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EVOLUTION
Arbovirus evolution in vivo is constrained by host alternation

Lark L. Coffey^*,, Nikos Vasilakis^*,, Aaron C. Brault^*,, Ann M. Powers^¶, Frédéric Tripet^||, and Scott C. Weaver^*,**

*Department of Pathology and Center for Tropical Diseases, University of Texas Medical Branch, Galveston, TX 77555; ^¶Division of Vector-Borne Infectious Diseases, Centers for Disease Control and Prevention, Fort Collins, CO 80521; and ^||Center for Applied Entomology and Parasitology, School of Life Sciences, Keele University, Newcastle, Staffordshire ST5 5BG, United Kingdom

Edited by Peter Palese, Mount Sinai School of Medicine, New York, NY, and approved March 11, 2008 (received for review January 8, 2008)

Abstract

The intrinsic plasticity of RNA viruses can facilitate host range changes that lead to epidemics. However, evolutionary processes promoting cross-species transfers are poorly defined, especially for arthropod-borne viruses (arboviruses). In theory, cross species transfers by arboviruses may be constrained by their alternating infection of disparate hosts, where optimal replication in one host involves a fitness tradeoff for the other. Accordingly, freeing arboviruses from alternate replication via specialization in a single host should accelerate adaptation. This hypothesis has been tested by using cell culture model systems with inconclusive results. Therefore, we tested it using an in vivo system with Venezuelan equine encephalitis virus (VEEV), an emerging alphavirus of the Americas. VEEV serially passaged in mosquitoes exhibited increased mosquito infectivity and vertebrate-specialized strains produced higher viremias. Conversely, alternately passaged VEEV experienced no detectable fitness gains in either host. These results suggest that arbovirus adaptation and evolution is limited by obligate host alternation and predict that arboviral emergence via host range changes may be less frequent than that of single host animal RNA viruses.

adaptation | RNA virus emergence | venezuelan equine encephalitis virus

Author contributions: L.L.C., N.V., A.C.B., A.M.P., and S.C.W. designed research; L.L.C., N.V., A.C.B., A.M.P., and S.C.W. performed research; L.L.C., N.V., A.C.B., F.T., and S.C.W. analyzed data; and L.L.C., A.C.B., and S.C.W. wrote the paper.

Present address: Unité des Interactions Moléculaires Flavivirus-Hôtes, Institut Pasteur, 75724 Paris, France.

Present Address: Department of Molecular Genetics and Biochemistry and Center for Vaccine Research, School of Medicine, University of Pittsburgh, Pittsburgh, PA 15261.

Present address: Department of Pathology, Microbiology and Immunology and Center for Vector-borne Diseases, University of California Davis, Davis, CA 95616.

The authors declare no conflict of interest.

This article is a PNAS Direct Submission.

**To whom correspondence should be addressed. E-mail: sweaver{at}utmb.edu

© 2008 by The National Academy of Sciences of the USA

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