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Plenty of Room at the Bottom?

Tiny animals solve problems of housing and maintaining oversized brains, shedding new light on nervous-system evolution

William G. Eberhard, William T. Wcislo

Grade-Change Mysteries

Grade changes reflect increases or decreases in the slopes and elevations of brain-body scaling relationships in different taxa. Evolutionary transitions between grades are poorly understood, but are obviously crucial to understanding how nervous systems function and how the diverse array of animal body sizes has evolved. Most previous discussions of grade changes have emphasized evolutionary transitions toward larger body size and more highly encephalized forms, probably due to a general fascination with the possible implications for greater intelligence. The new invertebrate data highlight evolutionary changes in the opposite direction—miniaturization—and the attendant central nervous system design problems at minute body sizes. A grade change can make it possible for much smaller body sizes to evolve than would have been possible if the animals had continued to use the slopes and elevations of brain-body lines from the previous grades. For example, if a 1-milligram animal used the scaling rule used by salamanders, it would have a brain that constituted a prohibitive 20 percent of its body, a proportion that is larger than that of any known animal. Grade shifts suggest that some particular taxa of small-sized animals, such as ants, have apparently solved scaling problems that seemed insuperable for animals of larger-sized taxa, although they do not explain how or why.

The changes in design that are associated with most grade shifts remain to be worked out, but it is likely that they are at least sometimes associated with the evolution of new neural design mechanisms. This can be illustrated by comparing two groups that are extremely different—the neuron-miserly nematodes, and the neuron-profligate vertebrates. The nematode C. elegans has a nervous system with only 302 neurons, and some other nematodes and tiny invertebrates have even lower numbers. Each C. elegans neuron has only about 25 synapses, and the neurons are connected in highly consistent and relatively simple ways.

The contrast between the brain of a nematode and that of a human could hardly be greater. Our brains have astronomical numbers of neurons, an estimated 85,000,000,000; huge numbers of synapses per neuron, such as 10,000 per pyramidal cell in the cortex; and extremely high degrees of connectivity. For example, there are roughly 101,000,000 possible circuits in the human cortex alone, which prompted Nobel laureate Gerald Edelman to describe the human brain as “the jungle in the head.” The functioning of our brain depends on populations of neurons—on the activity patterns in recurrently interconnected populations of neurons—rather than on the activity of individual cells. The activity of individual neurons is neither consistent nor useful in processing information, and patterned activity of neuronal populations can emerge in alternative ways from different subsets of the population. A single dysfunctional neuron can thus be inconsequential for a vertebrate but catastrophic for a nematode. The loss of one particular neuron in C. elegans, for instance, brings evolutionary fitness to zero because it leaves females unable to lay eggs.

2012-05EberhardF7.jpgClick to Enlarge ImageThe striking visual resemblance between the circuits on a computer chip and a wiring diagram of nerve fibers in the ventral nerve cord of a nematode draws attention to the computer-like traits of a nematode’s nervous system, with its fixed number of neurons with invariant connections. This design stands in contrast to the decidedly noncomputer-like traits of vertebrate nervous systems. The processes by which these two extreme types of nervous systems are built up as an organism grows are also strikingly different. Growth of the vertebrate nervous system is characterized by an extraordinary overproduction of neurons in young stages, followed by selective pruning of inactive neurons and synapses. The extent to which neurons die during development varies among, and within, species. For example, the percentage of retinal ganglion cells that die during development varies from 80 percent in cats to 60 to 70 percent in rats, mice, rhesus monkeys and humans, and to approximately 40 percent in chickens and amphibians. Selective pruning of neurons in nematodes is, on the other hand, nearly nonexistent. In C. elegans a total of 8 of 310 neurons, 2.6 percent, are discarded as the animal matures, and they are always exactly the same cells, resulting in the 302 neurons of the adult hermaphrodite; there is no indication that use or disuse is a factor influencing cell death. Similarly, a second instar spiderling and an adult of the orb weaver Argiope aurantia have approximately the same number of neuronal cells, despite an approximately 24-fold difference in total brain volume. Such extreme contrasts raise the possibility that nervous system function differs profoundly in different parts of the animal kingdom, in contrast to the generality of much of biochemistry, molecular genetics and molecular development. The miserly design typified by nematodes may represent adaptations that permitted the evolution of miniature body sizes.

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