Doctor of Philosophy, University of Michigan Ann Arbor (2018)
Bachelor of Arts, Cornell University (2013)
Tadashi Fukami, Postdoctoral Faculty Sponsor
Elevated atmospheric concentrations of CO2 increase endogenous immune function in a specialist herbivore.
The Journal of animal ecology
Animals rely on a balance of endogenous and exogenous sources of immunity to mitigate parasite attack. Understanding how environmental context affects that balance is increasingly urgent under rapid environmental change. In herbivores, immunity is determined, in part, by phytochemistry which is plastic in response to environmental conditions. Monarch butterflies, Danaus plexippus, consistently experience infection by a virulent parasite, Ophryocystis elektroscirrha, and some medicinal milkweed (Asclepias) species, with high concentrations of toxic steroids (cardenolides), provide a potent source of exogenous immunity. We investigated plant-mediated influences of elevated CO2 (eCO2 ) on endogenous immune responses of monarch larvae to infection by O. elektroscirrha. Recently, transcriptomics have revealed that infection by O. elektroscirrha does not alter monarch immune gene regulation in larvae, corroborating that monarchs rely more on exogenous than endogenous immunity. However, monarchs feeding on medicinal milkweed grown under eCO2 lose tolerance to the parasite, associated with changes in phytochemistry. Whether changes in milkweed phytochemistry induced by eCO2 alter the balance between exogenous and endogenous sources of immunity remains unknown. We fed monarchs two species of milkweed; A. curassavica (medicinal) and A. incarnata (non-medicinal) grown under ambient CO2 (aCO2 ) or eCO2 . We then measured endogenous immune responses (phenoloxidase activity, hemocyte concentration, and melanization strength), along with foliar chemistry, to assess mechanisms of monarch immunity under future atmospheric conditions. The melanization response of late-instar larvae was reduced on medicinal milkweed in comparison to non-medicinal milkweed. Moreover, the endogenous immune responses of early-instar larvae to infection by O. elektroscirrha were generally lower in larvae reared on foliage from aCO2 plants and higher in larvae reared on foliage from eCO2 plants. When grown under eCO2 , milkweed plants exhibited lower cardenolide concentrations, lower phytochemical diversity, and lower nutritional quality (higher C:N ratios). Together, these results suggest that the loss of exogenous immunity from foliage under eCO2 results in increased endogenous immune function. Animal populations face multiple threats induced by anthropogenic environmental change. Our results suggest that shifts in the balance between exogenous and endogenous sources of immunity to parasite attack may represent an underappreciated consequence of environmental change.
View details for DOI 10.1111/1365-2656.13395
View details for PubMedID 33241571
- Effects of diet and temperature on monarch butterfly wing morphology and flight ability JOURNAL OF INSECT CONSERVATION 2020
Interspecific variation and elevated CO2 influence the relationship between plant chemical resistance and regrowth tolerance.
Ecology and evolution
2020; 10 (12): 5416–30
To understand how comprehensive plant defense phenotypes will respond to global change, we investigated the legacy effects of elevated CO2 on the relationships between chemical resistance (constitutive and induced via mechanical damage) and regrowth tolerance in four milkweed species (Asclepias). We quantified potential resistance and tolerance trade-offs at the physiological level following simulated mowing, which are relevant to milkweed ecology and conservation. We examined the legacy effects of elevated CO2 on four hypothesized trade-offs between the following: (a) plant growth rate and constitutive chemical resistance (foliar cardenolide concentrations), (b) plant growth rate and mechanically induced chemical resistance, (c) constitutive resistance and regrowth tolerance, and (d) regrowth tolerance and mechanically induced resistance. We observed support for one trade-off between plant regrowth tolerance and mechanically induced resistance traits that was, surprisingly, independent of CO2 exposure. Across milkweed species, mechanically induced resistance increased by 28% in those plants previously exposed to elevated CO2. In contrast, constitutive resistance and the diversity of mechanically induced chemical resistance traits declined in response to elevated CO2 in two out of four milkweed species. Finally, previous exposure to elevated CO2 uncoupled the positive relationship between plant growth rate and regrowth tolerance following damage. Our data highlight the complex and dynamic nature of plant defense phenotypes under environmental change and question the generality of physiologically based defense trade-offs.
View details for DOI 10.1002/ece3.6284
View details for PubMedID 32607163
View details for PubMedCentralID PMC7319169
- Phytochemical changes in milkweed induced by elevated CO2 alter wing morphology but not toxin sequestration in monarch butterflies FUNCTIONAL ECOLOGY 2019; 33 (3): 411–21
Elevated atmospheric concentrations of carbon dioxide reduce monarch tolerance and increase parasite virulence by altering the medicinal properties of milkweeds
2018; 21 (9): 1353–63
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 CO2 , and measured changes in resistance, tolerance, and virulence. The most high-cardenolide milkweed species lost its medicinal properties under elevated CO2 ; 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.
View details for DOI 10.1111/ele.13101
View details for Web of Science ID 000440914500006
View details for PubMedID 30134036