NSF Org: |
IOS Division Of Integrative Organismal Systems |
Recipient: |
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Initial Amendment Date: | April 24, 2017 |
Latest Amendment Date: | July 30, 2019 |
Award Number: | 1651888 |
Award Instrument: | Continuing Grant |
Program Manager: |
Mamta Rawat
mrawat@nsf.gov (703)292-7265 IOS Division Of Integrative Organismal Systems BIO Direct For Biological Sciences |
Start Date: | September 1, 2017 |
End Date: | August 31, 2023 (Estimated) |
Total Intended Award Amount: | $964,898.00 |
Total Awarded Amount to Date: | $964,898.00 |
Funds Obligated to Date: |
FY 2018 = $253,032.00 FY 2019 = $503,970.00 |
History of Investigator: |
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Recipient Sponsored Research Office: |
2200 N SQUIRREL RD ROCHESTER MI US 48309-4401 (248)370-4116 |
Sponsor Congressional District: |
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Primary Place of Performance: |
2200 N Squirrel Rd Rochester MI US 48309-4479 |
Primary Place of Performance Congressional District: |
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Unique Entity Identifier (UEI): |
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Parent UEI: |
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NSF Program(s): | Symbiosis Infection & Immunity |
Primary Program Source: |
01001819DB NSF RESEARCH & RELATED ACTIVIT 01001920DB NSF RESEARCH & RELATED ACTIVIT |
Program Reference Code(s): |
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Program Element Code(s): |
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Award Agency Code: | 4900 |
Fund Agency Code: | 4900 |
Assistance Listing Number(s): | 47.074 |
ABSTRACT
Recent changes in global temperature variability make it vital to develop better predictive models for how temperature fluctuations influence species interactions like parasitism. This is particularly pressing for amphibians, many of which are threatened by temperature-dependent emerging diseases. One challenge in predicting temperature effects on parasitism is that both host and parasite have independent responses to temperature, and these responses are difficult to disentangle with infection experiments. To help solve this problem, this project will test a new Metabolic Theory (MT) based approach to modeling parasite-host interactions in variable-temperature environments. MT postulates that metabolic rates govern all biological rates, leading to the prediction that all physiological processes within a given organism should respond to temperature in similar ways. This means it should be possible to estimate key model parameters for the temperature-dependence of parasite infectivity or host resistance to infection, by measuring the temperature-dependence of metabolic proxies like parasite growth in culture or host respiration. This approach could be especially valuable for predicting temperature effects on multi-host pathogens like the amphibian chytrid fungus, because it is impossible to conduct infection experiments for every species threatened by this disease. These funds will also help to support: (1) a new thermal-physiology classroom lab activity for use in Introductory Biology and Project Upward Bound's summer academy, (2) an annual summer workshop to train graduate teaching assistants and early-career faculty in modern teaching methods, and (3) at least four graduate students and over a dozen undergraduate student researchers.
This project will test assumptions and predictions of a new Metabolic Theory (MT) based approach to modeling parasite-host interactions in variable-temperature environments, using chytrid fungus in amphibians as a model host-parasite system. Thermal performance curves for parasite infectivity and host resistance will be described using modified Sharpe-Schoolfield equations, and key model parameters (e.g., activation energies for parasite infectivity and host resistance) will be estimated by measuring the temperature dependence of host and parasite metabolic proxies. These separate thermal performance curves will then be combined into a predictive model for parasite growth rates on hosts, and maximum-likelihood statistics will be used to estimate remaining model parameters. To model thermal acclimation effects, key parameters will be allowed to vary as functions of host or parasite acclimation temperatures. The specific aims of this project are: (1) to test the core assumption that different organisms and physiological processes have similar values and thermal acclimation responses for key MT model parameters, (2) test the ability of MT based models to predict parasite transmission in variable-temperature environments, and (3) delve into the cellular and molecular mechanisms underlying thermal acclimation effects on host-parasite interactions. To achieve the third goal, we will measure effects of temperature and thermal acclimation on (5) cellular immune activity and (6) gene expression responses to chytridiomycosis infection. We will replicate experiments using arrays of custom-built experimental incubators and temperature-controlled outdoor mesocosms.
PUBLICATIONS PRODUCED AS A RESULT OF THIS RESEARCH
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PROJECT OUTCOMES REPORT
Disclaimer
This Project Outcomes Report for the General Public is displayed verbatim as submitted by the Principal Investigator (PI) for this award. Any opinions, findings, and conclusions or recommendations expressed in this Report are those of the PI and do not necessarily reflect the views of the National Science Foundation; NSF has not approved or endorsed its content.
The core scientific goal of this project was to develop, parameterize, and test assumptions of a new mathematical approach to modeling temperature dependent parasitic infections in cold-blooded animals. A key challenge with describing the temperature dependence of parasitism is that the host and the parasite are likely to each have their own independent responses to temperature, and it is difficult to tease apart these processes. For example, if a host becomes more infected at cooler temperatures, it is unclear whether this is due to higher parasite infectivity at cool temperatures or due to lower host resistance. We sought to disentangle these processes by developing mathematical models to describe thermal mismatches between parasite infectivity and host resistance, using models of thermal performance derived from metabolic theory (MT; Figure 1). Working with a pandemic chytrid fungus that infects frogs and salamanders, we found that this approach worked remarkably well to describe individual infection dynamics in at least two frog species. Work is ongoing to test how well this approach works in additional host species.
We also sought to determine how well our MT-based thermal mismatch models can be scaled up to predict transmission dynamics in host populations. In a population-level transmission experiment conducted in heated outdoor mesocosms (Figure 2), we found similar temperature dependence of infection for groups of African clawed frogs relative to infections in indivudually isolated frogs. However, overall infection intensities were much higher than in individual-level experiments. These higher infection levels were predicted by an individual-based model of transmission dynamics whose parameter values were derived from individual infection experiments. These results suggest that MT-based thermal mismatch models may be capable of successfully predict unexpected outcomes when scaling from individual infections to population level transmission dynamics.
This project also yielded evidence of interesting patterns in how thermal acclimation affected host thermal limits, metabolic rates, and resistance to infection, as well as evidence that the infective stage of the amphibian chytrid pathogen has either constitutive responses to temperature (i.e., no thermal acclimation effects) or fully acclimates to a new temperature within minutes of a temperature shift. This is consistent with MT-based predictions of rapid acclimation times in microorganisms, due to mass scaling relationships in which smaller organisms tend to have faster metabolic rates. Other experiments revealed that a “cooler is better” thermal acclimation effect on the metabolic rate of a model salamander species might be partially caused by a thermal mismatch between digestive efficiency and metabolic mass loss. This thermal mismatch appears to have led to lower energy reserves and correspondingly lower metabolic rates in warm-acclimated animals. Consistent with this hypothesis, a follow up experiment revealed similar patterns of gene expression in cold-acclimated axolotls following a period of fasting, compared to warm-acclimated axolotls that were given extra food.
As part of the educational component of this project, we designed and implemented multiple versions of a Thermal Metabolism Lab Activity to introduce students to the biological, chemical, and physical reasons why warm- and cold-blooded organisms respond to temperature in different ways. We implemented one version of this activity for the Project Upward Bound (PUB) Summer Academy, a program that prepares high school students for college. Over the course of four summers (not including pandemic years), at least 120 PUB students worked collaboratively to develop and test hypotheses about the temperature dependence of frog metabolism, human responses to cold exposure, the temperature dependence of chemical reactions, and the energetic costs of maintaining a high body temperature (Figure 3). We also designed and implemented online and in person versions of these activities for use in the introductory lab course for our undergraduate Biology majors (BIO 1201), reaching more than 1200 students in years 2-6 of the project.
As another educational component to this project, PI Raffel developed and implemented an intensive summer teaching workshop for graduate students, based on the FIRST IV program (Faculty Institutes for the Reform of Science Teaching) and aimed at introducing them to evidence-based teaching practices including constructive alignment, universal design for learning, and active learning pedagogies. This program is open to all graduate students at Oakland University and so far has awarded certificates of completion to 186 graduate students.
This project also supported two postdoctoral scholars and at least 50 students to conduct independent research with the Raffel Lab. These students included four PhD students (two successfully defended dissertations and two nearly complete), four completed Masters theses, and 42 undergraduate research assistants including eight who completed Honors College theses.
Last Modified: 12/20/2023
Modified by: Thomas Raffel
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