Tick-borne encephalitis virus subtypes emerged through rapid vector switches rather than gradual evolution

Abstract

Tick-borne encephalitis is the most important human arthropod-borne virus disease in Europe and Russia, with an annual incidence of about 13 thousand people. Tick-borne encephalitis virus (TBEV) is distributed in the natural foci of forest and taiga zones of Eurasia, from the Pacific to the Atlantic coast. Currently, there are three mutually exclusive hypotheses about the origin and distribution of TBEV subtypes, although they are based on the same assumption of gradual evolution. Recently, we have described the structure of TBEV populations in terms of a clusteron approach, a clusteron being a structural unit of viral population [Kovalev and Mukhacheva (2013) Infect. Genet. Evol., 14, 22-28]. This approach allowed us to investigate questions of TBEV evolution in a new way and to propose a hypothesis of quantum evolution due to a vector switch. We also consider a possible mechanism for this switch occurring in interspecific hybrids of ticks. It is necessarily accompanied by a rapid accumulation of mutations in the virus genome, which is contrary to the generally accepted view of gradual evolution in assessing the ages of TBEV populations. The proposed hypothesis could explain and predict not only the formation of new subtypes, but also the emergence of new vector-borne viruses.

Keywords: Clusteron; molecular clock; quantum evolution; tick hybrids; tick-borne encephalitis virus; vector switch.

Figure 1

Phylogenetic network of TBEV clusterons constructed on the basis of the sequences of the E protein fragment for all three subtypes. Three domains corresponding to the TBEV subtypes as well as relationships between all clusterons are shown. Clusterons are designated as described in the text and transition points by numbers in bold (see Results). *Sequence of the unique strain 179-78, being proposed as the fourth TBEV subtype, is included in the analysis to show its relationships with clusterons.

Figure 2

Two approaches to the calculation of the evolutionary age of TBEV. (A) Assuming the hypothesis of gradual evolution (genetic distances are calculated between “clusteron-founders” and putative common ancestor). The age of a branch corresponds to the age of the ancestor. (B) Assuming the hypothesis of quantum evolution resulting in a dramatic change of genetic features and nonlinear accumulation of mutations (genetic distances are calculated within “clusteron-founders”). TBEV subtypes or lineages are likely to emerge not from the putative ancestor but rather directly from the existing viral forms.

Figure 3

A plausible scenario for TBEV evolution and its spread over Eurasia. The proposed route of the virus distribution, associated with anthropogenic factors, the ages of subtypes, and sympatric zones are shown.

Figure 4

A hypothesized mechanism for the emergence of a new TBEV subtype (TBEV-Eu) in terms of quantum evolution, based on the formation of tick hybrids in the sympatric zone of Ixodes persulcatus and Ixodes ricinus in northwestern Russia.