This project examines how long-distance animal migrations affect the transmission of infectious diseases, using monarch butterflies and a protozoan parasite as a model system. Monarchs inhabit islands and continents worldwide and are best known for undertaking a spectacular migration in parts of North America. Parasites occur in all monarch populations examined to date and prevalence is highest in populations that breed year round and do not migrate. The investigator will conduct field studies to compare contemporary infection rates within and between multiple migratory and non-migratory monarch populations. A citizen science project, MonarchHealth, will involve volunteer observers to help track infected butterflies in N. America. Mathematical models and laboratory experiments will be developed to evaluate hypothesized mechanisms that could account for lower infection rates in migratory populations, including: host escape from contaminated habitats, costs of infection and immune defenses for monarch flight ability, and evolutionary changes in host resistance and parasite virulence.
Studying this migratory butterfly-parasite system will provide insights for effects of migration on the health of other animal species, including how human activities that alter host migratory patterns can affect pathogen spread. Proposed training activities include courses in the biology of infectious diseases and promoting environmental literacy among non-science majors at the University of Georgia. Because monarchs have captured the imagination of the public, the investigator will engage in outreach efforts that involve students and public citizens in science. These activities include a citizen science project, interactions with natural history centers and local teachers' groups, and developing a website to disseminate information on monarch butterfly parasites to the general public.
Every year, billions of animals migrate, some taking months to travel thousands of miles. Along the way, they can encounter pathogens while using different habitats and resources. A common assumption is that animal migration, like human travel across the globe, can transport pathogens long distances, and might even increase disease risks to humans. But for many animals, long distance migrations could lower the spread and prevalence of infectious disease, and might even promote the evolution of less-virulent pathogen strains. This project examined how long-distance animal migrations influence pathogen transmission and evolution, using monarch butterflies and a protozoan parasite as a model system. Monarchs inhabit multiple islands and continents worldwide and are best known for undertaking a spectacular migration in parts of North America. This NSF grant supported field studies to compare infection rates within and among multiple migratory and non-migratory monarch populations. Results showed that parasites occur in all monarch populations examined; parasite prevalence was lowest in the eastern North American population that migrates the farthest distance, and highest in several non-migratory populations. These differences might from infected monarchs migrating less successfully, or from parasite accumulation in habitats where monarchs breed year-round. Other work supported by this grant examined processes by which migration could keep prevalence low in migratory monarch populations. A citizen science project, MonarchHealth, involved hundreds of volunteers from 23 US states and 3 Canadian provinces to help track infected butterflies within the large migratory population in eastern N. America. Analyses from citizen science monitoring reports showed that parasite infections build up over time during the summer breeding season, and that high parasite prevalence is linked to high caterpillar density on milkweed plants. Thus, migration might offer monarchs a chance to escape from parasite-contaminated habitats at the end of the summer. Other field work showed that parasite prevalence decreased as the monarchs’ fall migration progressed, and that the prevalence of infection among monarchs wintering in Mexico was lower than for summer breeding or fall migrating monarchs. An explanation for these results is that many heavily infected monarchs do not survive the arduous fall migration journey. This idea was further supported by isotopic natal origin assignments of healthy and infected monarchs sampled at their wintering grounds in Mexico, which showed that healthy monarchs had traveled farther distances to reach their wintering sites than infected monarchs. Experiments involving monarchs and their parasites in captivity were also supported by this NSF grant. These experiments showed that harm caused by the protozoan parasite to monarchs can be beneficial for the parasite’s own transmission, and that parasite strains from the longest-distance migratory population were less harmful than strains from a short-distance migratory population, as might be expected if long-distance migration weeds out the most harmful parasites. Other work showed evidence for genetic variation in monarch resistance to the parasite, and indicated that monarch innate immune defense helps to suppress parasite replication. Immune defense appeared to be costly for monarchs by reducing the lipid stores available to fuel the fall migration, although monarch flight performance in captivity was similar for animals with high versus low immune defense. Additional experiments showed that parasites are susceptible to environmental degradation from heat, freezing and UV light. Although parasite strains from different source populations showed differences in their morphology, source population did not determine parasite resilience to these environmental stressors. Collaborators on this project developed mathematical models to evaluate hypothesized mechanisms that could account for lower infection rates in migratory populations; these models further asked how optimal migration strategies might shift for animal populations that are subjected to parasite pressure, relative to disease-free populations. Many migratory species are suffering population declines, with habitat loss and climate change disrupting their migration patterns. Because migration can affect their level of parasite infection, understanding the interactions between human activities, migration and infectious disease is crucial for predicting future disease risks for humans and wildlife. Results from this project indicated that if migratory populations are gradually replaced by ones that reside in the same habitats year-round, these resident populations could suffer from higher prevalence of more virulent parasites. This project also supported a number of educational activities including training 3 graduate students and 16 undergraduates in research, the development of undergraduate courses in the biology of infectious diseases, and promoting environmental literacy among non-science majors at the University of Georgia. Monarchs are a species of great public interest, and this project supported outreach efforts that involved students and public citizens in science through a citizen science projects. Other outreach efforts included interactions with natural history centers and local teachers’ groups, and the development of a website to disseminate information on monarch butterfly pathogens to the general public.
