Price, J.S. (2006) Behavioral ecology as a basic science for evolutionary psychiatry.  Behavioral and Brain Sciences, 29, 420-421.  (Commentary on : Keller MC & Miller G.  (2006) Resolving the paradox of common, harmful, heritable mental disorders: Which evolutionary genetic models work best?  Behavioral & Brain Sciences, 29, 385-452.)

Title:  Behavioral ecology as a basic science for evolutionary psychiatry

Abstract

To the evolutionarily oriented clinical psychiatrist, the discipline of behavioural ecology is a fertile basic science.  Human psychology discusses variation in terms of means, standard deviations, heritabilities, etc., but behavioral ecology deals with mutually incompatible alternative behavioral strategies, the heritable variation being maintained by negative frequency-dependent selection.  I suggest that behavioral ecology should be included in the interdisciplinary dialogue recommended by Keller and Miller.

 ______________________________________

The authors say that the heritability of mental disorders presents a problem for explanations in terms of function, because alleles conferring function should increase in frequency to fixation.  They claim the only satisfactory explanation for the high rate of mental disability is that mental disorders are caused by harmful mutations on hundreds of genes.  This argument restricts the field of evolutionary psychiatry to disorders which are not heritable and do not affect fitness.  However, it is possible that the authors have underestimated the prevalence and robustness of negative frequency-dependent selection .

I would like to draw the authors’ attention to the discipline of behavioural ecology, which is the study of behavior in relation to its function (Krebs & Davies, 1993).  Behavioral ecology could be said to be the basic discipline of evolutionary psychiatry.  It is concerned with strategy sets, which are sets of alternative strategies for dealing with problems.  For instance, the cold weather and reduced food supply of winter present a problem to many species.  Sometimes all members of a species deal with the problem in the same way, but sometimes there are alternative strategies for dealing with the problem.  Many bird species migrate;  in some of these all the individuals migrate, in other species only a proportion migrate and the rest stay where they are.  In very cold winters the rewards of migrating are greater than staying, but in mild winters the rewards of staying are greater.   It is not of great concern to behavioural ecologists just how the decision, to stay or migrate, is made.  It could be entirely genetic, so that a “staying” allele (or group of alleles) is competing with a “migrating” allele.  Or it could be entirely environmental;  for instance, it is thought that in the robin there is competition for territories in the autumn, and those birds who win territories stay and those who fail to win territories migrate.  Probably for most partially migrating species the decision-making mechanism is not known.  Similar considerations may apply to partially hibernating species of rodent;  the territory owners stay awake, and those who do not have territories go to sleep.

Coming closer to evolutionary psychiatry, let us consider the case of pairwise contests.  A rival for mates or other resources poses a problem for the individuals of most species, and various strategies have evolved to deal with it (Boone, 1992;  Crowley, 2003).  Most species have evolved the alternative strategies of escalation and de-escalation.  In territorial species, you either fight or run away.  In group living species, there is an alternative, appeasement, which enables you to continue living in the group, albeit at a lower social rank.  Each strategy has costs and benefits.  Behavioral ecologists such as Maynard Smith have studied the conditions under which alternative strategies could survive (Maynard Smith, 1982;  Parker, 1984;  Reichert, 1998).  Calling the escalating strategy the “hawk” strategy and the de-escalating strategy the “dove” strategy, they concluded that under certain conditions a mixture of hawk and dove is an “evolutionarily stable strategy” (ESS) in that it cannot be infiltrated and replaced by any other strategy, and in particular it cannot be replaced by a pure hawk or a pure dove strategy.  Thus variation in fighting behaviour is an ESS.  The variation is maintained by negative frequency dependent selection, because in a world of hawks it pays to be a dove, and in a world of doves it pays to be a hawk.  It does not matter whether the choice between hawk and dove is genetically or environmentally determined.  Nor does it matter whether the choice is a “once and for all” affair, such that type of parenting or some other variable made an individual hawk or dove, or whether each individual has the capacity to deploy both hawk and dove strategies, the choice depending perhaps on environmental cues or possibly on a random basis.

Both hawk and dove strategies have costs and benefits.  We think on the whole that the costs of being a hawk tend to take the individual to the casualty department, whereas the costs of being a dove take him or her to the psychiatric clinic (Price, Gardner & Erickson, 2004).  In other words, the costs of being a dove represent some of the “mental illness susceptibility alleles” of Keller and Miller.  And since the choice between hawk and dove can be either environmental or genetic, the problem of the partial heritability of the mental disorders does not affect the argument.

Another issue is dispersal.  Many species have both a maintenance phenotype, which is adapted to the natal territory, and a dispersal phenotype, which is adapted to occupying new habitats (Geist, 1989).  As each phenotype becomes rarer its fitness increases, so both are maintained by negative frequency-dependent selection.  During hominid evolution rapid dispersal must have been advantageous, as receding ice-sheets left new land available for occupation.  However, human groups tend to be united by a common belief system which differs from the belief system of all the groups they are competing with.  In order to facilitate dispersal, it may have been advantageous for an individual to undergo a change of belief system and to convert some of the group to the new belief system, and to take them off to a “promised land” (Price & Stevens, 1999;  Stevens & Price, 2000).  Thus two dispersal phenotypes may have evolved:  one is the schizotype who has the capacity to undergo a change of belief system, and one is the suggestible or dissociative person who has the capacity to be converted from the belief system with which he or she was indoctrinated during childhood and to adopt the new belief system of a prophet or cult leader.  The fitness costs of both these dispersal phenotypes would be grievous if dispersal was unsuccessful, but the benefits of successful dispersal might also be very great, leading to an adaptive radiation in a new habitat.  In 45 years of psychiatric practice I have seen many patients labelled schizophrenic who in different circumstances might have become effective cult leaders.

References

Boone, J.L. (1992) Competition, conflict, and development of social hierarchies.  In:  Evolutionary Ecology and Human Behavior, ed. E.A.Smith & B.Winterhalder.: Aldine de Gruyter.

Crowley, P.H. (2003) Origins of behavioural variability: Categorical and discriminative assessments in serial contests.  Animal Behaviour, 66, 427-440.

Geist, V. (1989) Environmentally guided phenotype plasticity in mammals and some of its consequences to theoretical and applied biology.  In: Alternative Life-history Styles of Animals, ed. M.N.Bruton.   Kluwer Academic Publishers. 

Krebs, J.R. & Davies, N.B. (1993) An Introduction to Behavioural Ecology, 3rd edition.    Blackwell Scientific Publications.

Maynard Smith, J. (1982) Evolution and the Theory of Games. Cambridge University Press.

Parker, G.A., (1984) Evolutionarily stable strategies. In: Behavioural  Ecology:  An Evolutionary Approach. Second Edition. ed. J.R.Krebs & N.B.Davies.   Blackwell Scientific Publications.

Price J.S., Gardner, R., Erickson, M. (2004) Can depression, anxiety and somatisation be understood as appeasement displays?  Journal of Affective Disorders, 79, 1-11.

 <htpp://www.johnprice.me.uk/site/default.asp?k=473>

Price, J. & Stevens, A. (1999)   An evolutionary approach to psychiatric disorders:  group splitting and schizophrenia.  In: The Evolution of the Psyche ed. D.Rosen & M.Luebbert.  Greenwood Publishing Group.

<htpp://www.johnprice.me.uk/site/default.asp?k=478>

Reichert, S.E. (1998) Game theory and animal contests.  In: Game Theory and Anmial Behavior ed. L.A.Dugatkin & H.K.Reeve. : Oxford University Press. 

Stevens, A., Price, J. (2000) Prophets, Cults and Madness.   Duckworth.

Acknowledgements

I am indebted to the late Michael Chance and members of his “Birmingham Group”, and to Russell Gardner, Jr., editor of the ASCAP (Across Species Comparisons and Psychopathology) newsletter, and to members of the ASCAP Society for discussion of these ideas.