CHEMICAL SIGNALS IN THE SEA: 

 MARINE ALLELOCHEMICS AND EVOLUTIO 



J. S. KiTTREDGE,'- FRANCIS T. TaKAHASHI,^ 



James Lindsey,^ and Reuben Lasker'^ 



ABSTRACT 



Observations in chemical ecology suggest the coevolution of "natural products" of plants and 

 the chemoreceptors of herbivorous insects. We have reviewed evidence which suggests that 

 this coevolution extends back to the primordial protistans. Thus, the evolutionary pressure 

 for the development of a chemosensory capability probably derived from the presence of 

 metabolic products in the milieu. These products are considered to have been both cues to 

 the location of prey and "membrane irritants" evolved in the initial phase of chemical 

 protection. Sometime later this chemosensory capability provided several functions in the 

 evolution of metazoans, i.e. the precursors of developmental signals, hormone function, and 

 synaptic transmission. 



We consider that most of the extant "natural products" of plants and marine invertebrates 

 are protective allomones. A feature of allomone function that has been termed "antifeedant" 

 or "feeding inhibitor" may represent the "cryptic odors" of Haldane. We provide evidence 

 that the naphthoquinones with a juglone or naphthazarin structure have this activity. Octo- 

 pus ink has a "cryptic odor" effect on moray eels. Marine Crustacea have, however, 

 evolved an ability to perceive the orthoquinone precursors of the ink, a warning signal. 



Evidence for an array of sex pheromones in a crab and a cycloid swimming pattern in a 

 copepod that may enable it to follow a chemical gradient indicate the complexity of 

 behavioral responses to chemical cues. 



The earliest form of interaction between organ- 

 isms was probably by means of chemical 

 agents. This interaction involved both conflict 

 and cooperation and its existence implies detec- 

 tion of these agents. Haldane (1955) first 

 suggested that chemical communication is the' 

 most primitive form of communication, orgin- 

 ating with primordial unicellular organisms. He 

 reasons that this primordial protistan com- 

 munication was a necessary prelude to the evo- 

 lution of metazoans and thus is a lineal pre- 

 decessor of synaptic transmission and hormone 

 reception. This early chemical communication 

 may have evolved as an accessory to the active 

 transport mechanism of the cell membrane 

 or as a "membrane sensitivity" to metabolic 

 by-products (Wynne-Edwards, 1962). That a 



' This work was supported by NSF grant GB-27703; 

 ONR Contract N00014-7I-C-0103; NOAA Institutional 

 Sea Grant 2-35 187; PHS NB 08599. 



- Marine Biomedical Institute, University of Texas 

 Medical Branch, Galveston, TX 77550. 



3 Zoology Department, Oregon State University, 

 Corvallis, OR 97331. 



* Department of Biological Sciences, University of 

 California at Santa Barbara, Santa Barbara, CA 93106. 



5 Southwest Fisheries Center, National Marine Fisheries 

 Service, NOAA, La Jolla, CA 92037. 



more detailed understanding of transducer 

 physiology is central to further advances in 

 neurobiology has been emphasized by Delbriick 

 (1970). He considers the stimulus-response 

 system represented by chemoreception or 

 synaptic transmission to be homologous. 



We wish to examine some of the recent con- 

 cepts of chemical ecology and to present 

 examples from the marine environment. Studies 

 of chemoreception are providing evidence for 

 the pervasive function of chemical signals in 

 the environment. The "membrane sensitivity" 

 concept of Wynne-Edwards may provide a clue 

 to both the initial evolution of a transducer 

 function and the continuing evolution of 

 receptor sites of greater diversity and specificity. 

 It is evident that this diversity has resulted from 

 a continual interplay of chemical counter- 

 measures and the development of neurosensory 

 and behavioral adaptations to these agents. 



ALLELOCHEMICS 



At all levels of life we are finding examples 

 of attack, defense, and behavioral response 



Manuscript accepted July 1973. 



FISHERY BULLETIN: VOL. 72, NO. 1, 1974 



1 



