Past Research

Virulence evolution

Conventional wisdom holds that parasites, given enough time, will evolve to be harmless, because they depend on their hosts for survival. However, virulence may evolve as an unavoidable consequence of natural selection on parasite transmission. This hypothesis is based on the idea that parasites increase their fitness by transmitting to new hosts, and that this transmission results in unavoidable harm to the host. We have used the protozoan parasite Ophryocystis elektroscirrha, which infects monarch butterflies (Danaus plexippus) in natural populations. This parasite infects monarch butterflies at the larval stage, when caterpillars ingest parasite spores that are deposited by adult butterflies on the milkweed plants that these caterpillars eat. Parasites replicate to large numbers in the monarch caterpillar, such that adult butterflies can carry millions of parasite spores. Our work has shown that large numbers of parasite spores increase parasite transmission. However, parasite growth is also detrimental to the monarch, and monarchs that carry large numbers of spores are more likely to die before the adult stage, and mate less well and live shorter as adults. This work showed that parasite fitness is greatest at intermediate numbers of parasite spores, suggesting that parasite virulence may indeed evolve as a consequence of selection on parasite transmission: by selecting for parasites that can transmit between hosts, nature selects for parasites that cause disease to their hosts.

Monarchs that are heavily infected with the protozoan parasite Ophryocystis elektroscirrha can become stuck in their pupal cases. In this case a paper wasp is taking advantage of the situation, collecting the monarch as food for its nest mates.

Virulence evolution and host heterogeneity

Most theoretical models on parasite virulence evolution assume that host populations are homogeneous. In reality, however, host populations are spatially structured, and consist of hosts that vary in their resistance to parasite infection. We have collaborated with Levi Morran to study the effects of genetic heterogeneity on virulence evolution, using Caenorhabditis elegans worms and their bacterial pathogens. This system is ideal because C. elegans has very short generation time, allowing experimental evolution in the lab.

Honey bees and parasitic mites: transmission and virulence

Honey bees are undergoing rapid declines worldwide, resulting in huge economic losses in pollination and crop production. Although the media often attribute these declines to “Colony Collapse Disorder” (a vague diagnosis with no known causes), the biggest current threat to honey bees are Varroa mites, which can wipe out large fractions of beekeeper’s colonies. Together with Berry Brosi (Emory University), Keith Delaplane (University of Georgia), Lewis Bartlett (University of Georgia) and Mike Boots (University of Californioa Berkeley), we have investigated whether the great damage done by these mites is the result of the unwitting selection of highly virulent mites through industrial bee-keeping practices. In particular, beekeepers regularly move infected bees between hives, apiaries (groups of hives) and even between different states as far apart as Georgia and California. These movements result in well-mixed bee and mite populations, and evolutionary theory has shown that parasites evolve higher virulence in such populations than in populations in which parasite transmission occurs locally. In addition to these evolutionary studies, we have investigated how high colony density contributes to mite transmission, and whether simple changes to apiary composition can reduce mite spread.

A Varroa destructor mite on the foraging honey bee on the left (photo by Jennifer Berry).

Within-host competition and evolution of drug resistance

Malaria infections often consist of a mix of drug-sensitive and resistant parasites. In theory, sensitive parasites are expected to suppress resistant parasites. Drugs could remove this suppression and thus give resistant parasites an advantage, a process known as “competitive release”. We found support for this hypothesis in rodent malaria: drug-sensitive parasites suppressed resistant parasites, and drug treatment removed this competition and led to increased transmission of resistant parasites. We have collaborated with Venkatachalam Udhayakumar (Centers for Disease Control and Prevention), to determine whether within-host competition occurs between malaria parasites in humans, and whether drug treatment can result in competitive release. Using cross-sectional studies in Ghana, Tanzania and Angola, we found strong evidence for competition, with malaria strains that are sensitive to the drug chloroquine suppressing chloroquine-resistant strains. We also found strong evidence for a cost of resistance, with resistant strains reaching lower densities in humans than sensitive strains. We have developed mathematical models to determine the role of within-host competition in the spread of drug resistance, finding that within-host competition can slow down the spread of drug resistance.

Drug-sensitive parasites suppress the growth of drug-resistant parasites in human malaria infections in Angola, Ghana and Tanzania.