfactory detection of MHC proteins to help them select mates that are genetically different from them. This phenomenon has now been observed in hundreds of species including mice, several kinds of fish, lizards, birds, and in lemurs, our primate cousins, and is lost when the sense of smell is impaired.65 This phenomenon is widely found but has varying strength. Some species have extremely strong preference for mates with different MHC proteins, while others do not really seem to care.
What about humans? You guessed it. We are no different. The first experiment of this type was done by asking forty-four men to take home a clean T-shirt and wear it for two days with no deodorant, antiperspirant, perfumes, or cologne. Then, they returned the T-shirt, each nicely saturated with the natural body odor of the man who wore it. The T-shirts were put in a box with a hole cut out for the aroma to escape. Forty-nine women were then asked to smell the odor coming out of some of the shirts (and an unworn shirt as a control) and select the ones that they found most and least attractive. There were no clear winners or losers; each male scent had its fans and its objectors. However, with striking consistency, the females favored the scent of men whose MHC proteins were most dissimilar to their own.66 Some of these women even admitted that the smells they liked, those from the men with dissimilar MHC proteins, reminded them of current or previous boyfriends/husbands.
There is another wrinkle in this MHC-odor preference phenomenon. The MHC preference of mice and some other species switches when they are pregnant. Instead of preferring to be with mice of different MHC proteins, they tend to associate with mice of similar MHC profiles.67 Similarly, in the study with the human women smelling the sweaty T-shirts, those on birth control (which somewhat mimics pregnancy in having high levels of estrogen and/or progesterone) behave in exactly the opposite way as well: they prefer the odors from men with MHC proteins that are similar to their own.68 What to make of this?
The simple interpretation is that female mammals are sniffing out potential mates when they are not pregnant, but preferring relatives when they are. But why? When one is pregnant, there is little need to look for potential mates. Instead, the preference for close relatives while pregnant is likely a desire for safety. Male relatives (father, brothers, sons) are much less likely to kill you or your baby than are strangers. As noted in chapters 7 and 8, there are reasons to be cautious around nonrelatives. There is value in seeking genetic diversity when you are looking to procreate, but once that is done, it is best to retreat to the safety of family. This is as true in mice as it is in humans.
Now it is time to clean up the apparent contradiction that has been brewing. First, I explained how humans are attracted to physical features that match those of their close opposite-sex relatives and how married couples tend to have overall greater genetic similarity to each other than to otherwise similar people. Then, I explained how humans and other animals are attracted to genetic diversity when it comes to the MHC proteins. This seems like I am saying two exactly opposite things and that they cannot both be true.
Not exactly. The preference that many people have for the physical features found in our family members is a form of biological nationalism (or, more darkly, racism). This speaks to the subtle ways that “the selfish gene” tends to promote its own success. In social animals, this leads to the creation of packs and herds and the creation of an “us versus them” mentality that we will discuss in more detail soon enough. Although these forces help shape highly competitive species due to their natural tendency to promote elitism and exclusivity, there is a downside: elitism and exclusivity can lead to heavy inbreeding. Heavy inbreeding leads to a great poverty of genetic diversity. Low genetic diversity makes an individual vulnerable to all kinds of threats, most especially pathogens such as bacteria and viruses. Without some diversity as insurance, one good virus can wipe out an entire species in no time.
This is where the MHC proteins come in. By preferring to mate with someone that has a different set of MHC proteins, we mammals have a built-in mechanism to resist the rest of our urges to become homogenous. Part of our sexual attraction is fueled by the preference for light inbreeding, which is good for the propagation of the family genes, and another part is fueled by the preference for genetic diversity in our MHC proteins, which is good for the survival of our offspring themselves. Remember that MHC proteins function in our immune system. It is not surprising that vertebrates have evolved special means to ensure that our immunological toolbox is stocked with the most diverse possible tools. In fact, in a very real sense, the quality of an immune system can be measured by the diversity of threats that it can handle. An individual with a monolithic array of MHC proteins is surely doomed.
There is something of a contradiction in these two natures of our sexual attraction, one toward those like us, and one toward those different from us. However, this is just the kind of push-pull relationship that we see throughout nature. We are always being pulled in multiple directions and natural selection usually settles on some kind of compromise. In birds, larger wings make better flyers. So why is it that all bird species do not have enormous wings? Because smaller wings are easier to tuck away while on the ground and do not require as much metabolic energy to build and maintain. Two forces pulling in opposite directions.
Sexual attraction is another such example. Inbreeding is great for rapid selection of an elite and well-adapted form, but out-breeding is necessary to maintain genetic diversity, without which we would quickly succumb to genetic diseases or infections. Freud and Westermarck were both right.
Gray, P. B., and J. R. Garcia. “Evolution and Human Sexual Behavior.” History and Anthropology 24 (2013): 513–515.
Wright, Robert. The Moral Animal: Why We Are the Way We Are; The New Science of Evolutionary Psychology. New York: Vintage, 1994.