Elevated atmospheric concentrations of carbon dioxide reduce monarch tolerance and increase parasite virulence by altering the medicinal properties of milkweeds

Abstract

Hosts combat their parasites using mechanisms of resistance and tolerance, which together determine parasite virulence. Environmental factors, including diet, mediate the impact of parasites on hosts, with diet providing nutritional and medicinal properties. Here, we present the first evidence that ongoing environmental change decreases host tolerance and increases parasite virulence through a loss of dietary medicinal quality. Monarch butterflies use dietary toxins (cardenolides) to reduce the deleterious impacts of a protozoan parasite. We fed monarch larvae foliage from four milkweed species grown under either elevated or ambient CO , and measured changes in resistance, tolerance, and virulence. The most high-cardenolide milkweed species lost its medicinal properties under elevated CO ; monarch tolerance to infection decreased, and parasite virulence increased. Declines in medicinal quality were associated with declines in foliar concentrations of lipophilic cardenolides. Our results emphasize that global environmental change may influence parasite-host interactions through changes in the medicinal properties of plants.

Annual environmental variation influences host tolerance to parasites

“…Trade-offs between different defence strategies may be particularly relevant for hosts that face consistent parasite pressure, yet live in variable environments, such as Galápagos mockingbirds. The ability to mount a successful defence may become even more challenging in the face of a changing climate [25,62]. Recent models predict increased variability and magnitude of El Niñ o and La Niñ a events [63], which are the primary climatic cycles that drive rainfall patterns in the Galápagos [34].…”

Phytochemical changes in milkweed induced by elevated CO2 alter wing morphology but not toxin sequestration in monarch butterflies

“…We expected sequestration profiles to mirror changes in plant chemistry induced by eCO 2 because factors that alter phytochemistry and consumption rates should also influence the types and amounts of PSMs monarchs sequester. We also predicted that changes in cardenolides and reductions in the nutritional quality of larval host plants grown under eCO 2 (Decker, de Roode, & Hunter, ; Robinson et al, ) would cause declines in the quality of the insect flight phenotype: smaller, thinner and rounder wings with lower wing loading values. Feeding on lower quality food with different types and amounts of cardenolides may engender a metabolic cost inflicting stress upon the insect and inducing morphological changes.…”

Host Plant Effects on Immune Response Across Development of a Specialist Caterpillar

“…This raises the possibility of trade-offs in defense strategies against multiple natural enemies, if the costs of sequestering PSMs outweigh the benefits of immune defenses or vice versa. Such trade-offs may become even more important in the presence of ecological perturbations, such as human-induced environmental change, which can lead to changes in host plant quality (Jamieson et al, 2015;Decker et al, 2018), range shifts of host plants or natural enemies (Jeffs and Lewis, 2013), the introduction of novel hosts (Jahner et al, 2011), and subsequently insect defense against natural enemies (Gherlenda et al, 2016).…”