AMER. ZOOL., 33:487-493 (1993) Body Odors and Neutral-basic Peptide Mimics: A Review of Responses by Marine Organisms 1 DAN RITTSCHOF Zoology Department and School of the Environment, Duke University Marine Laboratory, Beaufort, North Carolina 28516 SYNOPSIS. A review of body odor-mediated behaviors of hermit crabs, predatory gastropods, barnacle larvae and brachyuran crabs includes a model based on the hypothesis that all the behaviors are mediated by a similar chemical detection mechanism. A key assumption is behaviors evolved due to a selective advantage conferred by detection of information in body odors. In the model, exogenous trypsin-like proteases digest struc- tural proteins to generate neutral-basic peptides. The receptor is postu- lated to have resulted from a point mutation in a trypsin-like membrane protein. Transduction of the binding event is via second messenger medi- ated pathways. Examples of body odors functioning as cues, allomones and pheromones are presented. The model is supported by a review of structure-function studies employing synthetic neutral basic peptides and studies with other macromolecules. Developing ideas of how chemical senses evolved is the ultimate goal of my studies. A focus is transmission of specific infor- mation and its transduction into biochem- ical, physiological and behavioral responses. It is in this context that this review of our work on peptide mediated behaviors is pre- sented. What follows is a review of data that sup- port a scenario for the evolution of a family of peptide detection and response systems (Rittschof, 1990). In the scenario, a system evolved to use specific information con- tained in body odors. The odors result from the action of serine proteases on structural proteins. The information peptides are a variety of sizes, but always end in arginine or lysine. The detector, a peptide receptor, is postulated to be the result of a point muta- tion in the catalytic site of a serine protease such as trypsin (Rittschof et al., 1990a, Fig. 1 A). This concept is similar to that put for- ward as an explanation for the evolution of sex pheromone communication in arthro- pods (Kittredge and Takahashi, 1972). Once this hypothetical chemosensory system existed, it proliferated much as elec- 1 Invited review paper, Division of Comparative Endocrinology. tronic communication systems are prolif- erating today. Through selection, the pep- tide detection system came to mediate a variety of responses. Thus, fortuitous avail- ability and use of chemical information in body odors could be the basis of a family of communication systems. Several others (D. Morse, 1992; A. Morse, 1992) that work with chemically mediated phenomena are hypothesizing the existence of additional families. The reasoning for the evolution of a pep- tide body odor signaling system is based upon assumptions similar to those pro- posed by Tomkins (1975) in arguments for the evolution of metabolic communication systems. These assumptions are: 1) There are advantages to monitoring and respond- ing to the external environment. 2) Mem- brane bound enzymes, substrates and prod- ucts were available to secondarily acquire an information function. 3) Mutation can simultaneously eliminate catalytic activity of an enzyme and increase affinity for what was originally the product. Such a mutation is one way to convert an enzyme into a receptor (see Rittschof e? al., 1990a). 4) The information content of a molecule, i.e., how chemically unique it is, determines its potential role as a signal. For example, mol- ecules common to most organisms may sig- 487 Downloaded from https://academic.oup.com/icb/article/33/6/487/163352 by guest on 21 October 2021