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I always had a tankful of guppies when I was a kid, but if you had suggested then that my career would involve examining guppy behavior on an island in the Caribbean, I would have asked you to hush up so I could hear the Yankees game on the radio. But now, as a behavioral ecologist, I design and test models of social evolution, usually working with guppies in streams of Trinidad and Tobago. As I share some surprising facts about the guppy, keep in mind that this creature has a brain the size of an immature pea.
Animal behaviorists speculate that the females of many species copy each other in choosing mates. If one female likes a male, then other females show an interest. Where did we get the ﬁrst controlled experimental evidence of this phenomenon? From an unexpected source: the little guppy. A female guppy’s mate preference is strongly inﬂuenced by which male is chosen by a female she is observing. In short, culture—transmission via copying behavior—seems to inﬂuence mate choice in the guppy. Replace “guppy” with “teenage girl” and “mate” with “date” and the insight into culture is clearer.
Am I asserting that there is culture among ﬁsh with pebble-sized brains? Does cultural transmission affect mate choice in other creatures, as well? Does that list include humans? If so, we may need to rethink what we mean by cultural transmission and re-evaluate its power in the natural world.
Trial and Error or Social Learning?
In the everyday sense, culture might mean going to the opera or using your knife and fork correctly. A more formal use of the word might refer to the norms and rules that govern a society. This second deﬁnition resembles what some anthropologists mean when they discuss culture. For evolutionary biologists and behavioral ecologists, however, culture is important only as the result of a process: the process of cultural transmission.
A simple, well-accepted biological and psychological deﬁnition of cultural transmission is the process whereby individuals learn in a special way: by observing others. Thus we can speak of any particular culture as the product of learning by observing, and speak of the long-term dynamics of culture in a particular population as “cultural evolution.”
In Culture and the Evolutionary Process (University of Chicago, 1985), Robert Boyd and Peter Richerson, two theoreticians of cultural evolution, note that biologists and anthropologists often ask: “Why not simply treat culture as a …response to environmental variation in which the ‘environment’ is the behavior of conspeciﬁcs [fellow members of a species]?” This would reduce cultural transmission to just another means by which organisms adapt to the environment. After all, animals also learn about their environment by means of trial and error; why all the attention on social learning and cultural transmission?
There is a good answer to this. What is learned by trial and error requires the use of a single brain, that of the individual involved in the learning; the lesson dies when the learner dies. The effects of social learning, on the other hand, may be passed from individual to individual, and what is learned by one individual can reside in the brains of many others that have watched the original learner. When social learning (cultural transmission) is in play, what goes on in the brain of a single individual can affect what goes on in the brains of a population. That makes cultural transmission a powerful force, potentially on par with genetic transmission of behavioral traits.
Of course, we could have deﬁned culture and cultural transmission differently. For example, we might have spoken of culture in terms of language or symbolic representation (as do some anthropologists), but then we would have glossed over the rudiments of culture that permeate the animal world. Or we could have deﬁned culture as a product of the human mind. Or perhaps, in a more generous spirit, we might have said that culture is linked somehow with the neocortex. Maybe this sheetlike, layered structure, found only in the forebrains of mammals, is what enables cultural transmission of behavior. These deﬁnitions might make us feel good about being human (or at least mammalian), but they would not help us understand the evolution of culture. That is because animals lacking mammalian brains are capable of assimilating and transferring complex, culturally derived information, both within and across generations. Our deﬁnition allows for the possibility of culture in animals with brains very different from ours. If this is so, we will need to reassess our views of evolution and behavior.
Culture and Genetics in Transmitting Behavior
Behavioral biologists since Darwin have argued that the theory of genetic evolution and natural selection applies to behavior as well as physical traits. If behavioral options exist and have a genetic basis, they claim, then any behavior that confers advantages on its bearer should become more frequent over time—usually a very long time.
Cultural evolution works analogously, but cultural rules, not genes, are the units of transmission. Cultural transmission is directly tied to animal brains in a way that genetic transmission is not. Cultural norms that best compete (by increasing the reproductive success of individuals who adopt them) can spread over time, just as genes do. Suppose, for example, you are in a foreign country and facing a problem. Imagine that you can adopt one of two rules: “Do as you always have done when facing similar problems” or “Look around and adopt the behaviors used by locals.” If the latter rule works better (provides more beneﬁts), and other individuals learn this rule by imitation or through teaching, then cultural evolution will favor the “when in Rome” rule, and that behavior will increase in frequency through time.
Instead of moving through generations as chunks of DNA in cells, cultural rules move from brain to brain. This notion was introduced by Richard Dawkins in The Selfish Gene and recently has been popularized by Susan Blackmore in her fascinating book, The Meme Machine (Oxford University Press, 1999). Whether, following the nomenclature of different investigators, we call these units of information that move across brains “memes,” “cultragens,” or “Icultures,” cultural transmission is inextricably linked to the brain.
Another critical distinction between genetic and cultural evolution is the huge difference in the rates at which they operate. Even when genetic evolution operates quickly, it usually takes hundreds, if not thousands, of generations for a noticeable difference to appear, and tens of thousands of generations before real change takes place. Not so for cultural evolution, which can easily have a huge impact in a handful of generations or even within a lifetime.
When Cultural Evolution Trumps Genetic Evolution
There is another way to understand culture in an evolutionary context: Try to predict when cultural transmission of information should be more likely than genetic transmission of information. When might it benefit an animal—say, a gerbil— to be hardwired with knowledge of the prey that make up its diet, and when might it be better to learn from others what to eat? Evolutionary biologists usually argue that when environments are relatively stable, a fixed means of transferring information—one not reliant on the vagaries of learning from others—will be selected, and genetic transmission will be the dominant influence.
When the environment constantly changes, however, some means of transmitting new rules and innovations—even at the cost of occasional errors—works best. These means give access to information stored in other brains that may have learned a useful new means of handling a problem. The simple logic is that cultural transmission, by enabling one to get information by watching others, spreads a potentially beneficial behavior from brain to brain much faster than is possible by genetic changes.
The connection between cultural transmission and a variable environment ties in remarkably well with Stanford University biologist John Morgan Allman’s ideas on the evolution of more complex (and often larger) brains. Allman argues that environmental variability is a primary force behind the evolution of brains. The more variable the environment, the more important is a brain capable of complicated tasks. Thus the same factor, environmental variability, seems to underlie models of both brain evolution and cultural transmission, a demonstration of the intricate relationship between brain and culture.
There is yet another framework for predicting when cultural transmission should be favored for transferring information. Robert Gibson and Jacob Höglund suggest two scenarios.1 The ﬁrst involves discrimination. Some behaviors are complex. Imagine that the trait in question is choosing a mate. Individuals may need to examine all sorts of information about potential mates, including the choices others are making. Why not have as many tools as possible? Why not call on the knowledge stored in the brains of others? Perhaps their choices can help one ﬁne-tune a sense of who makes a good mate, honing one’s discriminatory skills.2,3 In such cases, cultural transmission should be favored. Of course, the individuals being imitated may know less than the imitators. In that case, the information stored in their brains is not particularly useful, and cultural transmission should not fare well. Other means of transferring information, such as the genetic, may prevail.
The second potential benefit of cultural transmission might involve “opportunity costs”—a concept, common in economics, that refers to the many other options that we must give up when we choose one. In the context of cultural transmission and mate choice, for example, instead of assessing a male for his suitability as a mate, females could have been eating, looking out for predators, or resting. If mate copying enables them to get information faster, by swiping it from the brains of those around them and thus freeing their time for other useful activities, copying should increase in frequency. Once again, however, such beneﬁts must be weighed against the potential of getting incorrect information.
Whether discrimination abilities, opportunity costs, or some other—as yet unknown—beneﬁt drives cultural transmission is a question for research.
The Diets of Rats, the Rain Dances of Chimps
There are hundreds of studies on social learning, spanning behavior from foraging to avoiding predators, from direction ﬁnding to making up after ﬁghts. I will use three examples to demonstrate the power of cultural transmission in animals and how this relates to our understanding of the brain.
Rats and Food
Rats eat what other animals will not. As scavengers, they are continually presented with opportunities to sample new foods. Probably this has been the case for most of the rat’s long evolutionary history; it has been particularly true over the last few millennia, during which humans and rats have had a close, if not pleasant, relationship. Many rat populations essentially subsist on discarded human food. When we add new items to our diet, so may rats. Therein lies the rat’s dilemma. On the one hand, a new food source may be an unexpected bounty. On the other hand, new foods may be dangerous—spoiled or containing elements that are ﬁne for humans but not for rats. New foods may smell so different from anything that rats have encountered that they do not know what to make of them. Here is the ideal environment for social learning.
The work of Jeff Galef, a psychologist at McMaster University, eloquently shows that the effects of social learning and food preference in rats run deep.4 In fact, it starts when rats are still in the womb. Rat fetuses can sense what food their mothers are ingesting; after they are born, the baby rats prefer that food themselves. In other words, rat fetuses learn what to eat from others (their mothers) while still in the womb. This sort of social learning easily meets most reasonable deﬁnitions of cultural transmission. Give a dozen rat mothers a dozen different foods, and the offspring of each will prefer the same one of the dozen foods. The choices and preferences of one group (the mothers) clearly and strongly inﬂuence the choices and preferences of another group (the offspring): cultural transmission.
Cultural transmission is also important in an adult rat’s foraging. In one study, rats were divided into two groups, observers and demonstrators, and the research question was whether observers can learn about a new, distant food source simply by interacting with a demonstrator that has experienced this new addition to its diet. After the rats had lived together in the same cage for a few days, a demonstrator rat was taken to another room, where it was given rat chow ﬂavored with either cocoa or ground cinnamon (given the often stressful life of a lab rat, this was a nice break). The demonstrator was then brought back to its home cage to interact with an observer for 15 minutes, at which time the demonstrator was again removed from the cage. For the next two or more days, the observer rats were given one of the two new foods. Although these rats had no personal experience with either of the novel food mixes, and had not seen the demonstrators eat them, they were more likely to eat the food that their demonstrators had eaten. Rats—more precisely, the brains of rats—are designed to pick up and use information via cultural transmission.
From a brain perspective, we can examine rat cultural transmission and foraging in two ways. At the broadest level, rats nicely ﬁt the Allman model of brain evolution, as well as general models for the evolution of culture. Being scavengers, they face a particularly variable environment when it comes to food, and so we might expect evolution to favor rat brains that can handle this variability. One means by which rats appear to tackle their variable environment is via cultural transmission, tapping into information stored in the brains of other rats, just as models for the evolution of culture predict.
Researchers have also examined which areas of the brain are associated with cultural transmission and foraging in rats. Gordon Winocur studied observer male rats that had lesions in the dorsal hippocampal and dorso-medial thalamic regions of their brains.5 Surprisingly, rats with such lesions learn via cultural transmission as well as control rats do. The catch, however, is that lesioned rats forget what they have learned much faster than rats without this brain damage. We can conclude from this that the power of cultural transmission (which will be stronger the longer acquired information is retained) can be linked in some yet unknown manner to the dorsal hippocampal and dorso-medial thalamic regions. Interestingly, these regions also appear to be associated with spatial and fear learning in rats. For example, in female rats estrogen- and progesterone-related changes in hippocampal circuitry have been linked to skills in spatial learning. Given this, it would be fascinating to examine how such endocrinological changes affect the hippocampal circuitry in relation to culturally transmitted information.
If cultural transmission inﬂuenced foraging rats alone, it might be of some academic interest, but it would scarcely reshape the way we think about animal behavior and about behavior’s relationship to the brain. Actually, however, cultural transmission related to foraging has been observed in cats, dolphins, lions, chimpanzees, coyotes, squirrels, moose, otters, meerkats, crows, and whales. Birds offer a classic example.
In the 1940s, English villagers were becoming increasingly irritated that the foil caps of their milk bottles were being torn off before they could bring in the freshly delivered bottles from their doorsteps. The culprit apparently was Parus caeruleus, as the blue tit is commonly known. J. J. Fisher and Robert Hinde suggested that this new behavior had been discovered by accident by a blue tit that was rewarded with a few sips of milk and that others learned the nifty trick, at least in part, from watching the original milk thief or thieves. By the time the mischief was breaking out all over the United Kingdom, the consensus was that it was a clear case of cultural transmission of a newly acquired feeding habit.
As charming as this story is, and as much as it paints a fair picture of the power of culture to shape animal behavior, the work was neither experimental nor controlled. For a more scientiﬁc study, we turn to the avian equivalent of the rat, Columbia livia, otherwise known as the pigeon. Like rats, pigeons are an ideal species in which to examine the cultural transmission of feeding behavior. Being primarily scavengers and feeding on human garbage, pigeons change their diets according to the ever-fanciful whims of human taste buds. The resulting uncertainty about what new foods will be available, and which of these will be safe, favors the transmission of behavior by paths such as imitation.
Over the last 15 years, Louis LeFebrve and his colleagues at McGill University have done intriguing experiments that attest to the strength of cultural transmission in shaping the diet of the pesky, but malleable pigeon. For example, Boris Palameta and LeFebvre examined cultural transmission in an experiment that again used observer and demonstrator animals.6 The task that observer pigeons needed to master was piercing the red half of a red-and-black piece of paper covering a box. Under the red paper was a bonanza of seeds for the lucky bird who made it that far.
An observer pigeon was placed in an area with such a food box and exposed to one of three scenarios. Some birds saw no demonstrator on the other side of a clear partition; none of them learned how to get at the hidden food. In another group, observers saw a demonstrator eating from a hole that the researchers had made in the paper. This second group of observers did not see the demonstrator solve the hidden food puzzle, although they did see it eating. Here again the observers obtained no useful information from the brains of the demonstrators, and they did not get to the food. But when a pigeon did observe another pigeon both pierce the red side of the paper and eat, it learned how to get food itself.
Like rats, pigeons rely heavily on cultural transmission to get the food they need to make it through the day. As with rat foraging, cultural transmission in the foraging pigeons ﬁts well with the idea that environmental variability (in this case, variability in food sources) selects for increased brain development and perhaps opens the door for cultural transmission.
While I could find no studies that specifically looked at brain activity and cultural transmission of information, in pigeons there is some suggestive evidence from research on hen chicks. In chicks, brain activity has been studied in connection with imprinting, a form of social learning by which the young learn specific information from their parents during a (sometimes narrow) time window. Fwu Shan Sheu and colleagues studied the effect of imprinting on two regions of the chick forebrain: the intermediate and medial part of the hyperstriatum ventrale (IMHV) and the wulst (home to the somatosensory and visual projection areas).7 After the chicks had imprinted, researchers found a significant increase in a neurochemical called MARCKS in the left IMHV but not in the right IMHV. Based on this and other evidence, Sheu and colleagues argue that the left IMHV and the right wulst sections of the brain are fundamental to understanding chick imprinting behavior—and therefore to one aspect of cultural transmission.
Whether or not the same processes, and perhaps similar brain areas, are at work in pigeon foraging remains to be seen. Chick imprinting involves much more than foraging behavior, so it is not clear that we should even expect to find in the pigeon the same kind of similarities between brain and behavior. If there are general areas of the brain consistently associated with imitation, however, perhaps we should. But if the area of the brain at work in cultural transmission is tightly tied to the setting in which culture is expressed (for example, foraging), perhaps we should not. Given that pigeon learning is a favorite subject of many laboratory-based behavioral researchers, and given the increased interest in both brain structure and function and cultural transmission, it seems inevitable that appropriate experiments will be undertaken, probably soon, to answer these questions.
In studies of human personality, no one is surprised to ﬁnd that people’s culture affects their personality. Under certain conditions, this seems to be true for other primates, as well. The best documented case of the cultural transmission of information affecting animal personality is the chimpanzee. In long-term studies of seven African chimp populations, scientists made a list of 65 behaviors that qualiﬁed as “cultural variants,” everything from using leaves as sponges, to picking out bone marrow while eating, to dancing at the start of rainstorms.8 Remarkably, of these 65 behaviors, 39 were present at some locations but utterly absent from others. Variation of this kind could not be genetic, but it is exactly what you would expect to see if cultural transmission were operating.
Nor need you journey to Africa to see it. In zoo and lab populations of chimps, new behaviors arise and spread. For example, in one zoo population studied by Andrew Marshall and his colleagues, frustrated males emit a sound dubbed the “Bronx cheer.” This “tradition” was started by a lone male when he was transferred to the zoo years ago.
Visit any of the seven African chimp populations and watch the animals for years, as scientists did, and you will see relatively stable patterns of innovative behavior spreading within each group. But you will observe very different clusters of culturally derived behaviors across the various groups. The core personality of chimps almost certainly differs dramatically at these seven African sites because of the cultural transmission of behavior. Chimp brains, so similar to human brains, appear to accommodate a wide diversity of cultural behavior—the widest diversity by far that we know in any nonhuman species.
Where might we look in the chimp brain for the basis of culture? That may depend on the context in which cultural transmission is operating (foraging, predation, mating). When it comes to the imitation of speciﬁc movement patterns, we know something about how the human brain is wired. For example, recent MRI work by Marco Iacoboni and colleagues found that two human brain areas—the inferior frontal cortex (opercular region) and the rostral-most region of the right superior parietal lobule—were particularly active during imitation of ﬁnger movements. Future research on chimpanzee brains and the imitation of movement patterns might start by focusing on similar brain regions.
The Interaction of Culture and Genetics
With a basic understanding of both genetic and cultural transmission, we can look now at how they can operate within the same system. If genetic and cultural transmission interact in complicated ways in a creature with a brain as small as a guppy’s, then such interaction may be common indeed among animals.
Recall that cultural transmission happens when female guppies imitate the mate choice that others in their population make. Guppy life is more complicated than that, however; females also have an innate preference for mating with males that have lots of orange body color. Here we have an ideal system in which to examine the relative importance of genetic versus cultural factors in shaping a speciﬁc behavior. In a 1996 experiment in my lab, I did just that. Essentially, I created an evolutionary soap opera. A female guppy’s genetic predisposition was “pulling” her toward a more orange male, but social cues and the potential to copy the choice of others were tugging her in the opposite direction—toward the drabber of two males. When males differed by small amounts of orange, females consistently chose the less orange males because they were copying the choice of a female placed near such a male. Here, culture (the tendency to copy the mate choice of others) overrode a genetic predisposition for orange males. If, however, males differed by large amounts of orange, females ignored the choice of others and preferred more orange males; genetic predisposition masked any cultural effects. In the eyes of female guppies, it is as if a threshold of color exists. Below that threshold, cultural effects predominate in determining the female’s choice of mates; above the threshold, genetic factors predominate.
For a tiny ﬁsh with a tiny brain, the ability to swipe information from the brains of other guppies—and so to override a genetic predisposition—is a powerful dynamic. Yet, with the exception of studies that looked at the processing of various toxins, little work has been done on the guppy brain, making any link between cultural transmission and the brain in this species a matter of conjecture. That said, two points are worth noting. The guppy populations in which cultural transmission has been demonstrated are generally from streams where guppies live in large groups and suffer intense pressure from predators. Both pressure from predators and membership in a large population have been suggested as forces that favor accelerated brain development, which would be needed to deal with those predators and the intricacies of group life.
If, indeed, these forces favor accelerated brain development in guppies (and that is a big “if”), this might set the stage for the cultural transmission we see in guppy mate selection. If so, cultural transmission should be much less common in the mating decisions of guppies that come from streams where group size is small and pressure from predators is weak. This prediction has not been tested in natural populations, but it is highly suggestive that pet-store guppies, which have had little pressure from predators for many generations, appear not to rely on any cultural transmission in choosing mates.
Other indirect evidence linking guppy brains to cultural transmission comes from studies of the guppy’s antipredator behavior. Andrea De Santi and her colleagues have discovered a functional specialization of the left and right sides of the guppy brain that may prove fruitful in the study of guppy culture. When guppies approach a potentially dangerous predator to inspect the threat, they often do so cooperatively. Their strategy, called tit for tat, has imitation built into it. De Santi found that a guppy is much more likely to cooperate during an inspection visit when a predator is in its right ﬁeld of vision. This suggests that different functions in the two sides of a guppy’s brain may be linked with inspection behavior and possibly with its cultural components. Additional research will be needed to determine the speciﬁc brain-behavior link.
Big Brains, Big Cultures?
Any discussion of the evolution of culture is inherently about the brain because cultural transmission is a complex behavioral phenomenon. But what about the relationship between brain size and composition and the distribution of culture in animals? Here the relationship between bird brains and bird culture is illuminating.
Ethologists, behavioral ecologists, and evolutionary biologists have hypothesized a link between forebrain size and cultural transmission. The premise is as follows: Since the forebrain appears to be associated with flexibility of behavior, including social learning, those with larger forebrains should be better learners. There are potential pitfalls in this approach, but it has proved useful in testing the relationship between innovations in foraging and forebrain size in North American and British bird groups.9
Researchers used the many brief reports about various bird species and their habits that had been published in nine ornithology journals to gather data on 322 foraging innovations: 126 in British Isle birds and 196 in North American birds. Innovations ranged from herring gulls “catching small rabbits and killing them by dropping them on rocks or drowning” to common crows “using cars as nutcrackers for palm nuts.” The distribution of innovations like these was examined across different orders of birds. Among North American, British, Australian, and New Zealand bird species, relative forebrain size correlated with foraging innovation: Bird orders containing individuals possessing larger forebrains were more likely to have high incidences of innovation, which are complex inventions that can spread through populations via cultural transmission.
This makes a point that has been repeatedly conﬁrmed: At the broadest level, the simple absence or presence of cultural transmission is not tightly linked (and may not be linked at all) to brain size or complexity. The foundations of cultural transmission are found in animals with brains as simple as the guppy’s and as complicated as the chimp’s. Having said this, I must add that, as we just noted in our discussion of forebrain size in birds, the structural complexity of cultural transmission may show a closer (but far from perfect) relationship with brain complexity.
More complex, diverse animal cultures tend to be found in animals with more specialized brains. For example, the form of cultural transmission we often see in fish—simply copying an existing preference—is fundamentally different from the complex set of 65 cultural variants found in chimps. Chimps are always coming up with new cultural variants, which permeate chimp life in a way that is fundamentally different from the operation of culture in guppies. The bird study on forebrain size seems to fall in the middle. In terms of brains and culture, then, it may be that we will find simple forms of cultural transmission in many different species, which use it to obtain and transfer information with survival value. The complexity of animal culture, however, does not appear to be equally distributed throughout the animal kingdom. The most complex cultures tend to cluster in creatures closest to humans. Whether this broad correlation will hold up when scientists give animal cultural transmission the attention it merits is an open question.
Whenever I settle into a new university, I start exploring other departments in search of compatriot researchers interested in behavior. This often leads me to psychology departments, which is what happened when I arrived at the University of Louisville. As a member of the biology department, I was invited to give a talk to the psychologists and spent an hour showing them slides of the guppy mate-copying work I have described here. Psychologists have a penchant for studying copying behavior in humans, so I thought that I might pick up a few nuggets of insight.
My luncheon seminar led to a collaboration with a social psychologist in which we undertook the first study (to my knowledge) of date copying in humans. Essentially, we asked if a person’s own dating preferences were influenced by learning that someone else found a potential date interesting enough to pursue. We hypothesized that females would be more affected by date copying than males, since females in general tend to be more choosy about their mates than do males. We did find that females relied more heavily on the opinions of other females than males relied on the opinions of other males. Cultural transmission, in other words, was stronger in females.
The most important lesson of this experiment was not the result per se. It was that without the insight gained in studying cultural transmission and mate copying in guppies, the first experiment ever on human cultural transmission and dating would never have taken place. I expect to see this kind of connection more and more often when we start to take animal culture seriously.
A National “Cultural Transmission Project”?
Cultural evolution has had a profound impact on the social fabric of human life, and its effects will surely increase with time. Yet culture is not humanity’s gift to the world; its rudiments exist throughout the animal kingdom. Chimps may not invest in stocks, but the roots of many such complex, culturally based human behaviors can be found in other primates. Guppies will not be appearing on The Dating Game anytime soon, but studying cultural transmission in these ﬁsh has helped us understand our own mating behavior. The zoological work on cultural evolution has revealed strange, even astonishing facts about animals—no matter how large or small their brains, even among some with what we can barely call a brain.
Large orders of magnitude separate the number of scientists sequencing genes from the number studying the evolution of culture, particularly when it comes to the role that the brain plays in animal cultural transmission. Could there be an equivalent of the Human Genome Project for cultural evolution? Right now the answer is a deﬁnitive no, because we have no uniﬁed theory of the biology of culture. But just as sequencing genes can have great importance for improving human life, so too will understanding the evolution of culture. The more we understand why animals do what they do, the more we will understand ourselves.
- Gibson RM, Höglund J. Copying and sexual selection. Trends in Ecology & Evolution 1992;7:229-232.
- Dugatkin LA. The interface between culturally-based preferences and genetic preferences: female mate choice in Poecilia reticulata. Proceedings of The National Academy of Sciences, U.S.A. 1996;93:2770-2773.
- Dugatkin LA. The Imitation Factor: Evolution Beyond the Gene. New York: The Free Press; 2000.
- Galef BG. Social enhancement of food preferences in Norway Rats: a brief review. In: Heyes CM, Galef BG, eds. Social Learning in Animals: The Roots of Culture. London: Academic Press; 1996:49-64.
- Winocur G. Anteretrograde and retrograde amnesia in rats with dorsal hippocampal or dorsomedial thalamic lesions. Behavioral and Brain Research. 1990;38:145-154.
- Palameta B, Lefebvre L. The social transmission of a food-finding technique in pigeons: what is learned? Animal Behaviour. 1985;33:892-896.
- Sheu FS, McCabe BJ, Horn G, Routtenberg A. Learning Selectively Increases Protein-Kinase-C Substrate Phosphorylation in Specific Regions of the Chick Brain. Proceedings of the National Academy of Sciences of the United States of America. 1993;90:27052709.
- Whiten A, Goodall J, McGrew W, et al. Cultures in chimpanzees. Nature. 1999;399:682-685
- Lefebrve L, Whittle P, Lascaris E, Finkelstein A. Feeding innovations and forebrain size in birds. Animal Behavior. 1997;53:549-560.