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The Chemistry of Phyletic Dominance*

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The Chemistry of Phyletic Dominance* Proc. Natl. Acad. Sci. USA Vol. 92, pp. 14-18, January 1995 Colloquium Paper This paper was presented at a coUoquium entitled "Chemical Ecology: The Chemistry ofBiotic Interaction," organized by a committee chaired by Jerrold Meinwald and Thomas Eisner, held March 25 and 26, 1994, at the National Academy of Sciences, Washington, DC. The chemistry of phyletic dominance* (chemical defenses/arthropod venoms/neurotoxins/steroidal pyrones/nucleoside glycoside) JERROLD MEINWALDt AND THOMAS EISNERt t582 Baker Laboratory and *W347 Mudd Hall, Cornell Institute for Research in Chemical Ecology, Cornell University, Ithaca, NY 14853 ABSTRACT Studies of arthropod defensive chemistry derived by specialization of localized regions of the epidermis. continue to bring to light novel structures and unanticipated In insects, as in arthropods generally, the epidermis is funda- biosynthetic capabilities. Insect alkaloids, such as the hepta- mentally glandular, being responsible for secretion of the cyclic acetogenin chilocorine and the azamacrolides, exem- exoskeleton. In their acquisition of special glands, arthropods plify both of these aspects of arthropod chemistry. Spider appear to have capitalized upon the ease with which epidermal venoms are proving to be rich sources of neuroactive compo- cells can be reprogrammed evolutionarily for performance of nents of potential medical interest. The venom of a fishing novel secretory tasks. The glandular capacities of arthropods spider, Dolomedes okefinokensis, has yielded a polyamine which are known to anyone who has collected these animals in the reversibly blocks L- and R-type voltage-sensitive calcium wild. Arthropods commonly have distinct odors and are often channels. Most recently, we have characterized, from the the source of visible effluents that they emit when disturbed funnel-web spider Hololena curta, a sulfated nucleoside glyco- (Fig. 1). Much has been learned in recent years about the side which serves as a reversible blocker of glutamate- function and chemistry of arthropod secretions. The insights sensitive calcium channels. The ability to synthesize or acquire gained have been fundamental to the emergence of the field an extremely diverse array of compounds for defense, offense, of chemical ecology. Our purpose here is to focus on some and communication appears to have contributed significantly aspects of the secretory chemistry of these animals, with to the dominant position that insects and other arthropods emphasis on a few recent discoveries. have attained. Arthropod Chemical Defenses Whether we chose as our criterion Erwin's generous estimate of 30 million species of insects (1) or the somewhat more In our earliest collaborative publication, we described the modest number favored by Wilson (2), it is clear that insects dramatic chemical defense mechanism of the whip scorpion, have achieved formidable diversity on Earth. On dry land they Mastigoproctus giganteus (6). This ancient arachnid is able to literally reign supreme. It has been estimated that there are spray a well-aimed stream of -85% acetic acid [CH3CO2H] some 200 million insects for each human alive (3). The containing 5% caprylic acid [CH3(CH2)6CO2H] at an assail- eminence of the phylum Arthropoda among animals is very ant. The role of the caprylic acid proved to be especially much a reflection of the success of the insects alone. interesting: it facilitates transport of the acetic acid through the A number of factors have contributed to the achievement of waxed epicuticle of an enemy arthropod. It is likely that this dominance by insects. They were the first small animals to simple strategy of using a lipophilic agent to enable a more colonize the land with full success, thereby gaining an advan- potent compound to penetrate a predator's cuticle has helped tage over latecomers. Their exoskeleton shielded them from this species to survive for as long as 400 million years. Many desiccation and set the stage for the evolution of limbs, other independently evolved arthropod defensive secretions tracheal tubes, and elaborate mouthparts, adaptations that make use of the same strategy (9). The whip scorpion defense were to enable insects to become agile, energetically efficient, mechanism helped us to appreciate the fact that chemistry and extraordinarily diverse in their feeding habits. Metamor- need not be complex to be effective. The virtue of simplicity phosis opened the option for insects to exploit different niches is further illustrated by the defensive use of mandelonitrile and during their immature and adult stages. The evolution ofwings benzoyl cyanide, easily decomposed precursors of hydrogen facilitated their dispersal as adults, as well as their search for cyanide (HCN), by certain millipedes and centipedes (10, 11). mates and oviposition sites. And there were subtle factors such While arthropod defensive secretions often rely for their as the acquisition of a penis (the aedeagus), which enabled effect on well-known aliphatic acids, aldehydes, phenols, and insects to effect direct sperm transfer from male to female, quinones, there are many cases in which compounds capable without recourse to an outer aquatic environment for fertili- of whetting the appetite of any natural products chemist are zation (3). utilized. For example, steroids play a dominant role in the A factor not often appreciated that also contributed to insect defensive chemistry of dytiscid beetles, and of the large water success is the extraordinary chemical versatility of these ani- bug, Abedus herberti. This bug discharges a mixture of preg- mals. Insects produce chemicals for the most diverse purpos- nanes in which desoxycorticosterone is the main component es-venoms to kill prey, repellents and irritants to fend off (12). A family of much more highly functionalized steroids, the enemies, and pheromones for sexual and other forms of lucibufagins, serves to render some species of firefly (lampyrid communication. The glands responsible for production of beetles) unpalatable to predatory spiders and birds (13-15). these substances are most often integumental, having been These cardiotonic steroids are closely related to the bufadi- enolides, whose only known occurrence among animals is in The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" in *This paper is no. 128 in the series Defense Mechanisms ofArthropods; accordance with 18 U.S.C. §1734 solely to indicate this fact. no. 127 is ref. 28. 14 Downloaded by guest on September 30, 2021 Colloquium Paper: Meinwald and Eisner Proc Natl Acad Sci USA 92 (1995) 15 I I I I I FIG. 1. Arthropod chemical defenses. (A) Blister beetle (Lyttapolita) reflex-bleeding from the knee joints; the blood contains cantharidin, one of the first insect toxins characterized (4). (B) Chrysomelid beetle larva (Plagiodera versicolora) emitting droplets of defensive secretion from its segmental glands; the fluid contains methylcyclopentanoid terpenes (chrysomelidial, plagiolactone) (5). (C) Whip scorpion (Mastigoproctus giganteus) discharging an aimed jet of spray in response to pinching of an appendage with forceps; the spray contains 84% acetic acid (6). (D) Millipede (Narceusgordanus) discharging its benzoquinone-containing defensive secretion from segmental glands (7). (E) Ctenuchid moth (Cisseps fulvicollis) discharging defensive droplets (chemistry unknown) from the cervical region. (F) Caterpillar of swallowtail butterfly (Battuspolydamas) with everted (two-pronged) osmeterial gland; the secretion contains sesquiterpenes (,3-selinene; selin-11-en-4a-ol) (8). (G) Stalked eggs of green lacewing (Nodita floridana), showing droplets of defensive fluid (chemistry unknown) on stalks. nucleus to a steroidal framework, since up to now there has been no general, convenient synthetic route to these steroidal pyrones. Our search has recently met with success (18), using the Pd°-promoted coupling of 5-trimethylstannyl-2-pyrone with an enol triflate (Eq. 1). o OSO2CF3 ,+ [1] t_ Desoxycorticosterone Lucibufagin C Sn(CH3)3 the poison glands of certain toads (16). The discovery that the lucibufagins also show antiviral properties (17) has prompted This direct synthesis of steroidal pyrones should make a us to seek a technique for joining a preformed a-pyrone variety of structures related to the lucibufagins (as well as to Downloaded by guest on September 30, 2021 16 Colloquium Paper: Meinwald and Eisner Proc. Natl. Acad ScL USA 92 (1995) the toad-derived bufadienolides) readily available for biolog- varivestis to determine the possible sources of both the 14-carbon ical investigation for the first time. How the insects themselves straight chain and the ethanolamine moieties ofepilachnene (28). manage to obtain their defensive pregnanes and steroidal Our results are summarized below: pyrones remains a mystery, since insects are generally consid- ered to lack the enzymatic machinery essential for steroid HCO2H o biosynthesis (19). In fact, we do not yet know whether these insect defensive steroids are produced de novo or whether they are derived directly or indirectly from a dietary source; this is N t N H 2 a subject which merits further study. Perhaps the most interesting arthropodan defensive com- Oleic acid > Epilachnene L-Serine pounds from the point of view of structural diversity are the alkaloids. While alkaloids had been believed to arise long only was to as a of it has 9,10-Dideuteriooleic acid shown to be converted di- consequence
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