Mothers and Others

by Sarah Blaffer Hrdy

  Once the practice of helping immatures gets started, the benefits of direct and indirect reproductive fitness can keep cooperative breeding going, especially in situations where costs are imposed on group members for not helping.66 But how does alloparental care get started in the first place? This question requires us to consider both ecological factors, such as those promoting philopatry, low turnover in group membership, and long lifespans, and factors having to do with behavior that shapes the architecture of animal brains through deep evolutionary time. Let’s begin with some ecological factors.

  ECOLOGICAL FACTORS IN THE EVOLUTION OF COOPERATIVE BREEDING

  When ornithologists surveyed the avian lineages where cooperative breeding has independently evolved or re-evolved, three sets of conditions stood out as important. First, birds who took a long time to mature and were likely to live a long time—that is, who had relatively slow life histories—were predisposed to evolve cooperative breeding. Second, cooperative breeding tends to be found in lineages that evolved under ecological conditions favoring year-round occupation of the same area.67 This is because in more seasonal climates, youngsters who did not disperse early or migrate someplace else to spend the winter would starve. Year-round occupation in the same locale is important and helps explain why so many of the avian taxa most prone to evolve cooperative breeding originated in Africa, Australia, and other regions in the southern hemisphere.68 For example, in Afrotropical regions, the proportion of avian species with cooperative breeding rises to 15 percent, higher than the proportion of cooperative breeding (9 percent) for birds worldwide.69 As it happens, many of the best-studied examples of cooperative breeding belong to the Australian-derived family Corvidae.

  Cooperative breeders of Australian origin include scrub jays, magpie jays, and other corvids such as jackdaws, famous for their eagerness to proffer food to individuals other than their own offspring, including nonrelatives. Corvid species not only seem preadapted to evolve cooperative breeding, they are also unusually adept at manipulating their environments in inventive ways.70 Their unparalleled problem-solving abilities along with their ingenuity in making and using simple tools (the star of this show being the tool-making New Caledonian crow) once led the cognitive psychologist Nathan Emery to ask provocatively if corvids should be considered “feathered apes.” It leads me to inquire whether there is some interaction between a deep history of cooperative breeding and offspring that grow up to be especially good at learning from others and manipulating their physical as well as social environments.

  The third factor conducive to the evolution of cooperative breeding has to do with special environmental challenges such as unpredictable rainfall or fluctuating food availability, which would make it especially hard to stay fed or keep young provisioned.71 Even among creatures that remain year-round in the same locale, seasonal shortages and harsh conditions may make some local resources especially worth defending, as is the case with stashes of acorns stored by woodpeckers. When such resources are passed on between generations, it adds extra value to philopatry.

  In spite of their nomadic lifestyles, hunter-gatherers often transmit customary rights to certain hunting areas and especially waterholes from generation to generation.72 Heritable resources, even when routinely shared with others, are still worth defending and add value to philopatry, as well as helping to maintain a viable group size. Other ecological factors conducive to the evolution of cooperative breeding that would also have pertained in the case of Pleistocene hominins include their year-round occupation of foraging areas in tropical Africa during a period when increasingly unpredictable rainfall meant significant fluctuations in food resources. All these factors would have made philopatry, extra providers, and alloparental assistance especially attractive.

  But even if early hominins encountered ecological conditions conductive to cooperative breeding, at a behavioral level what happened? What was the probable sequence of events through which apes who had not previously shared care and provisioning of young evolved cooperative breeding? In the case of still-extant cooperative breeders, we not only know a great deal about the phylogeny of different groups, but the consequences of individual behaviors can still be observed and measured, so that once again, birds of a feather provide useful models for comparison.

  BEHAVIORAL FACTORS IN THE EVOLUTION OF COOPERATIVE BREEDING

  The most persuasive explanation to date for the behavioral origins of cooperative breeding is known as the misplaced-parental-care hypothesis. Two ornithologists, David Ligon and Brent Burt, proposed this two-step process. Start with a species that bears particularly helpless and slow-maturing young, a species with a deep history of parental care requiring parents to be sensitive to cues emanating from these needy immatures. According to Ligon and Burt, a legacy of intense parental care in lineages with helpless young would predispose members of that species who remained in their natal groups to engage in alloparental care—provided that nonbreeders enjoy sufficient proximity to begging young.73

  Their hypothesis is consistent with the recent finding that cooperative breeding is nearly three times more likely to evolve in taxa that produce altricial (helpless) versus precocial (soon able to survive on their own) chicks.74 As Ligon and Burt put it, “The genetic basis for helping behavior is much older than previously appreciated . . . Helping behavior had its origins as a simple by-product of misplaced parental care associated with delayed dispersal or colonial living in lineages with altricial young.”75

  The best-studied cases of misplaced parental care involve brood parasitism in birds, a type of nurturing by alloparents that is unlikely to be adaptive for the duped. In most such cases, insufficiently discriminating responses of parents toward eggs (and eventually chicks) deposited in a nest by members of another species divert resources away from the nest-owners’ own young to young left by the brood parasite, often with disastrous consequences for the alloparents’ own reproductive success. Reed warblers duped by common cuckoos who lay eggs in their nests are essentially making an alloparental mistake. Once the alien hatches, a strapping cuckoo chick uses its body to heave its hosts’ own eggs up and out of the nest. With the nest all to himself, the unrelated chick then clamors to be fed with loud calls and a vivid, yawning yellow gape sufficient to mimic a whole clutch of its hosts’ own young. Duped parents find the urge to respond to this super-stimulus and satisfy this request irresistible. They respond so diligently, and for so long, that the imposter may grow to eight times the size of his hosts.76

  Over many generations, species subject to recurrent parasitization eventually adapt. For example, selection may favor more discriminating parents or else parents who abandon their nest as soon as they detect intrusions. But these are only the parasitized species that have survived to the present day. More often than we realize, I suspect that alloparental carelessness led to extinction.

  Based only on creatures that persisted long enough to be observed, the ultimate Darwin Award for maladaptive nurture goes to mouth-brooding cichlids. These mothers sequester their eggs inside their own mouths to keep them out of someone else’s. They are so eager to get all their eggs safely stashed that in the process they sometimes ingest the eggs of a local parasitic catfish. Catfish scoot in just behind the male cichlid as he fertilizes the female’s eggs and deposit their fertilized eggs right beside the cichlid caviar, where they too get gulped into the mom’s mouth. Once again, natural selection has set the bar low. Even if protection gets indiscriminately extended to the young of another, this outcome is usually a better option than condemning one’s eggs to immediate predation.

  Unfortunately, in this instance the much smaller eggs of the parasitic catfish quickly exhaust the nutrients stored in their own yolk sacs. Maturing posthaste, tiny, voracious changelings hatch and then bite into the yolk sacs of the other eggs in their nursery, digesting them and continuing to grow bigger and bigger until the catfish fry are able to swallow whole their mouth-brooding host’s entire wriggling clutch. Having eaten a
ll their mouthmates, the predators signal their foster mother to let them out. Off they go to feed, returning to the cichlid mother’s hospitably open mouth when danger threatens—houseguests from hell. Whereas birds in populations chronically subjected to parasitism by cuckoos may eventually be selected to discriminate their own eggs from imposters, poor mother cichlids appear not to do so. How could they? So heavy is the predation pressure in Lake Tanganyika that a moment’s hesitation in the mouth-brooder’s uptake means her eggs would be eaten anyway.

  Birds have a hardwired feeding response. It is not uncommon to see one species feeding another—something that nest parasites like cuckoos have evolved to take advantage of. Begging behavior by altricial chicks can trigger feeding behavior even in species that do not normally exhibit alloparental care, regardless of species—provided that the relevant cues are broadcast, as in this famous image of a cardinal responding to the open mouth of a goldfish from Welty and Baptista’s classic text, The Life of Birds. (Paul Lemmons)

  The misplaced-parental-care hypothesis assumes that ancient potentials for nurturing young were present in both males and females, along with opportunities for selection to favor responses to young that promoted caretaking—even in nonparents. This is one reason philopatry is so important to the evolution of cooperative breeding—because social and ecological conditions promoting repeated exposure to young are needed to activate the relevant behaviors. The reason food sharing is crucial is because it means that infants can remain dependent without imposing an overwhelming burden on their mothers. The precise formula for helping varies from species to species, but over time the availability of alloparental care sets the parameters for what a mother herself needs to provide. Among cooperatively breeding birds like superb fairy wrens, the more help a mother has, the less she has to provide herself. This means the mother can afford to lay smaller eggs with fewer nutrients—the avian equivalent of early weaning.77 In other situations (as with marmosets), good help means the mother can produce larger, more, or more closely spaced young.

  The misplaced-parental-care hypothesis looks promising at a theoretical level and is consistent with much natural history. But at a mechanistic level, in terms of the genes involved, can evolution actually work like that? New evidence from the comparative genomics of eusocial insects is gratifyingly consistent with this hypothesized link between maternal behavior and the evolution of shared care. A team in the Department of Entomology and the Institute for Genomic Biology at the University of Illinois has taken the first steps toward understanding the underlying processes at a molecular level.

  The entomologists analyzed the genomes from different individuals belonging to a primitively eusocial paper wasp (Polistes metricus). Early in the colony-building process, before the queen has daughters around to help her provision her larvae, she does it all, both producing and provisioning her own broods. Later in the course of colony development, once she has allomaternal assistance, the queen quits provisioning and devotes all her energy to egg production. When the researchers examined the genomes of the lone nest-founding queens as well as the daughter-workers, they found that gene expression in foundresses who still combine brood production and brood-tending is very similar to gene expression in workers. But once foundresses get a working colony established and cease to provision their broods, gene expression in these breeders becomes significantly different from that of the workers.78 These differences need not involve novel mutations. Rather, selection can operate on the molecular regulators in DNA that determine when, in the course of development, a gene for a particular trait will be expressed, or under what circumstances. In the case of established queens, genetic instructions for the provisioning trait are simply skipped over and are no longer expressed.

  That genes for brood production, nurturing, and provisioning behaviors could be expressed either together (as in the case of the solitary foundresses) or separately (as in the case of queens and workers who divide these tasks between them) illustrates the importance of flexibility in gene expression over the course of an organism’s development in a particular environment—the importance, in other words, of phenotypic flexibility. Even without novel mutations, genes that are expressed differently over the course of development produce novel phenotypes on which natural selection can act. This is what Mary Jane West-Eberhard terms “the dynamic role of development in the production of selectable variation”—a central concept for the argument developed in this book about the cognitive and emotional implications of cooperative breeding.

  Five years before these molecular genetic findings, West-Eberhard’s interest in the role of phenotypic flexibility had led her to anticipate the role trait loss was likely to play in the evolution of alloparental care and eusocial breeding systems.79 As she put it, “Brood care by worker females that have not themselves laid eggs may be stimulated out of sequence when a subordinate female encounters a hungry larva, even though it is not her own offspring, thus causing her to skip ahead in the normal reproductive cycle, deleting the oviposition phase. If such behavior happens to be advantageous (e.g., when the hungry larvae are genetic relatives), selection may favor maintaining such altered behavioral sequences in the new context.”80 Provided that caretaking enhanced the fitness of nonmothers, such a scenario would explain how allomaternal provisioning could get started and continue to be selected.

  DO HUMANS HAVE ANY EQUIVALENTS TO STERILE CASTES?

  Alpha female meerkats, marmosets, and wild dogs forge vicious contracts with subordinates, sometimes including their own daughters: “Breed now and I will kill your progeny, but if you help rear my young, perhaps even lactating to feed them, I will tolerate you, and you just might get a chance to breed one day yourself.” Readers who have come this far may sense a disconnect between hunter-gatherers and other cooperative breeders with their high levels of reproductive skew and the all-out, even murderous, competition between mothers seeking to monopolize resources for their own young. Nothing in the ethnographic literature for hunters and gatherers suggests that a single dominant woman monopolizes breeding opportunities or that reproduction among subordinates is suppressed. Nor among African foragers do we find infanticidal co-mothers. Is this due to some bias in the way anthropologists view their subject? Or is there a real difference between human and the many nonhuman cooperative breeders?

  The recognition that humans must have evolved as cooperative breeders is relatively new, and to date most research has focused on the benefits of alloparents. Far less attention has been paid to ways in which allomothers might compete with or interfere with mothers.81 I suspect there is much more to learn about competition between mothers for resources, as well as between their children, not to mention competition between the alloparents, yet I do not think we should ignore the assessment of generations of ethnographers. Furthermore, even if some lacunae in the ethnographic record on competition between mothers and cheating by alloparents are due to observational bias, we still have to explain why self-serving behaviors are so subtle as to confound trained observers.

  Virtually all African peoples who were living by gathering and hunting when first encountered by Europeans stand out for how hard they strive to maintain the egalitarian character of their groups, employing sanctions against bullies, braggarts, or those deemed stingy, consciously keeping social stratification and extreme skews in access to resources or in reproduction to a minimum. Men are socialized to suppress more chimpanzeelike domineering tendencies, and women may be as well. Both in their lifestyle and in their genetic histories, these south African !Kung, east African Hadza, and central African foragers provide the best available windows we are ever likely to have into the social lives of our ancestors.

  Among people living in small foraging bands, it is not uncommon for a woman to allow another woman’s baby to nurse at her breast. Such suckling appears to be carried out on a voluntary, sometimes reciprocal, basis. Other forms of shared care also appear voluntary, but when the young anthropologist Adam Boyette recently int
erviewed Aka children, asking them what would happen should they refuse to care for their younger siblings, nieces, nephews, or cousins, 57 percent answered that their mother might refuse them food; 30 percent mentioned “hitting”; 23 percent, insults. In fact, Boyette never actually saw any evidence of mothers punishing children by withholding food or hitting them (which is very rare among hunter-gatherers). The point is, children felt social pressure to help. When asked who taught them this, most replied that it was their mother. Not all children dragooned into helping are close kin. Another young anthropologist, Alyssa Crittenden, described a Hadza mother tying a sling with her infant in it onto a “protesting unrelated girl.” Reprimanding the babysitter, the mother then walked away, leaving the girl with little choice but to care for the child or risk further, even more general, disapproval. Oppressive expectations for help may also be placed on an orphan or distant relative fostered in from another group.82

  When I specifically asked Paula Ivey Henry, who worked among the patrilocal Efe, why there was so little competition among women, she replied that she had wondered the same thing. Do women new to the group compete for scarce and difficult-to-find resources? Jostle for place at fruiting trees or wild tuber patches? What happens when a woman does less work in communal fish-trapping ventures but still claims her share? When women go off to forage, she told me, “there is an interesting hierarchy in the way women position themselves at a food patch . . . The more established women in the group often gain more advantaged access. They were also able to send their children (multiple is better!) up through the limbs of trees to gather more.” When resources were scarce, there might be competition, but most plant foods were there for the taking by those willing to gather or extract them, and (for reasons explained in Chapters 8 and 9) there were almost always plenty of babysitters to go around.83