Host switching in Lyssavirus history from the Chiroptera to the Carnivora orders - PubMed (original) (raw)

Host switching in Lyssavirus history from the Chiroptera to the Carnivora orders

H Badrane et al. J Virol. 2001 Sep.

Abstract

Lyssaviruses are unsegmented RNA viruses causing rabies. Their vectors belong to the Carnivora and Chiroptera orders. We studied 36 carnivoran and 17 chiropteran lyssaviruses representing the main genotypes and variants. We compared their genes encoding the surface glycoprotein, which is responsible for receptor recognition and membrane fusion. The glycoprotein is the main protecting antigen and bears virulence determinants. Point mutation is the main force in lyssavirus evolution, as Sawyer's test and phylogenetic analysis showed no evidence of recombination. Tests of neutrality indicated a neutral model of evolution, also supported by globally high ratios of synonymous substitutions (d(S)) to nonsynonymous substitutions (d(N)) (>7). Relative-rate tests suggested similar rates of evolution for all lyssavirus lineages. Therefore, the absence of recombination and similar evolutionary rates make phylogeny-based conclusions reliable. Phylogenetic reconstruction strongly supported the hypothesis that host switching occurred in the history of lyssaviruses. Indeed, lyssaviruses evolved in chiropters long before the emergence of carnivoran rabies, very likely following spillovers from bats. Using dated isolates, the average rate of evolution was estimated to be roughly 4.3 x 10(-4) d(S)/site/year. Consequently, the emergence of carnivoran rabies from chiropteran lyssaviruses was determined to have occurred 888 to 1,459 years ago. Glycoprotein segments accumulating more d(N) than d(S) were distinctly detected in carnivoran and chiropteran lyssaviruses. They may have contributed to the adaptation of the virus to the two distinct mammal orders. In carnivoran lyssaviruses they overlapped the main antigenic sites, II and III, whereas in chiropteran lyssaviruses they were located in regions of unknown functions.

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Figures

FIG. 1

FIG. 1

Lyssavirus-rooted phylogenetic tree. The tree was estimated using the neighbor-joining method (39) on the basis of the ECTO nucleotide sequence. Bootstrap values of 1,000 replicates indicate the robustness of the corresponding node. The sequences retrieved from GenBank and those described in the work of Badrane et al. (3) are marked with * and †, respectively. RABV, Rabies virus; EBLV-1, European bat lyssavirus 1; EBLV-2, European bat lyssavirus 2; ABLV, Australian bat lyssavirus; DUVV, Duvenhage virus; LBV, Lagos bat virus; MOKV, Mokola virus.

FIG. 2

FIG. 2

Ratios of dN to dS along the G gene coding region. We plotted the d S/d N ratio for each pairwise comparison (17) of chiropteran (top graph) and carnivoran (bottom graph) lyssaviruses along their G gene coding regions. Threshold lines of the significance of the ratios are shown at values 1 and 2. A schematic representation of the G gene shows the different domains, SP, TM, ENDO, and ECTO, where antigenic sites are indicated with vertical black boxes. Horizontal black or open boxes represent regions of the chiropteran or carnivoran lyssavirus G gene, respectively, which accumulate significantly more d N than d S. *, d N > d S and d N ≤ 1; **, d N > 2_d_ S and d N ≤ 1.

FIG. 3

FIG. 3

Lyssavirus phylogenetic tree with a molecular clock (PHYLIP phylogeny inference package) derived from nonsynonymous corrected distances (23). Six of the seven Lyssavirus GTs are represented (except GT3). Bold branches distinguish chiropteran Lyssavirus lineages. The geographic locations and vectors of RABV main lineages are indicated. Curved arrows symbolize the two spillover events. Timing estimations of spillovers and of the most recent Lyssavirus ancestor are indicated on the scale.

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