Voice Part for a Duet

May 2, 2004
Outside Magazine
Outside magazine, August 1995

Voice Part for a Duet

The biology and mystery of monogamy
By David Quammen

Two intriguing statistics recently grabbed my attention. They concern that remarkable form of social behavior known as monogamy. Roughly 92 percent of all bird species are monogamous--at least through a single breeding season, if not for life. Among mammal species, it's 3 percent. By my clumsy arithmetic, that makes monogamy about 30 times more prevalent in the avian world than down here on solid ground among the class of plodding beasts to which you and I and Elizabeth Taylor belong. This of course leads to a question about mammals versus birds: Who are we to call them flighty?

If there are significant patterns within the particulars of those two statistics, they don't show themselves at first glance. Beavers are monogamous. The trumpet-eared bat is monogamous. The bowhead whale is monogamous. A fair number of doggy species are monogamous--the wolf, the coyote, the golden jackal, the red fox, the arctic fox, the Cape hunting dog, and others--but no cat species, no bears, no hyenas, and just one marsupial. The klipspringer, a dainty African antelope, is monogamous. So is the indri, the largest of the lemurs, an extraordinary animal whose ghostly yodeling haunts the rainforest of northeastern Madagascar. Most other mammals are not. Monogamy, then, is like flight: an exceptional phenomenon among mammals, a sort of defiance of gravity by alternate means. It occurs in certain species, but not many, and the circumstances have got to be special.

What accounts for this rarity of mammalian monogamy? Well, don't jump to the wrong conclusion when I say that some biologists attribute it to the invention of the breast.

In a paper published a dozen years ago in the Journal of Theoretical Biology, Allen T. Rutberg wrote, "The possession of mammary glands by female mammals encourages heavy parental care by females and biases mammalian mating systems in favor of polygyny." (Polygyny is the precise biological term for one male's matings with multiple females.) Birds don't experience that bias, since a male bird can provide parental care--incubating an egg or dropping worms into a hatchling's maw--in essentially the same ways as a female. The most vivid exemplar of that truth is the male of the emperor penguin, Aptenodytes forsteri. This steadfast papa spends two months in midwinter standing deserted on the Antarctic ice with his mate's single egg balanced on the tops of his feet. He keeps the egg warm there, beneath his abdominal flap, while the female goes off on a feeding excursion to build her weight back up. When she returns, at last, he gets his own turn for an overdue meal. His reward for paternal reliability is higher reproductive success than if he mated with many females and abandoned them all. If he chose the latter strategy instead, he might fertilize six or eight eggs from six or eight different mothers, but not a single offspring would survive. Life on the ice is so hard that it takes two emperor penguins, cooperating from start to finish, pulling long shifts, to rear one chick. The male can do his full share because breasts don't enter into it.

Among mammals, the canids aren't unique in their disposition toward monogamy. The primates lean that way too--not overwhelmingly, but disproportionally relative to the overall ratio for mammals--with about 15 percent of primate species monogamous. That figure includes the indri but no other lemurs. It might or might not also include Homo sapiens, since humans can be seen as either monogamous or polygamous, depending on which human culture you look at. According to one ethnographic source, monogamy is the standard marital arrangement in just 137 out of 849 societies that were examined. So human monogamy, such as it is, appears to be an odds-against exception (137/849, number of societies) within an odds-against exception (15/100, percentage of primate species) within an odds-against exception (3/100, percentage of mammal species) to prevailing patterns. Never mind the arithmetical bottom line. The point is that monogamy--among mammals in general and humans in particular--is an anomalous sort of behavior that can't be taken for granted.

Why do the evolutionary odds seem to set themselves so strongly against monogamous behavior among mammals? Is there more to it than the matter of breasts? And why have some species, breasts and all, flouted those odds?

Unfashionable thoughts: Monogamy is daring and mysterious.

Biologists have always been interested in mating habits--and who can blame them, since the subject holds great prurient interest as well as scientific import. But for the past thirtysome years, there has been increasing speculation about the origins of monogamy versus polygamy. Back in 1964, for instance, a researcher named Jared Verner published a paper titled "Evolution of Polygamy in the Long-Billed Marsh Wren," which helped launch the discourse into its modern phase. The ornithologist David Lack continued it in his 1968 book, Ecological Adaptations for Breeding in Birds, contributing some semantic clarity by dividing the general concept of polygamy into harem polygyny (one male monopolizing several mates for a period of time), successive polygyny (one male mating successively with several females), and polyandry (one female mating with several males). Lack also wrote of the pair-bond, an implicit behavioral contract that ramifies beyond the act of copulation itself and distinguishes polygyny and polyandry from sheer promiscuity. The pair-bond can be limited to a brief phase of consortship or to a single breeding season, though in some species (the Canada goose, the klipspringer, the indri) it lasts a lifetime. About polygyny, polyandry, and promiscuity, Lack said something notable: "The ecological factors making these abnormal types of pairing more advantageous than monogamy are not clear." The notable part is that he called them abnormal.

Edward O. Wilson, having come to theoretical ecology and sociobiology by way of the study of ants, was one later biologist who rejected the assumption that monogamy is normal. In his compendious 1975 volume Sociobiology, Wilson said that polygyny would be the natural arrangement for any species in which female sex cells (eggs) are larger and more expensive metabolically than male sex cells (sperm). Producing those big, nutrient-rich eggs requires the female animal to invest more bodily resources in each single act of mating than the male, who has little to lose by mating frequently. Wilson suggested that monogamy, on the other hand, might evolve secondarily in response to any of three ecological circumstances: (1) some sort of crucial habitat resource (a good nesting hole, say) is so scarce and localized that the cooperative effort of two adults is required to defend it against competition, (2) the physical environment is so difficult (as it is for the emperor penguin) that cooperative effort is required to cope with it, and (3) early breeding (at the first flush of spring, perhaps) is so advantageous that monogamy saves precious time that would otherwise be squandered on courtship. Wilson's third condition is relevant to the evolution of long-term pair-bonding. Finding a new mate each year might be amusing, but it's also costly, and lifelong monogamy--at least for some species--is a more economical reproductive strategy.

The zoologist Devra G. Kleiman published a hefty review article, "Monogamy in Mammals," in 1977. It's especially interesting for its attention to the social dimension, as well as the sexual dimension, of mating. Kleiman recognized that certain forms of gentle, sedate behavior--and not just the hot immediacy of courtship and copulation--play an important role among monogamous species. The simple act of resting together, for example, occurs conspicuously among beavers, among the antelopes known as dik-diks, and also among such monogamous primates as the marmosets, the tamarins, the siamang, and the gibbons. Another sort of amiable sociality is grooming--that is, picking carefully through another animal's fur to remove parasites--which is common among primates generally but shows itself in a special way among monogamous primates: Male partners more often perform the grooming on females, a nice little token of the pair-bond. Kleiman also mentioned the monogamous titi monkeys of the genus Callicebus, of which mated pairs sometimes sit side-by-side with their tails twined together. Tail-twining doesn't produce any new offspring or directly aid the survival of those already born, it doesn't even get rid of parasites, but it may well serve some adaptive purpose in the long run. It's another reaffirmation of the pair-bond.

Kleiman was intrepid enough to discuss the pair-bond between monogamous humans. She noted drily that, in Western society, "great emphasis is currently placed on maintaining high levels of sexual interactions in married couples" after they've started raising children. It's the old how-many-times-a-week question that young husbands and wives begin asking themselves, proudly or disconsolately, around their fifth anniversary. "Frequent sexual behavior is thought to contribute to the maintenance of a strong bond in humans," Kleiman wrote, whereas "clearly this is not the case in many species of monogamous mammals where contact and affiliative behaviors, such as resting together and grooming, are more common than sexual behavior." She and her titi monkeys were onto something.

In the 18 years since Kleiman's article, others have speculated further. James F. Wittenberger and Ronald L. Tilson described three preconditions that must exist before monogamy can evolve and five hypotheses that might account for just why it does evolve when it does. They judged each hypothesis against empirical evidence from various kinds of animals--colonial birds, carnivorous mammals, frogs and toads, wood roaches, dung beetles, horned beetles. Monogamy among the horned beetle Typhoeus typhoeus, you'll be excited to learn, is attributable to hypothesis three, the one about individual males stashing individualfemales away so that no other males can get to them. Details and tape at 11. C. P. Van Schaik and R. I. M. Dunbar also offered a short list of hypotheses, and from each hypothesis generated a handful of testable predictions, which they matched against known facts about the behavior of gibbons, indri, baboons, humans, and other primates.

What does all the theoretical work tell us? It tells us that monogamy isn't one behavioral pattern, but many, and that it might or might not arise for different reasons in different situations. The scientific literature on the evolution of monogamy is intricate, ingenious stuff. You could read your way through a fair portion of it, as I've lately done, and be almost assured of replacing your ignorance with confusion.

But maybe I can minimize your confusion, and relieve my own, by lumping all the hypotheses and preconditions together and rendering them down into just a few simplified points. First, monogamy is more likely if females of the species spread themselves thinly across the landscape than if they gather together in big sisterly aggregations. Why? Because if the females are too far apart, a male will run himself ragged trying to maintain a harem. Second, monogamy is more likely if males of the species have the physical or behavioral capability of making some crucial contribution toward the gestation and the rearing of offspring. That contribution might be direct--as in male birds or canids who carry food back to their young--or indirect, as in the male klipspringer, who stands lookout for predators while the female eats. It might involve the male of a given species defending a territory of rich habitat, in which his mate enjoys the right to feed without competition from other hungry females or interruption by randy males. It might even take the form of the male protecting his offspring from infanticide by rival males--murderous interlopers who covet his mate, his territory, or both. If the circumstances are right, the trend toward male contribution will be promoted by natural selection, as males who do contribute leave more offspring than males who don't. And the logical extreme of the trend is an exclusive helpmate relationship with one female.

Here's a third point: Monogamy is disproportionally common among primates because male parental investment is both more possible and more crucial than it is among other mammals. Remember, primates have dexterous hands and big brains. The big brains grow slowly and entail longer periods of juvenile dependency during which noninstinctive behaviors must be learned--and longer

dependency requires more parental investment. The dexterous hands allow males to contribute in a variety of ways, despite their pathetic, embarrassing lack of breasts. A male zebra just isn't capable of making himself as useful, paternally, as a male marmoset who carries his young through the treetops. So the zebra has no better option than to mate with multiple females and hope that some of his progeny will survive. The marmoset plays a different gamble.

Marmosets are small-bodied animals, and so are most of the other primates among which males carry the young or bring them food. Large-bodied monogamous primates, like the nine species of gibbon or the indri, generally don't provide that sort of direct paternal contribution. But they do form durable pair-bonds, which are manifested in various ways: traveling with the mate, sleeping beside her, grooming her, performing soulful singing duets with her. According to a tabulation by Van Schaik and Dunbar, seven of the nine gibbon species, as well as the indri and the Mentawei leaf monkey, engage in duetting. The duetting seems to be a means of reaffirming to each other, and announcing to the wider world of predators and competitors, an irrefrangible mutual commitment. What's the ultimate impetus for that commitment? Van Schaik and Dunbar gave a single answer, persuasively supported with logic and evidence: Among larger primates, pair-bonding prevents infanticide.

Like Kleiman before them, Van Schaik and Dunbar also ventured into the subject of human pair-bonding. Yes, their explanation was applicable to Homo sapiens, they argued: If human babies didn't face a high risk of fatal abuse, human adults might not be inclined toward monogamy. In support of this notion, Van Schaik and Dunbar cited two chilling sets of data. One study, done in Canada, indicated that stepchildren are 65 times more likely to die before their second birthday than children living with both biological parents. Another study, among the native Ache people of Paraguay, found a similar pattern: Children whose fathers died or departed were 15 times more likely to die as youngsters themselves. It makes monogamy seem mortally pragmatic.

But monogamy isn't mortally pragmatic. Not in all cases, anyway. If it were, we could understand it better. Just as surely as the weird, ethereal howling of an indri duet contains some transcendent dimension of grace--and it does, I promise you--so does the weird, narrow mystery of monogamy transcend Darwinian explanation. The data on which I base that assertion are less formal and orderly than Van Schaik and Dunbar's, but still persuasive: The world is filled (though sparsely) with voluntarily childless human couples whose bondings endure, even thrive, against all the social and biological odds.

Some people like to argue that childless couples are selfish. On a planet already worn threadbare beneath its burden of human population, that notion seems too perversely delusional to merit refuting. Anyway, I'm not going to bother refuting it, because the subject at hand is monogamy, not ecological overshoot. The subject at hand is tail-twining and song.

I can imagine a case of human monogamy in which all the hypotheses of the scientists don't apply. I can imagine a case in which the gestation and rearing of young doesn't figure and there's no egg to be held on the tops of the male's feet through a long Antarctic winter. I can imagine a case in which habitat resources aren't scarce, in which the physical environment isn't too difficult, in which early breeding at the first flush of spring isn't the least bit advantageous. A case in which infanticide presents no concern. I can imagine a case, say, in which the man spends a month in Madagascar or somewhere almost as remote and, with that absence, his heart grows fonder for no pragmatic Darwinian reason. I can even imagine that, when he hears duetting indri on a hillside in the northeastern forest, their glorious tangle of voices evokes in him a twinge of envious melancholy, as well as thrilled admiration. I can imagine that this sort of linkage between one human male and one human female might evolve slowly over a period of years, from the hot immediacy of youth to the sedate forms of affiliative behavior that become more important in middle age, and beyond. I'm talking now about that part of the social dimension even sociobiology can't explain.

Biologists call it pair-bonding. Others simply call it love. Let's us call it true and lasting love, as distinct from more familiar varieties. It's one of those unfunctional and gratuitous phenomena, like the sonnets of Shakespeare, the paintings of Mark Rothko, the music of Andrés Segovia, that make humanity just a little peculiar.

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