The usual uncertainty surrounding primate paternity is complicated in the callitrichid case because they are among the mammals (like ground squirrels, prairie dogs, dwarf mongooses, wild dogs, and various cats, including lions) where the same clutch or litter can have multiple progenitors. Twins can have different fathers. Trickier still, marmosets are among the only mammals in the world thought to have chimeric germ lines.
The phrase “germ line” refers to the inherited material that comes from the eggs or sperm (“germ cells”) and is passed on to offspring. Animals that have genetically distinct cells from two different germ lines are known as chimeras, named for a mythical Greek beast that was part lion, part goat, part serpent. It has long been known that, owing to a peculiarity of callitrichid placentas, the embryonic membrane enclosing fetal twins fuses so that somatic cells—those that form the nerves, muscles, bones, and so on (as distinct from germ cells)—migrate between twins in utero. But not until 2007 was it reported that germ cells can also travel from one twin to the other. In 2007, Corinna Ross, Jeffrey French, and Guillermo Orti at the University of Nebraska in Omaha discovered this phenomenon in Wied’s black tufted-ear marmosets, and it probably occurs in other marmosets as well.69 This sharing of cells between twins has interesting implications for genetic relatedness among marmoset family members. As French puts it, “There’s a male marmoset wandering around the forests of eastern Brazil with sperm in his testes that has alleles from his twin as well as his parents. This is a really twisted pedigree: the male is the uncle of offspring he produces.”70
Unlike ordinary fraternal twins, who share 50 percent of their genes by common descent, callitrichid brothers can be even closer relatives.71 It might also mean that offspring are more closely related to their mother than they would be to their own offspring.72 It is not yet known how chimerism affects body odors and other cues marmosets might use for kin recognition. However, Ross and her colleagues found that mothers pay less attention to infants with chimeric hair and saliva, while fathers actually pay more attention to chimeric young, carrying them for significantly longer periods than nonchimeric young. Perhaps fathers, who could also be uncles—or both—are picking up multiple cues of relatedness, so that the chimeric infant serves as a super-stimulus. Alternatively, mothers may simply find chimeric babies less attractive, and dads may be just picking up the slack.
In addition to their possible fathers and “more than fathers,” marmoset infants may also be tended by prereproductive groupmates. Typically, helpers are offspring from previous seasons who are close relatives. However, helpers may also be nonkin, wannabe breeders who have entered the group from outside. I return in Chapter 6 to the question of why unrelated group members help.
Given that female callitrichids give birth to twins or triplets as often as twice a year and provision their fast-growing young with unusually rich milk (not your usual dilute primate fare), mothers need all the help they can get.73 We know that the ancestors of modern callitrichids originally gave birth to singleton young. The likeliest scenario is that twinning and tripleting coevolved along with shared care and unusually high degrees of relatedness between family members.74 The payoff from all this assistance is a virtually unrivalled reproductive pace. The all-time birth record for any primate is held by a common marmoset female living in a captive colony at the University of Stirling in Scotland. Over a 13-year period, she gave birth 25 times to 64 offspring.75
When food is abundant, family groups in the wild expand rapidly, as breeding-age daughters with a sufficient complement of male and female helpers bud off to establish new families that colonize new areas. Not surprisingly, there is a linear correlation between availability of adult male helpers in newly formed groups and the likelihood that infants will survive. In mature groups, the correlation extends to the number of both male and female caregivers.76 The importance of alloparental help is one reason mothers strive for social dominance and fiercely defend access to this critical resource. The alpha female may drive away rival females or, if a subordinate female in her group (even her own daughter) does conceive and give birth, kill (and perhaps eat) her babies. Among common marmosets, alpha females are most infanticidal when they themselves are in the last stages of pregnancy.77 To avoid diverting energy to a doomed enterprise, subordinate females typically postpone ovulation until the alpha female dies or until they sense an opportunity to establish their own family someplace else.78
Because provisioning is involved, females in cooperatively breeding species compete for more than just childcare. In addition to the heavy lifting, callitrichid helpers respond to noisily begging babies by providing them with beetles, crickets, spiders, frogs, little birds, and other delectable, protein-rich tidbits. They can also be reflexively generous, sometimes volunteering food to immatures even without being begged. Still, there is considerable competition between babies, and handouts are especially sought after and critical for survival around the time of weaning. Too large to be sustained by milk alone, youngsters are still too inexperienced to entirely fend for themselves and are at a disadvantage in competing with full-grown adults.
As early as nine weeks, marmoset and tamarin alloparents deliver food to noisily begging babies. Youngsters continue to be provisioned this way until around nine months old, long after they can move about on their own. In one study of Saguinus oedipus, most food was proffered in response to begging, though some was volunteered. At about the same time that alloparents start to find the growing youngsters less appealing, juvenile marmosets and tamarins become more confident, greedier, and pushier in demanding food. Eventually, their table manners disintegrate altogether, and they are more likely to snatch or steal food than wait to have it offered.79
Cooperation in feeding young spills over into helpful tolerance in other realms. Tamarins (possibly the most similar to the ancient line of callitrichids that originally gave rise to marmosets) not only cooperate with the mother by carrying her young, they also cooperate with one another when harvesting oversized fruits and legumes. During the rainy season when little fruit is available in the forest, several moustached tamarins will work their canines in concert to strip off the hard husks from pods so they can use nimble fingers to pry them open and get at soft flesh and seeds within. The tamarins share afterward with no sign of antagonism, each taking a palatable portion and moving to a nearby spot to eat it. In Saguinus mystax the overall ratio of cooperative to aggressive acts is 52 to 1.80
This degree of mutual tolerance provides an excellent environment for youngsters to acquire information about diverse food sources in a relatively short time. Many primates utter special food calls when they encounter a food, recruiting group members to the feeding site. But so far, callitrichids are the only primates known to utter such calls more often when infants are present than when they are not. These staccato calls encourage infants to approach, expose them to palatable food, and invite them to sample new things to eat. As primatologists Lisa Rapaport and Gillian Brown note, the dynamics of cooperatively breeding callitrichids “require coordination with, and tolerance of, other group members” in ways that foster “both a predisposition to pay close attention to others and socially mediated learning.”81
When tested in laboratory experiments, tamarins and marmosets also turn out to be unusually altruistic, displaying a curiously humanlike impulse to give. In experiments where one individual has to perform a task so that an animal in a nearby cage gets food, callitrichids exhibit far greater concern for what their neighbors will receive than do other primates, most notably chimpanzees. Unusual levels of callitrichid altruism were first detected in 2003 during a series of experiments with a colony of tamarins (Saguinus oedipus) undertaken by Harvard psychologist Marc Hauser’s team. Subsequently, similar giving impulses (without the reciprocal component observed in the Hauser study) were reported from experiments at the University of Wisconsin.82 When the anthropologist Judith Burkart and her colleagues at the University of Zurich tried to replicate Hauser’s find
ings with a larger, carefully controlled series of experiments using another callitrichid species, common marmosets (Callithrix jacchus), they were astounded by how much “unsolicited prosociality” and “other-regarding behavior” these little monkeys exhibited.83
A single marmoset was placed in a cage next to another marmoset, but only one of them was in a position to pull a food tray within reach of the other. Both breeding and nonbreeding marmoset males, and breeding females (the same ones who were doing most of the infant care), proved significantly more likely to pull the food within range of the adjacent cage if it was occupied rather than empty. They demonstrated this considerate concern for their neighbor whether the marmoset next door was a relative or not. However, females who were not breeding and not currently in what might be called a “caretaking mode” displayed the least interest in providing food to others. Nonbreeding females were no more likely to place food within range of the cage next door when it was occupied than when it was empty.
Burkart’s experiments were specifically designed to facilitate comparisons with the “other-regarding” tests that had produced such dismal results back when Joan Silk and her colleagues showed that chimpanzees were indifferent to the well-being of others, particularly where food is concerned (see Chapter 2). Cooperatively breeding marmosets turned out to be more sensitive to the needs of others than larger-brained and generally much smarter chimpanzees. Apart from humans, callitrichids are the only primates among whom such giving impulses have been reported.
Not only do marmosets spontaneously go out of their way to provide food to others, but, like humans, tamarins keep track of and reciprocate material benefits (as in “We should probably have them over to dinner; they had us over last month”), and reputation seems to matter. The amazing thing about Hauser’s early experiments was how adept his tamarins were at remembering exactly which individuals were the helpful ones and which were not. Two separately caged tamarins from different families were given the opportunity to pull a cord that would provide food to the other as well as to himself or herself. But the apparatus was rigged so that half the subjects always delivered food to their neighbor, whereas the other half never did, even though they too pulled the cord. The more likely a tamarin was to provision his neighbor, the greater the probability the unrelated monkey would reciprocate. In what may be the best demonstration to date of reciprocal altruism and the importance of “reputation” in a nonhuman animal, tamarins were more generous to former benefactors, and grudging to the previously “stingy.”84
Marmosets and tamarins stand out among primates for just how eager fathers and alloparents of both sexes are to help mothers rear their young. Males expend so much energy carrying infants that they actually lose weight. To get ready for fatherhood, a callitrichid male whose mate becomes pregnant undergoes a hormonal transformation, gaining up to 15 percent of his body weight in anticipation of the energetic demands infant care will soon impose.85 Partway through gestation, even before the mother-to-be herself “shows,” he will begin to produce prolactin (a hormone best known for stimulating lactation in female mammals, but also known to promote nurturing responses in birds and mammals of both sexes) and bulk up. These prolactin effects are most pronounced in males with prior caretaking experience.86
Groups of golden lion tamarins frequently contain two adult males, often brothers who migrated into the group together. In most cases, there is only one breeding female per group. When she comes into estrus, the most dominant male monopolizes matings, but other males may also copulate with her. If a female dies, another female takes her place. In that case, a father and a son may both share sexual access. All males who have mated with the mother will later help rear her young (typically twins). In the upper left-hand corner, a male is passing infants back to the mother so they can nurse. Younger helpers (like the subadult in the foreground, who is catching a beetle) may be older offspring of the breeding pair or recent immigrants who have not yet begun to breed. (Pen and ink drawing, a treasured gift to the author from the artist Sarah Landry)
Men have also been known to exhibit these couvade-like (or “male pregnancy”) symptoms. We do not know what triggers them in either species. The primate endocrinologist Toni Ziegler has speculated that fetal metabolites in the urine of a tamarin male’s pregnant companion may be implicated. Elsewhere among the Callitrichidae, marmoset males have been observed to consume the placenta, ingesting along with this liverlike organ a rich cocktail of steroids in the surrounding fluids. In Chapter 5 we will see how human males as well are transformed both endocrinologically and behaviorally by spending time in intimate association with a pregnant woman or a newborn infant.
COOPERATIVE BREEDING’S DARK SIDE
Like all cooperative breeders, tamarin and marmoset mothers depend on others to help rear their young. Shared care and provisioning clearly enhances maternal reproductive success, but there is also a dark side to such dependence. Not only are dominant females (especially pregnant ones) highly infanticidal, eliminating babies produced by competing breeders, but tamarin mothers short on help may abandon their own young, bailing out at birth by failing to pick up neonates when they fall to the ground or forcing clinging newborns off their bodies, sometimes even chewing on their hands or feet.
It is not that uncommon for mother mammals to abandon ill-fated young, especially if they give birth to litters, and some cull large litters or discriminate against runts that are unlikely to survive. But among monkeys and apes reared in natural settings, abandonment is exceedingly rare. Except for young and inexperienced first-time mothers, who lose a disproportionate number of firstborns due to incompetence and failure to respond appropriately to infant cues, it takes extreme duress to induce a mother monkey or ape to abandon her infant—duress such as being in very poor physical condition or finding herself stalked day after day by a strange male intent on killing her infant. Instead, what stands out about primate mothers is their devotion to their singleton young. By far the most common exceptions to this general primate pattern are found in the family Callitrichidae—and among members of our own species.
Along with humans, marmosets and tamarins are virtually the only primates where mothers have been observed to deliberately harm their own babies or leave newborns to die. Staggeringly high rates of postpartum abandonment, up to 50 percent or more of live births, are reported from breeding colonies of cotton-top tamarins, mostly owing to mothers who give birth to twins or triplets under circumstances in which they have little help. According to one analysis of several decades of data from a large breeding colony, the probability that cotton-top tamarin babies would be abandoned or even viciously rejected rose from an average of 12 percent when the mother had older offspring to help her up to a whopping 57 percent when she had multiple young and was also short on alloparental assistance.87 Although infanticide is a hazard across the Primate order (having been reported now in several dozen species), observations almost always implicate either strange males or females other than the mother, not the mother herself. The high rates of maternal abandonment or infanticide seen among callitrichids and humans are unheard of elsewhere among primates. It would appear that highly contingent maternal commitment, along with a propensity to abandon young when mothers perceive themselves short of alloparental support—typically in the first 72 hours or so after birth—represents the dark side of cooperative breeding.88
More than 30 million years have passed since humans last shared a common ancestor with these tiny (rarely more than four pounds), clawed, squirrel-like arboreal creatures. New World monkeys literally inhabit a different world from that of their primate cousins who evolved in Africa. Theirs is a sensory world dominated by smell rather than sight. And of course there is considerably less genetic overlap between humans and New World monkeys than between humans and chimpanzees (where the overlap is greater than 96 percent).89 Yet in many respects callitrichids may provide better insight into early hominin family lives than do far more closely related species like chimpanz
ees or cercopithecine monkeys.
What humans have in common with the reproductively hyperburdened Callitrichidae is worth itemizing. In both types of primates, group members are unusually sensitive to the needs of others and are characterized by potent impulses to give. In both groups, a mother produces either multiple young or else sequential, closely spaced offspring whose needs exceed her capacity to provide for them. Thus the mother must rely on others to help care for and provision her young. When prospects for support seem poor, mothers in both groups are more likely to bail out than other primates are. Human and callitrichid mothers stand out for their pronounced ambivalence toward newborns and their extremely contingent maternal commitment. Infants have adapted, as we will see later, with special traits for attracting the attention of potential caregivers. And finally, humans, like their tiny distant relatives, breed unusually fast, and they have a marmosetlike ability to colonize and thrive in novel habitats.
DEMOGRAPHIC IMPLICATIONS OF SHARED CARE
Life history theory is the branch of evolutionary biology devoted to questions such as “How big should an organism grow to be?” “What size babies should it produce?” “How much time and energy should an animal spend on growing before starting to breed, and then how often should it breed?” And so forth. One widely accepted tenet of life history theory is that, across species, those with bigger babies relative to the mother’s body size will also tend to exhibit longer intervals between births because the more babies cost the mother to produce, the longer she will need to recoup before reproducing again. Yet humans—like marmosets—provide a paradoxical exception to this rule. Humans, who of all the apes produce the largest, slowest-maturing, and most costly babies, also breed the fastest.90
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