Benny Rice, PhD

Associate Research Scholar, EEB, Princeton University

2. Pathogen Persistence: Evolutionary Ecology of Parasite Diversity


Parasite taxa provide rich models to probe fundamental questions in ecology and evolutionary biology such as co-existence and trade-offs along the specialist-generalist continuum. My research focuses on a cross-scale approach, studying malaria parasites of humans and wildlife to probe drivers of parasite diversity from the species-level scale to characterizing patterns of genetic variation within parasite populations.

Genomic evidence suggests differences in a lineage’s repertoire of surface proteins disproportionately contribute to the divergence observed between Plasmodium parasite species, for example among the diverse parasite assemblage in Southeast Asia infecting a range of primate hosts, including humans (e.g., P. vivax and P. knowlesi) [9]. Given that the gene families encoding these surface proteins are thought to play crucial roles in host cell invasion and immune evasion, gene family evolution was hypothesized to associate with parasite host range (e.g., human vs nonhuman primates). Pointing to redundancy in invasion biology instead, we observed high rates of gene duplication, conversion, and loss across parasite lineages in the gene family analyzed (merozoite surface protein 3, msp3), unassociated with host preference [9]. There is rich potential to expand this work to additional parasite clades and gene families, where I aim to leverage my field expertise in Madagascar. Current grant applications in progress target Plasmodium parasites infecting reptiles (e.g., Furcifer chameleons [10]) and another primate radiation - lemurs in Madagascar. Empirical work with these host-parasite systems will be paired with ecological theory to investigate the determinants of parasite lineage co-existence and the role evolving host communities may play.

At the intra-species scale, how ecological, evolutionary, and epidemiological forces intersect to maintain parasite genetic variation within populations is of considerable applied relevance yet remains poorly characterized in many systems [11–13]. For example, patterns of genetic variation can be used to infer trends in parasite dynamics over time, with clear use for public health programs trying to reduce parasite transmission. Existing work has explored how landscape features such as proximity to forest and deforestation associate with heterogeneity in malaria infection in forest-adjacent populations in Madagascar [14–16]. Future work seeks to evaluate how the composition of the mosquito vector population shapes allelic diversity at a parasite locus (pfs47) involved in P. falciparum parasite replication in the vector, and how extreme weather events impact dynamics.

References

9. Rice BL, Acosta MM, Andreína Pacheco M, Carlton JM, Barnwell JW, Escalante AA. The origin and diversification of the merozoite surface protein 3 (msp3) multi-gene family in Plasmodium vivax and related parasites. Molecular Phylogenetics and Evolution. 2014;78: 172–184.
10. Raselimanana M, Rice B, Kappeler PM, Eckhardt F. Phenology and growth plasticity in a short-lived chameleon under climatic variation. Salamandra. 2021;57.
11. Daniels RF, Rice BL, Daniels NM, Volkman SK, Hartl DL. The utility of genomic data for Plasmodium vivax population surveillance. Pathogens and Global Health. 2015;109: 153–161.
12. Rice BL, Golden CD, Anjaranirina EJG, Botelho CM, Volkman SK, Hartl DL. Genetic evidence that the Makira region in northeastern Madagascar is a hotspot of malaria transmission. Malaria Journal. 2016;15: 596.
13. Rice BL, Acosta MM, Pacheco MA, Escalante AA. Merozoite surface protein-3 alpha as a genetic marker for epidemiologic studies in Plasmodium vivax: a cautionary note. Malaria Journal. 2013;12: 288.
14. Rice BL, Golden CD, Randriamady HJ, Arisco NJ, Hartl DL. Integrating approaches to study land use change and hotspots of malaria transmission in rural Madagascar: an observational study. The Lancet Planetary Health. 2018;2: S19.
15. Arisco N, Rice BL, Tantely LM, Girod R, Emile GN, Randriamady HJ, et al. Deforestation and malaria in Madagascar: a new framework to explore linkages in the absence of robust health reporting infrastructure. The Lancet Planetary Health. 2019;3: S14.
16. Rice BL, Golden CD, Randriamady HJ, Rakotomalala AANA, Vonona MA, Anjaranirina EJG, et al. Fine-scale variation in malaria prevalence across ecological regions in Madagascar: a cross-sectional study. BMC Public Health. 2021;21: 1018.



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