Cheating Monkeys and Citizen Bees: The Nature of Cooperation in Animals and Humans

by Lee Dugatkin

Overview

Cooperation is the fabric that keeps society together. Civilization could not have been achieved -- and will not be sustained -- without it. But what is it? How and why does it work? Could the secret of enhancing human cooperation lie in an investigation of the animal kingdom?
In Cheating Monkeys and Citizen Bees, evolution and animal behavior expert Professor Lee Dugatkin, known throughout the academic community for his ingenious animal behavior experiments, reports, from the cutting edge of scientific research on the startling evolutionary truth about cooperation and how it works. He explains the four paths to cooperation that we share with animals and provides the experimentally verified definitions of a behavior no one thought science could ever explain. The first path is through our families and demonstrates that blood really is thicker than water; the second shows why it makes biological sense to do unto others as they do unto you; the third reveals the dynamics of a kind of selfish teamwork; and the last and grandest path is to complete altruism Dugatkin illustrates his argument with marvelous behaviour in the natural world: baby-sitting mongooses and squirrels that willingly martyr themselves to save relatives; fish that switch sexes in order to share reproductive duties; and vampire bats that regurgitate blood for their hungry mates. With these colorful insights into the natural world, Dugatkin shows that what comes naturally to animals can teach us about the instincts that underlie the complex web of human social networks. We can use our understanding of these instincts to encourage purposeful human cooperation, even in situations where animals would not naturally band together.
Those readers with an interest in ecology, evolutionary biology, psychology, even anthropology will find Cheating Monkeys and Citizen Bees an essential handbook of the dynamics of cooperation. And everyone will find it to be a lucid introduction to the surprising evolutionary history of how we came to behave in the ways that we do, of how nature came to be less brutal than we tend to think.

Product Details

ISBN-13:	9781439136515
Publisher:	Free Press
Publication date:	02/12/1999
Sold by:	SIMON & SCHUSTER
Format:	eBook
Pages:	224
File size:	2 MB

About the Author

Lee Dugatkin, author of the award-winning Cooperation Among Animals, has written for Scientific American and many other popular and academic science journals. He conducts his research at the University of Louisville. He lives in Louisville, Kentucky.
Lee Alan Dugatkin is a professor of biology at the University of Louisville who has published more than 150 papers as well as numerous articles in Scientific American, The New Scientist, and Slate. He speaks frequently about his work and has been featured in The New York Times, The Wall Street Journal, The Washington Post, the Toronto Globe & Mail, and numerous other publications worldwide.

Read an Excerpt

Chapter One
All in the Family
And the man knew his wife Eve; and she conceived and bore Cain...and again she bore his brother Abel....And in the process of time it came to pass, that Cain brought of the fruit of the ground an offering to the Lord. And Abel, he also brought of the firstling of his flock and of the fat thereof. And the Lord had respect unto Abel and his offering, but unto Cain He had no respect. And Cain was very wroth, and his countenance fell. And the Lord said unto Cain: "Why art thou wroth? and why is thy countenance fallen? If thou doest well, shall it not be lifted?"
According to the Old Testament, the first human siblings were not particularly fond of one another. Fair enough -- we all know of cases of sibling rivalry, not to mention the animosity that we might hold for some of our more distant relatives who pop in for the occasional holiday dinner. But, in general, blood really is thicker than water despite tales of murderous brothers. Later in the story of Cain and Abel we encounter a poignant question: "And the Lord said unto Cain: where is Abel thy brother? And he said 'I know not; am I my brother's keeper?'" The answer, at least in terms of how we behave, is a qualified yes -- you are indeed your brother's keeper.
If your brother and a stranger were drowning, who would you save first? The reply most of us would expect -- "my brother, of course" -- suggests, but certainly does not demonstrate, the importance of the role of kinship in structuring human cooperative acts. Is it possible, however, that the reason we might choose our brother has nothing to do with the fact that he is a blood relative per se? Is it merely the fact that we have spent so much time with our siblings that drives our actions? A simple thought experiment might help us to understand whether this true. Imagine it is not a stranger with your brother there in the water, but your closest friend. How would you feel in that case? How would most people react? If kinship was the overarching theme, most should still reply "my brother, of course." This train of thought has led behavioral ecologists to appreciate just how important kinship is in the human social dynamic.
Family Accounting Schemes
The scenario in which you save your brother or someone else functions as a nice illustration of how kinship affects human cooperation, but it is not something one envisions as a starting place for significant scientific breakthroughs. Or is it? Evolutionary biologists' first introduction to the notion that blood relations affect social behavior actually came in the 1930s in a form similar to this example. It was then that J. B. S. Haldane, a founder of modern evolutionary theory, suggested that he would risk his life to save two (but not one) of his brothers and eight (but not seven) of his cousins. Haldane, quite versed in mathematics, made this rather bold statement by counting copies of a gene that might code for cooperative behavior. Such a gene-counting approach to kinship and the evolution of cooperation has been extended by theoreticians but in its most elementary form is the heart and soul of kinship theory. Let us see how this idea works and how it has been formalized into what is known as kin selection or inclusive fitness theory.
The evolutionary biologist's definition of relatedness and kinship may strike many as surprising, if not odd. In such a definition, relatedness centers on the probability that individuals share genes that they have inherited from some common ancestor (parents, grandparents, etc.). A jargon phrase summing up this approach in behavioral ecology is "identity by descent." For example, you and your sister are kin because you share some (in this case many) of the same genes and these have been inherited from common ancestors, mom and dad. Similarly, you and your cousins are kin, because you share genes in common (not as many as siblings) and common ancestors, your grandparents. Common ancestors are the most recent individuals through which two (or more) individuals can trace genes that they share in common.
Once we know how to find the common ancestry of two or more individuals, we can calculate their relatedness, which simply amounts to the probability that they share genes that are identical by descent -- genes that have been inherited from a common ancestor. In the literature on kinship, this probability is often labeled r (for "relatedness"). For example, you and your brother are related to one another by an r value of 1/2.
From a "gene's-eye" perspective, calculating relatedness is the first critical step in understanding how kinship can favor cooperative behavior among individuals. Genes' survival depends on the number of copies of themselves that they get into the next generation. This is often thought of in terms of what effect a given gene has on the individual in which it resides, but relatedness suggests that this is a myopic view. If relatives have a high probability of sharing a given gene, then that gene can potentially increase its chances of getting more copies of itself into the next generation by coding for some behavior that helps relatives. Again taking a gene's-eye view, relatives are just vehicles who are likely to have copies of you (the gene in question) inside them as well. But, and this is a big "but," relatives only have some probability (r) of having a copy of, for example, a gene for cooperation. A gene in sibling 1 "knows" that a copy of itself may reside in sibling 2, but only with a 50 percent probability. The more distant the relative, the less likely a copy of the gene resides in them as well. So, phrased in the cold language of natural selection, relatives are worth helping in direct proportion to their relatedness. This is because relatedness is a measure of genetic similarity, and genes are the currency of natural selection.
Behavioral ecologists are not so foolish as to assume that animals are able to calculate relatedness in the manner described above. We only assume that natural selection favors individuals who act in ways that make it appear as though they are able to make such calculations. How animals determine who is kin and who isn't is a matter of some debate these days. For example, one theory suggests that animals determine relatedness by matching a suite of traits (a template) that they possess against the same suite of traits in another individual. Depending on the degree to which traits match up, individuals are treated as full siblings (if many matches occur), half siblings (if fewer matches occur), cousins, and so on, down to the category "unrelated individual" (if, for example, no matches occur). Such "matching games" have their flaws; mistakes can be made in determining the level of overlap, and some relatives may erroneously be treated as nonrelatives, while some nonrelatives may be viewed as relatives, Often, however, rather than a suite of traits, a single characteristic is used to determine whether another individual is kin and if so, what type of kin. In many insect species, for example, kinship is assessed by odor. Individuals who smell like you (or your nest) are relatives, and how closely related they are is determined by how similar their odors are to yours.
While most behavioral ecologists accept that such matching (either of many cues or a single cue) is important, they believe that there is another, simpler explanation for how animals determine who qualifies as kin, an explanation that I'll refer to as the "no place like home" hypothesis. Under this hypothesis, animals simply treat all others that grew up in their nest (territory, burrow, etc.) as relatives. This very simple rule is often quite powerful. With the exception of some species that try to trick other species into raising their offspring, the odds are quite strong that those who grew up in your nest are in fact your siblings and parents.
The details of how animals evaluate relatedness are fascinating, but all we really need to know to examine kin-selected cooperation is that many animals do in fact behave in ways that allow them to distinguish between kin and nonkin and even to distinguish between different degrees of relatedness. Once we have calculated relatedness, we are very close to reaching a general rule for when cooperation among relatives should be favored and when it should not. We need only consider two more factors: the cost of the action to the individual cooperating and the benefit to the recipient of such a cooperative act. Let us call the cost of a cooperative act to the donor c, and the benefit to the recipient b. In 1964, W. D. Hamilton (now at Oxford University) showed that cooperation among relatives should evolve when the following holds true: r X b is greater than or equal to c.
In other words, cooperation among relatives is favored if, and only if, the benefit of the act multiplied by the relatedness of the actors is greater than or equal to the costs. This equation, r X b is greater than or equal to c, has become known as Hamilton's Rule. Essentially, Hamilton's Rule says the following: There is some cost (c) that "must be made up for" if the gene for cooperation is to evolve, as cooperating with others is often a risky business. One way to make up for this cost is through the benefits (b) a relative receives, because relatives may carry the gene for cooperation as well. But, relatives have only some probability of carrying the cooperation gene and so the benefits received must be devalued by that probability. If I pay a cost for undertaking an action, but there is only a probability that I will receive indirect benefits (in this case through my relatives), I need to factor that into my equation and that is just what r does.
We can illustrate the use of relatedness to predict cooperation among kin with a simple chart. Consider an action that you take that reduces your chances of survival by 50 percent (a very serious cost) but increases the probability of survival of the relative(s) you are trying to save by 50 percent each (a considerable benefit). Such extreme costs and benefits might, for example, mimic a situation in which you scream out when a gang of armed thugs is approaching. This serves to announce the presence of thugs to the relatives around you, but at the same time the scream draws the marauders' attention your way, a dangerous action indeed. Based solely on kin selection theory, the table shown here outlines the number of relatives that need to hear your scream before natural selection alone would favor such dangerous behavior on your part.
The table illustrates the fundemental point of inclusive fitness theory: the greater the degree of relatedness between individuals, the more likely that kin-selected cooperation is selected. There need only be two (or more) siblings around for you to make that scream, but you'd need eight or more cousins present (a much less likely event), if they were the only relatives in the vicinity! How exactly, though, do we use Hamilton's Rule to come up with the correct number of relatives in the table? Consider the case for siblings. If a single sibling hears an alarm call, then r = 1/2 and b and c are still each 1/2. In that case r multiplied by b is not greater than c, Hamilton's Rule is not met, and cooperation via kinship is not favored by natural selection.
Suppose, however, that three siblings hear the alarm call. Now b is tripled (three recipients), but c is the same (the alarm call still draws the predator's attention), so r X b = 1/2 X (1/2 X 3) for a total of 3/4, which is greater than c, and Hamilton's Rule is satisfied. The same logic can be applied to any relative in the table (or for that matter, any relative not in this table). Take note, as well, that the relatedness of an individual to his/her spouse is 0 (with the exception of marriages among relatives). Although one's spouse is kin in the everyday usage of the term, we don't generally share genes inherited from a common ancestor with our spouses and hence this category of relative is in effect removed from kin selection theory.
Of the four paths to cooperation that we will focus on, kinship is the best understood, most accepted, and least controversial. It is in every legitimate textbook on evolution and is cited in more papers in the field than any other set of theories. There is even a belief among some evolutionary and behavioral biologists that Hamilton's work in this area marks the start of the modern discipline of behavioral ecology. But even kin selection theory is not without its controversies.
One area of contention with respect to kinship and cooperation centers on whether it really matters where the genes we are counting are located. Kin selectionists correctly argue that blood relatives are more likely to carry the same gene than are individuals drawn at random from a population. But what if some other mechanism besides kinship could create groups in which individuals were all likely to carry one or more genes coding for cooperation? Does it really matter that such individuals don't share other genes, like kin do? After all, we are interested in the gene(s) coding for cooperation, and everything else is in some respects background material for that gene. Who cares whether individuals carry the same genes because of kinship or for some other reason -- shouldn't the process by which cooperation is selected for work just as well in both cases? The answer to this question, as Hamilton himself noted, is yes, the process works the same; whether individuals share the gene(s) for cooperation because of relatedness or some other factors is irrelevant.
Yet kin selection advocates are not so fast to roll over. Sure, mathematically speaking, you are right, they say, but in practice the distinction we are arguing about is still real and important. Give us, they say, a good example of how individuals sharing a gene are brought together, if relatedness (which automatically brings them together) is not in force. The answer typically given by kin selection critics is that individuals that share a gene for cooperation may gather together specifically to be near other cooperators, because cooperators do particularly well when around others like themselves and so should choose this option, when it becomes available. "Be specific," say kin selectionists, "give us a real example." And this is where the kin selectionists start looking a bit better than they did after losing the mathematics argument, because behavioral ecologists are usually stopped in their tracks when it comes to finding a good animal example to answer this question.
Although such examples may be hard to uncover in animals, those interested in enhancing human cooperation argue that the evidence for cooperators choosing other cooperators as partners in our own species is anything but scarce -- even when kinship is not in play. How others will act is one primary means by which we choose with whom we will interact. So, for humans then, while kinship is an extremely important force selecting for cooperation, there are many other ways cooperators may cluster together aside from kinship. We need to recognize this in our behavioral studies and our conjectures about human cooperation.
The above controversy is admittedly a semantic one in part, but semantic arguments can be quite illuminating. Hamilton's Rule -- which in words roughly translates to "all else equal, cooperation should be most common among close relatives" -- is as close as behavioral ecologists get to a "law of nature." It is an underpinning of all modern evolutionary approaches to social behavior and is, in many ways, as much an approach to behavioral biology as it is a theory. The data gathered to date certainly support the claim that Hamilton's Rule is extremely powerful. It is not a "law" in the sense that gravity is, but it is about as near to one as behavioral biologists can hope to come, given the astonishing complexity and variability that is an inherent part of the subject matter they tackle.
From the standpoint of reputation, Hamilton's Rule was quite good for the field of behavioral ecology, at least in one sense. While solid mathematical theory has been part of evolution since the seminal work of J. B. S. Haldane, Ronald Fisher, and Sewall Wright in the 1930s, it was not truly a centerpiece of evolutionary approaches to behavior until Hamilton's Rule. For many in the field of behavior, there was an unspoken envy of the hard sciences (physics, chemistry, even other parts of biology) that had steadfast "rules" that could be written out for skeptics (not to mention funding agencies). Hamilton's Rule provided such ammunition to behavioral ecologists. Let's take a look at some examples of why this is so, with a few cases from the animal kingdom, before moving on to how such scenarios can help us foster human sociality.
The Insect Police
The so-called social insects have been a godsend for advocates of kin-selected cooperation. The reason lies, at least in part, with the bizarre genetics of social insects such as bees, wasps, and ants (collectively known as hymenopteran insects). Humans (and most other animals) are diploid organisms, which means that we have two copies of each of our chromosomes. Our forty-six chromosomes are twenty-three matched pairs. The only stages of human life that are not diploid are sperm and egg, as they have only a single copy of each of our twenty-three distinctive chromosomes. Sperm and egg then are called haploid rather than diploid. Of course, sperm and egg later fuse to form diploid animals.
Much of life on earth, such as bacteria and viruses, is always in the haploid phase. Why some life on earth is diploid and some haploid is a fascinating question, but not one critical to the issues we are examining. What makes bees, wasps, and ants so bizarre is that females are diploid and males are haploid -- a genetic system known as haplodiploidy. What this means is that when a male fertilizes a female, only daughters are produced because the sperm and egg fuse to produce a diploid creature, and in most social insect species diploids are female. Females, however, produce sons from unfertilized eggs (eggs that have not fused with sperm) -- which means that sons never have fathers!
Haplodiploidy creates some very strange scenarios. In diploid and haploid creatures, relatedness between two individuals is symmetric; that is, if a father is related to his daughter by an r of 1/2, then a daughter is related to her father by the same value. Not true for the social insects. To see why, focus your attention on the father/daughter relationship. Fathers are haploid and give a copy of each chromosome they have to their daughters. Hence fathers are related to daughters by a value of 1. Daughters, however, are diploid, in that they get one copy of each chromosome from each parent, both mom and dad; so a daughter's relatedness to her father is 1/2 (half her chromosomes come from dad) -- fully half of her father's relatedness to her.
The most relevant effect of the strange genetics of the social insects is its impact on average relatedness within insect colonies. Before seeing this in detail, keep in mind that in many social insect colonies a single queen produces all the offspring for a group. This means that the vast majority of individuals in such colonies are sisters and brothers. Haplodiploidy has the twofold effect of making sisters "super-relatives" and making the relatedness between brothers and sisters only half of what it is in diploid brothers and sisters. Sisters end up with a relatedness value of 3/4 (50 percent greater than the same relationship in diploid species), and sisters are related to brothers by a value of 1/4 (half the value found in diploid creatures). So, a clear prediction from kin selection theory is that since females are much more related to their fellow colony members than are males, when colonies have more females than males (as in most social insects), cooperation should occur predominantly in this sex. And of course it does, as "workers" in insect colonies are almost always female! It is females that sacrifice their lives by stinging folks and ruining an otherwise pleasant summer day. It is also females that undertake virtually all of the everyday activities that keep a colony functioning -- food gathering, care for the young, and so on. One particularly interesting and unique behavior found among female social insects is "policing" behavior.
Bee colonies are rightly thought of as models of both efficiency and harmony. It is mind-boggling what a colony of tiny insects can accomplish in a short period of time: regulating the temperature of a hive, caring for young, defending against many predators, finding food, recruiting others to join in bringing back the booty, and a myriad of other activities. Some of this efficiency (and harmony) has been attributed to a single queen often producing all of the eggs for a colony, thus allowing worker females to spend their time on other hive-related necessities. Queens accomplish this enviable task by using a barrage of chemicals to inhibit other females -- the workers -- from reproducing. Yet, as with any chemical inhibition system, it is inevitable that some workers will escape these anti-aphrodisiacs and thus will have a much greater chance of reproducing than their subdued sisters. Once this fascinating new door is opened, we can ask whether kinship theory can guide us with respect to a rather nasty question: should the eggs laid by workers that ignore the queen's chemical castration cues be left alone by their sisters or vigorously attacked? The answer to this question is rather personal, if you happen to be the queen, as it depends on how many males you opt to mate with.
The relatedness between individuals in an insect colony depends on how many males inseminate the queen. The more males the female mates with, the more different lineages there are in a colony -- each line's ancestry going through the queen and a given male. Once again, however, the strange genetics of such insects creates a novel situation. Rather than showing a family tree more complicated than that of the British monarchy, it can be shown that if the queen of a colony mates with a single male, then female workers in the colony turn out to be more related to nephews than to brothers. If the queen mates with numerous males, however, that situation reverses itself and female workers in a hive are now more related to brothers than to nephews. We shall focus on the second scenario because of the fascinating kin-selected cooperation emerging from it.
Whether females in a social insect colony are more related to brothers than to nephews can have quite serious implications about when and whether we should see kin-selected cooperation, and if it exists, what form such cooperation should take. To see this, first recall that brothers are those individuals produced by the queen, while nephews are those produced by sisters that have somehow managed to avoid the queen's chemical anti-reproduction agent. A conflict of interest then arises between sisters that have managed to escape and those that have not.
Aside from the queen, females who can reproduce (i.e., those that do not fall victim to the queen's attempt to monopolize reproduction) are always selected to do so. When females reproduce they always produce males, since such females are almost never inseminated. This creates a problem, however, for those females who can't reproduce, as they are more closely related to the queen's offspring (their brothers) than to their sisters' children (their nephews). Kin-selected cooperation on the part of those nonreproducing female workers then favors any action that increases the odds of the queen's offspring surviving at the cost of nephews.
There is little a female can do to stop one of her sisters from reproducing, if her sister has avoided the queen's attempt to do so already. But there are options available. Once a worker has laid eggs behind the queen's back, her sisters could, for example, refuse to care for and help nephews. Or they could take more drastic action -- they could eat eggs destined to be their nephews! Francis Ratnieks and Paul Visscher examined this possibility in honeybees, where females mate with ten to twenty different males. Their results were astonishing. Those honeybee females who did not produce offspring "policed" the reproductive actions of their sisters. If their sisters produced eggs on the sly, policing females destroyed the eggs. Ratnieks and Visscher found that honeybee workers showed remarkable acumen in discriminating between sisters' eggs and the queen's eggs. In a controlled laboratory setting, after twenty-four hours, only 2 percent of the sister-laid eggs remained intact, while 61 percent of the queen-laid eggs remained unharmed! But, given that the actual act of egg laying is rarely observed, how could honeybees know which eggs were laid by sisters and which by the queen? The answer appears to be that eggs are chemically "marked," such that queen-laid eggs smell different from worker-laid eggs. Why eggs should be marked so is still unclear, but one tantalizing possibility is that the queen marks her eggs to encourage workers to police the activities of their sisters.
Kin-selected policing is qualitatively different from the other types of cooperation so often found in animals. Rather than having individuals form a cooperative unit to accomplish some task, cooperation in honeybee police work takes the form of stopping others from cheating -- a more subtle and complex action. At a more fundamental level, policing is powerful, because it provides a direct deterrent to cheating, whereas in many other cases, we simply rely on cooperation being somehow more profitable than cheating, and this holy grail is often difficult to obtain.
There are many other cases of cooperation in highly related social insects. I'll mention one other curious example: honeypot ants. In one species of these ants, the largest individuals actually hang from the top of a colony and act as living storage tanks for water and sugar. These "honeypot" individuals have soft and elastic abdomens, and if you watch long enough you will see other individuals come up and "turn on the faucet" to drink the resources stored there. For significant periods of time, honeypot individuals do nothing but hang from the rafters and supply this service.
It is fascinating to find policewomen and living storage bins in the insect world, but how much of the cooperation we see is strictly due to the bizarre haplodiploid genetics of social insects? Can we expect anything so dramatic among mammals?
"Eureka!" Naked Mole-Rats
Physics is not the only discipline in science that has "Eureka!" stories. Just as physicists can recount the bathtub adventures of Archimedes and his famous exclamation when coming up with his theory of buoyancy (specific gravity), so too can the ardent student of behavioral ecology recite the story of Richard Alexander and Jenny Jarvis's discovery of extraordinary cooperation in a bizarre creature, the naked mole-rat. Alexander, a professor of biology at the University of Michigan, traveled to various universities in the 1970s, giving lectures on the evolution of social behavior, particularly cooperative and altruistic behavior. One of his themes was why, despite significant effort, extreme sociality (like that seen in insects) had not been uncovered in mammals. Alexander described the characteristics he believed a mammalian system would need for insect-like ultrasociality to exist. He outlined a hypothetical creature that would undertake altruistic acts for relatives who lived in a safe environment with lots of food. He went so far as to give details: the species would eat large tubers (potato-like foods) and live in burrows in a tropical spot that had clay soil.
One day in May 1976, Alexander presented these ideas to some folks at Northern Arizona University. Afterwards, he was approached by someone in the audience who told him he had given a perfect description of the naked mole-rat of Africa. On the advice of this fellow, Alexander contacted Jennifer Jarvis (at the University of CapeTown), who knew more about naked mole-rats than anyone in the world. After much back and forth, which included trips by Alexander and his colleague Paul Sherman to Africa to actually see the creatures, Jarvis and Alexander realized that they indeed had found the first eusocial (ultrasocial) mammal.
After all the attention this animal has attracted from both scientists and the media, it is almost disappointing to see how bland the native habitat of the naked mole-rat actually is and how ugly these creatures are, even by rodent standards! Naked mole-rats are hairless and blind, with crinkled skin and two large incisor teeth sticking out from their mouths. And those are the adults; the babies are even harder to look at for very long. First collected in Ethiopia in 1842, naked mole-rats (whose scientific name is Heterocephalus glaber) live within groups averaging about seventy individuals (but ranging up to almost three hundred) in underground burrows, from which they rarely, if ever, emerge. Such burrows average about two miles in length. Naked mole-rats have been studied primarily in Kenya and are often found in arid areas covered with dust and brush. Typically found near dirt roads, colonies can be located by molehills that pock the landscape. But what naked mole-rats lack in beauty and scenic living conditions, they make up for in fantastic behaviors.
One female alone (among many in the colony) is responsible for all the reproduction in a naked mole-rat group (three or so males in the group are responsible for the male side of mating). No other mammal that we know of, except another species of naked mole-rats discovered later on, has a single "queen," and this finding sent shock waves through the behavioral biology community. Kin selection theory suggests that such extreme cooperation, wherein most individuals give up the opportunity to reproduce, should be limited to species in which individuals are somehow extremely related to each other, yet naked mole-rats are mammals and don't have the bizarre genetics that allow for the "super-relatives" we saw in the bees and ants. So how could such a bizarre system have evolved here? Before answering this question, let's get a more comprehensive sense of just how much cooperation goes on among these creatures.
The queen and the handful of males she mates with have a twofold advantage over others in naked mole-rat colonies: not only do they monopolize all colony reproduction, but they also live longer than their nonreproducing colony-mates. Yet in the relatively short time that nonreproductive males and females are around, they get a lot accomplished, and without their cooperation naked mole-rat colonies would surely come to a screeching halt. In fact, those individuals not specialized in reproducing take on virtually all of the everyday cooperative actions that are the very lifeblood of colony existence. They excavate new tunnels (an absolutely critical aspect of colony survival), sweep debris, groom one another as well as the queen, and take on the unenviable and dangerous task of defense against predators.
Why such dramatic examples of cooperation in a single species? What s

Table of Contents

Contents
Preface
INTRODUCTION The Four Paths to Cooperation
1 All in the Family
2 One Good Turn Deserves Another
3 What's in It for Me?
4 For the Good of Others?
CONCLUSION Possibilities and Pitfalls
Notes
Index

What People are Saying About This

Robert Trivers

An excellent introduction to a fascinating subject.

Introduction

Introduction

The Four Paths to Cooperation

It is true that certain living creatures, as bees and ants, live sociably one with another...[and] some men may desire to know why mankind cannot do the same. To which I answer:

First, that men are continually in competition for honor and dignity, which these creatures are not; and consequently amongst men there ariseth on that ground, envy and hatred, and finally war....

Secondly, that amongst these creatures, the common good differeth not from the private....But man, whose every joy consisteth in comparing himself with other men, can relish nothing but what is eminent.

Thirdly, that these creatures, having not, as man, the use of reason, do not see, nor think they see any fault, in the administration of their common business; whereas amongst men, there are very many, that thinks themselves wiser, or abler to govern the public, better than the rest; and these strive to reform and innovate...and thereby bring into distraction and civil war.

Fourthly, that these creatures, though they have some use of voice, in making knownst to each other their desires, and other affections; yet they want that art of words, by which some men can represent to others that which is good, in the likeness of evil; and the evil in the likeness of good....

Fifthly, irrational creatures cannot distinguish between injury and damage; and therefore as long as they be at ease, they are not offended with their fellows; whereas man is then most troublesome, when he is most at ease; for then it is that he loves to...control the actions of them that governth the commonwealth.

Lmodern or prehistoric, cooperation is the glue that binds us together. It is difficult to even imagine a society in which cooperation, at some level or another, has not been integral. Certainly all groups have the requisite cheaters among them, and we will spend a great deal of time on such individuals: How should we punish them? How can we avoid interacting with them? Why do cheaters act the way they do? Nevertheless, without joint actions aimed at the production of something useful -- that is, without cooperation -- a society, almost by definition, is bound to crumble.

One possible gauge for estimating just how important cooperation is in all aspects of life is to recognize that we teach it to our children as early as they are able to grasp a story about others. Consider The Little Red Hen, a tale read by millions of parents to their toddlers.

One morning the Little Red Hen was pecking in the barnyard when she came across some grains of wheat. "How nice it would be to plant the grains and grow some wheat and bake some bread." So the Little Red Hen gathered up the grains of wheat and said "Who will help me plant this wheat?"

"Not I," quacked the Duck. "Not I," meowed the Cat. "Not I," grunted the Pig. So the Little Red Hen planted the grains of wheat all by herself.

The Little Red Hen then solicits the duck, the cat, and the pig to help her cut the wheat, bring it to the mill, and bake the bread; each time she is answered with the same chorus of "Not I." Finally, the Little Red Hen

...baked a warm and tasty loaf of bread.

"Now, who will help me eat the bread?" called the Little Red Hen. "I will," quacked the Duck. "I will," meowed the Cat. "I will," grunted the Pig. "Oh, no you won't," said the Little Red Hen. "I planted the wheat. I cut the wheat. I took it to the mill to be ground into flour. And I baked this bread without any help from the three of you!"

Then the Little Red Hen took a bit of fresh butter, sat down under a shady tree, and ate the loaf of bread...all by herself!

Now, while it is true that in the end the Little Red Hen bakes her bread without the help of others, the message of the story really centers on the inaction of the duck, cat, and pig. From this trio, we learn that if you fail to contribute to the production of a resource that is potentially available to all group members -- in this case a loaf of bread -- you simply will not be allowed to get the resource for free and thereby parasitize the efforts of others. My four-year-old son doesn't quite articulate it as such, but that is the bottom-line message. Of course, we all know of many instances in which this ideal is not upheld, but the point is that we teach our children the ideal, because it reflects what so many of us believe about human nature, or at the very least what we want to believe about human nature.

We read our kids The Little Red Hen because we cannot avoid the shadow of cooperation in virtually everything we do, or at least attempt to do. Consider just a few examples for the moment; we will delve into many more in later chapters.

During my drive in to work, I often listen to National Public Radio. I recognize that public radio listeners need to face up to a fact: if you aren't going to be forced to listen to commercials about the fish food sale at your local pet store, somebody is going to have to pay the bills for broadc asting this stuff. And that means that the dreaded words you will be inundated with for one solid week -- pledge drive -- are always just around the corner.

The issue of cooperation arises for all public radio listeners. What should we do when pledge week comes around and everyone at the station, from the president to the assistant director of marketing, takes a stab at convincing us that we should pitch in and contribute? Although not glaringly obvious, there is a true dilemma here in terms of whether one should cooperate or not. After all, I can easily convince myself that if I don't contribute, enough people will, and the station will continue to operate. Not only could I convince myself of this, it would in all likelihood be true. So, perhaps I wouldn't cooperate and send in my pledge. But if this is true for me, it is true for every public radio listener. What if everyone decided not to contribute because others will? The answer is clear -- no more public radio. So, while public radio is not relying on any single person to contribute, thus providing a temptation not to contribute (you get the product free), if no one cooperates, everyone loses.

Enough people cooperate and contribute to keep public radio alive and well, but there are many other similar dilemmas where cooperation is not the inevitable outcome. Consider the brown-outs that are notorious in hot parts of the country during scorching summer days. Out of the blue, the electricity in large areas shuts down. Why? Could air conditioner owners, each deciding whether or not to cooperate, be responsible? Each owner believes that if she keeps her air conditioner on the maximum setting, that alone will not overload th e system -- so, to keep comfortable, that is precisely what she does. But if this holds true for one person, it is true for that person's neighbor, her neighbor's neighbor, and so on, and when everyone comes to the same decision to crank up the air conditioner, we get a brown-out. So the lack of cooperation imparts a price we all pay, like it or not. But it need not always be that way. Josh Weiner and Tabitha Doescher, for example, found that in a survey of utility customers, individuals were more likely to install control devices on their cooling units when they thought others would act in a similar fashion.

Returning to the public radio example, imagine that the story that airs after the pledge drive focuses on the nuclear arms race between the United States and the former Soviet Union. Hard as it may seem to swallow, this is yet another version of the same cooperation problem we just faced, except that in this case, countries are the decision makers and there is a lot more at stake. Let us assume, for the time being, that both parties (the U.S. and the former Soviet Union) would prefer to have no nuclear weapons on the planet. As such, mutual cooperation is the desired goal. But why, then, is it so hard to get there? Why were both the United States and the Soviet Union using strategies like "mutual assured destruction" (any nuclear attack would lead to the destruction of all parties) for so long? One possibility is that neither side could disarm its nuclear weapons first, because cooperation by one party and noncooperation by the other would be an intolerable position for the cooperator. Mutual cooperation is again best for everyone, but the temptation to cheat (not cooperate) is very st rong because of the consequences of unilateral action. Clearly, whether parties eventually cooperate in this instance and how they choose to do so has social and political consequences.

Philosophers and psychologists, economists and biologists have been making conjectures on the nature of human cooperation for as long as those professions have been around. Let's take just a few moments to look at some historical aspects of the study of cooperation, to put this subject in some perspective.

Philosophers tend to believe that humans are either naturally social and cooperative or naturally antisocial and uncooperative. Aristotle fell in the first camp and was quite adamant about it: "Man is by nature a social creature: an individual who is unsocial naturally and not accidentally is either beneath our notice or more than human. Society is something in nature that precedes the individual. Anyone who either cannot lead the common life or is so self-sufficient as not to need to and therefore does not partake of society is either a beast or a god" (Politics, 328 B.C.).

Aristotle believed that the function of man was to lead a life of reason, because it was this alone that separated us from the beasts. On the other hand, there have been those who believed mankind was capable of cooperation, but that individuals would only cooperate if some external force saw to it. The Sayings of the Fathers, a fourth-century compilation of advice on religion and social affairs, notes ominously: "Pray for the welfare of the government, since but for the fear thereof men would swallow each other alive."

The two most famous combatants to square off on the issue of whether people are by nature cooperative or not were undoubtedly John Locke and Thomas Hobbes, British philosophers and political scientists of the seventeenth century. Both Hobbes and Locke believed humans to be capable of cooperation; the question they differed on was whether we are innately cooperative. In essence the debate was on the most fundamental of all questions: are we naturally good or evil? As such, the debate was often cast in terms of whether war was the default state of human behavior or an aberration and whether some governmental unit was needed to enforce cooperation among civilians.

In Two Treatises of Government (1690), Locke sets out his rather far-sighted views that man is born free, that governments are not divinely appointed but rather a form of contract that can be broken by the people at any time, and that man is basically good and naturally inclined toward cooperation rather than destruction (via war): "And here we have the plain difference between the state of nature and the state of war, which however some men have confounded, are as distant as a state of peace, mutual assistance and preservation: and a state of enmity, malice, violence and mutual destruction are from one another."

Thomas Hobbes, whose Leviathan predates Locke's work by half a century, saw things in quite a different light. Mankind in its natural state, without a powerful government to keep citizens in line, was, Hobbes believed, "in a condition called war; and such a war as is of every man against every man." Government's function, according to Hobbes, was to enforce cooperation among its constituents, and he believed that the covenants formed between the governors and governed were based on force. In Hobbes's eyes, "cov enants, without the sword, are but words and of no strength to secure man at all." Hobbes went as far as codifying this view in his Fundamental Law of Nature, which includes the supposition that "every man has a right to every thing: even to another's body." Without governments to see that cooperation exists among constituents, Hobbes believed, life would be "solitary, poor, nasty, brutish and short." An interesting corollary to this "fundamental law" was that man was aware of his condition. Without government, people simply refused to invest in any public goods, since such goods would no doubt be usurped by others. The existence of government was not only needed to bring about cooperation per se, but was also the only means for people to procure investments and common goods. Somewhat surprisingly, despite his rather gloomy view of human nature, Hobbes believed that animals could be quite cooperative, by instinct (see his words at the beginning of this chapter).

The debate made famous by Locke and Hobbes still burns strong today. Are we inherently good? Do we tend toward cooperation, if given the chance? Today, however, the proponents are not particularly interested in the facts about cooperation; rather, they focus on how to make the opposing viewpoint seem foolish. Religions differ on our "fundamental" nature (good? evil? neither? both?), and even political parties can often be divided according to whether they believe that we are fundamentally good (as most liberals believe) or that we are neither good nor bad, but learn to be these things (as most conservatives believe). Resolving the differences between religions and different political parties is probably impossible and perhaps not ev en advisable. But given the tremendous advantages of actually understanding the very core of our behavioral repertoire, we must continue our investigation into this matter. While philosophy has certainly proved useful in illuminating the questions, perhaps it is not the ideal place to look for the answers about our cooperative tendencies (or lack thereof). But economics might be.

Economists and business people are, not surprisingly, acutely interested in cooperation, albeit for somewhat different reasons than philosophers. The approach taken in economics centers on the notion of the "rational man." Most, but certainly not all, economists argue that people, one way or another, assess the costs and benefits of taking some action that has economic consequences and use a simple rule of thumb. If the benefits of the action outweigh the costs, people undertake it; otherwise they do not -- hence the decision is considered rational. Extending this idea to cooperative behavior, people cooperate with one another when it is in their own interest to do so (the benefits are greater than the costs) and refuse to cooperate in other situations.

This notion of the rational man has its roots deep in the history of economics and can be traced back at least as far as Adam Smith's The Wealth of Nations, wherein he laid out his famous "invisible hand" theory. The "invisible hand" ensures that the self-interest of each party translates into a well-oiled economy.

It is not from the benevolence of the butcher, the brewer and the baker that we expect our dinner, but from regard to their own self-interest. We address ourselves not to their humanity but to their self-love and never talk t o them of our own necessities but of their advantages. Nobody but a beggar chooses to depend chiefly on the benevolence of his fellow citizens.

Cooperation, Adam Smith believed, is a natural result of individuals trying to maximize their profit. When cooperation fails to serve this function, people don't cooperate. This approach underlies the literally thousands of studies on the subject performed in the area of social psychology. In most of these economics-based psychology experiments, a group of people are assembled in a psychology lab and given instructions about a "game" that they are about to play. Typically, individuals are given a small amount of money and told that if enough people are willing to contribute a portion of the money they originally received, everyone in the group will get a relatively large bonus (notice the similarity to the public radio dilemma). For example, after being given $10 each, a group of eight subjects will be told that if four of them contribute $5 each, then everyone in the group, contributors and noncontributors alike, will be given a $10 bonus; but if fewer than four players contribute, no bonus will be given and those who contributed will be out their $5. Social psychologists then examine how such factors as group size and the ability of subjects to talk over the matter before deciding what to do affect whether the "cooperative bonus" is obtained and who is willing to contribute. Underlying all the manipulations, social psychologists are generally interested in whether people can figure out the rational choice that would bring them the most money.

The notion that humans are inherently selfish, cooperating only when it is in their economic best interest to do so, has certainly not gone unchallenged. In addition to the anecdotal cases we can all come up with, there have been numerous experimental attempts to determine whether we are continually acting as cost/benefit detectors, basing our decisions on this one element alone, or whether the story is more complex. Linnda Caporael and her colleagues, for instance, have argued that the rational man theory of cooperation (or the "egoistic incentive" theory, as they refer to it) is largely untested and based more on cultural beliefs than empirical evidence. In an attempt to test this, they examined whether people would cooperate with each other in the absence of economic incentives to do so. Caporael's team found that people indeed do cooperate without such incentives and that the participants themselves often cite "group welfare" as a primary cause for such "irrational" decisions.

In fact, the social psychology notion that people need to be tested to see if their acts are based solely on selfishness has its roots in the writings of the ancient prophets and is essentially what the story of Job is all about. In this parable, the Devil approaches God and puts forth the following argument: The only reason Job loves You is that You (God) have given Job everything he needs, and more. Take away that incentive, says the Devil, and You will see just how quickly Job reconsiders his devotion. God does just that, and of course Job, though a bit confused about what is going on, remains loving and devout in the absence of any economic incentives. How common the attitudes of Job and Caporael's subjects are remains a matter of debate, but they certainly pose a respectable alternative to s tandard economic thinking about cooperation.

Despite challenges to its universality, the rational man theory, because of its predictive power, has a very strong foothold not only in its home discipline of economics but in political science, psychology, anthropology, and even biology. There are, however, a few practical problems with this approach. First, there is the question of timescale. When we say that people will cooperate if the benefits of cooperation outweigh the costs, do we mean with respect to the immediate consequences of an action or to the longer-term consequences? If cooperating with you today harnesses me with some new cost, but five years down the road I receive a benefit as a result of my behavior, is it rational for me to perform the action now? Second, and in many ways more problematic, is how to incorporate many different currencies into an economic decision about whether to cooperate (in technical terms, this is a problem with utility functions). If cooperating with someone gets me three apples but not cooperating gets me an orange and $1, how do I decide what to do? Which is worth more (that is, which provides me with greater satisfaction)? This is the precise reason we have a monetary system with well-defined units, but translating across apples and oranges to dollars (or whatever currency you are using) is not always straightforward, and it is not clear that people even attempt to do this, in any real way, when deciding whether or not to make a deal.

The philosophical, psychological, and economic approaches to the study of cooperation are all illuminating in their own ways. But they fail to address a fundamental problem with respect to cooperative behavior: How could coo peration persist over long periods of time, when there seem to be so many ways that individuals who don't cooperate can circumvent the system? Over the course of many generations, why don't we see cheaters (those who fail to cooperate) slowly increase in frequency, replacing their cooperating peers? If you can benefit from others cooperating, why should you ever cooperate? Cheaters obtain the resources that cooperators obtain but don't pay the costs of cooperation.

To fully address these issues, we must now turn to the science of evolutionary biology. Here, using natural selection as our guidepost, we can examine the various means by which cooperative strategies can evolve over vast stretches of time, as well as the reasons cooperation often fails to manifest itself in certain conditions. It is with the techniques developed in evolutionary biology, and more specifically behavioral ecology, that we will pursue our study of cooperation throughout this book. As we shall see, evolutionary biology and behavioral ecology are uniquely suited to address questions surrounding the existence and maintenance of cooperation, as the conceptual and mathematical tools have already been developed (in other contexts) to address the evolution of cooperation. Behavioral ecology is a discipline whose primary function is to study the evolution of social behavior, and so it is the area of biology best suited to examine cooperation.

The work compiled by behavioral ecologists over the last twenty-five years or so is an untapped treasure -- not just as a checklist of cases of cooperation, but also as a conceptual spawning ground for ideas on how to promote human cooperation. Before examining the nuts and bolts of an evolutionary approach to the study of cooperation, let me put forth my hypothesis regarding precisely how the study of evolution and animal behavior can be used to foster and enhance cooperation in humans.

What we can learn about human cooperation by studying nonhumans begins with this assumption: We are much more cognitively sophisticated than animals. Despite considerable work done recently (some of it coming from my own lab) suggesting that animals are behaviorally far more complex than we have given them credit for, everything is relative. Animals can be much more sophisticated than we previously believed and still much less cognitively advanced than humans. It is worth emphasizing this point, because some have argued that one reason we can use animal examples to understand human nature is that some animals possess a rudimentary form of morality. It would require a separate book to elaborate on why I do not hold that view, but I believe animal work on cooperation can be profoundly useful for fostering human sociality nonetheless.

My hypothesis is that animal cooperation shows us what to expect when the complex web of human social networks, as well as the laws and norms found in all human societies, are absent, and so these studies act as a sort of baseline from which to operate. Animals show us a stripped-down version of what behavior in a given circumstance would look like without moral will and freedom. Only with this understanding of what a particular behavior looks like outside the context of some moral code can we use human morality to focus on and foster cooperation in our species.

Studies on cooperation in animals can be used to help us better understand and promote human cooperation in two ways. Both begin with a thorough search for common factors that have been found in many cases of animal cooperation. Once such factors are uncovered, one thing we can do is to identify areas in which we see failures in human cooperation, and then use our knowledge of animal cooperation to add critical factors to the human scenario. This might be referred to as the "missing element" approach. For example, if we have found that cooperation in animals is common when individuals frequently interact, we have identified a factor promoting animal cooperation. We can then examine how we might add this factor to the human scenario with which we are concerned. A second way of using animal studies is to identify human behavioral scenarios containing some of the factors that we know tend to favor cooperation in animals, and to use various techniques to amplify these factors and hence enhance the probability of cooperation. This might be thought of as the "nudge it over the top" approach.

Throughout this book, we shall constantly return to both of the above approaches. Put simply, the evolutionary work on cooperation in animals is a virtually untapped treasure chest in terms of understanding human cooperation. To overlook it would be a shame and perhaps much worse than that.

Before moving on to a few more detailed cases of how work on cooperation in animals can be used to foster human cooperation, I want to address a broad-based objection to the sort of approach I am advocating. One could argue that we humans are so different from animals that any attempt to study a phenomenon in animals is completely irrelevant with respect to that phenomenon in humans. There are literally thousands of e xamples one could give to refute this argument, but consider just one for the purpose of illustration.

Since the time of the Spanish explorer Ponce de Leon, people have been fascinated with the nature of getting old (in biological terms, the process of senescence). Our interest in why fruit flies get old, however, is probably a bit less heartfelt. Yet all across the world there are laboratories whose sole function is to study aging in fruit flies. This work has proven very productive and has shed a great deal of light on why humans, as well as fruit flies, get old and what we might do to affect the process of aging. Fruit flies are a model species, a means to reach an end, and they have proved quite useful in helping us better understand ourselves.

The reason that fruit flies help us understand aging in general is that they contain genes that are similar to the genes we believe underlie aging in humans. But many organisms have some genes in common with us. In fact, one unlikely candidate for studying aging in humans has proved a veritable gold mine -- yeast! About 31 percent of the yeast genome have counterparts (called homologs) in humans. David Sinclair and his colleagues at the Massachusetts Institute of Technology, armed with this information, have studied the sgs1 gene in yeast, which has a counterpart labeled WRN in humans, to better understand the aging process. Mutations in WRN are known to result in Werner's syndrome in humans, producing premature aging. Likewise, Sinclair and his colleagues found that sgs1 mutations caused premature aging in yeast cells. More than that, however, they were also able to understand some of the molecular details of how sgs1 caused aging. Studying yeast genes paid off by providing previously unknown details about the aging process in both yeast and humans. Similar arguments have been made with respect to yeast experiments and our fundamental understanding of the biology of cancer. Humans can be fundamentally different from flies and yeast and yet still share certain commonalities. To argue that this line of reasoning might be true for traits like aging but probably not for behavior is not grounded in any logic.

To guide us in examining how animal studies can shed light on human cooperation, we need a better understanding of how cooperation manifests itself in nonhumans. So let's take a look at some examples. Four different paths to cooperation have been outlined by behavioral ecologists (some routes being more controversial than others). These paths go by various names, but here we shall begin by labeling them (1) family dynamics, (2) reciprocal transactions, (3) selfish teamwork, and (4) group altruism. These four pathways provide a framework for evolutionary thinking on cooperation and have been examined in some detail in nonhumans.

The First Path: Family Dynamics

In an open field somewhere in California, a group of ground squirrels peacefully go about their normal daily activities. Seemingly out of nowhere, a hawk begins its deadly dive from the air, targeting the squirrels for its next meal. Suddenly a piercing shriek echoes through the valley -- the alarm call of one female squirrel. The field comes to life with squirrels making mad dashes toward their burrow or some other safe haven. Minutes later, when the hawk has clearly set its sights elsewhere, the squirrels slowly begin to resurface.

A puzz le emerges in this example. Why should an individual squirrel be the potential "sacrificial lamb"? After all, screaming alarm calls as loudly as possible must make you the single most obvious thing in the entire field. Why attract the hawk's attention and most likely make yourself its next snack? Why not let someone else take the risks? As with so many riddles in the field of evolution and animal behavior, the answer lies in the interaction between ecology and kinship.

The first step in unraveling the puzzle of why a female should volunteer to give a warning call lies in recognizing that the group of squirrels being warned of upcoming perils is not a random assortment of animals. Rather, these squirrels live in a society full of relatives, and for those who study the evolution of social behavior, that makes all the difference in the world. Your relatives, by definition, are more likely to carry the same genes that you possess than are a handful of strangers picked off the street. These genes are called "identical by descent" because the likelihood of sharing them is related to descent from some common ancestral relative. For example, the common ancestors among sisters are their mother and father, while those for cousins would be a grandmother and grandfather. What this means is that when a squirrel risks its own life to save the lives of its relatives, it is not being completely altruistic, because its relatives most likely carry the same genes that it does. Since sisters, for example, share (on average) 50 percent of their genes that are identical by descent, saving two sisters and losing your life is equivalent to an even swap, while saving three sisters and losing your life is a net positive fo r all parties involved! And if you are only risking, rather than necessarily giving up your life, you might do it if fewer relatives were around.

Yet, so far, we have only explained half the riddle -- the half surrounding why anyone should give alarm calls. Now let's look at who gives a call. One perplexing element in our story is that sex seems to play a role in establishing who our cooperative sentinel is. Over and over again, we see that females, not males, put their necks on the line. Why? Again, that overriding theme in the evolution of behavior -- kinship, this time mixed with choice of living venue -- plays a role.

In many species of animals, males and females do not make the same decision about where to set up residence. Once an individual is mature enough to survive on its own, it is faced with a rather daunting decision: should it live near where it grew up or emigrate elsewhere? Despite what your teenager will tell you, this is not a straightforward decision. Living in the old neighborhood clearly has both costs (e.g., competition from local rivals) and benefits (e.g., security), as does moving to a new location. Furthermore, the costs and benefits can be very different depending on whether you are male or female, and in the animal kingdom we see every combination possible -- males stay and females leave, males leave and females stay, both sexes leave when reaching maturity, and both sexes remain in the natal home area. Among squirrels, it is the males that leave home to set up shop elsewhere and the females that stay in their old stomping grounds.

Once males leave and females stay put, an interesting imbalance occurs. Females now find themselves surround ed by relatives, while males are in areas with complete strangers. This asymmetry in relatedness then favors dangerous alarm calling in females, since they will be assisting kin, but the same does not hold true for males. Blood, then, explains both why an individual should put itself in harm's way by calling out when a predator is sighted and who should be most likely to do so. If this is true, then an interesting prediction can be made. On the rare occasions when females are forced to emigrate to new groups, these newcomers, despite being female, should be among the least likely individuals to give alarm calls. Sure enough, that is precisely what we find.

The Second Path: Reciprocal Transactions

Walk a bit along the beautiful, calm streams of the Northern Mountains of Trinidad, West Indies, and you will quickly see that one species common to these waters is the guppy. In many streams, the water is crystal clear and the behavior of guppies can be seen from the bank. If you sit there for a few hours, you will probably observe a pair of guppies breaking away from their group and approaching a dangerous predator. This alone is bizarre enough, given that the fish could just as easily have headed for cover, rather than toward this menace. But not only do some fish take the risks inherent in approaching a predator, they actually seem to return to their group and somehow pass on the information they just obtained.

Our risk-taking guppies are trapped in a dilemma. The temptation to cheat is always there -- the best thing that could happen to guppy 1 is for guppy 2 to take the risks and pass the information on to the other guppy for free. But if both individuals opt to wait for the other to go o ut and do the dirty work, they may be worse off than had they just gone and done it as a team. Many other examples of this dilemma pervade everyday animal life.

Is there an escape from this dilemma? Can we identify any sort of cooperation in this example? The answer is yes, providing a pair of individuals finds themselves in a similar predicament many times -- certainly plausible for both guppies. When partners are paired up many times, evolutionary theory predicts that individuals should use what is called the "tit-for-tat" strategy. Tit-for-tat is just another term for the "eye for an eye" rule found in Exodus. That is, start out cooperating with your partner, but if he cheats on you, cheat right back in the same manner he did. Despite having a brain not much bigger than a pinhead, guppies appear to use the tit-for-tat rule on their sorties toward potentially dangerous predators. Each fish keeps track of what the other is doing when both go out to examine the predator. Should one fish lag a little behind, the other fish slows down and makes sure that the distance does not become too great. To top it off, guppies genuinely prefer to spend their time hanging around other guppies who cooperated with them during their danger-filled sorties, presumably to be in their vicinity again, should the situation arise once more! If guppy predator inspection reminds you of guard duty in the army, you are not alone, but more on that after a few additional animal examples.

The Third Path: Selfish Teamwork

Watching lionesses hunt a gazelle on the plains of Africa is a savage, beautiful, and mesmerizing event. Lionesses don't just mindlessly chase after a gazelle; rather, the hunt is a mas terpiece of coordinated action aimed at one result -- a gazelle meal. Often one lioness will flush the gazelle and one or more of the others will chase it, or each hunter will come at the prey from a different angle, limiting maneuvering room for the gazelles. Such coordinated hunting is seen in other animals as well. But is it cooperation? Might it not be the case that each lioness strictly has her own interest, and that alone, at heart? Yes, but this does not detract from the fact that the hunt is clearly a coordinated action set to accomplish a particular goal (motives and psychology aside). In fact, this type of cooperation, one in which joint action is predicated only on the self-interest of all parties involved, may be the most common type of animal cooperation.

The Fourth Path: Group Altruism

The Sonoran Desert is home to a fascinating species of ants named Acromyrmex versicolor. Although ant nests are usually initiated by sisters, Acromyrmex queens are unrelated. Despite not being relatives, queens in this species are friendly -- no one attacks anyone else in the nest, all food is shared equally by everyone, and all the queens have about the same number of offspring. Yet in the midst of this cooperation fest, a riddle emerges: only one queen in the whole nest goes out and gets food for everyone. This sounds particularly odd because the underground nest is a pretty safe place to be, but going out into the desert is rather like stepping into a minefield. Any number of species out there view queens as juicy morsels, and many foraging ventures end in the demise of the forager. On top of all that, which queen ultimately becomes the group's food provider seems to be determ ined by chance -- no one is coerced into taking the job.

How could such dramatic, "for the good of others" cooperative behavior ever come to be? If these queens are not related, why should any one of them accept the role of food gatherer with all of its risks, when the booty that comes in is divided between all group members equally and ultimately leads to all nestmates producing similar numbers of offspring? The answer to these questions lies in changing perspectives. Rather than viewing this strictly in terms of the costs and benefits to the individual who is the gatherer, one must expand the notion of costs and benefits to the group. This perspective is called group selection.

The basic premise of group selection is quite simple. When considering any behavior, one must examine the effect the behavior has on the individual undertaking it and those around it. If the behavior is beneficial to all involved, no obstacles exist to its evolution. If the behavior has negative effects on all parties involved, then such behavior disappears very quickly. But what about the queens in our example? Here we have a case where the behavior (food gathering) has a negative impact on the forager but a positive impact on the group. When should we expect this sort of cooperation to persist? The answer, though it can be couched in complex mathematics, is also just plain intuitive -- when the group-level positive effects outweigh the individual-level negative effects.

Despite costs to the queen, who takes all the risks associated with sorties from the safety of the nest, the group-level benefits of this action are so great that the behavior persists. To see why, we need yet one more piece of i nformation about Acromyrmex versicolor. And that is that once queens raise their offspring, everyone comes up to the surface and what amounts to all-out warfare between individuals in different nests occurs. Only one group will survive. The odds of surviving are directly related to the number of fighters each group has, and that is simply connected to how much food queens had and how many offspring they could produce.

So, in the extreme, imagine nests in which no one would go out and forage and everyone would try to produce just whatever progeny they could from their stored body fat. Such a nest would surely perish in the nastiness to come, and hence the group-level benefits of having a specialized food gatherer outweigh the costs to the individual undertaking the action.

Examples such as these, in conjunction with evolutionary theory, serve as a starting point for our discussion of how cooperation in animals can better help us foster cooperation in humans. We will journey into beehives and naked mole-rat colonies to see a single female producing all the offspring for an entire group and a vast array of others who seem intent on cooperating with each other to help such a queen. Fish (and worms) switch sexes in order to divide up reproduction in a cooperative manner. Impalas cooperate with each other by pulling parasites off hard-to-reach places on the bodies of their friends to make them more hygienic. Mongooses take turns baby-sitting for each other. What will tie together these stories of cooperation in animals, however, is what they can and cannot tell us about cooperation in humans. In this context, we are interested not only in how natural selection has shaped a vast array of coo perative acts in a very diverse group of organisms, but also in how we can use the specifics of such animal studies to focus our attention, in the most productive manner, on making ourselves a more cooperative species.

Recall our guppy risk takers and what underlies their behavior. Evolutionary models predict this sort of cooperation when individuals have a high probability of bumping into each other and finding themselves in the same predicament again in the near future. Guppies show every sign that this is precisely what drives their risk taking, as they remember each other's actions for days and only cooperate with those that have reciprocated their kindness.

Can we learn anything about human cooperation from the guppy example per se? It depends. It would certainly be difficult to argue that any single example of animal cooperation is particularly useful to us in this context. Search hard enough in the animal world and you will find isolated examples of any behavior you can imagine, but isolated examples are hardly the framework on which to build a theory. Rather, it is the fact that underlying elements of the guppy example (multiple interactions among individuals, individual recognition) are played out over and over again in the animal world, in all sorts of species and in many different contexts, that makes the guppy case and those like it useful to us.

How might we go about using the moral of the guppy story to foster human cooperation? One way to address this problem is to construct a human scenario that probably has the same sorts of costs and benefits associated with it. What about guard duty in the army? Are not the costs and benefits of this situation similar to those in our guppy r isk-taking scenario? Surely they are, in that one certainly receives a benefit if others on guard duty go out and inspect a potential danger, but if no one goes out, everyone is in trouble. It is important to stress here that I am comparing only the costs and benefits of risk taking in guppies and guard duty in soldiers. My example says nothing about how much more complex human soldiers are than guppy patrollers nor anything about the cognitive processes involved in each case; it simply looks at costs and benefits.

Given the analogies between the guppy case and the army case, what can we glean from them? When soldiers are placed in dangerous situations in which they must take turns assuming risks, the best social environment is one in which the military unit is relatively small and has been together for a long time, so that all members of the group know what to expect from each other and know that if they take risks, they will (or will not) be reciprocated. Memory, individual recognition, and scorekeeping all facilitate the use of the tit-for-tat strategy that we introduced earlier, and keeping fighting units small and stable should make such cooperation so much the more likely. This logic holds true for any human scenario that involves risks and turn taking, not just army guard duty. Always keep in mind, however, that in this example, like all that we will look at, we are not trying to copy (or not copy) nature, but rather to use what we have learned from nature to suggest where we should focus our moral compass.

Can we use the cooperating lionesses story to somehow foster human cooperation? Suppose that we wish to foster cooperation in a small community of people that is in need of many resour ces: is the lion example of any use? Female lions hunt cooperatively when going after large prey but hunt smaller morsels alone. In other words, when the resource is large enough to both require more than one hunter and be shared (if the hunt is a success), cooperation occurs; otherwise it does not. Is there some way to create an environment in our community of humans in which people need to go after large resource items that are divisible rather than smaller items that can be obtained by solo players? Can a community-based incentive system be created to facilitate this?

In many urban areas today, planting large-scale gardens to spruce up a previously neglected area is common. Such gardens could be managed in many different ways. One way would be to allocate a small amount of land to each participant, allowing him to reap the fruits he sows. A second plan would be similar but with a critical twist. In addition to being given her own plot of land to do with as she pleases, each gardener would need to agree to spend some small amount of time working on a communal section of the garden. Individuals would then get the fruits grown on their own area and some portion of the communal crops, but only if they cooperated in the communal part of the garden.

The guppy and lion cases are only two of the many animal examples that will be put forth to help us understand how to use animal studies to facilitate human cooperation. While I believe that my approach to these issues is novel and will shed new light on human sociality, it can be better understood once we have some history under our belts.

Darwin's Bulldog versus Russia's Anarchist

Given the monumental impact that Charles Darwin's works T he Origin of Species and The Descent of Man and Selection in Relation to Sex have had in both the social and the physical sciences, it is often surprising to many that Darwin's ideas with respect to natural selection are straightforward -- in fact, remarkably straightforward. Consider any measurable characteristic of an organism -- height, weight, ability to see, and so on. If variations in this characteristic exist (for example, differences in height among individuals in a population), and if there exists a means by which individuals produce offspring that resemble themselves with respect to this trait, then any variant that outreproduces others will spread through the population over time. If taller individuals, perhaps because they have access to greater food resources, have more young, over time we expect to see the average height of individuals in that population increase. This argument holds true even if being just a little taller gives you a very slight edge in terms of the number of offspring you raise; through evolutionary time small differences can accumulate into large changes.

Behavioral biologists from the time of The Origin on have argued, as did Darwin himself, that the theory of natural selection applies not only to anatomical and physiological traits but to behavioral traits as well. In fact, one of Darwin's staunchest advocates was George Romanes, a founding father of social psychology. The argument is the same as before: if a number of different behavioral options exist and there is some means for these behaviors to be transmitted across generations, then any behavior that has a slight advantage in terms of its effect on individual reproduction will incr ease in frequency. So too for cooperation: if it increases fitness (roughly speaking, number of offspring), it should increase in frequency in a population.

Darwin himself was quite interested in, and sometimes troubled by, the evolution of cooperative and altruistic behavior. Through his observations he concluded, for instance, that the "most common service in the higher animals is to warn one another of danger by means of the united senses of all." Yet not all of the cooperation in the animal kingdom was easily explained. Darwin viewed the self-sacrificial behavior of bees and wasps (stinging intruders to guard the nest, but usually dying in the process) with a degree of awe, but he also realized that such extreme altruism was a challenge to the very core of natural selection thinking. After all, how could giving up your own life in defense of your nest ever be selected? Darwin had the creative insight to come up with the solution, known as kin selection (although the mathematics were not actually formalized for another hundred years). Darwin recognized that cooperation plays an important role in man as well as in animals, and while he centered his argument on "primitive man," it takes little imagination to extend it to modern societies:

When two tribes of primeval man, living in the same country came into competition, if (other circumstances being equal), the one tribe included a great number of courageous, sympathetic and faithful members, who were always ready to warn one another of danger, and to aid and defend each other, this tribe would succeed better and conquer the other. It must not be forgotten that although a high standard of morality gives but a slight advantage to eac h individual man and his children over the other men of the same tribe, yet that an increase in the number of well endowed men and an advancement in the standard of morality will certainly give an immense advantage to one tribe over the other (The Descent of Man and Selection in Relation to Sex, 1872)

It didn't take long for Darwin's ideas on natural selection applied to cooperation to stir up quite a hornet's nest. It was bad enough that Darwin's ideas shook up people's notion of their place in the universe, but now he was suggesting that our defining moral attributes -- being compassionate and cooperative -- are really just results of a history centered around chimps and other primates.

While Darwin believed that cooperation and competition were both prevalent in the animal world, two more extreme camps began to polarize the issue. On one side was none other than Darwin's friend, the eminent Thomas Henry Huxley, arguing that in the animal world cooperation was an anathema. Huxley, also known as "Darwin's Bulldog" because of his never-ending defense of Darwin's ideas, put forth his "gladiator" view of the world in the popular British newspaper called The Guardian. In Huxley's eyes the animal kingdom was a ruthless jungle, and a soft-bellied cooperator would stand no chance against a more cunning individual who would stop at nothing. With respect to cooperation, Huxley had adopted Herbert Spencer's view of "nature, red in tooth and claw":

From the point of view of the moralist, the animal world is on about the same level as the gladiator's show. The creatures are fairly well treated, and set to fight, whereby the strongest, the swiftest and the cunningest live to fight another day. The spectator has no need to turn his thumb down, as no quarter is given the weakest and the stupidest went to the wall, while the toughest and the shrewdest, those who were best fitted to cope with their circumstances, but not the best in any other way, survived. Life was a continuous free fight, and beyond the limited and temporary relations of the family, the Hobbesian war of each against all was the normal state of existence (The Struggle for Existence and Its Bearing upon Man, 1888)

This nasty picture -- I certainly wouldn't want my kid going to school in that neighborhood -- was vigorously opposed by many. In particular, the writings of Alfred Russell Wallace and Petr Kropotkin show a nature that is almost diametrically opposed to that painted by Huxley.

Alfred Russell Wallace had great insight but bad timing. He came up with the theory of natural selection at the same time as Darwin. Historians of science argue that Wallace was an even more avid "Darwinian" than Darwin himself in that Wallace believed in the almost unlimited, unending power of natural selection. Where Darwin and Wallace parted, however, was on the issue of humans, and particularly the human psyche. While Darwin viewed human evolution in the same light in which he viewed all evolution, Wallace did not.

Wallace felt that human morality and intelligence were somehow outside the realm of natural selection, and that "the whole reason, the only raison d'etre of the world...was the development of the human spirit in association with the human body." Although it is always difficult to prove such a claim, I'd venture to guess that Wallace's views were tied to his deep-seated religi ous beliefs about man's role in the cosmos, as Wallace essentially became a spiritualist and gave up science later in life. Given his views on morality and intellect, it should come as no surprise that he viewed cooperation as the norm in nature, rather than the exception. Contrast his remarks below with Huxley's gladiator view and you will see how radically two great minds can differ:

On the whole, then, we conclude that the popular idea of the struggle for existence entailing misery and pain on the animal world is the very reverse of the truth. What it really brings about is the maximum of life and of enjoyment of life with the minimum of suffering. (Darwinism, 1891)

Prince Petr Kropotkin was an even more fascinating man than Wallace. Prince of Russia, Kropotkin gave up his royal position to become an anarchist (he was one of the founding fathers of the discipline), a geologist, and a natural historian. As a natural historian and traveler, Kropotkin was a keen observer of animal social behavior. Huxley's gladiator scenario could not be further removed from what Kropotkin saw on his journeys, and he engaged in a spirited written exchange with Huxley in The Guardian. This exchange led to Kropotkin's classic Mutual Aid (1908). In this wonderfully written book, Kropotkin tells of seeing animal cooperation (that is, mutual aid) at every turn: "In all these scenes of animal life which crossed before my eyes, I saw mutual aid and mutual support carried on to an extent which made me suspect in it a feature of the greatest importance for the maintenance of life, the preservation of each species and its further evolution."

Daniel Todes has recently put for th a fascinating hypothesis to explain the stark difference between the views of Kropotkin and Huxley. It appears that many Russian naturalists and evolutionary biologists of Kropotkin's era believed that cooperation was the default state of nature, while most Europeans tended to line up more with the Huxley-like view that nature was much more nasty than cooperative. The difference, suggests Todes, is that Russian biologists and naturalists made their observations in rather hostile environments, such as Siberia, while most European biologists of the day were off studying in the tropics. So, not only were the Europeans getting a suntan, but they were observing an environment in which competition was the driving social agent. The Russians, however, were viewing animals that needed to cooperate with one another to fight against a harsh physical environment. We will return to this notion of cooperation in harsh environments later on.

Todes's arguments show once again how a behind-the-scenes view of science and scientists often reveals that unexpected, often idiosyncratic, factors can shape what is studied and why. Those researchers steeped in social behavior such as cooperation or even aggression may be more prone to having their ideologies affect their research. It is hard to imagine how your political leanings could affect your work if you were studying, for example, the shape of red blood cells in mammals, while it takes little imagination to see how this might happen if your research centered on the evolution of pro-social behaviors -- cases in point being Wallace's spiritualism and Kropotkin's avid social libertarianism. Of course we all hold political views, myself included. No doubt my Judeo-Ch ristian heritage, as well as my strong belief in one God who holds people accountable for their actions, affects every aspect of my life, in some form or another. How could such a belief system not? My hope, as I would assume is the case for most scientists who are also religious, is that while my belief system may draw me (directly or indirectly) toward certain scientific questions over others, it has no impact on my objectivity when performing experiments. Something is always responsible for drawing scientists to the questions they eventually address.

The Kropotkin/Wallace versus Huxley debates on cooperation made for good reading and good natural history (two things that the British were quite fond of in the 1880s), but they did little to formalize an evolutionary model of cooperation that could help us predict when we should expect cooperation and when we should not, nor did they address the different types of cooperation seen in nature. These issues have been addressed only in the last twenty to thirty years. The Huxley/Kropotkin debates were mainly about how common cooperation was and why each side believed that they had painted an accurate picture of nature. To fully understand modern theories of cooperation, however, we need to grasp how the questions surrounding cooperation have been framed, and that is where history plays a role.

Prince Kropotkin was the most vociferous, but not the lone, spokesman for the view that cooperation is the norm in nature and that, left on their own, animals will naturally cooperate in many instances. Accordingly, if humans wish to be more cooperative, we must merely look to nature -- which to Kropotkin and others of his day meant not only animals but primitive human societies -- and imitate it. Again, Kropotkin in his own words: "If we resort to an indirect test and ask Nature: Who are the fittest: those that are continually at war with each other, or those who support one another? We at once see those animals which acquire mutual aid are undoubtedly the fittest" (Mutual Aid.)

While it probably pulls on our heartstrings to believe that the natural world is quite a cooperative place indeed and that mimicking nature is the way to cooperation, the literature on every sort of noncooperative act imaginable suggests that this view is naive -- nice in principle, wrong in fact.

On the flip side of the coin were those who believed that nature was a never-ending bloodbath and that little could be learned from observing the carnage. A more extreme position on this theme was put forward by Huxley, who essentially argued that rather than copying nature, we should be doing everything we can to oppose it. This was not just another in a line of questions Huxley addressed, but rather one of his passions. Huxley implored his audience to admit "once and for all, that the ethical progress of society depends, not on imitating the cosmic process, still less in running away from it, but in combating it." But the looming presence of both cooperation and carnage in nature suggests that a simple guidepost like "do the opposite of what occurs in nature" is an argument that lacks much vigor.

Most evolutionary biologists reject both the "imitate nature" and "oppose nature" arguments and adopt what I will call "the one long argument" approach. In a wonderfully readable book entitled One Long Argument, Harvard University's Ernst Mayr, a founding father of modern evolutionary thinking, puts forth the idea that all of Darwin's numerous books and papers have one theme -- that one must understand history and the process of natural selection, and its typical outcome of adaptive evolutionary change, to understand whatever one is studying. While all reasonable biologists believe natural selection to be a powerful force, adherents of the one long argument approach argue that the facts of nature tell us nothing about morality. Sometimes natural selection favors cooperation, sometimes not. Stephen Jay Gould, among others, has popularized this general notion in his monthly articles in Natural History magazine:

There are no shortcuts to morality. Nature is not intrinsically anything that can offer comfort or solace in human terms -- if only because our species is such an insignificant latecomer in a world not constructed for us. So much the better. The answers to moral dilemmas are not lying out there, waiting to be discovered They reside, like the kingdom of God, within us -- the most difficult and inaccessible spot for any discovery.

I take exception to Gould's characterization of humans as "insignificant latecomers" but agree that it is dangerous to use natural selection thinking to guide human behavior. Unfortunately, ever since E. O. Wilson published his classic book Sociobiology, a number of biologists, psychologists, and anthropologists have used evolutionary approaches to make preposterous, unsubstantiated claims about human nature -- on humans as inherently warlike (or inherently peaceful), on the nature of sexuality and parenting, and so on. This is so common that it even has its own name -- pop sociobiology -- and it has rightly been criticized by many. The danger of this sort of thinking, as Robert Wright points out in The Moral Animal, is that it leads one to the mistaken impression that feelings like sympathy, guilt, and the notion that right should be rewarded and evil punished are really just natural selection manifesting itself and should circumstances change, natural selection may simply favor the converse emotions in humans. This is an unacceptable thought for anyone with a sense of absolute right and wrong.

The scientific brute facts of nature tell us nothing about what is a moral act and what is an immoral act -- they could not possibly do so, for that is not what science is about. Whether a lion killing a gazelle is a moral act is not something science can address, as there is no experiment that would allow one to come to that conclusion or to reject that proposition. I do nonetheless believe that studying animal examples of cooperation (or the lack of it) can be quite useful in helping us structure human interactions.

Animal cooperation often shows us, as I suggested earlier, what to expect when the complex web of human social networks, as well as the laws and norms found in all human societies, are absent, and acts as a sort of baseline from which to operate. I am not arguing that animal cooperation is the rule or the exception in nature, just that it occurs often enough to make it an irresistible subject. Moreover, while natural selection is the driving force shaping cooperation in animals, and I present animal examples as a means to enhance human cooperation, I am not arguing that natural selection thinking should be the guidepost we use in shaping our own behavior. And I am by no means falling into the trap of the "naturalistic fallacy" -- that because something "is" in nature, then it "ought" to be that way. Whether natural selection favors something in nonhumans, or even whether natural selection might favor a behavior in humans if we stripped away culture, is not the primary issue with respect to shaping human cooperative tendencies. Rather, the critical point is that we can use animal examples as a means for focusing our moral compasses on the right elements, from the right perspective, in such a manner as to make human cooperation more likely.

The logic underlying the guppy and lioness examples alluded to earlier, and how such cases can be used to foster human cooperation, form the framework on which this book is built. We will walk our way through each of the four paths to cooperation, looking at how and why they work and the controversies surrounding each. Investigating often dazzling, almost incredible examples of cooperation in nonhumans will take us to all corners of the earth.

Copyright © 1999 by Lee Dugatkin

Editorial Reviews

A new way of thinking about human society, as well as a host of amazing stories.

New Scientist

Evolutionary biologist Dugatkin (Cooperation Among Animals) is unabashed in his belief that "the study of evolution and animal behavior can be used to foster and enhance cooperation in humans." Without resorting to simple minded biological determinism, he argues forcefully that the behavioral predisposition of humans may be predicted by evolution. Thus, he asserts that research in animal behavior can provide baseline information about parallel behavior in (admittedly more complex) humanity. Such investigations may ultimately help us better understand the underpinnings of human behavior and allow us to restructure our environments to promote more cooperation. Dugatkin explains that cooperation arises through four pathways, "family dynamics, reciprocal transactions, selfish teamwork, and group altruism." He devotes one chapter to each pathway, clearly explaining the underlying evolutionary theory and providing myriad animal examples. His fascinating instances range widely from vampire bats willing to regurgitate blood for starving neighbors to mongooses who take turns baby-sitting. Each chapter concludes with an attempt to tie the lessons learned from animals to suggestions for public policy issues as diverse as class size in elementary schools and partnering in police departments. These applications, however, are the weakest part of an otherwise startling and eye-opening glimpse into the evolution of behavior. (Feb.)

Publishers Weekly - Publisher's Weekly

Can the study of cooperation in animals facilitate human sociability, asks evolutionary biologist Dugatkin? Yes, he concludes-after a run through evidence from the animal kingdom-though exactly how remains unclear

Kirkus Reviews