Reconstructing the evolutionary origins and phylogeography of hantaviruses

Abstract

Rodents have long been recognized as the principal reservoirs of hantaviruses. However, with the discovery of genetically distinct and phylogenetically divergent lineages of hantaviruses in multiple species of shrews, moles, and insectivorous bats from widely separated geographic regions, a far more complex landscape of hantavirus host distribution, evolution, and phylogeography is emerging. Detailed phylogenetic analyses, based on partial and full-length genomes of previously described rodent-borne hantaviruses and newly detected non-rodent-borne hantaviruses, indicate an Asian origin and support the emerging concept that ancestral non-rodent mammals may have served as the hosts of primordial hantaviruses.

Keywords: Chiroptera; Eulipotyphla; evolution; hantavirus; host-switching.

Figure 1

Hantavirus phylogenies, based on sequences of the S (small), M (medium), and L (large) genomic segments, derived using maximum likelihood methods. The full-length coding region was used for each segment when available. Bayesian methods produced similar topologies. Bootstrap support values for nodes of interest supported >50% of the time (1000 replicates, implemented in RAxML under the GTR+gamma model of evolution [81]) are shown at nodes. Virus lineages are color-coded according to host order (green, Rodentia; blue, Eulipotyphla; brown, Chiroptera), with rodent and eulipotyphlan families indicated to right. Scales bars indicate substitutions per site. Abbreviations: GTR, general time reversible; RAxML, randomized axelerated maximum likelihood. Figure created using RAxML Blackbox (http://embnet.vital-it.ch/raxml-bb/).

Figure 2

Hantavirus and mammalian host co-phylogenies. Maximum likelihood (ML) phylogenetic trees of hantaviruses based on concatenated S, M, and L coding sequences (left) and their hosts based on cytochrome b sequences (right). Hantavirus tree is rooted on TPMV and relatives as indicated by BEAST v1.8 MCMC analyses to 50 million generations [69]. Host tree is rooted on Carnivora representatives. Horizontal lines represent host associations, colored by host class (green, Rodentia; blue/purple/violet, Eulipotyphla; brown, Chiroptera) and further shaded within these classes by host subfamily. Bootstrap support, based on 1000 ML replicates implemented in RAxML Blackbox under the GTR+gamma model of evolution [81], is shown at key nodes. Abbreviations: BEAST, Bayesian evolutionary analysis by sampling trees (http://beast.bio.ed.ac.uk/); MCMC, Markov chain Monte Carlo; TMPV, Thottapalayam virus; other abbreviations are given in Figure 1 legend. Figure created using RAxML Blackbox and R statistical program, ape package (http://cran.r-project.org/web/packages/ape/).

Figure 3

Phylogeography of hantaviruses. Maximum clade credibility tree based on the S segment from BEAST v1.8 (MCMC run for 50 million generations [82]), with estimates of node geographic state indicated by color of the descending branch and probability at node. The scale bar indicates substitutions per site. Abbreviations: see legends to Figures 1,2. Figure created using BEAST v1.8 (http://beast.bio.ed.ac.uk/Main_Page) and the included TreeAnnotator v.1.8.