Phylogeography of Puumala orthohantavirus in Europe

Abstract

Puumala virus is an RNA virus hosted by the bank vole (Myodes glareolus) and is today present in most European countries. Whilst it is generally accepted that hantaviruses have been tightly co-evolving with their hosts, Puumala virus (PUUV) evolutionary history is still controversial and so far has not been studied at the whole European level. This study attempts to reconstruct the phylogeographical spread of modern PUUV throughout Europe during the last postglacial period in the light of an upgraded dataset of complete PUUV small (S) segment sequences and by using most recent computational approaches. Taking advantage of the knowledge on the past migrations of its host, we identified at least three potential independent dispersal routes of PUUV during postglacial recolonization of Europe by the bank vole. From the Alpe-Adrian region (Balkan, Austria, and Hungary) to Western European countries (Germany, France, Belgium, and Netherland), and South Scandinavia. From the vicinity of Carpathian Mountains to the Baltic countries and to Poland, Russia, and Finland. The dissemination towards Denmark and North Scandinavia is more hypothetical and probably involved several independent streams from south and north Fennoscandia.

Keywords: bank vole (myodes glareolus); co-evolution; phylogeography; puumala orthohantavirus.

Figure 1

Puumala virus (PUUV) Phylogenetic tree constructed from the complete coding sequence of the small (S) segment by maximum likelihood (ML) method implemented in PhyML 3.0 under the general time reversible (GTR) +G+I substitution model. Branches of the tree clustered within a same PUUV lineage are collapsed to make overall tree visually clear. Eight known PUUV lineages are indicated. The list of sequences belonging to each lineage is indicated in Table S1 together with their geographic origin. Nodes representing most recent common ancestor of North-Scandinavian (N-SCA) lineage, Finnish (FIN), Russian (RUS) and Latvian (LAT) lineages, and Alpe-Adrian (ALAD) and Central European (CE) lineages are indicated, respectively, by the letters A, B, and C.

Figure 2

Ancestral geographical reconstructions based on phylogenetic trees obtained by the Bayesian method (Beast program) (A) and ML methods, F81 algorithms, (PastView program) (B) from the complete coding sequence of the S segment. The red arrows point the nodes in disagreement between Bayesian and ML methods. Tree-like representations of transitions were computed with BEAST (C), PastView (D), and PastML (E) programs. For (C) and (D), transition maps are summarized with PastView program and numbers indicate the counts of identical transitions having the same ancestor. For (E), transition map is done by PastML program and circle diameters are proportional to the number of tips of the initial tree contained in each cluster. Consensus transitions between the three programs are highlighted in blue, red, and green.

Figure 2

Ancestral geographical reconstructions based on phylogenetic trees obtained by the Bayesian method (Beast program) (A) and ML methods, F81 algorithms, (PastView program) (B) from the complete coding sequence of the S segment. The red arrows point the nodes in disagreement between Bayesian and ML methods. Tree-like representations of transitions were computed with BEAST (C), PastView (D), and PastML (E) programs. For (C) and (D), transition maps are summarized with PastView program and numbers indicate the counts of identical transitions having the same ancestor. For (E), transition map is done by PastML program and circle diameters are proportional to the number of tips of the initial tree contained in each cluster. Consensus transitions between the three programs are highlighted in blue, red, and green.

Figure 3

Global view of the waves of post-glaciation dispersal of PUUV in Europe. The three main identified dispersion routes are represented by blue, red and green arrow. Potential routes of PUUV to Denmark are represented by dashed arrows. Dashed circles represent assumed bank vole glacial refugia from which PUUV spread into Europe.