Malaria parasites in the genus Plasmodium are well known as causing disease in humans, but half of the roughly 200 species in this genus use lizards as their vertebrate hosts, and many of these species can be found in lizards in Panama. These parasites have been the focus of studies on ecology, epidemiology, and behavior, but their taxonomic classifications and patterns of diversification remain unclear, and this has hindered their use as a model for studying disease. The first goal of this study is to resolve the taxonomy of these Panamanian parasites. Malaria parasite species are traditionally classified based on differences in their morphology, but the simple and changing morphology of the Panamanian species has confounded taxonomists for decades. Their taxonomy will be revised by analyzing genetic information using novel species-delimitation methods. The second goal of this study is to clarify the patterns of diversification in the widespread lizard parasite Plasmodium floridense. It is distributed in southern North America, throughout the Caribbean, and in Middle America, but like most malaria parasites, its history of colonization remains unknown. Newly collected samples from Panama will be combined with previously collected samples from across the parasite?s range, and these will be used to elucidate the parasite?s pattern of diversification.

The results of this research will be disseminated broadly and used to promote teaching and learning. Curriculum materials will be developed in partnership with the Gottesman Center at the American Museum of Natural History (AMNH) to be used in New York City high school biology classrooms. Lectures and laboratory activities will also be developed as part of the Science Research Mentoring Program at the AMNH. Both will introduce urban high school students to the vast diversity of parasite species from across the tree of life. Finally, results of this research will be posted over several entries on two blogs, each of which is well established and has a wide readership, to facilitate the dissemination of the research to the general public.

Project Report

Parasites are ubiquitous, comprising a significant portion of biodiversity and occurring in host species across the tree of life. Nonetheless, both parasites and the processes contributing to parasite diversification are, in general, poorly studied. This dissertation research centered on the malaria and pinworm parasites of a model host group, the Caribbean Anolis lizards, in order to shed light on parasite diversification. The first part of our research focused on the Caribbean lizard malaria parasite Plasmodium floridense, where we tested the hypothesis that clonal reproduction shapes evolution in the parasite species. Clonal reproduction may affect evolution of malaria parasites if the parasites’ transmission and life cycle – wherein they alternate between sexual reproduction in an invertebrate host and asexual reproduction in a vertebrate host – favors sex between two identical parasite clones. Clonal reproduction is predicted to result in: (1) morphologically cryptic (i.e. superficially indistinguishable) species that exhibit (2) low within-species variation and (3) recent between-species divergence. We collected and identified 63 single-infection samples of P. floridense from across the parasite’s range, and sequenced seven mitochondrial, apicoplast, and nuclear genes. We used these data to test our three predictions, and each was supported: (1) we identified and described 11 provisionally cryptic species within P. floridense; (2) each of these species exhibits low within-species genetic variation; and (3) the divergence times between species are very recent (some pairs diverged ~110,000 years ago). Combined with other studies, these results have strong implications for malaria parasite classification and suggest that the evolution of malaria parasites has been strongly shaped by clonal evolution. The second part of our research focused on pinworm parasites and asked questions about the affect of host specificity on parasite diversification. Host specificity is one of the potential factors affecting parasite diversification because gene flow may be facilitated or constrained by the number of host species that a parasite can exploit. We tested this hypothesis using a co-structure approach, comparing two sympatric pinworm parasites that differ in host specificity – Parapharyngodon cubensis and Spauligodon anolis – on the Puerto Rican Bank and St. Croix in the Caribbean. Spauligodon anolis specializes on Anolis lizards, whereas P. cubensis parasitizes Anolis lizards as well as many other species of lizards and snakes. We collected lizards from across the Puerto Rican Bank and St. Croix, sampled them for S. anolis and P. cubensis, and generated nuclear and mitochondrial sequence data from the parasites. We used these data to show that P. cubensis is comprised of multiple cryptic species that exhibit limited population structure relative to S. anolis, which is consistent with our prediction based on their host specificity. Our results are consistent with the hypothesis that host specificity shapes parasite diversification, and suggest that even moderate differences in host specificity may contribute to substantial differences in diversification. Two main conclusions can be drawn from this research. First, parasite diversity in Caribbean Anolis lizards is largely underestimated, and molecular data are necessary to effectively delimit both malaria and pinworm parasites. Second, parasite transmission – between host individuals and host species – affects parasite diversification, and differences in transmission may be among the most important factors shaping the diversity of parasites alive today.

Agency
National Science Foundation (NSF)
Institute
Division of Environmental Biology (DEB)
Type
Standard Grant (Standard)
Application #
1210547
Program Officer
Simon Malcomber
Project Start
Project End
Budget Start
2012-07-01
Budget End
2014-06-30
Support Year
Fiscal Year
2012
Total Cost
$14,452
Indirect Cost
Name
American Museum Natural History
Department
Type
DUNS #
City
New York
State
NY
Country
United States
Zip Code
10024