All things are poison, and nothing is without poison."
-Paracelsus
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Terms such as nutrient, stress, food, and toxin are part of our everyday vocabulary. Yet, anyone thinking seriously about the meaning of these terms will find that they can be misleading. For instance, humans require calories from food in order to develop and reproduce, yet excessive caloric intake can lead to disease and shortened lifespan. Plants produce toxic chemicals to ward off consumers, yet some of these toxins appear to have health benefits at low levels, even if their complete absence from the diet produces no obvious pathology. On a more global scale, human activities such as agriculture and fossil fuel combustion are increasing the availability of many nutrients that have historically been in limited supply for plants and their consumers. While nitrogen fertilization generally benefits plants, increases in nitrogen availability do not always benefit consumers and can even be detrimental to insects.
The above examples illustrate the reality that many substances cannot be classified solely as nutrients or stressors but rather fall along a nutrient-stressor continuum. The challenge of predicting how organisms will respond to such substances requires an integrated approach, combining insights from evolutionary theory with knowledge of underlying developmental mechanisms and surrounding ecological context. Understanding the diversity of organismal responses to variation in stress and nutrition is of broad importance to areas ranging from conservation biology to human health.
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My research aims to understand why individuals, populations, and species vary in their responses to changes in stress and nutrition. I approach this problem both theoretically and empirically using a variety of model animal systems. My empirical work typically integrates measures of whole organism performance with underlying molecular and genetic mechanisms.
Currently, I am exploring this problem in three research themes, outlined below:
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Monarch caterpillar on a milkweed plant at Cedar Creek Ecosystem Science Reserve, late August 2021
Humans are drastically altering the availability and distribution of many nutrients that have been historically limiting for organisms. While modest changes in nutrient availability may be neutral or even beneficial for organisms, drastic changes are likely stressful. With Dr. Emilie Snell-Rood and members of her lab, I have been studying how anthropogenic changes in nutrient availability affect organismal development and performance, focusing on insect pollinators in roadside habitats as a model system. Roadside verges provide considerable habitat for insect pollinators such as butterflies, yet roads are significant sources of macronutrients (e.g., nitrogen from vehicles) as well as micronutrients (e.g., sodium from road salt and zinc from brake pad wear and tear). These nutrients can accumulate in soil and plant tissue of roadside plants, where they become available to foraging insects. This situation provides an opportunity to study the ecological and evolutionary consequences of anthropogenic changes in nutrient availability, while at the same time generating useful insights for insect conservation.
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My research on roadside nutrition has primarily focused on two model insect systems: the cabbage white butterfly (Pieris rapae), a widely distributed agricultural pest species that frequently inhabits plants along roadsides and other urban areas; and the monarch butterfly (Danaus plexippus), a charismatic species of conservation concern whose habitat is currently being considered for restoration along roadside verges. My research in this area has found that with respect to zinc - a micronutrient that quickly becomes stressful at higher levels - monarchs are less tolerant than the disturbance-adapted cabbage white, yet zinc concentrations typically observed in roadside plants do not appear to severely impact the performance of either species (Shephard et al., 2020 Insect Conservation and Diversity). Furthermore, cabbage white genotypes that are more tolerant of zinc pollution show very few performance costs of tolerance and even perform better than less tolerant genotypes under non-polluted environments, which may be due to the fact that this species is highly dispersive and widely distributed, experiencing selection in both polluted and non-polluted environments (Shephard et al., 2021 Evolutionary Applications). I hypothesize that in populations under such patchy selection with pollutants, selection may erode performance costs of tolerance. Despite the lack of evidence for global costs of tolerance, I found that monarch butterflies experience costs of zinc tolerance at more local scales, particularly in contexts where critical dietary macronutrients (e.g., nitrogen and phosphorous) are in low supply (Shephard et al., in review). However, when dietary macronutrients are abundant, monarchs tend to benefit from zinc. These results point to the hypothesis that whether zinc acts as a toxicant or a nutrient may depend on the relative availability of dietary macronutrients. While monarch zinc tolerance is influenced by variation in macronutrient availability, tolerance is not impacted by the availability of other micronutrients such as sodium, even though roadside sodium pollution appears to be more stressful than zinc (Shephard et al., 2021 Conservation Physiology). Current research on this front is continuing to investigate interactions between anthropogenic increases in macronutrient and micronutrient availability, as well as how evolutionary history may influence how populations and species respond to nutritionally novel environments.
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Theme 1:
Organismal responses to anthropogenic changes in nutrient availability
Biomedical research has consistently found that developmental pathways tied to stress resistance and nutrition play key roles in aging. How do these factors contribute to the evolution of aging? I am exploring this question using two approaches: ​
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1) Impacts of stress, nutrition, and reproduction on monarch butterfly lifespan:
The monarch butterfly displays incredible plasticity in longevity between its summer morph (reproductive and short-lived) and migratory morph (non-reproductive and long-lived). Using this unique system, I am currently investigating how oxidative stress and dietary antioxidant intake interact with reproductive investment to affect lifespan.
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2) Experimental evolution of stress resistance and lifespan in nematodes:
In Fall 2021, I will be starting an Interdisciplinary Doctoral Fellowship in collaboration with the Institute on the Biology of Aging and Metabolism (iBAM) at the University of Minnesota. For this project, I will take an experimental evolution approach using C. elegans as a system to study how stress resistance and nutrition affect aging.
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Monarch butterflies aging in the laboratory, early September 2021
"Enlarged C. elegans" from Wikimedia Commons, courtesy of National Human Genome Research Institute
Theme 2:
The roles of stress and nutrition in the evolution of aging
Effects of various concentrations of dietary exposure to anthropogenic increases in zinc on survival to adulthood in the monarch butterfly (left) and the cabbage white butterfly (right). Image from Shephard et al. 2020 Insect Conservation and Diversity
Proportion surviving zinc pollution
Reproductive effort
(relative to body size)
Cabbage white butterfly families that are more tolerant of anthropogenic increases in dietary zinc (i.e., higher proportion of butterflies in the family surviving zinc pollution) also have greater reproductive effort (egg number x average egg size) under non-polluted conditions. Image from Shephard et al., 2021 Evolutionary Applications
Theme 3:
What is stress? Evolutionary, developmental and philosophical perspectives
I have a keen interest in the philosophy of science, and I am particularly interested in drawing connections between disparate areas of research to generate new hypotheses and insights. I believe that this is not only useful for advancing scientific thought but is also one of the most beautiful and rewarding aspects of science. Stress is one topic that is widely studied across biological disciplines, yet a unified concept of stress remains elusive. I am working to understand how our modern evolutionary concepts of stress may be modified or refined through integration of mechanistic insights from cellular, molecular, and developmental biology.
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