© Thomas Eisner, Cornell University. Scent Brush of a Male Moth Bugs, Behavior, and Biomolecules: The Naturalist’s Guide to the Future Thomas Eisner, Jerrold Meinwald, and John Hildebrand This presentation was given at the 1881st Stated Meeting, held at the House of the Academy on May 12, 2004. Thomas Eisner is the Jacob Gould Schurman Pro- Thomas Eisner I was soon to learn that this was no freak event. fessor of Chemical Ecology at Cornell University I offered Utetheisa to a diversity of spiders, in- and Director of the Cornell Institute for Research cluding orb-weavers, wolf spiders, and jump- in Chemical Ecology. He has been a Fellow of the Exploration and Discovery ing spiders, and found that they all rejected the American Academy since 1969. moth. Utetheisa was decidedly distasteful, and My interest in Utetheisa ornatrix dates back to so was its larva. When I offered Utetheisa cater- Jerrold Meinwald is Goldwin Smith Professor of an occasion some forty years ago when I saw pillars to wolf spiders, the spiders consistently Chemistry at Cornell University and a founding an individual of this beautiful multicolored refused to take them. member of the Cornell Institute for Research in moth species fly into a spider’s web. I fully ex- Chemical Ecology. He has been a Fellow of the pected the spider to make a meal of its catch, Eventually, working with my wife Maria and American Academy since 1970. but not so. The moment the moth struck the my students, and with my friend Jerry Mein- wald and his associates from Cornell’s chem- John Hildebrand is Regents Professor of Neurobiol- web the spider darted toward it, only to refrain istry department, we discovered why Utetheisa ogy and Professor of Biochemistry and Molecular from biting it and to proceed to cut it loose. Sys- is unpalatable to spiders. As a larva, Utetheisa Biophysics, Cellular and Molecular Biology, and tematically, by use of its fangs and palps, the feeds on leguminous plants of the genus Crota- Entomology at the University of Arizona. He has spider cut each of the silken strands that were laria that contain highly bitter toxins called been a Fellow of the American Academy since 2001. imprisoning the moth, until the moth fell free. pyrrolizidine alkaloids (pas). Utetheisa larvae are unaffected by pas and are able to incorpo- 26 Bulletin of the American Academy Summer 2004 rate the compounds without having to detoxi- ½nd one another. In Utetheisa, as in moths gen- fy them. They retain the chemicals systemically By mating selectively with erally, it is the female that attracts the male. She through metamorphosis, with the result that strongly scented males, fe- does so in conventional fashion, by emission the adults themselves come to possess the com- of a pheromone, a mixture of unsaturated hy- pounds. males are assured that their drocarbons, that she produces in a pair of glands that open on the abdominal tip. We observed We proved that it is the pas that give Utetheisa offspring will be larger–that early on that the female Utetheisa, during the its bad taste. We were able to raise in Utetheisa hour or so after dusk when she broadcasts her the laboratory on a pa-free diet, thereby gener- their sons will be more com- pheromone, undergoes a conspicuous throb- ating moths that lacked pa. Such moths, which bing of the abdomen. Thanks to the efforts of were perfectly normal in other respects, proved petitive in courtship and Bill Conner, a student in my laboratory at the palatable to spiders. We also showed that crys- time, we learned that this throbbing is the visi- talline pa, when added to the surface of insects their daughters more fecund. ble concomitant of a rhythmic compression ordinarily eaten by spiders, renders such in- and decompression of the pheromonal glands sects decidedly less acceptable. ploits. The Utetheisa female retains a vestige of that causes the contained secretion to be emit- each sperm package it receives, a small tubular ted in pulses. The advantage that the female remnant that stays with it for life. These ves- derives from such discontinuous delivery of tiges, each a carte de visite from an individual attractant appears to be economic. By pulsing, male, can be accessed by dissection of the fe- the female may be able to cut back on the male, and counted. Having on average as many amount of pheromone released. as eleven partners clearly indicates that the female Utetheisa makes every effort to exploit the male’s gift-giving capacity. Utetheisa differs in the quantity of pa it seques- ters as larvae, and as a consequence has varying pa content as an adult. For the female, which is dependent on receipt of pa from males, it is of some importance to know how much pa a prospective mate holds in store, since this may determine the magnitude of the nuptial gift she receives. Interestingly, the female Utetheisa puts the males to the test during courtship. The fe- males assess the males’ pa load and mate se- lectively with males richest in pa, ensuring thereby that they will be more generously pro- Figure 1: A male Utetheisa moth wiping its evert- ed scent brushes against the female in courtship. visioned. And how can females tell that a male has a higher quantity of pa? It turns out that Utetheisa transmits pas to its eggs. Eggs laid by the male gives off a scent, a pheromonal signal, Utetheisa that we raised on the pa-free diet were by which he reveals his alkaloid load. He emits themselves pa-free, and, as a consequence, that signal from two brush-like structures that vulnerable to attack. Eggs endowed with pa, he everts during close-range precopulatory Figure 2: Caterpillar of Utetheisa inside a seed in contrast, proved unacceptable to ants, green interaction with the female. The pheromone, pod of its Crotalaria food plant. lacewing larvae, ladybugs, and parasitoid wasps. hydroxydanaidal (hd), is derived by the male Courtship in is evidently a ½ne-tuned from pa, in quantity proportional to his pa Utetheisa affair. Chemical signaling is the rule of the game, Utetheisa adults have a life span of three to four load. Therefore, by favoring males more in- both in the initial attractant phase of the be- weeks. The female, over that period, lays hun- tensely scented with hd, females are guaran- havior, and in the subsequent interactive phase, dreds of eggs. How, we wondered, does she man- teed receipt of larger amounts of pa. It turns when the female assesses the male. Is the mat- age to protect them all? Does she have enough out that males selected for high hd content pa ing strategy of unusually complex? stored in her body to provision her entire are also physically the largest, which has im- Utetheisa Most probably not. Other insects are bound to brood? The answer is that she is not, in fact, portant consequences for Utetheisa, because be discovered that have equally sophisticated ordinarily suf½ciently endowed, but that she body size is heritable in this moth. Thus, by pa sexual communicative systems. Are chemical is able to obtain supplementary by mating. mating selectively with strongly scented males, signals likely to play major roles in these other The Utetheisa female is promiscuous, and she females are assured that their offspring will be pa species as well? Most probably. Chemical in- receives from each male with the sperm larger–that their sons will be more competi- teraction is the most common form of sexual package. The number of partners that a female tive in courtship and their daughters more fe- interaction in animals of all kinds. Studies of takes over her lifetime is astonishing. Under cund. Evidently, by being “choosy,” the female animal courtship are therefore likely to remain natural conditions, in established populations Utetheisa bene½ts both phenotypically and multidisciplinary and to continue to be depen- of the moth, females mate, on average, with genetically. eleven males. Prima donnas may take more dent on the collaboration of behaviorists, ecol- than twenty partners. I know this because the Interesting also is the mechanism by which ogists, neurobiologists, and chemists. female Utetheisa keeps a sort of diary of its ex- Utetheisa males and females ensure that they Bulletin of the American Academy Summer 2004 27 lecular formula of quinone is C6H4O2, meaning that its molecules are composed of six atoms The chemist’s world is not of carbon, four of hydrogen, and two of oxy- the naturalist’s. One impor- gen. But their composition alone does not ade- quately de½ne what quinone is. It was only in tant difference is the matter the mid-nineteenth century that chemists real- ized that molecules also have speci½c struc- of scale; the chemist’s world Figure 3: A pyrrolizidine alkaloid (left) and its tures and shapes. In order for a molecule to be pheromonal derivative, hydroxydanaidal. quinone, its twelve constituent atoms need to is very much smaller, in the My research on the chemical ecology of insects be bonded to one another in one speci½c way. sense that its basic entities has been supported since 1959 by the National Figuring out how the atoms are connected in Institutes of Health (grant AI02908), and more any given compound–determining its struc- are molecules rather than recently also by funds from Johnson & Johnson. ture–can be a daunting task. For compounds A more comprehensive account of our work of the complexity of cholesterol or morphine, cells, organisms, popula- it required several chemists’ lifetimes of re- on Utetheisa ornatrix can be found in my recent search.