ORIGINS OF OLFACTORY SYSTEMS

Consideration of the origins and evolution of chemosensation can help one to begin to understand the themes of olfaction and chemical communication that are common to diverse phyletic groups. This section emphasizes ideas that were propounded with characteristic clarity and elegance by the late Vincent Dethier in his 1990 R. H. Wright Lectures on Olfaction. Because the published version of those lectures (1) may not be widely accessible, some of Dethier's main points are restated here.

Origins of Chemoreception

The universal chemoreceptive capacity of living organisms surely must have arisen in the earliest cells, at the dawn of life billions of years ago (1). That capacity enables a cell to respond to substances without the necessity of internalizing or metabolizing them and is fundamental to the living state.

Studies of unicellular organisms have afforded insights about the origins of chemosensory processes and mechanisms exhibited by metazoa. Thus, modern bacteria such as Escherichia coli (2, 3) sense and respond to chemicals in ways that probably resemble those of ancient prokaryotes. E. coli possess finely "tuned" receptors for specific substances in the environment, mechanisms for transducing the stimuli and for decoding, integrating, and transmitting information about them, and means to generate appropriate behavioral responses. The motifs of chemoreception are conserved and elaborated in the protists and especially the slime molds (1, 4), suggesting subsequent evolutionary transitions. Dethier observed (1):

With the advent of multicellularity many cells lost some of their ancient skills, but the organism's capability of sensing the chemical richness of the world was not impaired. Chemoreception became the prime function of specialized strategically situated cells anchored in epithelial sheets. The coupling of chemoreception to motility, that is, to behavioral responses, was accomplished by close association with transmitting systems. Transitional stages between the two functional levels, self-contained unicellular systems and neurally-linked multicellular systems, are preserved in contemporary coelenterates. Here are to be found the earliest metazoan chemoreceptors. In the further evolution of the nervous system there was a division of labor associated with a diversification of kinds of neurons, segregation in which like units gathered together, and compartmentalization of functional assemblies within ganglia.

Whence Olfaction?

Evolution of metazoan chemoreception eventually gave rise to anatomically and functionally distinct chemosensory systems—olfac-



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