Biological transmission of arboviruses: reexamination of and new insights into components, mechanisms, and unique traits as well as their evolutionary trends

Abstract

Among animal viruses, arboviruses are unique in that they depend on arthropod vectors for transmission. Field research and laboratory investigations related to the three components of this unique mode of transmission, virus, vector, and vertebrate host, have produced an enormous amount of valuable information that may be found in numerous publications. However, despite many reviews on specific viruses, diseases, or interests, a systematic approach to organizing the available information on all facets of biological transmission and then to interpret it in the context of the evolutionary process has not been attempted before. Such an attempt in this review clearly demonstrates tremendous progress made worldwide to characterize the viruses, to comprehend disease transmission and pathogenesis, and to understand the biology of vectors and their role in transmission. The rapid progress in molecular biologic techniques also helped resolve many virologic puzzles and yielded highly valuable data hitherto unavailable, such as characterization of virus receptors, the genetic basis of vertebrate resistance to viral infection, and phylogenetic evidence of the history of host range shifts in arboviruses. However, glaring gaps in knowledge of many critical subjects, such as the mechanism of viral persistence and the existence of vertebrate reservoirs, are still evident. Furthermore, with the accumulated data, new questions were raised, such as evolutionary directions of virus virulence and of host range. Although many fundamental questions on the evolution of this unique mode of transmission remained unresolved in the absence of a fossil record, available observations for arboviruses and the information derived from studies in other fields of the biological sciences suggested convergent evolution as a plausible process. Overall, discussion of the diverse range of theories proposed and observations made by many investigators was found to be highly valuable for sorting out the possible mechanism(s) of the emergence of arboviral diseases.

FIG. 1.

Phylogram of flaviviruses using a neighbor-joining inference method (MEGA) based on the complete RNA-dependent RNA polymerase domain of the NS5 gene of 35 viruses deposited in GenBank. The numbers at nodes indicate % branch supports by bootstrap sampling with 500 replicates. Distances were calculated with Poisson correction. Virus abbreviation-virus name (GenBank accession number): ALKV-Alkhurma virus (NC004355); APOIV-Apoi virus (AF160193); BAGV-Bagaza virus (AY632545*); BSQV-Bussuquara virus (AY632536*); CFAV-cell fusing agent virus (M91671); DTV-deer tick virus (NC003218); DENV-1—dengue serotype 1 (U88535); DENV-2—dengue serotype 2 (M20558); DENV-3—dengue serotype 3 (M93130); DENV-4—dengue serotype 4 (M14931); ENTV—Entebbe bat virus (AY632537*); IGUV—Iguape virus (AY632538*); ILHV—Ilhéus virus (AY632539*); JEV—Japanese encephalitis virus (M18370); KRV—Kamiti River virus (NC005064); KEDV—Kédougou virus (AY632540*); KOKV—Kokobera virus (AY632541*); LGTV—Langat virus (NC003690); LIV—louping ill virus (Y07863); MODV—Modoc virus (AJ242984); MMLV—Montana myotis leukoencephalitis virus (NC00419.1); MVEV—Murray Valley encephaliltis virus (NC000943); OHFV—Omsk hemorrhagic fever virus (AY193805); POWV—Powassan virus (L06436); RBV—Rio Bravo virus (AF144692); ROCV—Rocio virus (AY632542*); SEPV—Sepik virus (AY632543*); SLEV—St. Louis encephalitis virus-Argentine 66 (AY632544*); TABV—Tamana bat virus (AF285080); TBEV—tick-borne encephalitis virus (U27495); USUV—Usutu virus (NC006551); WNV—West Nile virus (AF196835); YFV—yellow fever virus (X03700); YOKV—Yokose virus (AB114858); and ZIKV—Zika virus (AY632535*). *, sequence deposited by G. Kuno and G.-J. J. Chang.