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HOME > PAST ISSUE > May-June 2012 > Article Detail

FEATURE ARTICLE

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

Problems of Miniaturization

2012-05EberhardF3.jpgClick to Enlarge ImageBy focusing on evolutionary increases in brain size, biologists have generally overlooked a basic miniaturization problem that follows from Haller’s Rule: Where can a relatively large brain fit in a small body? In salamanders and fish, for example, the brain is housed within a cavity formed by skull bones. In miniaturized forms, some of these bones are lost or reduced in size, freeing up room for the relatively large brain. Arthropods have external skeletons, which they can deform to some extent to create more internal space. A nymph of the orb-weaving spider, Anapisona simoni, with a body mass of less than 0.005 milligram, appears as a speck of dust to the unaided eye. In these minute orb weavers, nearly 80 percent of the cephalothorax is filled with the brain. To house their relatively large brains, minute spiders (including tiny spiderlings of species with large-bodied adults) have a conspicuous outward bulge in the sternum, which increases the internal volume of the cephalothorax, where brain tissue is housed. In some species of spiders and mites, the relatively large brain takes up so much room that it overflows into the legs, giving new meaning to the phrase “thinking on your feet.”

2012-05EberhardF4.jpgClick to Enlarge ImageIn some groups of tiny insects, such as strepsipterans, the shape of the brain is modified to pack it tightly against internal structures and muscles. Although the “brain” is conventionally construed to be that part of the central nervous system that is housed in the head, some tiny beetles and other insects blur this distinction because they displace some or all of their large brains from the head to the thorax or even to the abdomen. In general the anatomical trade-offs that result from the displacement of other tissues have not been identified, nor have their costs been determined. The design changes imply that some features are sometimes sacrificed to house enlarged central nervous systems in very small animals, which may play a role in setting the lower limits of body size in a given taxon. A minute hooded beetle (Sericoderus; Corylophidae), for example, has fewer muscles in its head and thorax than do larger related beetles. The space taken up by the enlarged brain of a nymph of the jumping spider Phidippus clarus comes at the cost of reduced space for digestive diverticula. In both cases it is likely that there are as yet undetermined costs associated with these changes. If, for instance, it were advantageous for an adult spider to have digestive tissue in the cephalothorax, then a similar design would seem likely to have been advantageous for a nymph if it were not encumbered with a relatively large brain.

Another approach to solving the housing problem would be to reduce neuron size, thus reducing overall brain size while maintaining similar numbers of neurons and the degree of connectivity. The sparse available data suggest, however, that such adjustments are incomplete, and that within any given taxon, smaller animals usually have fewer neurons. Reductions in neuron size are possible, but only to a point. Nobel laureate physicist Richard Feynman discussed general limitations regarding storing and retrieving information at extremely small scales and concluded that “there’s plenty of room at the bottom” when building artificial information-processing systems at nanoscales. In biology, however, neuron-based information-processing systems bottom out at sizes where Feynman just gets going. There is a theoretical lower physical limit on the functional diameter of an axon (about 0.1 micron). Below this size, an axon can no longer transmit reliable information because the signal is swamped by noise from spontaneous depolarizations of the membranes. In addition, the minimum size of a neuron cell body is limited by the size of its nucleus, which in turn is limited by the animal’s genome size. The nucleus comprises up to 80 to 90 percent of the volumes of small neuron cell bodies in tiny insects. One route to miniaturization among arthropods would be to delete chromosomes, pack the chromatin more tightly or eliminate the nucleus, which would permit a smaller neuron. Such modifications had been documented in vertebrates but were unknown in invertebrates until just recently. Alexy Polilov of Lomonosov Moscow State University has shown that most of the neurons of minute parasitic wasps, Megaphragma sp. (Trichogrammatidae), with body lengths of 170 to 200 micrometers, lack nuclei. The pupal central nervous system has about 7,400 nuclei, but near the end of pupal development most neuronal cell bodies break open, or lyse, and lose their nuclei. The adult central nervous system, therefore, has about 7,000 cells without nuclei, and only 339 to 372 cells with nuclei, of which only 179 to 253 are in the brain.

Lysis also is associated with volumetric changes in the nervous system. The pupal brain volume of about 93,600 cubic micrometers decreases to 52,200 cubic micrometers in the adult. In addition, numerous folds are present in the cuticle of the back of the head, the occipital area, and the size of the head capsule in this area is reduced. Remarkably, the central nervous system of M. mymaripenne has orders of magnitude fewer neurons in comparison with other flying insects, such as Musca flies, which have 340,000 neurons. A somewhat larger trichogrammatid wasp, Trichogramma evanescens, for example, has 37,000 neurons in just one part of the brain, the supraesophageal ganglia. Despite their extreme central nervous system modifications, Megaphragma wasps nevertheless perform behavior such as mating, flying, host searching and recognition, although the details have not been studied. The kinds of compensatory mechanisms that enable this behavior with only a greatly reduced number of neurons, most of which lack nuclei, are not known.








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