Brainless behavior: a myxomycete chooses a balanced diet.

I t is puzzling that primitive organisms that lack any kind of nervous system show sophisticated behaviors that we assume require a nervous system with some sort of centralized brain or ganglion. Many examples noted in the past belie this assumption and show that organisms without nerves have remarkable behaviors. Perhaps the pioneer in revealing such behaviors was H. S. Jennings (1), who showed many years ago that protozoa such as Paramecium could orient to various environmental cues and even have a primitive kind of learning and memory. This ability has been very much on my mind in my studies on the multicellular migrating cell masses in Dictyostelium, a cellular slime mold. These slugs are a bag of many thousands, or millions, of unicellular amoebae encased in a thin slime sheath. They move in one direction with a front and hind end, and they are oriented by light, by temperature gradients, and by gas (oxygen and ammonia) gradients, which guide them to form fruiting bodies in an optimal spot for the dispersal of their spores. In PNAS, Dussutour et al. (2), working on another kind of slime mold, report an even more advanced and sophisticated behavior that again is achieved without a nervous system. These true slime molds, or myxomycetes, are related only distantly to cellular slime molds (3): Instead of having masses of single cells, they are syncytial. Myxomyetes start off as a uninucleate zygote, and as they grow, feeding on dissolved food, the nuclei continue to divide, but no cell walls are formed; they end up as a very large, glistening multinucleate mass of naked protoplasm called a “plasmodium” (Fig. 1). They are grown easily in the laboratory and live happily on a diet of oats strewn on nonnutrient agar in Petri dishes. It has long been known that these plasmodia seek out patches of food. If a plasmodium is placed on an agar plate some distance from a spot of food, it will send out a spidery network of vein-like avenues in which the protoplasm pulses back and forth, more in one direction that the other, creating and expanding a front. They are attracted to a source of food, and once it is found, they surround it. As Dussutour et al. point out, some previous studies, notably those of Nakagaki et al. (4), have shown that in their food seeking, myxomycete plasmodia can find the shortest, and therefore the most efficient route to their meal through an artificially imposed maze. [Recently the same group has shown that these plasmodia will find and flow to numerous spots of food, also with maximum efficiency (5).] Dussutour et al. (2) begins with the prior knowledge that plasmodia are attracted to food and are clever in getting to it by the most efficient route. The plasmodia not only get to the food, but, if given a choice of different foods—carbohydrates and proteins—and different concentrations of one or the other, or mixtures, they choose what appears to be optimal for their nutrition: They can balance their own diet. In animals, this kind of experiment goes back to the pioneer work of Curt Richter (see ref. 6 for a summary). He began with the observation that if, through surgery or disease, adrenal gland function of a human being was lost, the individual had a great desire for NaCl, which, in fact, was essential to maintain life. The same desire for NaCl was seen in laboratory rats whose adrenals had been surgically removed. This observation led him to ask if a rat would balance its diet if offered a free choice of pure foods such as carbohydrates and proteins. He found that his rats were quite capable of choosing the optimal diet. Although this discovery was followed by some controversy, with many detailed qualifications, the basic idea stands. Rats and human beings, however, have an enormous nervous system with an elaborate brain; the myxomycetes are brainless. As the authors show, myxomycetes, too, can seek out optimal concentrations of food and, even more important, find the optimal ratios of carbohydrates and proteins. In this limited sense, they are as smart as we are. These observations on myxomycetes raise important and fundamental questions: How do they do it? What is the physiological and biochemical mechanism? And, if we find that mechanism, will it tell us anything about the nervous system? My feeling is that there is something fundamental that we have missed, and finding this unknown mechanism will take us on a fascinating journey forward. Fig. 1. The life cycle of the myxomycete Physarum polycephalum. The minute spore germinates (Upper Left), giving rise to a gamete which, depending upon the environmental conditions, is either an amoeba (dry environment) or a flagellated cell (wet environment). After fertilization the zygote grows into a large multinucleate plasmodium that eventually turns into many spore-bearing fruiting bodies. The lower drawings are at low magnifications; the upper ones of the cells are greatlymagnified.DrawingbyMargret LaFarge. (FromBonner JT, 1980 The Evolution of Culture in Animals, p 79; with permission from the Princeton University Press, Princeton, NJ.)