Whereas males in cooperatively breeding birds like dunnocks and superb starlings discriminate between chicks, providing more food to chicks likely to be their own (based on how frequently the male copulated with the female around the time those eggs were fertilized), superb fairy wren males have not been observed to exhibit this kind of favoritism toward their own offspring.41 So what motivates them? So far as the young male helpers go, their motives are complex, but fear is certainly one motive. Helpers who slack off will be attacked by the territory owner.42 Given how few chances a male is likely to have to sire offspring during his lifetime, the dominant male not only helps to rear broods whose paternity he is less than certain of, he pressures subordinates to help out as well. When you think about it, the fairy wren territory holder’s options are not really much different from those confronted by Bari and Ache husbands, as described in Chapter 5. Constrained by harsh conditions, unpredictable resources, and high mortality rates, they too tolerate high levels of infidelity by their mates in exchange for the chance of pulling at least a few offspring through.43
SITUATIONS WHERE IT IS MORE COSTLY NOT TO CARE
No question about it, kinship is integral to the origin of caregiving. But by itself, degrees of relatedness are insufficient to explain all observed cases of alloparental care. The cost/benefit components in Hamilton’s famous expression play a much larger role in explaining cooperative breeding than was initially assumed. These include costs attendant on being attacked or ostracized from a group as well as the benefits of remaining in a group’s territory when all other suitable habitats are filled.44 Consistent with this “ecological-constraints hypothesis,” high adult survival rates are often correlated with low rates of adult dispersal. With no new breeding opportunities open to them, nonbreeders remain in their natal group, biding their time, available to help rear a dominant breeder’s young.45
Yet the cooperation of these cooperative breeders is not always as voluntary as it appears. On closer inspection, it turns out that quite a few seemingly utopian colonies swarming with civic-minded altruists bent on helping their kin more nearly resemble police states where dominant breeders attempt to control groupmates. A second-generation Hamiltonian entomologist, David Queller, recently summed up current thinking as follows: “A little more or less kinship can matter less than larger differences in the costs and benefits of altruism.”46
Tie a thin filament around the wasp waist of a paper wasp queen to constrain her, as the entomologist Mary Jane West-Eberhard did, and then what happens? Once the breeding female can no longer keep wayward relatives away from empty brood cells, the workers start filling them with their own eggs.47 Sensitive to any threat of defection, a paper wasp queen normally retaliates against any worker who slacks off grubtending or gets too close to empty cells. Considering how few neurons they have in their brains, workers are remarkably astute at predicting just when their boss is and is not likely to punish them. When experimenters literally caused the queen to “chill” by lowering her body temperature, the workers (whose body temps were not affected) also slacked off, as if sensing that the queen would not be doing anything about it.48
Or consider what goes on in the subterranean tunnels occupied by naked mole rats. Among these endearingly ugly mammals, a single highly fecund breeding female mates with one to three males, who subsequently help their queen and other hivemates defend and maintain the colony. The trouble is, some workers aspire to reproduce themselves. Toward that end, they cut corners so as to conserve vital bodily reserves for the big push. This is why, as the biologist Hudson Reeve put it in the title of an article in Nature magazine, there has to be “queen activation of lazy workers in colonies of the eusocial naked mole-rat.” Ever on the qui vive either for slackers or for a female who might be inclined to operationalize an ovary of her own, the queen attacks them, shoving and hissing. Remove the queen, though, and workers work less—especially the larger workers with the best breeding prospects, or workers who happen to be less closely related to the queen. As Harvard’s cynical former president, Larry Summers, once noted, “Conscience is the knowledge that someone [powerful] is watching.” Fear has long been an effective way to induce individuals to cooperate.
Animals with brains no bigger than a bird’s, with no more neurons than a paper wasp, motivated by no more empathy than a mole rat, respond to the appropriate cues and go through the motions of being cooperative team players, even when their hearts (or stomachs) are not in it. Among Australia’s white-winged choughs, helpers fly back to the nest and deliver food into the gaping mouths of begging chicks, only to snatch the food back from the chicks and gulp it down themselves when the parents are not looking.49 The need for subterfuge underscores one of several other-than-altruistic rationales for helping. These birds are not really behaving altruistically—they just have to pay to stay, and occasionally they only pretend to pay at that. Indeed, even in the most highly “cooperative” breeders, such as eusocial insects with sterile castes, cheating is widespread if unconstrained by the policing of other hive members. Among leaf-cutting ants, for example, a few fathers sire larvae that grow larger and in other ways bias their chances in favor of growing up to be the hive’s designated breeder.50
Some of the best-documented examples of paying rent and reaping the repercussions of cheating derive from experiments with creatures who are far from warm-hearted. Think scaly, cold-blooded fishes, creatures so insensitive that for centuries anglers (wrongly) convinced themselves that fish feel no pain when hooked in the mouth. Not only do brain scans reveal that fish do indeed register pain, but cooperatively breeding fish behave in ways consistent with the same cost/benefit calculations that can also be documented in marmosets, mole rats, meerkats, and men. As Emlen stressed from the outset, whether in birds, men, or fish, “natural selection can operate on the decision-making process itself.”51
Allomaternal care (not including provisioning) has been reported in eight species of fish, almost all of them belonging to the Cichlidae, a highly social family characterized by extensive parental care.52 Even though warm-blooded mammals are arguably cuddlier, more affectionate, and more interested in tactile contact, the Walt Disney story about finding Nemo, the empathetic-seeming fish with the obsessively caring dad, is actually not as far-fetched as all that. To learn why not, travel with me to the clear waters of Lake Tanganyika in east Africa, home to many species of mouth-brooding cichlids.
Neolamprologus pulcher is the species that biologists Ralph Bergmuller and Michael Taborsky selected in order to learn how breeders “decide” which helpers to tolerate and which to exile. Cichlid helpers assiduously tend broods, using their tails to fan eggs and newly hatched larvae in order to keep them parasite-free. Alloparents also housekeep by nibbling up detritus and by preventing sand from collapsing on the eggs. Some alloparents who are not even particularly close relatives of the breeders nevertheless act as guards, keeping predators away. Even when the territory-owning occupants are replaced by newcomers, helpers keep right on helping.
By staying in the group, young fish not only remain safer from predators, they continue to grow and reserve their place in line, should they survive long enough to inherit the territory and its attendant breeding opportunities. But there is a revealing twist to this tale. Once helpers reach a certain size, parents become less tolerant of their tenants, allowing them to remain only during the period in the parents’ reproductive cycle when help is actually needed. Furthermore, if workers slack off (as when Bergmuller and Taborsky experimentally interfered with their performance), territory owners cease to tolerate them altogether and drive the slackers off.53
Nor should we overlook the misfortunes that await subordinates who do manage to breed. In the most ambitious long-term field study ever undertaken of a cooperatively breeding mammal, Tim Clutton-Brock and his team from Cambridge University have monitored a population of nearly 200 meerkats (Suricata suricatta) living in 13 groups in the Northern Cape of South Africa, including several groups
recently elevated to stardom in the Meerkat Manor television series. Even though social mongooses live in groups of 3–50 individuals, a single dominant female usually accounts for about 80 percent of the pups produced. The soap opera could just as well have been called Meerkat Dynasty.
Once promoted to top female, a meerkat undergoes a remarkable estrogen- and progesterone-linked growth spurt. She literally grows into her new role. Like a newly elevated naked mole rat alpha, who undergoes a lengthening of her torso and a marked increase in brain cells, the meerkat alpha gains 6 percent of her body weight and develops a swollen head (expanding by 3 percent).54 Thus buffed up, she is ready for her new job as breeder in residence. She will produce litters of 3–8 pups as often as four times a year. The bigger she is, the more pups she produces. Should any of the smaller, subordinate females in the group (usually her own daughters) manage to mate and conceive, she will drive out the wayward breeder, especially if she is pregnant herself. Even if the reigning alpha allows a pregnant subordinate to remain (perhaps because help is short at the time), she will likely kill and cannibalize her pups rather than share allomaternal assistance.55 But there is an intriguing meerkat tit-for-tat. Given the opportunity, pregnant daughters have also been known to kill their mother’s pups.
GOOD HELP IS HARD TO FIND
Only a dozen or so meerkat infanticides have actually occurred above ground and been witnessed by researchers. Hence, it is impossible to precisely quantify how many pups are lost in these unseemly family squabbles over who gets to use the babysitters. But it’s a lot. If even a single killing is observed above ground, the rest of the litter (left underground) is never seen again. Tim Clutton-Brock along with his coworker Andrew Young now believe that such infanticides are a main cause of litter failure. On 13 of 16 occasions when dominant females lost litters, there was a pregnant subordinate still in the group at the time with both opportunity and motive. It is probably in order to preclude such lethal and literal “aunting to death” that dominant females preemptively expel daughters who become pregnant.56 Thus does a meerkat mater familias enhance the survival chances of her forthcoming litter by condemning her grandoff-spring to an untimely death.
Kin they may be, but meerkat alphas are decidedly less than kind. Nor are alpha meerkats the only cooperative breeders prone to kill their subordinates’ progeny. Wild dogs, dingos, and brown hyenas, as well as marmosets, exhibit similarly lethal proclivities, especially when the alphas are in the final stages of pregnancy or have new pups themselves.57 Infant death may be a direct result of wounds inflicted by the dominant female, or it may come about from neglect when a dominant female prevents the subordinate mother from nursing or otherwise caring for her offspring. Among African wild dogs, an infanticidal alpha has even been known to leave one or more of the offender’s pups alive so she will continue to produce milk that the alpha female’s larger pups can use, exploiting the subordinate female like a wet nurse.58
The all-too-real threat of infanticide explains why many subordinates opt to forgo conceiving. From marmosets to mongooses, subordinate females respond to domination by suppressing their own ovulation rather than waste resources on a doomed gamble. Suppressed reproduction was such a striking part of family life among marmosets, meerkats, wolves, and wild dogs that many mammalogists initially considered it an essential attribute of cooperative breeding and made it part of the definition.59 However, it now seems clear that interference by dominants that leads subordinates to suppress their own reproduction is just one of several possible tactics by which some mothers ensure care for their own offspring. Eliminating the offspring of subordinates, extracting help from kin, tolerating outsiders in the group, punishing slackers, or (as we will see in Chapter 8) evolving females with long postreproductive lifespans so that postmenopausal grandmothers and great-aunts will be on hand are all just different routes to the same end: ensuring advantageous ratios of helpers to infants. When help is really in short supply, some cooperative breeders even set out to recruit or kidnap caretakers from other groups.
A pair of white-winged choughs that attempts to breed without having sufficient help is doomed to fail. This is probably why, when group size falls below the set point for success, group members (sometimes the helpers rather than the breeding pair) may raid a smaller neighboring group and kidnap recently fledged young. Over a period of days, the neighbors will be attacked and harassed, sometimes resulting in destruction of some of their eggs. Then, with the weaker group’s adults diverted by defensive skirmishes, some of the attackers herd young choughs back to their own territory. The kidnappers provision the stolen fledglings until they complete maturation, at which point these foster children help rear chicks in their new group (their alternatives at this point being too limited to do otherwise).60
BENEFITS OF GROUP MEMBERSHIP
This brief survey of cooperative breeding animals leaves little doubt that alloparental care need not always be directed toward close kin. Even for nonrelatives kidnapped or fostered in from smaller or weaker groups, remaining as a second-class citizen can be preferable to life as a vulnerable vagrant. Plus, there is always the chance that local opportunities will open up. Some helpers take advantage of their situation to advertise their particular merits. In other words, many alloparents are helping because they lack better options or because they seek to avoid punishment or, worse still, they dread ostracism from the group. For social animals, living outside a group, even during temporary migrations, represents an unusually dangerous condition. Alloparents have many excellent reasons for staying put, rather than simply decamping to seek less oppressive company.
There are also good reasons for remaining in a familiar and demonstrably habitable place, where one has an inside track on local resources and escape routes. The benefits of remaining in one’s birthplace (philopatry) are augmented still further when local habitats are saturated, and suitable places to live and breed are in short supply, or when access to local resources are worth preserving and being passed down through the generations.61 Acorn woodpeckers, found throughout the oak woodlands of California, provide the best-studied example, apart from our own species, of how philopatry and family togetherness can be motivated by inheritance prospects from accumulated resources.
As I write, one of these handsome red-crowned woodpeckers is laboriously drilling a hole in an oak tree outside my window. Acorn woodpeckers will drill line after line of these carefully spaced holes, then stuff each hole with a single gathered acorn that is pressed tightly in place to prevent squirrels and other marauders from prying them loose. These stashed meals serve as emergency rations to tide the woodpeckers over when food is scarce. In a big colony, these labor-intensive granaries may contain tens of thousands of acorns that will be passed down from generation to generation as insurance against highly seasonal and unpredictable food supplies.62
Besides having access to physical resources, animals have access to social resources in their natal group, since kin are typically more supportive than strangers. Networks of kin are a big reason why animals who can afford to do so stay home. For a maturing son, philopatry means access to his father and brothers, the males likely to make the most reliable allies. The downside of philopatry is that females eager to avoid breeding with a male familiar from birth will refuse to mate with him, putting a stay-at-home male at a disadvantage. Female preferences for novel or unfamiliar males—a defense against inbreeding—is a big reason why in many species, including the majority of primates, males take the risk of migrating while the females remain behind, joined by males from outside their natal group.
For females, the greatest benefit of philopatry is that matrilineal kin will be on hand. This is especially important for a primate at the time of her first birth, when an inexperienced young female is especially in need of social support and has so much to learn in order to be a competent mother and pull her especially vulnerable firstborn infant through.63 For relatively long-lived mammals like whales or elephants, and also some primates, ne
arby matrilineal kin pass along knowledge about local resources and childrearing to the next generation.64 Yet the long-lived Great Apes are exceptions to the widespread mammalian pattern of female philopatry. As in many bird species, by and large it is males rather than females who remain in their natal place. Typically, Great Ape females push off as they approach breeding age, though important exceptions are known where particularly dominant or well-connected chimpanzee females managed to stay (discussed in Chapter 8).
As we return to primates, two points need to be kept in mind. For almost all members of this order it is extremely important to live in a viable group, and other things being equal it is advantageous for a mother to be in a group that contains close kin. Nowhere has this principle been more clearly demonstrated than among the well-studied savanna baboons at Amboseli. Analysis of the long-term behavioral, demographic, and genetic data from this population reveals that the more socially integrated a female is and the more social contacts she is able to maintain, the more likely her young are to survive. And what better way to be integrated than to grow up among close kin.65 Never easy to precisely measure, the cost/benefit components in Hamilton’s rule are nevertheless omnipresent. Relatedness is not the whole story, but almost invariably kinship plays some role in biasing the ratio toward helpfulness.
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