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Deborah M. Gordon Because most of the dynamic systems that we design, from machines to governments, are based on hierarchical control, it is dif- ficult to imagine a system in which the parts use only local information and the whole thing directs itself. To explain how biological systems operate without central control — embryos, brains and social- insect colonies are familiar examples — we often fall back on metaphors from our own products, such as blueprints and programmes. But these metaphors don’t correspond to the way a liv- ing system works, with parts linked in regulatory networks that respond to environment and context. Recently, ideas about com- plexity, self-organization, and emergence — when the whole is greater than the sum of its parts — have come into fashion as alternatives for metaphors of control. But such explanations offer only smoke and mirrors, function- ing merely to provide names for what we can’t explain; they elicit for me the same dissatis- faction I feel when a physicist says that a part icle’ s behaviour is caused by the equivalence of two terms in an equation. Perha ps there can be a general theory of complex systems, but it is clear we don’ t have one yet. A better route to understanding the dynamics of apparently self-organizing systems is to focus on the details of specific systems. This will reveal whether there are general laws. I study seed-eating ant colo- nies in the southwestern United States. In each ant colony, the queen is merely an egg-layer , not an authority figure, and no ant directs the behaviour of others. Thus the coordinated behaviour of colonies arises from the ways that workers use local information. If you were the chief executive of an ant colony , you would never let it forage in t he way that harvester ant colonies do. Put down a pile of delicious mixed bird-seed, right next to a foraging trail, and the ants will walk right over it on t heir way to search for buried shreds of seeds 10 metres fur- ther on. This behaviour makes sense only as the outcome of the network of interac- tions that regulates foraging behaviour. Foraging begins early in the morning when a small group of patrollers leave the nest mound, meander around the forag- ing area and eventually return to the nest. A high rate of interactions with returning patrollers is what gets the foragers going, and through chemical signals the patrollers determine the foragers’ direction of travel. Foragers tend to leave in the direction that the patrollers return from; if a patroller can leave and return s afely , without getting blown away by heavy wind or eaten by a horned lizard, then so can a forager. Once foraging begins, the number of ants that are out foraging at any time is regulated by how quickly foragers come back with seeds. Each forager travels away from the nest with a stream of other forag- ers, then leaves the trail to search for food. When it finds a seed, it brings it directly back to the nest. The duration of a forag- ing trip depends largely on how long the forager has to search before it finds food. So the rate at which foragers bring food back to the nest is related to the availability of food that day. Foragers returning from successful trips stimulate others to leave the nest in search of food. But why do foragers walk right past seed baits? We learned recently that during a day, each forager keeps returning to the same patch to search for seeds. Once a forager’s destination for the day is set, apparen tly by the first find of the day, even a small mountain of seeds is not enough to change it. In this system, the success of a forager in one place, returning quickly to the nest with a seed, stimulates another forager to travel to a different place. A good day for foraging in one place usually means a good day everywhere; for example, the morning after a heavy rain, seeds buried in the soil are exposed and c an be found quickly. The regulation of foraging in harvester ants does not use recruitment, in which some individuals lead others to a place with abundant food. Instead, without requiring any ant to assess anything or direct others, a decentralized system of interactions rap- idly tunes the numbers foraging to current food availability. It is difficult to resist the idea that gen- eral principles underlie non-hierarchical systems, such as ant colonies and brains. And because organ- izations without hierarchy are unfamiliar, broad analogies between systems are reassur- ing. But the hope that general principles will explain the regu- lation of all the diverse c omplex dynamical systems that we find in nature, can lead to ig noring anything that doesn’t fit a pre- existing model. When we learn more about the specifics of such systems, we will see where analogies between them are useful and where they break down. An ant colony can be compared to a neural network, but how do colonies and brains, both using interactions among parts that respond only to local stimuli, e ach solve their own distinct set of problems? Life in all its forms is messy, surprising and complicated. Rather than look for p er- fect efficiency, or for another example of the same process observed elsewhere, we should ask how each system manages to work well enough, most of the time, that embryos become recognizable organisms, brains learn and remember, and ants cover the planet. Deborah M. Gordon is i n the Department of Biological Science, Stanford University , Stanford, California 94305-5020, USA. FURTHER READING Gordon, D. M. Ants at Work (W. W. Norton and Co., New York, 2000). Haraway, D. J. Crystals, Fabrics, and Fields: Metaphors of Organicism in Twentieth-Century Developmental Biology (Yale Univ. Press, New Haven, 1976). Lewontin, R. C. The Triple Helix: Gene, Organism and Environment (Harvard Univ. Press, Cambridge, 2000). For other essays in this series, see http:// nature.com/nature/focus/arts/connections/ index.html Control without hierarchy Understanding how particular natu ral systems operate without central control will reveal whether such systems share general properties.     J  .     K     A     P     U     S     T     A     /     I     M     A     G     E     S  .     C     O     M 143 NATURE|Vol 446|8 March 2007       C       O       N       N       E       C       T       I       O       N       S Putting the pieces together ESSAY

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Deborah M. Gordon

Because most of the dynamic systems thatwe design, from machines to governments,are based on hierarchical control, it is dif-ficult to imagine a system in which theparts use only local information and thewhole thing directs itself. To explain how biological systems operate without centralcontrol — embryos, brains and social-insect colonies are familiar examples— we often fall back on metaphors fromour own products, such as blueprints andprogrammes. But these metaphors don’tcorrespond to the way a liv-ing system works, with parts

linked in regulatory networksthat respond to environmentand context.

Recently, ideas about com-plexity, self-organization,and emergence — when thewhole is greater than the sumof its parts — have come intofashion as alternatives formetaphors of control. Butsuch explanations offer only smoke and mirrors, function-ing merely to provide namesfor what we can’t explain; they 

elicit for me the same dissatis-faction I feel when a physicistsays that a particle’s behaviouris caused by the equivalenceof two terms in an equation.Perhaps there can be a general theory of complex systems, but it is clear we don’thave one yet.

A better route to understanding thedynamics of apparently self-organizingsystems is to focus on the details of specificsystems. This will reveal whether there aregeneral laws. I study seed-eating ant colo-nies in the southwestern United States. In

each ant colony, the queen is merely anegg-layer, not an authority figure, and noant directs the behaviour of others. Thusthe coordinated behaviour of coloniesarises from the ways that workers use localinformation.

If you were the chief executive of an antcolony, you would never let it forage in theway that harvester ant colonies do. Putdown a pile of delicious mixed bird-seed,right next to a foraging trail, and the antswill walk right over it on their way to searchfor buried shreds of seeds 10 metres fur-ther on. This behaviour makes sense only 

as the outcome of the network of interac-tions that regulates foraging behaviour.

Foraging begins early in the morningwhen a small group of patrollers leave the

nest mound, meander around the forag-ing area and eventually return to the nest.A high rate of interactions with returningpatrollers is what gets the foragers going,and through chemical signals the patrollersdetermine the foragers’ direction of travel.Foragers tend to leave in the direction thatthe patrollers return from; if a patrollercan leave and return safely, without gettingblown away by heavy wind or eaten by ahorned lizard, then so can a forager.

Once foraging begins, the number of 

ants that are out foraging at any time isregulated by how quickly foragers comeback with seeds. Each forager travels away from the nest with a stream of other forag-ers, then leaves the trail to search for food.When it finds a seed, it brings it directly back to the nest. The duration of a forag-ing trip depends largely on how long theforager has to search before it finds food.

So the rate at which foragers bring foodback to the nest is related to the availability of food that day. Foragers returning fromsuccessful trips stimulate others to leavethe nest in search of food.

But why do foragers walk right past seedbaits? We learned recently that during a day,each forager keeps returning to the samepatch to search for seeds. Once a forager’sdestination for the day is set, apparently by the first find of the day, even a smallmountain of seeds is not enough to changeit. In this system, the success of a foragerin one place, returning quickly to the nest

with a seed, stimulates another forager totravel to a different place. A good day for

foraging in one place usually means a goodday everywhere; for example, the morning

after a heavy rain, seeds buried in the soilare exposed and can be found quickly.

The regulation of foraging in harvesterants does not use recruitment, in whichsome individuals lead others to a place withabundant food. Instead, without requiringany ant to assess anything or direct others,a decentralized system of interactions rap-idly tunes the numbers foraging to currentfood availability.

It is difficult to resist the idea that gen-eral principles underlie non-hierarchical

systems, such as ant coloniesand brains. And because organ-

izations without hierarchy areunfamiliar, broad analogiesbetween systems are reassur-ing. But the hope that generalprinciples will explain the regu-lation of all the diverse complexdynamical systems that we findin nature, can lead to ignoringanything that doesn’t fit a pre-existing model.

When we learn more aboutthe specifics of such systems,we will see where analogiesbetween them are useful and

where they break down. Anant colony can be compared toa neural network, but how docolonies and brains, both usinginteractions among parts that

respond only to local stimuli, each solvetheir own distinct set of problems?

Life in all its forms is messy, surprisingand complicated. Rather than look for per-fect efficiency, or for another example of the same process observed elsewhere, weshould ask how each system manages towork well enough, most of the time, thatembryos become recognizable organisms,

brains learn and remember, and ants coverthe planet. ■

Deborah M. Gordon is in the Department

of Biological Science, Stanford University,

Stanford, California 94305-5020, USA.

FURTHER READINGGordon, D. M. Ants at Work (W. W. Norton and Co., NewYork, 2000).Haraway, D. J. Crystals, Fabrics, and Fields: Metaphors of 

Organicism in Twentieth-Century Developmental Biology 

(Yale Univ. Press, New Haven, 1976).Lewontin, R. C. The Triple Helix: Gene, Organism and

Environment (Harvard Univ. Press, Cambridge, 2000).

For other essays in this series, see http://

nature.com/nature/focus/arts/connections/

index.html

Control without hierarchyUnderstanding how particular natural systems operate without central control will reveal

whether such systems share general properties.

    J .    K    A    P    U    S    T    A    /    I    M    A    G    E    S .    C

    O    M

143

NATURE|Vol 446|8 March 2007

      C

      O      N      N      E      C      T      I      O

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Putting the pieces together

ESSAY