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Biparental Defensive Endowment of Eggs with Acquired Plant Alkaloid In Proc. Natl. Acad. Sci. USA Vol. 85, pp. 5992-5996, August 1988 Evolution Biparental defensive endowment of eggs with acquired plant alkaloid in the moth Utetheisa ornatrix* (pyrrolizidine alkaloid/defense/parental investment/nuptial gift/sexual selection) DAVID E. DUSSOURDi*, KAREL UBIK§¶, CARL HARVIS§, JAMES RESCH§II JERROLD MEINWALD§, AND THOMAS EISNERt Departments of tNeurobiology and Behavior and Chemistry, Cornell University, Ithaca, NY 14853 Contributed by Thomas Eisner, April 13, 1988 ABSTRACT The eggs of Utetheisa ornatrix contain pyrro- female. Hydroxydanaidal plays a key role in mediating lizidine alkaloids. These compounds are contributed by both acceptance of the male by the female. Males reared on a parents, who sequester them as larvae from their food plants. laboratory diet devoid of alkaloid produce no hydroxyda- Females receive alkaloid from the males at mating, apparently naidal and as a consequence are substantially less successful by seminal infusion, and transmit this alkaloid together with in courtship (6). This finding led to the suggestion that alkaloid of their own to the eggs. Field and laboratory tests hydroxydanaidal plays a subtle communicative role. Given showed that the alkaloids protect eggs from predators. The its derivation from systemic alkaloid, the pheromone could alkaloidal contribution of the male, although smaller than that provide the female with a measure of the male defensive of the female, itself provides significant egg protection. A alkaloid load and, hence, with an indirect indication of his previously identified pheromone, derived by the male from the larval alkaloid-sequestering ability, a trait potentially herita- alkaloid and emitted during precopulatory behavior, may ble (6, 7). We now find this hypothesis restrictive after we announce the male alkaloidal worth to the female. discovered that the male transfers some alkaloid to the female at mating as a "nuptial gift" for eventual incorporation into The egg is perhaps the most endangered stage in the life cycle the eggs. Hydroxydanaidal could thus serve directly as a of an insect. Motionless and often conspicuous, it is highly measure of this gift, rather than merely indirectly for assess- vulnerable to both predators and parasites. Many insects ment of male fitness. Our data are advanced within this defend their eggs by concealing them, affixing them to stalks, conceptual context. or endowing them with deterrent chemicals (1). As a rule, Specifically, we show that (i) field-collected eggs of U. only the female parent provides for such defenses. Biparental ornatrix contain pyrrolizidine alkaloid matching that in the contribution to egg defense is rare in insects (2) and appears natural larval food plants ofthe moth; (ii) eggs parented in the unnoted in regard to bestowment of chemical weaponry. We laboratory contain alkaloid contributed by both parents; (iii) present evidence that in the moth Utetheisa ornatrix (family unmated males contain substantial levels of alkaloid within Arctiidae) egg defense is achieved by pyrrolizidine alkaloids, their reproductive tract; and (iv) pyrrolizidine alkaloids effec- sequestered by the parent insects from their larval food tively protect Utetheisa eggs against predators, even in the plants, and supplied to the eggs by both sexes. amount supplied to the egg by the father alone. The larval food plants of U. ornatrix are legumes of the genus Crotalaria, plants long known to contain pyrrolizidine alkaloids [for example, monocrotaline (compound I) and MATERIALS AND METHODS Chemical Analyses. Monocrotaline (compound I) was ob- tained by extraction of Crotalaria spectabilis seeds using a C20H standard procedure (8). Its N-oxide was prepared by treating the free base with hydrogen peroxide (9). Alkaloids were OH CHO isolated from Utetheisa parts and eggs using a microscale H20 adaptation of standard protocol (8). Because pyrrolizidine alkaloids occur naturally as both free bases and N-oxides, total content ofmonocrotaline or usaramine in a given sample was measured by reducing any N-oxides to the corresponding I If ,4' free base with zinc dust before analysis. usaramine (compound H)]. Utetheisa larvae feed preferen- Each sample was extracted for 24 hr at room temperature tially on the seeds of these plants, where the alkaloids are with methanol. This extract was filtered and evaporated to concentrated (3, 4). The larvae tolerate the alkaloids, which give a residue that was distributed between 1 M sulfuric acid they accumulate systemically and retain through metamor- and chloroform. The acidic aqueous layer was stirred with phosis into the adult stage. The acquired alkaloid protects zinc dust for 3 hr, the zinc was removed by filtration, and the both larvae and adults against predation (ref. 5; T.E., unpublished results). Male Utetheisa produce a courtship Abbreviations: PB, pinto bean; CS, Crotalaria spectabilis; CM, Crotalaria mucronata. pheromone, hydroxydanaidal (compound Il), which they *Report 86 ofthe series Defense Mechanisms ofArthropods. Report derive chemically from the alkaloid. They secrete the sub- 85 is ref. 31. stance from a pair of brush-like structures, the coremata, tPresent address: Department of Entomology, University of Mary- during their close-range precopulatory interactions with the land, College Park, MD 20742. VPresent address: Czechoslovak Academy of Science, Institute of Organic Chemistry and Biochemistry, Flemingovo n. 2, 116-10 The publication costs of this article were defrayed in part by page charge Prague 6, Czechoslovakia. payment. This article must therefore be hereby marked "advertisement" Present address: Stuart Pharmaceuticals, Biomedical Research in accordance with 18 U.S.C. §1734 solely to indicate this fact. Department, Wilmington, DE 19897. 5992 Downloaded by guest on September 26, 2021 Evolution: Dussourd et al. Proc. Natl. Acad. Sci. USA 85 (1988) 5993 filtrate was brought to pH 10 by addition of concentrated components of the reproductive system, and each part was ammonium hydroxide. Total alkaloid was then obtained by analyzed for monocrotaline content. extraction with chloroform. Survivorship ofEggs in the Field. Relative survivorship was In those instances where it was of interest to differentiate determined of Utetheisa eggs parented by moths reared on between free base and its N-oxide, an aliquot of the initial either PB diet or CS diet. (The former eggs could be expected acidic aqueous solution was removed before zinc dust re- to be alkaloid-free and the latter to contain monocrotaline.) duction. Basification with ammonium hydroxide, followed Eggs ofeach category were collected from cages housing -20 by chloroform extraction, yielded only that part of total adults, where females mated repeatedly, as they do in nature alkaloid present as the free base. N-Oxide content was cal- (14). Wax paper in the cages provided the oviposition sub- culated by subtracting free base titer from total alkaloid con- strate. Egg clusters were collected daily, adjusted to a tent. standard 10 eggs per cluster (by removing excess eggs), and Alkaloid samples were quantified by conversion to volatile immediately placed in the field. A total of 100 clusters per trimethylsilyl (Me3Si) derivatives, using Supelco Sylon BTZ category were tested. [bis(Me3Si)acetamide/Me3SiCI/M3Si-imidazole, 3:2:3] rea- The test was done in midsummer near Lake Placid, FL, in gent under standard conditions, followed by gas chromato- a dense stand of Cr. mucronata where Utetheisa was natu- graphic analysis (3% OV-17 or OV-101 on Gaschrom Q; 160- rally established. The clusters, each still affixed to a piece 280°C at 40C/min) using perylene as internal standard. Under (=2 cm2) of wax paper, were pinned in pairs (one of each our conditions, usaramine was converted into its bis-Me3Si category per pair) to the underside of individual Cr. mucro- derivative, whereas monocrotaline yielded a mixture of nata leaves. These leaves are typically trifoliate; paired mono-Me3Si and bis-Me3Si derivatives. Consequently, mo- clusters were consistently pinned to the outer two leaflets of nocrotaline contents were calculated by summing the values the leaf. After 48 hr a count was taken of the total number of for its mono- and bis-derivatives. eggs per category that had disappeared (entirely or with only remnants of egg shell remaining). Intact eggs were kept for Experimental Animals. Except where noted, all Utetheisa determination of parasite emergences and viability. Eggs were from our laboratory culture, established with stock were judged viable if the larvae hatched, died in hatching, or taken near Lake Placid and Gainesville, FL. Voucher spec- had visibly developed to maturity (head capsule discernable) imens of adults, which conform in appearance to the sub- but failed to hatch. No hatchings occurred during field species Utetheisa ornatrix bella (10), have been deposited exposure of the clusters because Utetheisa eggs require =4 (lot 1154) in the Cornell insect collection. days to mature. At their original field sites, the Utetheisa are found asso- Degree of Protection Conferred by Each Parent's Alkaloid ciated with two principal food plants, Cr. spectabilis and Contribution to Egg. A bioassay with a predaceous beetle, Crotalaria mucronata, differing in pyrrolizidine alkaloid Coleomegilla maculata (Coccinellidae), was developed for composition. Cr. spectabilis contains primarily monocrota- determination ofpalatability of Utetheisa eggs. Co. maculata line (compound I), and Cr. mucronata contains mostly includes
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