It is widely expected that where animals lay eggs will be under strong natural selection, leading to oviposition preferences that maximize fitness. For immobile, immature insects, fitness may not only be determined by the quality of the resource on which eggs were laid, but also on the local level of predation and competition. In addition, oviposition preferences are shaped by factors endogenous to the female, such as energetic needs and previous experiences. We tested for oviposition preference and caterpillar performance of monarch butterflies (Danaus plexippus), which encounter a diverse range of milkweed host plant species during their multi-generational annual migratory cycle. Using four closely-related milkweeds that span a 10-fold range in toxicity (concentrations of cardenolides) we examined caterpillar performance, sequestration of plant cardenolides (as a proxy for defense against predators), and adult female oviposition preference. To understand the degree of plasticity in oviposition, we next examined the influences of nectar availability and previous experience on oviposition choices. Finally, we tested for the influence of competition on oviposition preference using the presence of a conspecific caterpillars and conspecific adults.
We show that caterpillar performance was lowest on Asclepias incarnata pulchra, a low cardenolide plant on which sequestration was also low. A. i. pulchra had the highest latex exudation and highest densities of leaf trichomes, both of which provide resistance. Counterintuitively, oviposition preference was consistently highest for this species. Oviposition preference was neither influenced by previous oviposition experience nor by the presence of a nectar resource (milkweed flowers for nectar foraging). Nonetheless, oviposition preferences were completely reversed when a conspecific caterpillar was present on the preferred host plant, indicating an important effect of competition larval competition on oviposition choices. The presence of conspecific adults, however, did not impact oviposition decisions. Our study demonstrated a consistent preference for A. i. pulchra contrary to offspring development and defense. This preference may be a sensory trap, reversible only in the presence of caterpillar competition.