the adaptive value of maladaptive behavior, or you've got to be stupid in order to be smart

The Adaptive Value of Maladaptive Behavior, or You've Got to be Stupid in Order to be Smart

Irwin S. Bernstein Department of Psychology, University of Georgia, Athens, and The Yerkes Regional Primate Research Center of Emory University

The genetic contribution to primate behavior may include a predisposition to vary responses to the same stimuli. Such variability produces a mix of " e r roneous" responses to stimuli, but such errors may serve to monitor change in contingencies in the environment. Social relationships are to be regarded as a consequence of monitoring and adapting to a changing social environment rather than as direct consequences of genetic fitness strategies. Primate social behavior represents a much greater degree of fine tuning to specific partners and contexts than could be obtained through genetic pro- gramming. Specific responses may serve to produce information and should not necessarily be regarded as op- timum solutions to a particular problem. It may be the ability to vary responses and modify behavior that is selected for rather than a particular response itself.

Key Words: Primates ; Optimality theory; Social behavior.

The study of any phenomena begins with description. One must begin by describing what is being studied. So it is with behavior, but the de- scriptive phase is often rapidly overshadowed by "why" questions. Social scientists often ex- amine the events immediately preceding behavior, searching for the stimuli that elicit specific responses. When such stimuli are identified, they ask how specific stimuli came to be linked to particular responses. The history of the individual is examined to see when the first links appeared and under what conditions. This ontogenetic approach examines the interaction of learning and modifications of responses to stim-

Accepted April 9, 1984. Address reprint requests to: Irwin S. Bernstein, Depart-

ment of Psychology, University of Georgia, Athens, GA 306O2.

Ethology and Sociobiology 5:297-303 (1984) © Elsevier Science Publishing Co., Inc., 1984 52 Vanderbilt Ave., New York, New York 10017

uli as a function of the outcomes of responses (reinforcement) with the maturation of genetic factors that influence behavior, thus introducing the famous nature-nuture question in development.

Biologists have asked evolutionary questions concerning the genetic contributions to behavior. They have focused on the function of such responses in terms of consequences influencing genetic fitness and they have searched for the evolutionary mechanisms that result in selection for certain genetic inputs to behavior.

Sociobiology has focused attention on the evolutionary causes of behavior, and functional consequences, and has tried to apply evolutionary selection theory to behavior, in attempts both to predict and explain behavior. Whereas many neophyte sociobiologists simplified the principles of sociobiology in a reduction ad ab- surdum and used the sloppy language of meta- phor as description, more sophisticated sociobiologists have decried such practices and plead for recognition of the complexity of questions regarding the "why" of behavior. No single focus on one aspect of the why of behavior, be it evolutionary influences or life experiences, will ever explain all of what an organism does. The recent book, Current Problems in Socio- biology, edited by the King's College Socio- biology Group from Cambridge (1982), reviews many of the pitfalls in naive sociobiological theo- rizing and nicely demonstrates the steady ad- vance and increasing sophistication of sociobiology.

PITFALLS IN SOCIOBIOLOGY

The first naive assumption is often that whatever we see must be adaptive. Thelma Rowell (1979)

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298 Irwin S. Bernstein

warned us of the pitfalls of such an assumption, and Peter Jarman (1982) repeats that warning. The fallacious argument goes something like this: After millions of years (an infinity to us) organisms must be perfectly adapted to their natural habitats. Behavior in the laboratory may not be adaptive, but it must be in the wild, or it would have been selected against and elimi- nated. The assumption is that organisms are optimally adapted. The hidden premises to support such an argument include:

1. All attributes are primarily influenced by genes; all mutations are possible and all possible mutations have occurred in time (or worse, that they occur on demand).

2. Selective pressures in the natural habitat are constant. (If we say that once upon a time, long long ago, there was an ice age, this is clearly a fairy tale about a temporary aber- ration, or at best accounts for fossils where no present population exists.) The "natural habitat" is always assumed to be preserved in nature.

3. Random processes, alleles lost due to bottle- necks, crashing populations and such "ac- cidents ," and alleles fixed due to founder ef- fects, and other statistical or random processes, represent an inconsequential fo rce - - tha t is, given enough time, random processes always cancel.

In fact, mutations do not occur on demand, environments are not static and predictable, and E. A. Thompson (1982) demonstrates that structural selection (due to population fluctuations) may be a more powerful force than natural selection with regard to gene loss and fixation. Thompson argues convincingly that mutations occurring during periods of rapid population increase are much more likely to be preserved in the population than mutations that occur during population declines or crashes. Small differential influences on genetic fitness due to these mutations will be completely overshadowed by mortalities and reproductive success reflecting structural population changes in " r " selected populations.

Jarman (1982) suggests that the methodology used in applying sociobiological theory often promotes considerable circularity. A common method is:

1. Use experience and intuition to discover correlations (induction).

2. Measure the correlations. 3. Use imagination to concoct a plausible evo-

lutionary story to account for these correlations.

This method begins with the usual first step in science; use experience, search the literature and conduct pilot work so as to induce possible relationships between variables. Once the process of induction has led to theoretical explanations involving causality (something never to be proven scientifically), the next step is to use deductive logic to produce an experimental hypothesis predicting the result of a specific ma- nipulation. Returning to pilot data to measure correlations that you have already observed only confirms that your inductions were due to a regularity in your past experience. Accounting for this regularity in the past may be very satisfying, but the degree of satisfaction is not a proof; in fact it is what E. O. Wilson (1975) calls the fal- lacy of "affirming the consequent ." Nonethe- less, many budding sociobiologists survey the literature, offer an explanation for what they have found, and rest content that the +'literature" proves that what their theory predicts has in fact occurred and that their theory is therefore supported.

Dunbar (1982) states flatly that most predic- tions in sociobiology are postdictions, historical +explanations in disguise. Bateson (1982) reminds us of the principle of equif inal i ty-- that there is more than one path to a solution, or more than one solution to a problem. Dunbar (1982) and Bertram (1982) each warn that due to our mental ingenuity we often have an excess rather than a dearth of explanations.

OPTIMIZATION AND VARIANCE

When we look at behavior, our view is usually cross sectional. We cannot expect any moment in time to be an example of an animal maximizing fitness. Life history strategies are selected rather than individual acts. In fact, D.I. Rubenstein (1982) argues, convincingly, that rather than always maximizing average fitness, increasing or decreasing the variance of payoffs according to conditions, may be crucial. Since reproductive success is likely to be a sigmoid, or other non- linear, function of resources, an individual must respond not only to payoffs under average conditions but also to the variance. If monkeys find

The Adaptive Value of Maladaptive Behavior 299

a habitat where the average monthly food supply is incredibly rich, but the variance is such that there is one month when there is no food . . . .

Rubenstein 's argument, of course, is not based on the variance in payoff over time for the same individual but considers the consequences of variance in payoff over all individuals exer- cising the same options (strategies). If the relationship between resources obtained and genetic fitness were linear, than a variance of l unit in resource acquisition in either direction would produce the same change in genetic fitness, al- beit positive in one case and negative in the other. In the case where a curvilinear relationship applies, however, where the curve is con- vex, an increase of one unit in resources obtained will produce a small increment in genetic fitness, whereas a decrement of one unit in resources obtained will produce a large decrement in genetic fitness. A minimization of variance is thus desirable. On the other hand, the relationships are reversed at points where the curve is concave and a maximization of variance is desirable.

If one considers a population where the adults are successfully breeding at a rate close to biological capacity, there is little reason for an individual to risk change. No improvement in resources is likely to improve genetic fitness. On the other hand, juveniles, or adults in a population that has exceeded carrying capacity, may engage in much riskier behavior, such as dis- persal, since failure to find suitable new habitat will result in little loss, whereas success may improve genetic fitness enormously. If the mean increase in resources to be expected from strategy A is one unit with very little variance, whereas the mean increase in resources for strategy B is less, but the variance is much greater, the mean change in genetic fitness may be greater with strategy B if the population is at the concave portion of the curve relating genetic fitness to resources obtained.

How can an individual 's behavior be selected for fine tuning to particular environmental conditions? An individual may start with broad pre- dispositions which are fine tuned by life experiences. Marler (1982) has made exactly this point with regard to avian and primate communication behavior.

OPTIMIZATION AND EXPLORATION

There is no question that there is a genetic input to behavior. There is no question that behavior

can influence survival and reproduction, and that selective pressures can therefore operate on individuals as a consequence of their behavior. There is no question that certain behavior patterns are far more efficient than others in im- proving an individual 's genetic fitness and may therefore be "optimal strategies" for maximizing genetic fitness. The question then is why is behavior often so inefficient and why are organisms apparently so "s tup id" with regard to what would most enhance their genetic fitness?

As a psychologist I began my study of behavior looking at responses at particular instants in time. I wondered why the very smartest animals persisted in making errors on the simplest learning tasks. Even after a thousand trials, a monkey will choose the nonrewarded blue circle over the red triangle on 10%-15% of trials. Why isn't it "optimizing its foraging strategy" and why does it waste energy with unreinforced responses?

Moreover, I found that monkeys in their natural habitats were often wasteful and inefficient. I could see this inefficiency in field and laboratory, because I knew where the food reward was, or because I can, after the fact, calculate more efficient activity patterns in the wild. If environments never changed, if we could sub- stitute hindsight for foresight, and if psychologists were 100% consistent, then a particular action would always be best. But if environments are not static, and if devious psychologists start putting larger quantities of more preferred foods under previously unrewarded stimuli, how is a poor monkey to know?

In fact, a monkey must make "e r ro r s" in order to detect change. " E r r o r s " are only a way of monitoring the environment, a form of exploration, if you wish. Rubenstein (1982) indicates that under the worst conditions, riskier behavior is favored. When times are good, conservative behavior pays off best, but it is precisely when conditions change that specialists, with near per- fect solutions to life's problems, find themselves most disadvantaged. An opportunistic species must constantly explore alternatives in order to - discover new opportunities. In the process of exploration, many "e r ro r s" are repeated and mis- takes are made, but there are few alternatives to such exploration in acquiring information about a changing environment.

Sackett (1971) long ago indicated that in order for an organism to learn anything new, it must


first inhibit its typical or initial response tendency. If an organism is to be able to fine tune its adjustment to its particular momentary life con- dition, and to take full advantage of its ability to modify behavior, to learn, it must make mis- takes; it must be able to inhibit any "genetic" tendency to respond in a specific fashion to a specific stimulus. The more variable the organism's responses to stimuli, the greater are its opportunities to discover the full range of reinforcement contingencies operating.

Primates, with the greatest ability to learn, therefore should show the lowest percentage of "optimally adaptive" behavior in individual situations, by this logic. On the other hand, organisms that show neither genetic variance nor variable behavior are not responsive to selective pressures that would favor the utilization of an alternate behavioral pattern and, by this argument, should also rarely, if ever, show optimal patterns maximizing genetic fitness. It is variability in behavior itself that can be adaptive, and the variance in payoffs may preclude the fixation of activities which are, in the average situation, those with the greatest payoff.

Simpson (1949, p. 61) has forcefully stated that in evolution "what can happen usually does h a p p e n . . , the course of evolution follows op- portunity rather than plan." Kummer (1971, p. 99) eloquently reminds us that "Discussions of adaptiveness sometimes leave us with the impression that every trait observed in a species must by definition be ideally adaptive, whereas all we can say with certainty is that it must be tolerable, since it did not lead to extinction. Ev- olution, after all, is not sorcery." There are so many chance factors operating in the production of new genotypes, and so many chance factors operating in evolutionary processes, that if we were to begin all over again, it is hardly likely that the same species we see in the world today would appear again. One need go no further than the present moment to realize that the diversity. of life forms in the world today reflects not only habitats but geography. Malagasy, Australian, South American, and Asian habitats support vastly different fauna and flora more as a function of geographic isolation than as a function of differences in climate, soils, and topography.

Then why is it that when we deal with species and individuals we expect organisms in their behavior to do that which would "optimally max- imize" their genetic fitness?

SIX QUESTIONS RELATING TO AGONISTIC BEHAVIOR

When the idea for the present symposium was first presented, each of the participants was asked to consider six questions, relating dominance, aggression, reproductive success, recip- rocation, and kinship. By posing such questions we undoubtedly expected to find answers. We can rationalize, argue, advocate, implore, and beseech one another to accept a particular explanation or scenario, when the truth may well be that there are no answers to these questions.

How Is Dominance Status Correlated with Reproductive Success?

The literature on the function of dominance status and aggression has expanded enormously in the last 10 years. In 1974, Tom Gordon and I published an article arguing that aggression was not simply a destructive social force but that it served many social functions as well (Bernstein and Gordon 1974). In 1981, I published an article reviewing the concept of dominance and the functions it might serve, and found that functional considerations were so central to the issue that it was difficult to separate descriptions of dominance from theories regarding its function (Bernstein 1981). Despite this theoretical entan, glement of structure and function, it is possible that dominance status may not influence reproductive success. Dominance relationships may exist, ranks may or may not exist, but since dominance is not a permanent attribute of an individual, and changes, not only with age, but with the social context in which individuals find themselves, it is possible that there is little cor- relation between mechanisms that minimize costs of aggressive competition between individuals and the reproductive success associated with individuals utilizing one of these mechanisms at a particular moment during their lives. If dominance is age related, then individual dominance will vary over a lifetime. One cannot se- lect for 8 year olds and expect to change the frequency of replicators for "8-year-oldness." If dominance is not an attribute of the individual, but a consequence of other attributes in relationship to others in the population, then these attributes and not dominance may be selected for. It remains to be seen if rank allows you to predict any aspect of an individual's behavior, in different groups or in groups of various sizes.


Moreover, what happened when a group is com- posed entirely of alpha individuals from different groups? Do they all become alpha or is only one alpha and another actually an omega?

Is There a Fundamental Difference in the Behavioral Repertoires Used in Agonistic Interactions with Kin Compared to Nonkin, Particularly with Respect to the Intensity of Behavior and Duration of Interaction?

It is possible that many individuals do not rec- ognize kin very precisely, especially males who leave their natal groups. Whereas agonistic behavior may be influenced by familiarity with an opponent, and by a past history of interactions with that opponent, and whereas such familiarity may correlate with kinship to some degree, there need be no proximal or distal causal relationship between kinship per se and agonistic expression. Fighting may be viewed as a maximum escala- tion of competitive conflicts, and the energetic cost, increased predator vulnerability, and risk of injury and death may be sufficient to allow for selection to favor alternative means of con- flict resolution, where possible, regardless of the genetic mix of an opponent. A history of past interactions may regulate dominance and agonistic expression and, in animals with long periods of biological dependency, kin will have long his- tories of past association, but looking for natural selection to modify agonistic expression on the basis of degree of gene~i¢ consanguinity is to confuse function with cause.a~l evolution.

Sociobiologists are very keen on the problem of altruism and look for kinship explanations as a solution, Even reciprocal altruism may be en- hanced by kinship, but reciprocal altruism, like mutualism, may be advantageous without regard to kinship.

What Are the Probable Mechanisms Involved in the Formation of Reciprocal Agonistic Aiding Relationships?

Nagel (1979) and Kummer (1971) have both stressed the social specializations of the primates indicating that this order has few other ecological specializations. Joint action on the environment has been crucial to success and is a widespread characteristic of primates. Nagel indicates that primate social behavior can be di- vided into those patterns reflecting joint action

and those patterns that establish social relationships that make such joint action possible and predictable. Social patterns that establish and maintain social relationships may be seen as in some way the proximal cause or enabling mechanism behind joint action on the environment. If the establishment of social bonds is strongly influenced by ontogeny, then there may be strong correlations with kinship, as several au- thors have demonstrated. Yet it is the individuals who benefit immediately and directly in joint action on the environment. Reinforcements are immediate and proximal and distal causes need not necessarily be contingent upon the genetic similarities of interacting individuals. "Joint action on the environment" in a social species will surely include the social environment, and primates may be expected to use their primary ecological specialization--sociality and joint action--in dealing with environmental problems, including those posed by active con- specifics. Agonistic aiding relationships, coali- tions, may therefore be seen as an example of joint action on the social environment. It may be regarded as a specific case where the social specialization of primates results in two or more individuals responding to an environmental challenge. Inasmuch as primates are social animals, it may be possible to respond to the social environment itself with the same joint action patterns useful in dealing with any environmental challenge. The formation of reciprocal agonistic aiding relationships is, therefore, a specific case involving a more general mechanism.

What Behavioral Strategies Are Correlated with Success in the Acquisition of Material Resources?

The social specialization of the primates de- scribed in answer to the previous question has been suggested to be the primary ecological specialization of the primates. As Kummer puts it, "Nonsocial ecological techniques are poorly de- veloped in primates. Their specialization must be sought in the way they act as groups" (Kum- mer 1971, p. 38).

What Roles Do Time and Energy Conservation Play in Agonistic Interactions?

Much as genes may set the limits on the phen- otype, time and energy limits how much of a


behavior pattern an individual can exhibit. Agonistic behavior is certainly potentially costly energetically and may consume considerable time. The same is true of play, and yet no one really believes that play and exploration are maximally efficient operations in providing whatever functional benefits accrue to participants. Agonistic behavior, as a social behavior, operates in situations where the willingness of the opponent to invest time and energy, as well as the abilities of the opponent, will strongly influence the optimal strategy for an individual in an encounter. Since this is based on the relationships between the participants rather than the absolute attributes of each, and since there will surely be ontogenetic variation from birth to old age, it is difficult to see how genetic mechanisms could fine tune the agonistic expression of an individual in each encounter, although certainly there will be absolute genetic constraints on expressions, time and energy investment. Perhaps even the ability to assess, choose, learn, and remember which patterns worked best with which opponents may be genetic, but the specific choice of activity in the behaviorally malle- able primates is hardly likely to be rigidly ge- netically controlled. Many responses in an agonistic exchange probably serve primarily to assess the ability and willingness of an opponent to escalate and continue the encounter.

How Do Individuals of Different Dominance Rank, Age, and Sex Deal with the Same Agonistic Situation?

Variably, to be sure, and perhaps no more so than individuals of the s a m e age- sex and dominance ranks; ontogenetic factors and particular life experiences will surely have enormous influences on the behavior of an individual. Age and sex are powerful variables. Dominance relationships may influence agonistic expressions, but dominance ranks may be meaningless out- side of a particular theoretical framework. I have already argued elsewhere that many measures and tests of dominance and dominance ranks preclude falsification of the hypothesis and are imposed on the data (Bernstein 1981). Relation- ships and ranks are not one and the same, and no universal agreement on either definition or measure exists.

CONCLUSION

Nevertheless, these can all be important empirical questions. I have attacked each question only to ensure that no preconceived notions will leap forth as if they were empirical data to answer the question. Evolutionary biology is a powerful organizer of material. Social scientists have often neglected evolutionary concepts, barely acknowledged ontogenetic concepts, looked at functional consequents only in terms of immediate or learning outcomes, and concen- trated heavily on proximal causes. Evolutionary considerations must be included in any balanced approach to questions in biology and behavior, but looking for an evolutionary explanation for every detail of behavior is just as myopic as the early "s t imulus-response" psychologists who examined stimuli in exquisite detail in order to explain the specific responses which they elic- ited. The "ul t imate" concerns should not be our sole concerns. The crucial word is b a l a n c e .

Behavior must be understood in complete contexts. It must be seen as a continuous on- going chain. Hereditary influences will interact with experience in ontogeny to link particular activities to particular proximal "causes" and, to the extent that the past is our best predictor of the future, we may analyze behavior in terms of functional ou tcomesmbut predicting consequences will always be imperfect in a less than perfectly determined w o r l d R a n d no b e h a v i o r - - no matter how rigorously selected for in the pas t - -wi l l always have an adaptive future consequence.

There are no "shor tcu ts" or "more important" aspects. Nothing should simply be accepted as intuitively obvious. There is little room in science for advocates who will debate, selec- tively marshall evidence, and refuse to consider tests of hypotheses that include the possibility of falsif icat ion--reject ion and/or acceptance of a null hypothesis that states that there is n o ev-

i d e n c e that a relationship exists between a particular independent and a particular dependent variable. We cannot assume that everything we see is adapt ive- - regardless of how plausible our explanation. Plausible explanations are not data. Of course we can never prove the null hypothesis, that a behavior pattern is n o t adaptive, but in the absence of evidence that it is, we accept the null until such time as contrary data are pro- duced. We demand evidence to reject a null hy-


pothesis, not explanations for why such evidence is not forthcoming. Perhaps it is a very conservative position, but I still believe that ex- plaining a failure to produce evidence is not evidence.

REFERENCES

Bateson, P.P.G. Behavioural development and evolutionary processes. In Current Problems in Socio- biology, Cambridge Kings College Sociobiology Group (Eds.). Cambridge: Cambridge University Press, 1982, pp. 133-152.

Bernstein, I.S. Dominance: The baby and the bath- water. The Behavioral and Brain Sciences 4: 419- 457 (1981).

- - - , Gordon, T.P. The function of aggression in primate societies. American Scientist 62:304-311 (1974).

Bertram, B.C.R. Problems with altruism. In Current Problems in Sociobiology, Cambridge Kings Col- lege Sociobiology Group (Eds.). Cambridge: Cam- bridge University Press, 1982, pp. 251-268.

Dunbar, R. I. M. Adaptation, fitness and the evolutionary tautology. In Current Problems in Socio- biology, Cambridge Kings College Sociobiology Group (Eds.). Cambridge: Cambridge University Press, 1982, pp 9-28.

Jarman, P.J. Prospects for interspecific comparison in sociobioiogy. In Current Problems in Sociobiology, Cambridge Kings College Sociobiology Group (Eds.). Cambridge: Cambridge University Press, 1982, pp. 323-342.

Kummer, H. Primate Societies. Group Techniques of Ecological Adaptation. Chicago: Aldine-Atherton, 1971.

Marler, P.R. Avian and primate communication: The problem of natural categories. Neuroscience and Biobehavioral Reviews 6:87-94 (1982).

Nage !, U. On describing primate groups as systems: the concept of ecosocial behaviour. In Primate Ecology and Human Origins; I.S. Bernstein and E.O. Smith (Eds.). New York: Garland STPM Press, 1979, pp. 313-339.

Rowell, T. How would we know if social organization were not adaptive? In Primate Ecology and Human Origins, I.S. Bernstein and E.O. Smith (Eds.). New York: Garland STPM Press, 1979 pp. 1-22.

Rubenstein, D.I. Risk, uncertainty and evolutionary strategies. In Current Problems in Sociobiology, Cambridge Kings College Sociobiology Group (Eds.). Cambridge: Cambridge University Press, 1982, pp. 91-112.

Sackett, G.P. Unlearned responses, differential rear- ing experiences and the development of social at- tachments by rhesus monkeys. In Advances in Pri- mate Behavior, L.A. Rosenblum (Ed.). New York: Academic, 1970, pp. 11 !-140.

Simpson, G.G. The Meaning of Evolution. A study of the History of Life and its Significance. New Haven, CT: Yale University Press, 1949.

Thompson, E.A. Gene competition with selection. In Current Problems in Sociobiology, Cambridge Kings College Sociobiology Group (Eds.). Cam- bridge: Cambridge University Press, 1982, pp. 111- 132.

Wilson, E.O. Sociobiology: The New Synthesis. Cam- bridge, MA: Harvard University Press, 1975.

the adaptive value of maladaptive behavior, or you've got to be stupid in order to be smart

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