Love in the Time of Monkeys

The importance of food, jealousy, and paternal care in the evolution of owl monkey monogamy

C. Valeggia/Owl Monkey Project

Even though there is great diversity in the organization of human societies, we all fall in love. Many of us maintain long relationships with the person we love romantically—or, as biologists state it, establish pair bonds—and together we form families and raise children, albeit with different levels of paternal involvement. Although we cannot pinpoint when a predisposition for pair bonding and monogamy evolved, it was surely long ago, well before we organized ourselves with religion, law, government, and complex technology. Most likely love and pair bonding evolved due to the influence of a specific set of ecological and biological factors. We know this because we see it in other primates, nonhuman primates that allow us to examine the biological basis of monogamy without the influences of language, religion, and technology.

Monogamy comes in different shapes and sizes. Researchers have described it in taxa as diverse as amphibians, birds, shrimp, and termites, but monogamy is relatively rare in mammals—only about 10 percent of mammalian species and 25 percent of primates organize around a breeding adult pair. Why is monogamy so uncommon among mammals? First, because mammalian fertilization is internal, a “father” may risk investing time, energy, and resources in a baby that he cannot be sure he has sired. Even more important, a female mammal is reproductively limited by pregnancy and lactation, whereas a male is unfettered by these time and energy constraints. To illustrate the point, one can contrast the most reproductively prolific woman, Valentina Vassilyeva of eighteenth-century Russia, credited with the birth of 69 children (including many twins, triplets, and even quadruplets), with the most reproductively prolific man, the Emperor of Morocco, Moulay Ismael (1672-1727), who allegedly had 888 children. Given that male and female mammals have such different reproductive potentials, how then did a mating strategy evolve that, without the guarantee of paternity, limits the male to breed with a single female?

Nearly two decades ago, I set off for Argentina in the hope of answering that question. I had just finished my doctoral dissertation investigating monogamy in titi monkeys (Callicebus cupreus) at the University of California, Davis, and was eager to study monogamous monkeys in the wild. My wife and I, along with our two young sons, moved to the rainforests of northeastern Argentina with a small grant from the Leakey Foundation and lots of dreams. To establish a field site and balance research with family life was a labor of love: my wife, Claudia Valeggia, a biological anthropologist as well, was beginning her field research on the reproductive ecology of the Toba-Qom indigenous communities of northern Argentina. We had to juggle our incipient projects with two kids attending school, along with a large number of volunteers and assistants in need of logistical (and emotional) support in the field. Some days, I would start at four or five o’clock in the morning, racing between home and the rainforest. Other times, it was more efficient to stay in the forest for several days at once. And so I started to study Azara’s owl monkeys (Aotus azarae), known to locals as mirikiná, a species believed to find a partner, establish a monogamous pair bond, and share parental duties quite evenly.

Azara’s owl monkeys are distinctive: in addition to being socially and genetically monogamous, they are regularly active during the day unlike many of their tropical relatives.

G. van der Heide/Owl Monkey Project, Formosa-Argentina

In Argentina, owl monkeys live only in the eastern portion of the Formosa and Chaco provinces in the northern tip of the country. Both provinces are part of the South American Gran Chaco, a vast expanse of flat land that includes forests growing along rivers (gallery forests), savannas, and patches of forest immersed in those savannas. Most of the region is privately owned, and the main activity is raising cattle that graze on the open savannas. It was with the help of gauchos  (Argentine cowboys) at Estancia Guaycolec, a 62,000-acre cattle ranch [see photograph on page 21], that I was able to establish a research camp, carving out nearly ten miles of trails through 170 acres of forest. The owl monkey’s habitat—a hot, dense and often mosquito-swarmed atmosphere— has earned the name el Infierno Verde, the Green Hell. Yet the Chaco’s outstanding biodiversity is worth the effort, with more armadillo species than any other place in the world; a host of large mammals, including capybara, tapir, and puma; and two species of monkeys, the black and gold howler monkey (Alouatta caraya) and the owl monkey.

Subtropical forest, prime owl monkey habitat,in Argentina’s Gran Chaco

E. Fernandez-Duque/Owl Monkey Project, Formosa-Argentina

Owl monkeys are arboreal and relatively small primates, weighing roughly three pounds, which poses some challenges for detailed observation of their distant, scurrying bodies. To our eyes they are sexually monomorphic: body size and coloring are identical between males and females. A lack of obvious differences between the sexes tends to be associated with pair-living species, as in the case of gibbons in southeast Asia, titi monkeys in the Amazon, and a number of lemurs in Madagascar. Fortunately, though, while the other eleven owl monkey species in Central and South America are nocturnal, the Azara’s owl monkeys of the Chaco are cathemeral, with a mix of diurnal and nocturnal activity that allowed us to observe them in the daylight.

Early in my research, we made little progress in understanding the social behavior of owl monkeys, because this required the identification of individuals, their age, and their sex. Four years into the project, a description of a group would still frequently read, “3 adult-size individuals, 2 smaller, 1 dependent infant.” Even so, we had begun to fill in our image of owl monkey life. We learned that their social lives centered on tightly affiliated and territorial units that consisted of two reproducing adults and one to three nonreproducing individuals. We suspected that these could be a pair of breeding adults and their offspring, but could not precisely define the relatedness between group members. Occasionally, a few animals looked distinctive to us. In 1998, we spotted an individual with a ten-inch tail, rather than the typical fifteen inches, and Cola Corta (“short tail” in Spanish) became easy to identify; he lived at least fourteen years and sired five infants. Sometimes we classified individuals as female if we saw them nursing. Nonetheless, it became clear that we had to capture and mark the animals, examine their genitalia, measure them, and obtain genetic samples if we were going to have a groundbreaking project on primate monogamy. The project needed new tools.

Radio collars proved to be efficient and reliable tracking tools that led to discoveries about pair bonding and paternal care.

G. van der Heide/Owl Monkey Project, Formosa-Argentina

A breakthrough came in 1999, once we were able to use radio collars and telemetry receivers to track individuals. The efficiency and reliability of locating the monkeys via telemetry was what finally let us address the questions about monogamy that had taken me to Argentina in the first place. As of today, we have tagged 166 individuals. My colleagues and I have found a surprising amount of biparental care. Mom is always around, but her main interaction with the infant is limited to nursing. Males often play with and carry the infants, with equal or perhaps greater doggedness than the mother. When owl monkey males (presumed fathers) skitter through the trees, their young typically go along for the ride.

We also gathered valuable information on the relationships between pair bonding, monogamy, paternal care, and life-history traits. Owl monkeys have a remarkably slow life history for being so small: infants are wholly dependent until six months of age, and following weaning, both males and females continue to grow until four years of age, at which time they tend to disperse from their natal groups. Reproducing for the first time when they are at least six years old, individuals may produce in a lifetime four to six offspring, one at a time. Although our study has not lasted long enough to establish their lifespan conclusively, we estimate that some individuals have lived as long as fifteen years.

Tight-knit group: An infant owl monkey (second from right) huddles between its mother and father in the company of two older siblings (far left).

M. Corley/Owl Monkey Project, Formosa-Argentina

So why are the mirikiná socially monogamous? We believe that the answer lies partly in how food is distributed in the forest. Their habitat is a subtropical forest where seasonal variation in both temperature and rainfall creates periods of food abundance and scarcity. There are sharp peaks in the abundance of preferred food items for owl monkeys and, conversely, lulls, which may constitute critical periods when the monkeys struggle to meet nutritional demands. We collaborated with botanists to examine the owl monkeys’ feeding ecology: we created large plots within the forest to survey the production of leaves, flowers, and fruits, and we assembled a database detailing the forest structure, including the distribution and size of tree species. Since 2003, we have collected monthly data on food availability from 425 trees in those plots. We learned that owl monkey foods are not laid out in continuous buffets, but are distributed in smaller plates throughout the forest. While there are many dishes, they are separated, and each “plate” can only sustain a single female. Therefore, the distribution of food separates females who disperse into their individual plates, or territories. What are males to do given this spacious distribution of females? If a male wants to be close to one female, he will necessarily be far away from any other. In other words, the distribution of females may make it impossible for the male to control more than one of them.

Yet, this would only explain why there is social monogamy, not why the males are committed to the care of infants they may or may not have fathered. Just because a male stays with a female doesn’t mean he will help with parenting. So why are male owl monkeys exceptionally good fathers? Genetic monogamy is a reasonable explanation. Social monogamy refers to the structure of groups, groups that only include one adult male and one adult female. Genetic, or reproductive, monogamy is about fidelity; it is about who has offspring with whom. This is a crucial distinction when attempting to understand the evolution of paternal care and monogamy, because what counts in evolution is the offspring produced.

Juvenile owl monkey with its father. Paternal care may facilitate the evolution of genetic monogamy.

B. Finkel/Owl Monkey Project, Formosa-Argentina

Are male owl monkeys guaranteed of their parentage? For an answer, we examined jealousy and mate guarding in male and female owl monkeys. Absolute control of a mate’s reproduction can be a behavioral mechanism to ensure fidelity. If one partner constantly watches out for and fends off competition, there won’t be an opportunity for the other to mate outside of the pair; there won’t be an “extra-pair copulation.” We have learned that owl monkeys are territorial, each group not only occupying a well-defined space within the forest, but actively defending a portion of it as well. Both adults take part in protecting the group from intruders who attempt to supplant one of them. Their young too will rally against the intruder, with serious consequences. When an intruder approaches the group and a fight ensues, sometimes one of the individuals may die in the aggressive encounter. Furthermore, when we examined demographic records from eighteen groups over ten years, we discovered that owl monkeys that succeed in preserving their monogamous relationship produce 25 percent more offspring than those who are forced to take on a new partner. In other words, there are significant costs and benefits of this extreme mate guarding, and both sexes appear to be preserving their bond with equal stake. Such behavioral and demographic data supported the critical importance of monogamy to the mirikinás, but genetic data was still the holy grail to definitively confirm whether owl monkeys are reproductively monogamous and faithful in practice, not just in appearance.

Modern technology provided us much-needed answers. These days, a droplet of blood, a single baby hair, or a little saliva from a pacifier are enough to run a paternity test. The biological samples we had collected from 166 individuals during ten years allowed us to examine paternity relationships in owl monkeys. One of our first and most significant findings using genetic data was to confirm that the socially monogamous groups of owl monkeys are not always “families” of biological parents and offspring. We suspected this from the demographic data showing changes in the adult composition of these groups—many intruders were indeed successful. But the genetic data provided conclusive proof that intruders sometimes supplanted biological parents as stepparents, and the intense territoriality we observed was justified by legitimate threats. Still, the question remained: did a pair bond guarantee the father paternity of the offspring in his group?

To answer that question we examined the genetic relationships between thirty-five infants and thirty-five male and female pairs. In 100 percent of cases, the male in the group was the biological father of the infant. Combined with the absence of any observations of extra-pair copulation in seventeen years, these findings
strongly indicate that owl monkey mates are always faithful, making them socially and genetically monogamous. They are socially monogamous because of ecological issues that limit their chances of having multiple partners, and intolerance towards competitors protects the couple and keeps them genetically monogamous. Owl monkeys are the first primate species, and only the fifth mammal, for which there is substantial evidence of genetic monogamy. Our analyses show that, once social monogamy has evolved, paternal care, and potentially close bonds as well, may facilitate the evolution of genetic monogamy. This helps to explain why males play an unusually dominant role in parenting. With biparental care, the female can recover more easily from pregnancy; having two attentive parents increases an infant’s chances of survival; and the male gets a better guarantee of replicating his own genes.

Gauchos herd cattle at the Estancia Guaycolec, home of the Owl Monkey Project in Formosa, Argentina.

B. Finkel/Owl Monkey Project, Formosa-Argentina

The study of monogamy, pair bonding, and alloparental care is of special interest to anthropologists and evolutionary biologists because pair bonding was likely a fundamental adaptation of our early ancestors. In human societies everywhere, couples develop relationships that are qualitatively different from the relationships they have with other adults. Psychologists, anthropologists, behavioral ecologists, economists, historians, and poets have all testified to this ubiquitous phenomenon: a pair bond, attachment, or love that develops between a couple with a commitment to share space, time, resources, offspring, and labor. As the research continues, under the auspices of the Owl Monkey Project of Argentina, we will continue to take advantage of one of the few primate models in which we can explore the interactions between behavior, ecology, demography, and genetics, in shaping primate behavior and life history.

--EF-D, BF

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