Table Of ContentReference: Biol. Bull. 202: 2S3-288. (June 20(12)
Self-Organization and Natural Selection in the
Evolution of Complex Despotic Societies
C. K. HEMELRIJK
Department ofInformation Technology andAnthropological Institute and Museum.
University ofZurich. Switzerland
Abstract. Differences between related species are usually side effect of the change of one single trait proper to an
explained as separate adaptations produced by individual se- egalitarian society, in the real world a despotic society may
lection. Idiscussinthispaperhow relatedspecies, whichdiffer alsohave arisen as asideeffectofthe mutation ofasingle trait
in many respects, may evolve by a combination of individual ofan egalitarian species.
selection, self-organization, and group-selection, requiring an Ifgroups withdifferent intensitiesofaggression evolve in
evolutionary adaptation ofonly a single trait. In line with the this way, they will also have different gradients of hierar-
supposed evolution ofdespotic species of macaques, we take chy. When foodis scarce, groups with the steepest hierarchy
as a stalling point an ancestral species that is egalitarian and may have the bestchance to survive, because at leastasmall
mildly aggressive. We suppose it to live in an environment number of individuals in such a group may succeed in
with abundant food and we put the case that, iffood becomes producing offspring, whereas in egalitarian societies every
scarce and more clumped, natural selection at the level ofthe individual is at risk ofbeing insufficiently fed to reproduce.
individual will favor individuals with a more intense aggres- Therefore, intrademic group selection (selection within an
sion (implying, for instance, biting and fierce fighting). interbreeding group) may have contributed to the evolution
Using an individual-centered model, called DomWorld, I of despotic societies.
show whathappenswhen the intensity ofaggression increases.
In DomWorld,grouplifeisrepresentedby artificial individuals Introduction
that live in a homogeneous world. Individuals are extremely
simple: all they do is flock together and, upon meeting one The assumption that evolution occurs through a single
another, they may perform dominance interactions in which evolutionary process is no longer tenable (e.g., see Plotkin
tihneteenfsfietcytsofofawgignrensisnigonanidnltohseinmgoadreelselisf-irnecinrfeoarsceidn,g.aWchoemnpltehxe oa1rn9id9e4s;OdhMlaaivyneng-asSlrmodweleSy,mibt1e9hc81ao)nm,deaSmnzdoartmheumlaatrciycp,leep-1tl9ee9dv5e;(le.Mgsi.et.lteeHcltodigooernfwetahgne,d-
feedback between the hierarchy and spatial structure results; Wilson, 2000). Multiple-level selection processes may in-
via self-organization, this feedback causes the egalitarian so- clude some, or all. of the following factors: the multi-level
ciety to change into a despotic one. The many differences character of biological systems and natural selection oper-
between the two types ofartificial society closely correspond ating on them (Lewontin, 1970; Hogeweg, 1994; Sober and
tothose between despotic and egalitarian macaques in the real Wilson, 1998), self-organization and its consequences for
world. Given that, in the model, the organization changes as a evolution (Boerlijst and Hogeweg, 1991), and nonlinear
genotype-phenotype mappings (Kauffman, 1993; Huynen
E-mail: [email protected] and Hogeweg. 1994; Kauffman. 1995).
This paper was originally presented at a workshop titled The Limits in Within this framework of multiple-level selection theo-
Self-Organization inBiologicalSystems.Theworkshop,whichwasheldat ries, I present in this paper an example ofthe way in which
the J. Erik Jonsson Center ofthe National Academy ofSciences, Woods a certain type of society may evolve. In studies of animal
HfoorleA.dvMaasnscaecdhuSsteutdtise,sfirnotmhe11S-p1a3ceMaLiyfe20S0c1i.enwceassastpothnesoMraerdinbey tBhieolCoegnitcealr behavior, a distinction is usually made between twotypes of
Laboratory, and funded by the National Aeronautics and Space Adminis- societies egalitarian and despotic. In her studies of birds,
tration underCooperative Agreement NCC 2-896. Vehrencamp (1983) distinguishes between these two on the
283
284 C. K. HEMELRIJK
basis of reproductive success. In egalitarian societies, the Dominance Rules Grouping
reproductive success of all female group members is more
or less the same, whereas in despotic ones there is a great
variation in the reproductive success of individual females.
When the terms egalitarian and despotic are used for other
taxa, such as primates, these terms denote their so-called dom-
inance style rather than their reproductive success (Hand, (OJHERSMAXVIEW
1986). Dominance style depends on the gradient of the hier- / ~v~
archy (van Schaik. 1989): despotism signifies that the domi- [ IYES] [NO]
nance hierarchy is steep (which means that there is a great TURN
difference in the success in fighting between individuals); ISEARCH-ANGLEI
egalitarianism implies that the hierarchy is weakly developed.
Furthermore, in primates, particularly ofthe genus macaques, Figure 1. Flow chart fur the behavioral rules ofagents.
these societies differ in a number of other characteristics: in
despotic societies aggression is more unidirectional, social in order to rejoin its group. In this way individuals tend to
behavioriscorrelatedmorestrongly withdominance,grouping remain in a group.
is less cohesive (de Waal and Luttrell. 1989; Thierry, 1990), If, however, an agent sees another agent close by, within
mate choice is more selective, and male migration is more its personal space (PersSpace = 2 or 4). a dominance
frequent (Caldecott, 1986). Whereas each ofthese differences interaction takes place. The likelihood that an agent initiates
between related species is usually explained as a separate an aggressive interaction increases with its chance to defeat
adaptation shapedby individual selection, I proposetoshow in its opponent (Hemelrijk, 2000). The agent's capacity to be
this paper how a despotic species may evolve from an egali- victorious (reflected in its dominance value) depends on
tarian one by a combination of individual selection, self-orga- chance, on its current dominance value (which initially is
nization, and group-selection, involving an evolutionary adap- the same for all individuals), and on the self-reinforcing
tation in one single trait only. effect of the outcome (winning a fight increases the proba-
How individual selection and self-organization may op- bility ofwinning the next one and losing decreases it). This
erate, I will explain with the help of an individual-centered is known as the "winner and loser" effect and has been
model of a group-living species, called "DomWorld" empirically established in many animal species (e.g., see
(Hemelrijk, 1999a,b. 2000). How group selection may favor Chase, 1985). After victory, the dominance value of the
the survival of groups with the steepest hierarchy above victorious agent increases and that of its defeated opponent
groups with weakergradients ofthe hierarchy. I will explain is reduced by the same amount. When, unexpectedly, an
with the help of an ecological model at an evolutionary agent defeats a higher ranking opponent, the dominance
time-scale designed by Ulbrich ct til. ( 1996). values of both opponents are changed by a greater amount
than when an agent conquers, as expected, a lower ranking
opponent(thisresultconforms todetailedbehavioral studies
The Model DomWorld (Dominance World) on bumblebees by Honk and Hogeweg. 1981). In this way
the model allows forrankreversals. Afterafight, the winner
AsummaryofDomWorldmay suffice(foramorecomplete chases the opponent, and the defeated agent flees.
description, see Hemelrijk ( 1999b. 2000)). The model isbased Groups usually consist of8 to 10 individuals. The behav-
ononlyasmall numberofessentialsofsocial life. It represents ior of the agents is analyzed by means of behavioral units
a homogeneous virtual world inhabited by agents that are and statistical methods similar to those used for observing
provided with only two tendencies: to group (right halfofFig. real animals.
1) and to perform dominance interactions (left pail ofFig. 1).
Why agents actually do group (whether this is to avoid pred- Natural Selection and Self-Organization
ators or because resources are clumped) is not specified and
irrelevant to the model. The same holds for dominance inter- Group life of primates (including macaques) is generally
actions. They reflect competition for resources (such as food supposed to have evolved as a protection against predators
and mates), but these resources are not specified. (van Schaik and van Hooff. 1983; van Schaik, 1989). Egali-
When an individual is activated and it does not see tarian primate societies,at least thoseofmacaques, arethought
another agent close by (within its personal space, see Pers- to precede despotic ones evolutionarily (Matsumura, 1999:
Space in Fig. I ), then grouping rules come into effect. It Thierry ct til., 2000). Correspondingly, let us suppose that a
starts looking for others at greater and greater distances group-living egalitarian species lives in an environment in
(Near View = 24 and Max View = 50 units). Ifeven then which food is abundant, and therefore its competition is low
no one else is in sight, it turns over a SearchAngle (Fig. 1 ) and its aggression mild (consisting of, for instance, threats and
EVOLUTION OF COMPLEX DESPOTIC SOCIETIES 285
286 C. K. HEMELRIJK
animals when unfamiliar individuals are put in a group to- Contest Competition
gether, but the decline of aggression has so far never been Food Scarcity
attributed to a widening of the group.) A consequence of the (2)
declineofaggression isthatthehierarchybecomesmore stable
((3) in Fig. 3). Further, because low-ranking individuals flee
fromeveryone else, they end up at the periphery ofthe group;
this automatically leaves the dominants in the center ((5) in FoodAbundance +
Fig. 3). This spatial structuredevelops in spiteofatotal lackof
any preference ofthe individuals to be in the center. Yet such Most DespoticGroups
a preference (a so-called centripetal instinct) is assumed in the with Steepest
"selfish herd" theory by Hamilton (1471). It is supposed to HierarchiesSurvive
have been evolved because individuals are better protected in
the center, where they are shielded on all sides from possible
predators. However, the model shows thateven without such a
centripetal instinct, whenever the hierarchy is steep, we must
expect a spatial structure with dominants in the center.
Spatial centrality, in turn, stahili/.es the hierarchy and
supports its differentiation ((5) and (6) in Fig. 3). This arises
because the spatial structure causes individuals to be close
to partners of similar dominance rank: therefore, ifinciden-
tally a dominance-reversal occurs, it is usually between
individuals that are similar in dominance, and thus the
extent to which dominance values are changed is only a
minor one. In this way, the spatial structure strengthens the
hierarchy ((?) and (6) in Fig. 3). Thisbecomes evident when
we eliminate spatial centrality. We can dothis by decreasing
the SearchAngle. If the SearchAngle for returning to the
group is made smaller, so that individuals return more
slowly and the group therefore spreads out more and more,
no spatial structure develops. In this case (for the same
number of dominance interactions), the hierarchy becomes
weaker (i.e., dominance values differentiate less) than in
cohesive groups (Hemelrijk. 1999a). The steeper hierarchy
in cohesive groups is thus partly due to a feedback rein-
forcement of the hierarchical development under the influ-
ence of spatial structure.
We mayalsoincludethesexesinthe model;forinstance,by
making two classes of individuals that differ in initial domi-
nance value and intensity ofaggression (both are made higher
lor"males" than lor"females"). Unexpectedly, it turns out that
at ahigh intensity ofaggression, femaledominanceovermales
is greater than at a low one. This arises because a stronger
differentiation of the hierarchy causes some females to reach
high dominance and some males to become very low in rank.
Consequently, some females become dominant over some
males. This is of interest, because in comparative studies
between egalitarian macaques (with mild aggression) and des-
potic ones (with tierce aggression). Thierry (1990) notes that
despotic adult females remain dominant over fast-growing
adolescents longer than females in egalitarian species do
(which is in accordance with DomWorld). He attributes this to
astrongercoalitionary tendency among kin-related individuals
in despotic species than in egalitarian ones. DomWorld, how-
ever, shows that greaterfemale dominance may also arise as a
EVOLUTION OF COMPLEX DESPOTIC SOCIETIES 287
model represents, among other things, colony survival, repro- notype and the phenotype). These results of DomWorld may
ductivebehavior,thekindofcompetitionforfood("contest"or alsoberelevanttoresultsofaselectionexperimentwith fishby
"scramble" competition), and feeding behavior. If food is Ruzzante and Doyle (1991. 1993). After two generations of
clumped, it leads to contest competition, whereby dominants selection for speed of growth, an increase in growth speed
get more than subordinates; ifit is scattered and unpredictable, among fish fed on clumped food (leading to intense competi-
everyone gets aboutthe same (so-called scramblecompetition, tion) was accompanied by three effects: a decrease in aggres-
see Nicholson. 1967). Results show that during levels offood siveness,anincreaseindensityofschooling,andan increasein
scarcity, colonies where there is contest competition survive social tolerance. According to the authors, selection for fast
longerthan colonies in which competition is ofthe scrambling growth results in a high threshold for aggression, and this
type.This isaconsequenceofthe steeperdominance hierarchy threshold also genetically influences the other two features of
and, therefore, greatervariety in body-size ofmembers, which social behavior cohesion and social tolerance. These find-
allows a small number of dominant individuals to eat all the ings resemble those from DomWorld; but in DomWorld only
food so that at least some of the females are sufficiently the intensity of aggression is changed "genetically." and all
nourishedtoreachreproductiveage. Inthisway,becausesome other changes of social behavior are mere side effects. Such
individuals in more intensely despotic groups are likely to parsimoniousexplanations may be relevant to many speciesof
survive and reproduce, the group itselfmay survive (although despotic animals that have been studied and possibly even to
the number ofits members decreases during periods ot dimin- plants, where akind ofdespotism is alsodescribed (forastudy
ished food availability). In contrast, in groups with a weaker on a hemiparasite, see Prati et ai, 1997).
hierarchy, food will be distributed more evenly and no single Groupswithdifferentdegreesofintensityofaggression may
individual may reach reproductive success (see also Rypstra. be liabletogroupselection similartothat suggestedforspiders
1993). Thus, severe shortage offood in clumped patches may by Ulbrich et til. ( 1996). Group selection has always been a
result in groupselection in favorofthe most despotic societies controversialissue.Theonly studiesinwhichanyevidencehas
((3) to (4) in Fig. 4). been produced (Bradley. 1999) concern invertebrates (namely,
Note that in macaques, adult males usually migrate from aspeciesofvirus,social spider,andant). However,designating
their natal group to other groups. Therefore, the degree of group selection as a useful explanation for behavior of (non-
despotism in macaques is defined on the basis of the dom- human) primates is usually avoided (Bradley, 1999). Yet.
inance hierarchy among the females. Also, the survival and primates utter alarm calls that, though they are at the expense
extinction of"the group" implies the core group offemales of the fitness of the individual that uses them, may serve to
only, because they are the resident sex. Among such female protect group members (both kin and non-kin). When alarm-
resident core-groups, we may expect that when food is calls are more beneficial for the group than they are costly for
scarce, group selection will lead to better survival of those the individual, they will evolve by group selection, as ex-
groups that have a steeper hierarchy (in accordance with the plained by differential selection among groups for the same
findings in social spiders). trait so-called intrademic group selection (Wilson. 2001).
Computer models show how such an intrademic group selec-
Discussion tion favors altruistic traits, particularly under harsh conditions
(Mitteldorfand Wilson. 2000; Pepper and Smuts. 2000).
Changing only one trait intensity ofaggression in the Similarly, I suggest that group selection may operate on a
model leads to a great number of phenotypic differences at non-altruistic trait, namely intensity of aggression, in primate
the level of the individual and of the group. Thus, by societies in which there is sharp contest competition for food
changing the intensity of aggression in DomWorld, as sug- (during harshconditions). Such strongercompetition leadstoa
gested by the hypothesis for egalitarian and despotic ma- more asymmetrical distribution offood intake, and by guaran-
caques (McKenna. 1979; Thierry. 1985a. b. 1990). we may teeing that at least some individuals ofa group reproduce, aids
switch from an egalitarian society to a despotic one. Inten- group survival (ofthe core group of the resident sex).
sity ofaggression is not the only variable, however, thatcan Note that in the othertransition, fromdespotic societiesto
produce such a cascade of effects. If we increase cohesion egalitarian ones (see Fig. 4). progressively milder aggres-
under one and the same level of intensity of aggression sion would be favored by selection on the level of the
(which must lie somewhere between medium and high individual and the group, because less energy is wasted on
values), the society becomes more despotic in all its char- conflicts. In this case, selection at t'te level ofthe group and
acteristics (Hemelrijk. 1999a). The question of whether the individual will be weak, and self-organization will not
stronger cohesion ofgroups is also accompanied by greater be operative. Thus, a different numi'fr of processes are at
despotism in real primates must be studied empirically. work depending on the direction of t'io transition between
Thus, the model shows how self-organization causes non- egalitarian and despotic societies.
linearity in theconnection between thebehavioral rulesand the The different ways in which selection may act (namely,
observed behavior (which respectively correspond to the ge- on self-organized patterns, and on the level ofthe individual
2X8 C. K. HEMELRUK
and the group) illustrate how we may envision a multiple- Kaut'fman, S. A. 1993. The Origins of Order: Self-organisation and
level selection theory for the creation ofa despotic society. Selection in Evolution. Oxford University Press, New York.
Although, for the sake of clarity in the sketch I have given Lewontin. R. C. 1970. The units ofselection. Anim. Rev. Eeol. S\st. 1:
1-18.
above. I have made individual selection, self-organization, Matsumura. S. 1999. The evolution of 'Egalitarian' and 'Despotic'
and group selection function one after the other, in reality social systems among macaques. Primates 40: 23-31.
they operate mostly simultaneously in different proportions MaynardSmith.J..andE.Szathmary. 1995. TheMajorTransition.*, in
(Lewontin, 1970). Evolution. W. H. Freeman. New York.
McKenna, J. J. 1979. The evolution ofallomothering behavior among
Acknowledgments Colobine monkeys: function and opportunism in evolution. Am. An-
thropol. 81: 818-840.
I thank Rolf Pfeiter and Bob Martin for continuous sup- Mittt-ldorf, J. and D. S. Wilson. 2001). Population viscosity and the
port. I am grateful to Scott Camazine for inviting me to the evolution of altruism. ./. Theor. Biol. 204: 481-496.
workshop on "The Limits to Self-organization in Biological NichSoplrisnotn;,HAa.rbJo.r19S6v7m.p. SQeulafn-ta.djBuisotl.me2n2t:of15p3o-p1u7l3a.tions to change. Cold
Systems," and to Bernard Schmidt and Jens Krause for Pepper,J. W.,and B. B.Smuts. 2000. Theevolution ofcooperation in
making me aware of similarities between DomWorld and anecological context: anagent-basedmodel. Pp.45-76in Dynamic* in
plant and fish communities. This work is partly supported Human anil Primate Societies: Agcnt-hosea1 Mode/ing ofSocial and
by a grant from the A. H. Schultz foundation. SpatialProcesses, T. Kohler and G. Gumerman. eds. Oxford Univer-
sity Press. New York.
Literature Cited Plotkin,H.C.,and F..1.Odling-Smee. 1981. A multiple-level model of
evolution and its implications for sociobiology. Behav. Brain Sci. 4:
Boerlijst,M. C.,and P. Hogeweg. 1991. Self-structuringandselection: 225-268.
spiral wavesasasubstrateforevolution. Pp. 255-276inArtificialLife Prati, D., 1). Matthies,and B. Schmid. 1997. Reciprocal parasitization
II. C. G. Langton, C. Taylor. J. D. Farmer, and S. Rusmussen. edv inRhinanthus serotinus: amodel systemof physiological integrationin
Addison-Wesley, Redwood City, CA. clonal plants. Oiko.s 78: 221-229.
Bradley, B.J. 1999. Levelsofselection, altruism and primate behavior. Ruzzante. D. E., and R. W. Doyle. 1991. Rapid behavioral changes in
Q. Rev. Biol. 74: 171-194. medaka caused by selection for competitive and noneompetitive
Caldecott, J. O. 1986. Mating patterns, societies and ecogeography of growth. Evolution 45: 1436-1946.
macaques. Anini. Behav. 34: 208-220. Ruzzante,D. K.,and R. \V. Doyle. 1993. Evolutionofsocial behaviour
Chase, I. D. 1985. The sequential analysis of aggressive acts during m a resource rich, structured environment: selection experiments with
hierarchy formation: an application of the 'jigsaw' pu/zle approach. medaka. Evolution 47: 456-470.
,4/i/Hi. Behav. 33: 86-100. Rypstra,A. L. 1993. Prey size,socialcompetition,andthedevelopment
de Waal, F. B. M., and L. M. Luttrell. 1989. Towards a comparative ofreproductivedivisionoflaborin social spidergroups.Am. Nat. 142:
socioecology of the genus Macaco: different dominance styles in 868-SXO.
rhesus and stumptuil monkeys. Am. J. Primatol. 19: 83-104. Sober, E., and D. S. Wilson. 1998. Unto Others. Harvard University
Hamilton,W.D. 1971. Geometry fortheselfishherd.J. Theor. Biol 31: Press. Cambridge.
295-311.
Thierry, B. 1985a. Patterns ofagonistic interactions in three species of
Hand..1.L. 1986. Resolutionofsocialconflicts:dominance,egahturianism. macaque (Macaco mulatto, M. fascicu/aris. M. tonkeana}. Aggress.
spheres ofdominance, andgametheory. Q. Rev. Biol. 61: 201-220. Behav. 11: 223-233.
Hemelrijk, C. K. 1990a. A matrix partial correlation test used in inves- Thierry, B. 19851). Social development in three species ofmacaque (Ma-
Hemetlleivgreailtj.ikoJ,n.s(T.o'h.feKor.re.ci1p9Bri9oo0lc1.)i.ty14a3Mn:odd4eo0tl5hs-e4ro2fs0.o.cainadl tiensttesrafcotr.iornecpiaptrtoecrintsy,atunaidgirroeucp- Thieemriatrceyaa,qnnuBi.elat1mi9oa9d,0e.Ml.. fJF.aesecTidhcebuoalracr.kisB,liooMlo..pt1bo4en5tk:weea5ne1an]1.-k5iB2ne1sh.haivp.aPnrdocdeosmsi1n1a:nc8e9:-9t5h.e
Btieohnaavl.a3n9d: o1t0h1e3r-1s0oc2i4a.l interaction patterns at a group level. Anim. Thierry, B., A. N. Iwaniuk, and S. M. Pellis. 2000. The influence ol
Hemelrijk, (.'. K. 1999a. Effects ofcohesiveness on intersexual domi- phytogenyon the social behaviourofmacaques(Primates: Cercopithe-
ennatnitciees.relPapt.io5n2sh4i-p5s34andinsApialtviualncis'tsruicntuArretiafimcoianlgLigfreo.upF-ilftihvinEgurvoipretuaanl Ulbrciicdhae,,Kg.,enJu.sR.MaHceancsoc)h.elE,tFh.olJoelgtysc1h0.6:an7d13C-.7W2i8s.sel. 1996. Modelling
ConferenceonArtificialLife. Vol. 1674.D.Floreano,J-D. Nicoud.and individual variability in asocial spidercolony (Stegodyphusditmieola:
F. Mondada, eds. Springer Verlag, Berlin. Eresidae) in relation to food abundance and its allocation. Proc. 13th
Hemelrijk,C. K. 1999h. An individual-oriented model on theemergence Int. Congr. Arachnol., Geneva, 3-8 Sept. 1995. Rev. SuisseZoo/, vol.
ofdespoticandegalitariansocieties. Prt>c. R. Sue. Lund. B266: 361-369. hors serie: 661-670.
Hemelrijk.C.K.2000. Towardstheintegrationofsocialdominanceand van Schaik. C. P. 1989. The ecology of social relationships amongst
spatial structure. Anim. Behav. 59: 1035-1048. female primates. Pp. 195-218 in Comparative Socioecology, the Be-
Hogeweg. P. 1994. Multi-level evolution: replicators and the evolution liovioiiral Ecology ofHumans and Other Mammals, V. Standen and
ofdiversity. Phyxica D 75: 275-291. G. R. A. Foley, eds. Blackwell. Oxford.
Honk,C.v.,andI'.Hogeweg. 1981. Theontogenyofthesocialstructurein vanSchaik.C.P..andJ. A.R.A.M.vanHooff. 1983. On the ultimate
acaptiveBomhux lerrestrixcolony. Behav. Eeol. Sociohiol. 9: 111-] 19 causes of primate social systems. Behaviour85: 41-117.
Huynen,M.A.,and P. Hogeweg. 1994. Patterngenerationin molecular \ehreiicamp, S. L. 1983. A model for the evolution ofdespotic versus
evolution: exploitation of the variation in RNA landscapes. J. Mol. egalitarian societies. Anim. Behav. 31: 667-682.
Evol. 39: 71-79. Wilson, I). S. 2001. Cooperation and altruism. Pp. 222-231 in Evolu-
K.iiitlin in. S. 1995. At Home in the Universe. The Search for La\vs of tionary Ecology: Concepts and Case Studies. C. W. Fox. D. A. Roff.
CoinplcMt\. Penguin Group. London. and D. J. Fairbairn, eds. Oxford University Press. Oxford.
