Utetheisa ornatrix (Lepidoptera: Arctiidae): The Rattlebox Moth
Sexual selection is an important area of behavioral ecology that explains phenomena including exaggerated male traits, female mating preferences, precopulatory courtship signals, and postcopulatory sperm selection. A great deal of my research is focused on the reproductive biology of Utetheisa ornatrix, commonly known as the rattlebox moth, that is found in the southeastern United States. Tom Eisner introduced me this fascinating lepidopteran during graduate school at Cornell University, and I have been working to unravel the mysteries of its mating system ever since.
The details of this moth’s reproductive strategy are complex. During the larval stage, Utetheisa feeds on plants of the genus Crotalaria (family Fabaceae) that contain poisonous pyrrolizidine alkaloids. Utetheisa is insensitive to the alkaloids, and the larva stores the chemicals systemically, retaining them through metamorphosis into the adult stage. At mating, the male transfers a substantial fraction of his alkaloidal load to the female with the sperm package (spermatophore). The gift is transmitted by the female in part to the eggs, together with a supplement of her own alkaloidal supply. All developmental stages of Utetheisa are protected by the alkaloid, the larvae and adults against spiders, and the eggs are avoided by ants and coccinellid beetles. The spermatophore is of substantial size, amounting on average to over 10% of male body mass. It also contains nutrient, which the female invests in egg production. Females mate on average with four to five males over their lifespan of 3 to 4 weeks. With each mating, the female is able to increase her fecundity by 15%. Fecundity in Utetheisa is also a function of intrinsic female body mass: large females lay greater numbers of eggs.
Female Utetheisa do not mate randomly with males but do so selectively with males of higher alkaloid content. The female does not gauge male alkaloid content directly but does so indirectly, on the basis of a pheromone (hydroxydanaidal) that the male produces from alkaloid, in proportion to his alkaloid load, and airs during close-range precopulatory interaction with the female. Males richest in alkaloid, having the strongest pheromonal scent, are also largest, and apt to bestow the largest alkaloidal (and presumably nutritive) gifts. In essence, by selecting males of high alkaloid content, the female is selecting males of large size. My doctoral research demonstrated that, by favoring larger males, females obtained both direct phenotypic benefits (higher offspring survivorship) and indirect genetic benefits in the form of higher lifetime fecundity for daughters (“good genes” benefits) and greater reproductive success for sons (Fisherian benefits) (PDF). I continued to investigate the relative roles of direct and indirect selection in the evolution of female choice in the rattlebox moth in my postdoctoral work, where I tested sexual selection models by quantifying the strength, heritability, and sex-linkage of the female mating preference (for large males) in Utetheisa. In Utetheisa, as in all lepidopterans and birds, males are homogametic (ZZ) whereas females are heterogametic (ZW). Interestingly, the female mating preference gene(s) are Z-linked, which means that they are strictly paternally inherited (PDF). This result highlights the importance of indirect genetic benefits in the evolution and maintenance of sexual selection in this moth.
Recent work in my lab has confirmed that indirect genetic benefits are strong selective forces in this mating system, and that the critical genetic trait under selection is larval competitive ability. Competition in the rattlebox moth is especially important during the larval stage, where access to the limited resource of seeds rich in defensive compounds affects adult body size (and therefore, reproductive success). My Master’s student Justin Walsh investigated the roles of residency, size, sex and relatedness on larval competition (PDF), and the results have led to many more questions involving the strategies regarding interacting larvae and ovipositing females.
Utetheisa ornatrix continues to be a gold mine for studying sexual selection because females are highly promiscuous over their 3-4 week lifespan and may take as many as 22 mates, each of whom delivers a substantial spermatophore containing both genetic and non-genetic material (nutrients and defensive compounds). Furthermore, lepidopterans have a complex reproductive system with the potential for postcopulatory sperm selection, and other studies on this moth have revealed biased paternity for twice-mated females. The most exciting new frontiers involve postcopulatory selection, as my recent Master’s student Andrea Egan used molecular paternity analyses to determine whether female polyandry drives selection for male sperm competitiveness (PDF). In addition to being one of the few empirical tests of the sexy-sperm hypothesis, this research has also led to new directions in our research program, as we are now preparing to more closely investigate the mechanism of postcopulatory selection. Despite over 20 years of intensive field and laboratory research on this species, U. ornatrix continues to reveal complexities in the reproductive strategies of both sexes, and we welcome both undergraduate and graduate students to participate in our laboratory and field experiments that may resolve unanswered questions in this moth and impact our understanding of mating systems in general.