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

Abstract

Environmental change has the potential to influence trophic interactions by altering the defensive phenotype of prey. Here, we examine the effects of a pervasive environmental change driver, elevated atmospheric concentrations of CO2 (eCO2), on toxin sequestration and flight morphology of a specialist herbivore. We fed monarch butterfly larvae, Danaus plexippus, foliage from four milkweed, Asclepias, species of varying chemical defence profiles grown under either ambient or eCO2. We also infected a subset of these herbivores with a protozoan parasite, Ophryocystis elektroscirrha, to understand how infection and environmental change combine to alter herbivore defences. We measured changes in phytochemistry induced by eCO2 and assessed cardenolide, toxic steroid, sequestration and wing morphology of butterflies. Monarchs compensated for lower plant cardenolide concentrations under eCO2 by increasing cardenolide sequestration rate, maintaining similar cardenolide composition and concentrations in their wings under both CO2 treatments. We suggest that these increases in sequestration rate are a by‐product of compensatory feeding aimed at maintaining a nutritional target in response to declining dietary quality under eCO2. Monarch wings were more suitable for sustained flight (more elongated) when reared on plants grown under eCO2 or when reared on Asclepias syriaca or Asclepias incarnata rather than on Asclepias curassavica or Asclepias speciosa. Parasite infection engendered wings less suitable for sustained flight (wings became rounder) on three of four milkweed species. Wing loading (associated with powered flight) was higher on A. syriaca than on other milkweeds, whereas wing density was lower on A. curassavica. Monarchs that fed on high cardenolide milkweed developed rounder, thinner wings, which are less efficient at gliding flight. Ingesting foliage from milkweed high in cardenolides may provide protection from enemies through sequestration yet come at a cost to monarchs manifested as lower quality flight phenotypes: rounder, thinner wings with lower wing loading values. Small changes in morphology may have important consequences for enemy evasion and migration success in many animals. Energetic costs associated with alterations in defence and morphology may, therefore, have important consequences for trophic interactions in a changing world. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13270/suppinfo is available for this article.

Transcriptomics of monarch butterflies (Danaus plexippus) reveals that toxic host plants alter expression of detoxification genes and down‐regulate a small number of immune genes

“…Therefore, the up‐regulation of ABC transporters when feeding on low‐cardenolide milkweed compared to feeding on high‐cardenolide milkweed might be related to an increased rate of cardenolide sequestration. Although larvae may exhibit a relatively lower sequestration rate when feeding on A. curassavica than A incarnata , given the drastic difference in foliage cardenolide concentration (95‐fold), the total amount of cardenolide sequestered in larval tissue likely is much higher when fed A. curassavica , which has been demonstrated in previous studies (Decker, Soule, de Roode, & Hunter, ; Jones et al, ).…”

Effects of diet and temperature on monarch butterfly wing morphology and flight ability

“…Specifically, we expected larval growth rate to increase with temperature (Lemoine et al 2015), and for monarchs reared at higher temperatures to exhibit lighter integument wing pigmentation (Davis et al 2005), which indicates larval energy reserves (Davis 2014). Furthermore, we expected monarchs reared on the same host plant to have wing shapes more similar to one another than those reared on a different milkweed species (Berns 2012); specifically, monarchs reared on milkweed with lower cardenolide concentrations were expected to have longer, thinner wings than those fed higher cardenolide milkweed (Decker et al 2019).…”

“…Further, larval diets with high concentrations of cardenolides and foliar nitrogen decrease larval growth rate (Tao et al 2014), though high leaf nitrogen on its own increases larval growth rate (Couture et al 2015). The cardenolide concentration in larval diet can also affect the shape and symmetry of adult monarch forewings (Berns 2012;Decker et al 2019). Generally, high dietary concentrations of cardenolides are beneficial for monarch fitness when large populations of natural enemies are present, but in cases where populations of natural enemies are small, the negative effects of consuming cardenolides may outweigh the benefits.…”

“…Environmental variables such as temperature (Zhang et al 2016;Kunz et al 1995) and atmospheric gas concentrations (Decker et al 2019;Murray et al 2013) can indirectly influence insect flight ability by altering the dietary nutrient content. Moreover, rising global temperatures impact the habitat ranges (Dinh et al 2016) and developmental periods (Tan et al 2010) of some flying insect species.…”

Are Eastern and Western Monarch Butterflies Distinct Populations? A Review of Evidence for Ecological, Phenotypic, and Genetic Differentiation and Implications for Conservation

“…contributions to migration-associated traits may be particularly important for understanding differences observed between wild-caught eastern and western monarchs, especially in light of studies showing that larval host plant species can influence adult monarch size (e.g. Pocius et al 2017, Decker et al 2019, Freedman et al 2020.…”