Plenty of Room at the Bottom?
Tiny animals solve problems of housing and maintaining oversized brains, shedding new light on nervous-system evolution
Problems associated with miniaturization are much more general than they might first appear. In addition to the many species with miniaturized adults, there are many more species with moderate-sized adults that have very small, free-living, immature stages. A mature female of the giant golden-orb-weaver Nephila clavipes weighs on the order of 2,000 milligrams, for example, but each of her newly emerged spiderlings weighs only 0.7 milligram and has tell-tale adjustments to small size, including extensions of its brain into a bulging sternum and into its legs. The ecological problems relating to energy intake and expenditure of smaller, young individuals are likely to be different from those of larger conspecific adults. Because of their higher metabolic costs, smaller animals may be more likely to be living on the edge of energetic limitations and less buffered against temporary food shortages. An increased susceptibility to unfavorable energy balances could have significant biological repercussions, such as limiting an animal’s geographic distribution or its ability to survive food shortages or other stresses, and might select for alternative ecological strategies. Parasitic wasps (Hymenoptera) that use insect eggs as hosts are among the smallest known adult insects, perhaps because their larvae hatch into a host environment that contains all the necessary nutrients, thus permitting greatly reduced egg sizes and lower energy reserves.
Small immature stages of species may represent the leading edge of evolutionary innovations to solve size-related physiological problems as a lineage evolves toward smaller body size. Are grade changes associated with innovations that result in energetic efficiencies in the central nervous system? For instance, weevils have a low allometric brain-body line compared with many other insects. Are there economies of design that make their nervous systems more efficient in generating behavioral abilities? And are these efficiencies associated with the evolutionary and ecological success of weevils, one of the most speciose taxa of all animals? Answers to such questions are unknown, in part because they are rarely asked. We agree with Princeton biologist John Bonner, who emphasizes in a recent book that “size matters” in ecology and evolution. An understanding of the evolution of brain form and function requires comprehensive data on neuroanatomy, neurophysiology, behavior and ecology from a diverse array of species, not just a few models. Studies dealing with the nervous systems and behavior of very small animals are likely to reveal phenomena not seen in the larger animals that are typically studied. Tremendous opportunities await for neuroethological studies of taxa with miniature animals, and syntheses of data and ideas from disparate fields such as brain allometry, animal behavior, ecology, neurobiology, classic invertebrate zoology and molecular and developmental biology. An understanding of the patterns and processes involved in evolutionary decreases in body and brain size is also likely to illuminate those associated with evolutionary size expansion, and both are likely to further our understanding of crucial evolutionary transitions from one evolutionary grade to another.
We can’t conclude this discussion of brain and body sizes without acknowledging that we have ignored the proverbial 500-pound gorilla lurking in the room throughout this discussion. We have examined many different consequences of Haller’s Rule, but we have given no explanation for why the rule should be true. Why should organisms ranging from the different castes of ants in a single nest, from primates to salamanders to beetles, so consistently have relatively larger brains when they have smaller bodies? The new invertebrate data help by ruling out some previous explanations that were only reasonable for particular groups of vertebrates. But we do not have an alternative general explanation. It is very unusual in biology that such a general trend as Haller’s Rule should have such a depauperate array of hypotheses lined up as possible explanations. More often the problem is having too many competing ideas to test. Understanding why Haller’s Rule is so generally true is likely to be important in answering central questions regarding the evolution of the central nervous system and how and why different grade changes evolved.
- Bonner, J. 2006. Why Size Matters. Princeton, NJ: Princeton University Press.
- Eberhard, W. G. 2011. Are smaller animals behaviorally limited? Lack of clear constraints in miniature spiders. Animal Behaviour 81:813–823.
- Eberhard, W. G., and W. T. Wcislo. 2011. Grade changes in brain-body allometry: Morphological and behavioral correlates of brain size in miniature spiders, insects and other invertebrates. Advances in Insect Physiology 40:155–214.
- Grebennikov, V. V., and R. G. Beutel. 2002. Morphology of the minute larva of Ptinella tenella, with specific reference to effects of miniaturization and the systematic position of Ptiliidae (Coleoptera: Staphylinoidea). Arthropod Structure and Development 31:157–172.
- Hanken, J., and D. B. Wake. 1993. Miniaturization of body size: Organismal consequences and evolutionary significance. Annual Review of Ecology and Systematics 24:501–519.
- Misunami, M., F. Yokohari and M. Takahata. 2004. Further exploration into the adaptive design of the arthropod ‘‘microbrain’’: I. Sensory and memory-processing systems. Zoological Sciences 21:1141–1151.
- Polilov, A. A., and R. G. Beutel. 2009. Miniaturization effects in larvae and adults of Mikado sp. (Coleoptera: Ptiliidae), one of the smallest free-living insects. Arthropod Structure and Development 38:247–270.
- Quesada, R., E. Triana, G. Vargas, M. Seid, J. Douglass, W. G. Eberhard and W. T. Wcislo. 2011. The allometry of CNS size and consequences of miniaturization in orb-weaving spiders. Arthropod Structure & Development 40:521–529.