Elsevier

Current Opinion in Virology

Volume 21, December 2016, Pages 67-74
Current Opinion in Virology

Transmission and evolution of tick-borne viruses

https://doi.org/10.1016/j.coviro.2016.08.005Get rights and content

Highlights

  • Tick-borne viruses are classified into six virus families, including Flaviviridae.

  • The mechanisms of virus transmission by ticks are reviewed.

  • Tick-borne flaviviruses comprise geographically and ecologically distinct lineages.

  • Virus diversity is shaped by RNA inference and transmission bottlenecks.

Ticks transmit a diverse array of viruses such as tick-borne encephalitis virus, Powassan virus, and Crimean-Congo hemorrhagic fever virus that are reemerging in many parts of the world. Most tick-borne viruses (TBVs) are RNA viruses that replicate using error-prone polymerases and produce genetically diverse viral populations that facilitate their rapid evolution and adaptation to novel environments. This article reviews the mechanisms of virus transmission by tick vectors, the molecular evolution of TBVs circulating in nature, and the processes shaping viral diversity within hosts to better understand how these viruses may become public health threats. In addition, remaining questions and future directions for research are discussed.

Introduction

Tick-borne viruses (TBVs) are highly focal infections that persist in nature by continuous transmission among vector ticks and wild animal hosts [1]. Although the natural history varies considerably for each virus, at their core, they all require a permissive environment that supports the spatial and temporal overlap of the virus, vector, and vertebrate host. These viruses often remain undetected until humans encroach upon the natural transmission cycle, become infected, and develop clinical illness leading to their identification. In recent decades, a number of established TBVs have emerged as public health concerns including tick-borne encephalitis virus (TBEV) in Europe and Asia [2], Crimean-Congo hemorrhagic fever virus (CCHFV) in Asia and Africa [3], and Powassan virus (POWV) in North America (Table 1) [4]. Meanwhile, new TBVs are continually being discovered including severe fever with thrombocytopenia syndrome virus or Huaiyangshan virus in East Asia [5], and Heartland and Bourbon viruses in the U.S. [6, 7]. These trends are driven by the proliferation of ticks in many regions of the world and by human encroachment into tick-infested habitats. In addition, most TBVs are RNA viruses that mutate faster than DNA-based organisms and replicate to high population sizes within individual hosts to form a heterogeneous population of closely related viral variants termed a mutant swarm or quasispecies [8]. This population structure allows RNA viruses to rapidly evolve and adapt into new ecological niches, and to develop new biological properties that can lead to changes in disease patterns and virulence [9]. The purpose of this paper is to review the mechanisms of virus transmission among vector ticks and vertebrate hosts and to examine the diversity and molecular evolution of TBVs circulating in nature. This article also describes recent research on viral genetic changes occurring during tick-borne transmission to better understand how these viruses interact with their hosts and emerge as health problems.

Section snippets

Taxonomy of tick-borne viruses

TBVs comprise a diverse array of viral entities that are classified into to six virus families: Flaviviridae, Bunyaviridae, Orthomyxoviridae, Rhabdoviridae, Reoviridae, and Asfarviridae (Table 1). The most important TBVs belong to the family Flaviridae and Bunyaviridae and include numerous viral agents that cause encephalitis or hemorrhagic fever in humans. Virus families differ in many fundamental characteristics including nucleic acid type, morphology, and replication strategy that are the

Virus transmission by tick vectors

Both Argasidae (soft-ticks) and Ixodidae (hard-ticks) can transmit viruses; however, the vast majority of TBVs of human and agricultural importance are transmitted by hard-ticks [20]. Hard-ticks have three distinct life-stages; larvae, nymph and adults with each stage dependent on blood from a vertebrate host for either molting or oogenesis. Consequently there are repeated opportunities for TBV transmission which can occur through a number of mechanisms.

Horizontal virus transmission to ticks

Molecular phylogenetics of tick-borne flaviviruses

Phylogenetic approaches have been used to investigate the genetic diversity, evolution and dispersal patterns of tick-borne flaviviruses circulating in nature [40, 41, 42••, 43]. These viruses were shown to form a highly asymmetric phylogenetic tree with a relatively constant rate of branching [44]. The high proportion of deep nodes within the tick-borne flavivirus tree reflects the survival of ancient viral lineages. An earlier analysis found that tick-borne flaviviruses formed a genetic cline

Viral population diversity

Viruses exist within and between hosts as a collection of unique viral variants [54]. This is especially true for RNA viruses which are the majority of the TBVs. These complex populations arise because viruses exist as large populations, have short generation times and encode for RNA-dependent RNA polymerases that lack proofreading capabilities [54]. This population structure enables them to explore sequence space and consequently emerge, adapt and persist in new or changing ecological niches [

Conclusions

The TBVs represent a large and diverse group of viruses, many of which adversely affect human and livestock populations, yet their transmission and evolution are poorly understood. In recent years, there have been advances in the molecular phylogenetics of tick-borne flaviviruses; however, the same cannot be said for the vast majority of other TBVs and continued research is needed. In addition, the mechanisms and kinetics by which TBVs infect and disseminate within ticks and how they are

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

We thank Dr. Nathan Grubaugh for help with figure preparation and his useful discussions. This work was supported in part by grants from the Centers for Disease Control and Prevention (U50/CCU116806-01-1), the US Department of Agriculture Hatch Funds (CONH00773), and Multistate Research Project (NE1443).

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