- Email: [email protected]
Phylogeography and evolutionary history of rodent-borne hantaviruses
MEEGID 1806
No. of Pages 7, Model 5G
27 November 2013 Infection, Genetics and Evolution xxx (2013) xxx–xxx 1
Contents lists available at ScienceDirect
Infection, Genetics and Evolution journal homepage: www.elsevier.com/locate/meegid 4 5
Phylogeography and evolutionary history of rodent-borne hantaviruses
3 6
Q1
W.M. Souza a,⇑, G. Bello b, A.A. Amarilla c, H.L. Alfonso c, V.H Aquino c, L.T.M. Figueiredo a,⇑ a
7 8 9
Virology Research Center, School of Medicine of Ribeirao Preto of University of São Paulo, Ribeirao Preto, São Paulo, Brazil Laboratório de AIDS & Imunologia Molecular, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil c Departamento de Análises Clínicas, Toxicológicas e Bromatológicas, Faculdade de Ciências Farmacêuticas, Universidade de São Paulo, Ribeirão Preto, São Paulo, Brazil b
10 11
a r t i c l e
1 2 3 5 14 15 16 17 18
i n f o
Article history: Received 20 August 2013 Received in revised form 10 November 2013 Accepted 13 November 2013 Available online xxxx
19 20 21 22 23 24
Keywords: Hantavirus Rodent-borne Evolution Phylogeography
a b s t r a c t Hantavirus (Family Bunyaviridae) are mostly associated to rodents and transmitted to man by inhalation of aerosolized infected excreta of these animals. The human infection by hantaviruses can lead to severe diseases such as hemorrhagic fever with renal syndrome (HFRS) in Asia and Europe, and pulmonary syndrome (HPS) in the Americas. To determine the origin, spreading and evolutionary dynamics of rodentborne hantaviruses, 190 sequences of nucleoprotein (N) of hantaviruses isolated in 30 countries, from 1985 to 2010, were retrieved from the GenBank and analyzed using the BEAST program. Our evolutionary analysis indicates that current genetic diversity of N gene of rodent-borne hantaviruses probably was originated around 2000 years ago. Hantavirus harbored by Murinae and Arvicolinae subfamilies, probably, were originated in Asia 500–700 years ago and later spread toward Siberia, Europe, Africa and North America. Hantavirus carried by Neotominae subfamily, probably, emerged 500–600 years ago in Central America and spread toward North America. Finally, hantaviruses associated to Sigmodontinae occurred in Brazil 400 years ago and were, probably, originated from Neotominae-associated virus from northern South America. These data offer subsidies to understand the time-scale and worldwide dissemination dynamics of rodent-borne hantaviruses. Ó 2013 Published by Elsevier B.V.
26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41
42 43
1. Introduction
44
Viruses of the genus Hantavirus, family Bunyaviridae, are enveloped viruses containing three segments of single-stranded and negative-sense RNA genome. These segments are designated based on their size as small (S), medium (M) and large (L) (Jonsson et al., 2010; Vaheri et al., 2013). The S segment encodes both the nucleoprotein (N) and a small nonstructural protein (NSs) in an overlapping (+1) open reading frame, the M segment encodes two envelope glycoproteins (Gn and Gc), and the L segment encodes the RNA-dependent RNA polymerase (RdRp) (Jaaskelainen et al., 2007; Vera-Otarola et al., 2012). Unlike other members of the Bunyaviridae family, which are transmitted by arthropods, hantaviruses are transmitted to humans particularly by Muridae or Cricetidae rodents through inhalation of excreta or aggressive interactions between animals (Jonsson et al., 2010). Nevertheless, novel hantaviruses continue to be described in a wide range of species, including shrews and bats whose cross-species transmission and virus-host co-divergence have played important roles in hantavirus evolution (Arai et al.,
45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61
Q2
⇑ Corresponding authors. Address: Virology Research Center, School of Medicine of Ribeirao Preto, University of São Paulo, Av. Bandeirantes, 3900, 14049-900 Ribeirao Preto, São Paulo, Brazil. Tel.: +55 163602 4580; fax: +55 163602 3376. E-mail addresses: [email protected], [email protected] (W.M. Souza), ltmfi[email protected] (L.T.M. Figueiredo).
2008; Guo et al., 2013; Weiss et al., 2012). The rodent-borne hantaviruses produce emerging infectious diseases that have a substantial impact on public health: the hemorrhagic fever with renal syndrome (HFRS) in Eurasia, and the hantavirus pulmonary syndrome (HPS) in the Americas (Jonsson et al., 2010; Vaheri et al., 2013). As the phylogenetic inference of the rodent-borne viruses appear to be largely congruent with that of their hosts, hantaviruses were often considered to have co-diverged with rodent hosts over time-scales of millions of years (Hughes and Friedman, 2000; Morzunov et al., 1998; Nemirov et al., 2002). However, recent studies estimated that the Hantavirus exhibit a short-term substitution rate too fast (10 2 to 10 4 substitutions/site/year) and divergence times too recent (<1000 years ago) that are not compatible with a codivergence with their hosts (Ramsden et al., 2009; Ramsden et al., 2008). Thus, it has been proposed that apparent similarities between phylogeny of hantaviruses and that of their mammalian hosts are the result of a more recent history of preferential host switching and local adaptation (Ramsden et al., 2009). To better understand the origin and the dissemination process of rodent-borne hantaviruses, we have analyzed a comprehensive data set including 252 S gene sequences of hantaviruses detected in humans and rodents worldwide. Spatial and temporal information of sequences were analyzed by a Bayesian method allowing
1567-1348/$ - see front matter Ó 2013 Published by Elsevier B.V. http://dx.doi.org/10.1016/j.meegid.2013.11.015
Please cite this article in press as: Souza, W.M., et al. Phylogeography and evolutionary history of rodent-borne hantaviruses. Infect. Genet. Evol. (2013), http://dx.doi.org/10.1016/j.meegid.2013.11.015
62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86
MEEGID 1806
No. of Pages 7, Model 5G
27 November 2013 2
W.M. Souza et al. / Infection, Genetics and Evolution xxx (2013) xxx–xxx
89
the reconstruct a time-scale and migration routes of Hantavirus infecting Murinae, Arvicolinae, Neotominae and Sigmodontinae subfamilies of rodents.
90
2. Materials and methods
87 88
91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108
2.1. Sequence dataset Complete S gene sequences (1319 bp) of rodent-borne hantaviruses deposited until November 2012 were retrieved from GenBank (www.ncbi.nlm.nih.gov). Two unpublished sequences of Araraquara virus isolated in Brazil were also included in the study (Supporting Figure 1). Known recombinant sequences were excluded from the analysis. In our initial data set, samples from China were overrepresented (n = 86, 34%) when compared to those from other countries (n 6 21). To avoid potential biases in the phylogeographic reconstructions (ancestral root location and viral gene flow estimates) due to sampling heterogeneity (Faria et al., 2012; Salemi et al., 2005), we obtained a ‘‘non-redundant’’ representative Chinese subset. Highly similar (identity P 97%) sequences from China were clustered with the CD-HIT program (Li and Godzik, 2006) using an online web server (Huang et al., 2010) and only one sequence per cluster was selected. It was obtained a final data set of 190 N gene sequences identified from 30 countries over the past 25 years (Table 1).
109
2.2. Evolutionary and phylogeographic analyses
110
Nucleotide sequences were aligned using the CLUSTAL W program (Thompson et al., 1994) and hand edited. Alignment is available from the authors upon request. Based on this alignment, the spatial–temporal and demographic dynamics of dissemination of
111 112 113
Table 1 Nucleotide sequences of rodent-borne hantavirus analyzed in the study. Region
Country
N
Sampling dates
South America
Argentina Bolivia Brazil Chile Paraguay Peru Venezuela
11 4 15 4 4 1 1
1997–1999 1992–2008 2001–2006 1997–1999 1995–2000 1996 1994
Costa Rica Panama Mexico USA
1 1 8 11
1989 2000 2006 1985–2006
Croatia Czech Republic Denmark Finland Germany Greece Poland Latvia Serbia Slovakia Sweden Russia
1 1 1 3 15 3 2 5 1 6 16 21
2000 1995 2000 1991–2000 1997–2008 1999 1995 2000–2008 1997 2001–2004 2004–2005 1993–2005
China Kazakhstan Japan Russia South Korea Singapore Thailand
25 1 10 21 10 4 2
1999–2007 1995 1995–2010 1993–2005 1997–2009 2006 1998–2004
Guinea 30
2 190
2004 1985–2010
Central and North America
Europe
Asia
Africa 4
rodent-borne hantavirus was reconstructed using the Bayesian Markov Chain Monte Carlo (MCMC) approach using the BEAST 1.7.4 program (Drummond et al., 2012). For these analysis, use the general time reversible GTR + I + G nucleotide substitution model as determined by jModeltest (Posada, 2008), an uncorrelated Lognormal relaxed molecular clock model (Drummond et al., 2006) and a Bayesian skyline coalescent model (Drummond et al., 2005), as previously described (Ramsden et al., 2009). Time-scale was inferred using an informative substitution rate interval (1.0 10 4 to 1.0 10 3 substitutions/site/year) previously estimated for the N gene of rodent-borne hantavirus (Ramsden et al., 2009; Ramsden et al., 2008). Sequences were assigned to 15 geographic locations: China, Japan, South Korea, Southeast Asia (Thailand and Singapore), former URSS (Kazakhstan, Latvia and Russia), Central/Eastern Europe (Croatia, Czech Republic, Germany, Greece, Poland, Serbia and Slovakia), Northern Europe (Denmark, Finland and Sweden), USA, Mexico/Central America (Costa Rica and Panama), Argentina, Brazil, Chile, Bolivia/Paraguay/Peru Venezuela and Guine. Migration events between discrete locations were reconstructed by applying a Bayesian phylogeographic approach that models the unobserved diffusion process as a reversible continuous-time Markov chain process (Lemey et al., 2009). MCMC chain was run for 1 108 generations and adequate chain mixing was checked, after excluding an initial 10%, by calculating the effective sample size (ESS) using TRACER v1.4 program (http://www.beast.bio.ed.ac.uk/Tracer). Maximum clade credibility (MCC) trees were summarized from the distribution of trees with TreeAnnotator and were visualized with FigTree v1.4.0 (http://tree.bio.ed.ac.uk/software/figtree).
114
3. Results
143
The Bayesian phylogenetic analysis of 190 hantavirus S gene sequences confirmed the existence of two highly supported (Posterior Probability [PP] = 1) monophyletic clades associated with the rodent host families Muridae (subfamily Murinae) and Cricetidae (subfamilies Arvicolinae, Neotominae and Sigmodontinae) (Fig. 1A). Viruses included in the Cricetidae family were subdivided in two reciprocally monophyletic clades (PP = 1) related to Arvicolinae and Neotominae/Sigmodontinae subfamilies. The Sigmodontinae hantaviruses branched in a well-supported (PP = 1) monophyletic subcluster that was nested within the paraphyletic group of Neotominae hantaviruses. The analysis also suggest a subdivision of hantaviruses into genus or tribe of their rodent hosts (Fig. 1B). Muridae-borne hantaviruses adapted to rodents of genus Apodemus and Rattus. The Arvicolinae-associated viruses were mostly found in hosts of the genus Myodes or Microtus. Neotominae-associated hantaviruses adapted to genus Peromyscus and Reithrodontomys (both belong to Reithrodontomyini tribe). The Sigmodontinae hantaviruses were found principally in Oryzomyini and Akodontini tribes. The estimated rate of nucleotide substitutions per site per year for the N gene of hantavirus was 6.8 10 4. The 95% HPD interval of such estimate (2.5 10 4 to 1 10 3 subst./site/year) almost coincided with the informative prior interval (1.0 10 4 to 1.0 10 3 subst./site/year), thus indicating a correlation between both data. According to this estimated rate, the most recent common ancestor (TMRCA) for all rodent-borne hantaviruses occurred 1915 years before present (ybp) (95% HPD: 5541–922 ybp); whereas the major hantaviruses subfamily clades emergerded around 500–600 ybp: Murinae (573 ybp, 95% HPD 1644–339 ybp), Arvicolinae (628 ybp, 95% HPD 1782–384 ybp) and Neotominae/Sigmodontinae (549 ybp, 95% HPD 1555–341 ybp) (Fig. 1A). The posterior root state probability (PRSP) distributions at the nodes of the rodent subfamilies clades in the Bayesian tree, allowed to infer on the spreading of hantaviruses around the world
144
Please cite this article in press as: Souza, W.M., et al. Phylogeography and evolutionary history of rodent-borne hantaviruses. Infect. Genet. Evol. (2013), http://dx.doi.org/10.1016/j.meegid.2013.11.015
115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130 131 132 133 134 135 136 137 138 139 140 141 142
145 146 147 148 149 150 151 152 153 154 155 156 157 158 159 160 161 162 163 164 165 166 167 168 169 170 171 172 173 174 175 176
MEEGID 1806
No. of Pages 7, Model 5G
27 November 2013 W.M. Souza et al. / Infection, Genetics and Evolution xxx (2013) xxx–xxx
3
Fig. 1. Time-scaled Bayesian Maximum Clade Credibility tree for hantavirus based on the S segment of their genomes. (A) Branches are colored according to the most probable location state (geographic position) of their descendent nodes. Branches with undefined location states (PSRP < 0.6) are colored in gray. (B) Branches are colored according to genus or tribe of rodent hosts. The legends for the colors are shown on the left. The asterisk denotes Caño Delgadito virus found in the Tribe Sigmodontini (Sigmodontiane subfamily). The median age (with 95% HPD interval in parentheses) and the PP support of those monophyletic clades associated with different families and subfamilies of rodents are indicated. Horizontal branch lengths are drawn to scale with the bar at the bottom indicating years. The tree was automatically rooted under the assumption of a relaxed molecular clock.
177 178 179 180
(Figs. 2 and 3). The Murinae clade displayed the best defined root location. Our analysis placed the majority of the PRSP mass of this clade in China (PRSP = 0.68) (Fig. 2). This country was the most probable epicenter from where the virus was disseminated to
South Korea, Southeast Asia (Thailand and Singapore) Russia, Europe (Denmark. Germany, Greece, Slovakia, and Slovenia) and Africa (Guinea Conakry) (Figs. 1A and 3). Secondary migrations of Murinae hantaviruses from Europe to Russia were also detected
Please cite this article in press as: Souza, W.M., et al. Phylogeography and evolutionary history of rodent-borne hantaviruses. Infect. Genet. Evol. (2013), http://dx.doi.org/10.1016/j.meegid.2013.11.015
181 182 183 184
MEEGID 1806
No. of Pages 7, Model 5G
27 November 2013 4
W.M. Souza et al. / Infection, Genetics and Evolution xxx (2013) xxx–xxx
Fig. 2. Geographic location of hantavirus ancestors of the principal clades (named based on their subfamilies of rodent-reservoirs). Graphics depict the posterior probability distributions of location state at the first ancestral nodes of major hantaviruses lineages at the Bayesian MCC tree.
185 186 187 188 189 190 191 192 193 194 195 196 197 198 199 200
(Figs. 1A and 3). The PRSP mass for the Arvicolinae viruses was mainly placed in Asia (PRSP = 0.39) and the former URSS (PRSP = 0.27) (Fig. 3). Countries from the former URSS (Russia and Latvia) seems to have been an important source of Arvicolinae hantaviruses introduced in Japan and Europe (Finland, Germany, Slovenia and Sweden) (Fig. 1A). In the New World, the hantaviruses are mainly associated to rodents subfamilies Neotominae and Sigmodontinae. The root location of the Cricetidae clade (from which Neotominae and Sigmodontinae viruses originated) was traced with quite similar probability to the Old (PRSP = 0.53) and New (PRSP = 0.47) World (Fig. 2). Irrespective of the precise origin, our analysis suggests that modern populations of hantaviruses circulating in the Americas evolved from a single founder strain introduced in rodents of Central America or Mexico (PRSP = 0.48) (Fig. 2). From there, the hantaviruses first disseminate to other Neotominae populations of North America
and then to Sigmodontinae populations in South America (Figs. 1A and 3). Brazil was the most probable location at the root of the Sigmodontinae viruses (PRSP = 0.51) (Fig. 3) and is an important hub of dissemination of viruses to Argentina, Bolivia, Paraguay and Peru (Fig. 1A). Viral migrations from Argentina back to Brazil and to Bolivia, Chile and Panama were also evident (Fig. 1A).
201
4. Discussion
207
In Hantavirus genus, for a long time, it was believed that rodents were the primordial resevoirs hosts of ancestral hantaviruses. However, a recent study suggests that hantaviruses first appeared in Chiroptera (bats) or Soricomorpha (moles and shrews), before emerging in rodents. Bat-borne and shrew/mole-borne hantaviruses are not associated with human disease (Guo et al., 2013).
208
Please cite this article in press as: Souza, W.M., et al. Phylogeography and evolutionary history of rodent-borne hantaviruses. Infect. Genet. Evol. (2013), http://dx.doi.org/10.1016/j.meegid.2013.11.015
202 203 204 205 206
209 210 211 212 213
MEEGID 1806
No. of Pages 7, Model 5G
27 November 2013 W.M. Souza et al. / Infection, Genetics and Evolution xxx (2013) xxx–xxx
5
Fig. 3. World map showing probable origin and migratory routes of rodent-borne hantavirus. Point lines represent supposed spreading routes based on the Bayesian MCC tree and the PRSP analysis. The lines including question marks represent migratory routes without statistical support in the MCC tree. 214 215 216 217 218 219 220 221 222 223 224 225 226 227 228 229 230 231 232 233 234 235 236 237 238 239 240 241 242 243
For the rodent-borne it has been observed a codivergence between hantaviruses and their hosts for decades. Therefore, there is a phylogenetic congruence between main hantaviruses clades and subfamilies of rodent natural hosts (Hughes and Friedman, 2000; Hugot et al., 2006; Nemirov et al., 2002). However, recent studies showed that hantaviruses exhibit fast short-term evolutionary rates (1 10 4–1 0 3 subst./site/year) and relatively recent TMRCA estimates (<1000 ypb) that were not compatible with a codivergence with their rodents hosts (Ramsden et al., 2009; Ramsden et al., 2008). In the present study, the TMRCA estimations for all rodent-borne hantaviruses (1500 ybp) and for major subfamily clades (500–600 ybp) are quite older than those previously reported (850 ybp; 200–250 ybp), but still much more recent than the estimated origin of rodent’s subfamilies (10– 20 Mybp) (Ramsden et al., 2009; Steppan et al., 2004). We show here that all major clades of hantaviruses probably arose between 500 and 600 ybp. This relatively recent origin of major hantavirus clades apparently contradicts the viral-host codivergence. However, some caution must be taken when interpreting our results because we have estimated the genetic diversity age based only on N nucleotide sequences current. Therefore, the Bayesian method is extremely sensitive excluding extant or extinct basal viral lineages in the data set (Duffy et al., 2008; Holmes, 2008; Ramsden et al., 2009). A recent study using this method, showed that molecular clock analyses calibrated by modern sequences may produce quite accurate inferences over short-term scales, but errors could arise at larger time scales for fast evolving RNA viruses due to stringent evolutionary constraints and saturation by nucleotide substitutions in the same site (Worobey et al., 2010). As a consequence, it would be possible to obtain relatively
recent TMRCAs estimates for viral lineages that diverged many years ago. Our phylogeographic study suggests that the Murinae-associated hantaviruses probably originated in China, being the ancestors of Hantaan virus, the prototype of Hantavirus genus, from striped field mouse (Apodemus agrarius) and a causative of HFRS (Lee et al., 1978). The geographical position of China and the presence of both Rattus and Apodemus genera, probably, played a key role in virus dissemination to other countries (Fig. 3). Once well adapted to the Chinese population of Rattus, ancestral hantaviruses probably moved from China to South Korea originating the modern Seoul virus, the probable causative of a HFRS outbreak that affected more than 3000 United Nations soldiers during the Korean War (1950–1953) (Lee et al., 1982). Probably, these viruses also moved from China to Southeast Asia originating Thailand and Jurong viruses, both well adapted to rodents of Rattus genus (Hugot et al., 2006; Johansson et al., 2010). Murinae hantaviruses, probably carried by Apodemus rodents, also arrived to Siberia and Europe originating Dobrava virus and their variations, that are cause of HFRS in that regions (Papa, 2012). Finally, Murinae hantaviruses moved from Asia into Africa, probably crossing through the Middle East; although this route is largely speculative due to the paucity of hantaviruses described in those regions. Until now, only one specie of rodent-borne hantavirus was reported in Africa (Guinea Conakry), in Hylomyscus simus rodents (Klempa et al., 2012). Hantaviruses related to the Arvicolinae rodent subfamily probably emerged in China or Siberia (Fig. 3). Most of these Asian Arvicolinae hantaviruses adapted to genus Myodes and gave rise to different species, such as Puumala, Khabarovsk and Ussuri viruses in Russia, and Shenyang and Yuanjiang viruses in China (Jonsson
Please cite this article in press as: Souza, W.M., et al. Phylogeography and evolutionary history of rodent-borne hantaviruses. Infect. Genet. Evol. (2013), http://dx.doi.org/10.1016/j.meegid.2013.11.015
244 245 246 247 248 249 250 251 252 253 254 255 256 257 258 259 260 261 262 263 264 265 266 267 268 269 270 271 272 273
MEEGID 1806
No. of Pages 7, Model 5G
27 November 2013 6
W.M. Souza et al. / Infection, Genetics and Evolution xxx (2013) xxx–xxx
327
et al., 2010). The lineage related to Arvicolinae probably spread from Siberia to Japan, originating Hokkaido virus (Kariwa et al., 1999) and from Russia to Scandinavia adapting to Myodes rodents (previously known as Clethrionomys). This initial lineage migrated and adapted in Myodes giving rise to Puumala virus and their variations, responsible for nephropathia epidemica (NE) in Scandinavia (Jonsson et al., 2010). Simultaneously, Arvicolinae hantavirus adapted to Microtus genus hosts and spread toward Asia (Kazakhstan), Europe and North America. In Asia and Europe, an ancestral Arvicolinae hantaviruses originated Tula virus which is, probably, non-pathogenic to humans (Schlegel et al., 2012). In North America Arvicolinae hantaviruses originated Isla Vista and Prospect Hill virus (Jonsson et al., 2010). The exact migration route of these viruses from Asia/Europe to North America is unknown. Hantavirus associated to Neotominae (genus Peromyscus and Reithrodontomy) probably emerged in Central America or Mexico and evolved to originate Carrizal virus, Huitzilac virus (Mexico), and Rio Segundo virus (Costa Rica) (Kariwa et al., 2012). Hantavirus from Central America and/or Mexico spread northward and probably gave rise to Sin Nombre virus that was responsible for the first outbreak of HPS, in 1993 (Nichol et al., 1993) (Fig. 3). There was also a Neotominae hantavirus that migrated southward and originated Caño Delgadito virus in Venezuela, related to Sigmodon alstoni. Notably, Caño Delgadito virus branched between Neotominae hantaviruses from Central America and Sigmodontinae hantaviruses from South America (Fig. 1), thus, suggesting an evolutionary link between these two viral clades. Most South American Sigmodontinae hantaviruses are adapted to rodents of Oryzomyini and Akodontini tribes (Parada et al., 2013). Sigmodontinae hantaviruses were also reported in Central America, Choclo virus was described in Panama associated to Oligoryzomys fulvescens (Vincent et al., 2000). The origin of Sigmodontinae clade of Hantavirus was traced to Brazil were originated Juquitiba, the first hantavirus causing HPS reported in Brazil, and Araraquara virus that produces HPS with the highest case fatality ratio in the world (Figueiredo et al., 2009). From Brazil, probably, Sigmodontinae hantaviruses were exported to Bolivia, Peru and Paraguay originating Rio Mamore virus and Laguna Negra virus (Bharadwaj et al., 1997; Chu et al., 2006; Johnson et al., 1997; Powers et al., 1999; Richter et al., 2010) and to Argentina originating Andes virus, the first hantaviruses identified in South America, in 1993 (Lopez et al., 1996) (Fig. 3). The Sigmodontinae hantaviruses probably spread from Argentina to Chile and back to north reaching Brazil, Bolivia and Panama. In conclusion, our study supports a relatively recent origin for the rodent-borne hantavirus (2000 ybp) and hantaviruses associated with major rodent subfamilies (500 ybp). The phylogeographic analysis also suggests that Asia was the most probable epicenter of dissemination of both the Murinae and the Arvicolinae subfamilies, meanwhile Central America and Brazil were traced as the most probable places of origin of Neotominae and Sigmodontinae subclades, respectively. These data provide important insights for better understanding the spatio-temporal dynamics of spreading of the rodent-born hantaviruses.
328
5. Uncited reference
274 275 276 277 278 279 280 281 282 283 284 285 286 287 288 289 290 291 292 293 294 295 296 297 298 299 300 301 302 303 304 305 306 307 308 309 310 311 312 313 314 315 316 317 318 319 320 321 322 323 324 325 326
329
Q3
Firth et al. (2012).
330
Appendix A. Supplementary data
331
Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/ j.meegid.2013.11.015.
332 333
References
334
Arai, S., Ohdachi, S.D., Asakawa, M., Kang, H.J., Mocz, G., Arikawa, J., Okabe, N., Yanagihara, R., 2008. Molecular phylogeny of a newfound hantavirus in the Japanese shrew mole (Urotrichus talpoides). Proc. Nat. Acad. Sci. U.S.A. 105, 16296–16301. Bharadwaj, M., Botten, J., Torrez-Martinez, N., Hjelle, B., 1997. Rio Mamore virus: genetic characterization of a newly recognized hantavirus of the pygmy rice rat, Oligoryzomys microtis, from Bolivia. Am. J. Trop. Med. Hyg. 57, 368–374. Chu, Y.K., Milligan, B., Owen, R.D., Goodin, D.G., Jonsson, C.B., 2006. Phylogenetic and geographical relationships of hantavirus strains in eastern and western Paraguay. Am. J. Trop. Med. Hyg. 75, 1127–1134. Drummond, A.J., Ho, S.Y., Phillips, M.J., Rambaut, A., 2006. Relaxed phylogenetics and dating with confidence. PLoS Biol. 4, e88. Drummond, A.J., Rambaut, A., Shapiro, B., Pybus, O.G., 2005. Bayesian coalescent inference of past population dynamics from molecular sequences. Mol. Biol. Evol. 22, 1185–1192. Drummond, A.J., Suchard, M.A., Xie, D., Rambaut, A., 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969–1973. Duffy, S., Shackelton, L.A., Holmes, E.C., 2008. Rates of evolutionary change in viruses: patterns and determinants. Nat. Rev. Genet. 9, 267–276. Faria, N.R., Hodges-Mameletzis, I., Silva, J.C., Rodes, B., Erasmus, S., Paolucci, S., Ruelle, J., Pieniazek, D., Taveira, N., Trevino, A., Goncalves, M.F., Jallow, S., Xu, L., Camacho, R.J., Soriano, V., Goubau, P., de Sousa, J.D., Vandamme, A.M., Suchard, M.A., Lemey, P., 2012. Phylogeographical footprint of colonial history in the global dispersal of human immunodeficiency virus type 2 group A. J. Gen. Virol. 93, 889–899. Figueiredo, L.T., Moreli, M.L., de-Sousa, R.L., Borges, A.A., de-Figueiredo, G.G., Machado, A.M., Bisordi, I., Nagasse-Sugahara, T.K., Suzuki, A., Pereira, L.E., deSouza, R.P., de-Souza, L.T., Braconi, C.T., Harsi, C.M., de-Andrade-Zanotto, P.M., Viral Diversity Genetic Network, C., 2009. Hantavirus pulmonary syndrome, central plateau, southeastern, and southern Brazil. Emerg. Infect. Dis. 15, 561– 567. Firth, C., Tokarz, R., Simith, D.B., Nunes, M.R., Bhat, M., Rosa, E.S., Medeiros, D.B., Palacios, G., Vasconcelos, P.F., Lipkin, W.I., 2012. Diversity and distribution of hantaviruses in South America. J. Virol. 86, 13756–13766. Guo, W.P., Lin, X.D., Wang, W., Tian, J.H., Cong, M.L., Zhang, H.L., Wang, M.R., Zhou, R.H., Wang, J.B., Li, M.H., Xu, J., Holmes, E.C., Zhang, Y.Z., 2013. Phylogeny and origins of hantaviruses harbored by bats, insectivores, and rodents. PLoS Pathog. 9, e1003159. Holmes, E.C., 2008. Evolutionary history and phylogeography of human viruses. Annu. Rev. Microbiol. 62, 307–328. Huang, Y., Niu, B., Gao, Y., Fu, L., Li, W., 2010. CD-HIT Suite: a web server for clustering and comparing biological sequences. Bioinformatics 26, 680–682. Hughes, A.L., Friedman, R., 2000. Evolutionary diversification of protein-coding genes of hantaviruses. Mol. Biol. Evol. 17, 1558–1568. Hugot, J.P., Plyusnina, A., Herbreteau, V., Nemirov, K., Laakkonen, J., Lundkvist, A., Supputamongkol, Y., Henttonen, H., Plyusnin, A., 2006. Genetic analysis of Thailand hantavirus in Bandicota indica trapped in Thailand. Virol. J. 3, 72. Jaaskelainen, K.M., Kaukinen, P., Minskaya, E.S., Plyusnina, A., Vapalahti, O., Elliott, R.M., Weber, F., Vaheri, A., Plyusnin, A., 2007. Tula and Puumala hantavirus NSs ORFs are functional and the products inhibit activation of the interferon-beta promoter. J. Med. Virol. 79, 1527–1536. Johansson, P., Yap, G., Low, H.T., Siew, C.C., Kek, R., Ng, L.C., Bucht, G., 2010. Molecular characterization of two hantavirus strains from different rattus species in Singapore. Virol. J. 7, 15. Johnson, A.M., Bowen, M.D., Ksiazek, T.G., Williams, R.J., Bryan, R.T., Mills, J.N., Peters, C.J., Nichol, S.T., 1997. Laguna Negra virus associated with HPS in western Paraguay and Bolivia. Virology 238, 115–127. Jonsson, C.B., Figueiredo, L.T., Vapalahti, O., 2010. A global perspective on hantavirus ecology, epidemiology, and disease. Clin. Microbiol. Rev. 23, 412–441. Kariwa, H., Yoshida, H., Sanchez-Hernandez, C., Romero-Almaraz Mde, L., Almazan-Catalan, J.A., Ramos, C., Miyashita, D., Seto, T., Takano, A., Totani, M., Murata, R., Saasa, N., Ishizuka, M., Sanada, T., Yoshii, K., Yoshimatsu, K., Arikawa, J., Takashima, I., 2012. Genetic diversity of hantaviruses in Mexico: identification of three novel hantaviruses from Neotominae rodents. Virus Res. 163, 486–494. Kariwa, H., Yoshimatsu, K., Sawabe, J., Yokota, E., Arikawa, J., Takashima, I., Fukushima, H., Lundkvist, A., Shubin, F.N., Isachkova, L.M., Slonova, R.A., Leonova, G.N., Hashimoto, N., 1999. Genetic diversities of hantaviruses among rodents in Hokkaido, Japan and Far East Russia. Virus Res. 59, 219–228. Klempa, B., Witkowski, P.T., Popugaeva, E., Auste, B., Koivogui, L., Fichet-Calvet, E., Strecker, T., Ter Meulen, J., Kruger, D.H., 2012. Sangassou virus, the first hantavirus isolate from Africa, displays genetic and functional properties distinct from those of other murinae-associated hantaviruses. J. Virol. 86, 3819– 3827. Lee, H.W., Baek, L.J., Johnson, K.M., 1982. Isolation of Hantaan virus, the etiologic agent of Korean hemorrhagic fever, from wild urban rats. J. Infect. Dis. 146, 638– 644. Lee, H.W., Lee, P.W., Johnson, K.M., 1978. Isolation of the etiologic agent of Korean Hemorrhagic fever. J. Infect. Dis. 137, 298–308. Lemey, P., Rambaut, A., Drummond, A.J., Suchard, M.A., 2009. Bayesian phylogeography finds its roots. PLoS Comput. Biol. 5, e1000520. Li, W., Godzik, A., 2006. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22, 1658–1659.
335 336 337 338 339 340 341 342 343 344 345 346 347 348 349 350 351 352 353 354 355 356 357 358 359 360 361 362 363 364 365 366 367 368 369 370 371 372 373 374 375 376 377 378 379 380 381 382 383 384 385 386 387 388 389 390 391 392 393 394 395 396 397 398 399 400 401 402 403 404 405 406 407 408 409 410 411 412 413 414 415 416 417
Please cite this article in press as: Souza, W.M., et al. Phylogeography and evolutionary history of rodent-borne hantaviruses. Infect. Genet. Evol. (2013), http://dx.doi.org/10.1016/j.meegid.2013.11.015
MEEGID 1806
No. of Pages 7, Model 5G
27 November 2013 W.M. Souza et al. / Infection, Genetics and Evolution xxx (2013) xxx–xxx 418 419 420 421 422 423 424 425 426 427 428 429 430 431 432 433 434 435 436 437 438 439 440 441 442 443 444 445 446 447 448 449 450
Lopez, N., Padula, P., Rossi, C., Lazaro, M.E., Franze-Fernandez, M.T., 1996. Genetic identification of a new hantavirus causing severe pulmonary syndrome in Argentina. Virology 220, 223–226. Morzunov, S.P., Rowe, J.E., Ksiazek, T.G., Peters, C.J., St Jeor, S.C., Nichol, S.T., 1998. Genetic analysis of the diversity and origin of hantaviruses in Peromyscus leucopus mice in North America. J. Virol. 72, 57–64. Nemirov, K., Henttonen, H., Vaheri, A., Plyusnin, A., 2002. Phylogenetic evidence for host switching in the evolution of hantaviruses carried by Apodemus mice. Virus Res. 90, 207–215. Nichol, S.T., Spiropoulou, C.F., Morzunov, S., Rollin, P.E., Ksiazek, T.G., Feldmann, H., Sanchez, A., Childs, J., Zaki, S., Peters, C.J., 1993. Genetic identification of a hantavirus associated with an outbreak of acute respiratory illness. Science 262, 914–917. Papa, A., 2012. Dobrava-Belgrade virus: phylogeny, epidemiology, disease. Antiviral Res. 95, 104–117. Parada, A., Pardinas, U.F., Salazar-Bravo, J., D’Elia, G., Palma, R.E., 2013. Dating an impressive Neotropical radiation: Molecular time estimates for the Sigmodontinae (Rodentia) provide insights into its historical biogeography. Mol. Phylogenet. Evol. 66, 960–968. Posada, D., 2008. jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 25, 1253–1256. Powers, A.M., Mercer, D.R., Watts, D.M., Guzman, H., Fulhorst, C.F., Popov, V.L., Tesh, R.B., 1999. Isolation and genetic characterization of a hantavirus (Bunyaviridae: Hantavirus) from a rodent, Oligoryzomys microtis (Muridae), collected in northeastern Peru. Am. J. Trop. Med. Hyg. 61, 92–98. Ramsden, C., Holmes, E.C., Charleston, M.A., 2009. Hantavirus evolution in relation to its rodent and insectivore hosts: no evidence for codivergence. Mol. Biol. Evol. 26, 143–153. Ramsden, C., Melo, F.L., Figueiredo, L.M., Holmes, E.C., Zanotto, P.M., Consortium, V., 2008. High rates of molecular evolution in hantaviruses. Mol. Biol. Evol. 25, 1488–1492. Richter, M.H., Hanson, J.D., Cajimat, M.N., Milazzo, M.L., Fulhorst, C.F., 2010. Geographical range of Rio Mamore virus (family Bunyaviridae, genus
7
Hantavirus) in association with the small-eared pygmy rice rat (Oligoryzomys microtis). Vector Borne Zoonotic Dis. 10, 613–620. Salemi, M., Lamers, S.L., Yu, S., de Oliveira, T., Fitch, W.M., McGrath, M.S., 2005. Phylodynamic analysis of human immunodeficiency virus type 1 in distinct brain compartments provides a model for the neuropathogenesis of AIDS. J. Virol. 79, 11343–11352. Schlegel, M., Kindler, E., Essbauer, S.S., Wolf, R., Thiel, J., Groschup, M.H., Heckel, G., Oehme, R.M., Ulrich, R.G., 2012. Tula virus infections in the Eurasian water vole in Central Europe. Vector borne and zoonotic diseases 12, 503–513. Steppan, S., Adkins, R., Anderson, J., 2004. Phylogeny and divergence-date estimates of rapid radiations in muroid rodents based on multiple nuclear genes. Syst. Biol. 53, 533–553. Thompson, J.D., Higgins, D.G., Gibson, T.J., 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680. Vaheri, A., Strandin, T., Hepojoki, J., Sironen, T., Henttonen, H., Makela, S., Mustonen, J., 2013. Uncovering the mysteries of hantavirus infections. Nat. Rev. Microbiol. 11, 539–550. Vera-Otarola, J., Solis, L., Soto-Rifo, R., Ricci, E.P., Pino, K., Tischler, N.D., Ohlmann, T., Darlix, J.L., Lopez-Lastra, M., 2012. The Andes hantavirus NSs protein is expressed from the viral small mRNA by a leaky scanning mechanism. J. Virol. 86, 2176–2187. Vincent, M.J., Quiroz, E., Gracia, F., Sanchez, A.J., Ksiazek, T.G., Kitsutani, P.T., Ruedas, L.A., Tinnin, D.S., Caceres, L., Garcia, A., Rollin, P.E., Mills, J.N., Peters, C.J., Nichol, S.T., 2000. Hantavirus pulmonary syndrome in Panama: identification of novel hantaviruses and their likely reservoirs. Virology 277, 14–19. Weiss, S., Witkowski, P.T., Auste, B., Nowak, K., Weber, N., Fahr, J., Mombouli, J.V., Wolfe, N.D., Drexler, J.F., Drosten, C., Klempa, B., Leendertz, F.H., Kruger, D.H., 2012. Hantavirus in bat, Sierra Leone. Emerg. Infect. Dis. 18, 159–161. Worobey, M., Telfer, P., Souquiere, S., Hunter, M., Coleman, C.A., Metzger, M.J., Reed, P., Makuwa, M., Hearn, G., Honarvar, S., Roques, P., Apetrei, C., Kazanji, M., Marx, P.A., 2010. Island biogeography reveals the deep history of SIV. Science 329, 1487.
451 452 453 454 455 456 457 458 459 460 461 462 463 464 465 466 467 468 469 470 471 472 473 474 475 476 477 478 479 480 481 482 483 484 485
Please cite this article in press as: Souza, W.M., et al. Phylogeography and evolutionary history of rodent-borne hantaviruses. Infect. Genet. Evol. (2013), http://dx.doi.org/10.1016/j.meegid.2013.11.015
No. of Pages 7, Model 5G
27 November 2013 Infection, Genetics and Evolution xxx (2013) xxx–xxx 1
Contents lists available at ScienceDirect
Infection, Genetics and Evolution journal homepage: www.elsevier.com/locate/meegid 4 5
Phylogeography and evolutionary history of rodent-borne hantaviruses
3 6
Q1
W.M. Souza a,⇑, G. Bello b, A.A. Amarilla c, H.L. Alfonso c, V.H Aquino c, L.T.M. Figueiredo a,⇑ a
7 8 9
Virology Research Center, School of Medicine of Ribeirao Preto of University of São Paulo, Ribeirao Preto, São Paulo, Brazil Laboratório de AIDS & Imunologia Molecular, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil c Departamento de Análises Clínicas, Toxicológicas e Bromatológicas, Faculdade de Ciências Farmacêuticas, Universidade de São Paulo, Ribeirão Preto, São Paulo, Brazil b
10 11
a r t i c l e
1 2 3 5 14 15 16 17 18
i n f o
Article history: Received 20 August 2013 Received in revised form 10 November 2013 Accepted 13 November 2013 Available online xxxx
19 20 21 22 23 24
Keywords: Hantavirus Rodent-borne Evolution Phylogeography
a b s t r a c t Hantavirus (Family Bunyaviridae) are mostly associated to rodents and transmitted to man by inhalation of aerosolized infected excreta of these animals. The human infection by hantaviruses can lead to severe diseases such as hemorrhagic fever with renal syndrome (HFRS) in Asia and Europe, and pulmonary syndrome (HPS) in the Americas. To determine the origin, spreading and evolutionary dynamics of rodentborne hantaviruses, 190 sequences of nucleoprotein (N) of hantaviruses isolated in 30 countries, from 1985 to 2010, were retrieved from the GenBank and analyzed using the BEAST program. Our evolutionary analysis indicates that current genetic diversity of N gene of rodent-borne hantaviruses probably was originated around 2000 years ago. Hantavirus harbored by Murinae and Arvicolinae subfamilies, probably, were originated in Asia 500–700 years ago and later spread toward Siberia, Europe, Africa and North America. Hantavirus carried by Neotominae subfamily, probably, emerged 500–600 years ago in Central America and spread toward North America. Finally, hantaviruses associated to Sigmodontinae occurred in Brazil 400 years ago and were, probably, originated from Neotominae-associated virus from northern South America. These data offer subsidies to understand the time-scale and worldwide dissemination dynamics of rodent-borne hantaviruses. Ó 2013 Published by Elsevier B.V.
26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41
42 43
1. Introduction
44
Viruses of the genus Hantavirus, family Bunyaviridae, are enveloped viruses containing three segments of single-stranded and negative-sense RNA genome. These segments are designated based on their size as small (S), medium (M) and large (L) (Jonsson et al., 2010; Vaheri et al., 2013). The S segment encodes both the nucleoprotein (N) and a small nonstructural protein (NSs) in an overlapping (+1) open reading frame, the M segment encodes two envelope glycoproteins (Gn and Gc), and the L segment encodes the RNA-dependent RNA polymerase (RdRp) (Jaaskelainen et al., 2007; Vera-Otarola et al., 2012). Unlike other members of the Bunyaviridae family, which are transmitted by arthropods, hantaviruses are transmitted to humans particularly by Muridae or Cricetidae rodents through inhalation of excreta or aggressive interactions between animals (Jonsson et al., 2010). Nevertheless, novel hantaviruses continue to be described in a wide range of species, including shrews and bats whose cross-species transmission and virus-host co-divergence have played important roles in hantavirus evolution (Arai et al.,
45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61
Q2
⇑ Corresponding authors. Address: Virology Research Center, School of Medicine of Ribeirao Preto, University of São Paulo, Av. Bandeirantes, 3900, 14049-900 Ribeirao Preto, São Paulo, Brazil. Tel.: +55 163602 4580; fax: +55 163602 3376. E-mail addresses: [email protected], [email protected] (W.M. Souza), ltmfi[email protected] (L.T.M. Figueiredo).
2008; Guo et al., 2013; Weiss et al., 2012). The rodent-borne hantaviruses produce emerging infectious diseases that have a substantial impact on public health: the hemorrhagic fever with renal syndrome (HFRS) in Eurasia, and the hantavirus pulmonary syndrome (HPS) in the Americas (Jonsson et al., 2010; Vaheri et al., 2013). As the phylogenetic inference of the rodent-borne viruses appear to be largely congruent with that of their hosts, hantaviruses were often considered to have co-diverged with rodent hosts over time-scales of millions of years (Hughes and Friedman, 2000; Morzunov et al., 1998; Nemirov et al., 2002). However, recent studies estimated that the Hantavirus exhibit a short-term substitution rate too fast (10 2 to 10 4 substitutions/site/year) and divergence times too recent (<1000 years ago) that are not compatible with a codivergence with their hosts (Ramsden et al., 2009; Ramsden et al., 2008). Thus, it has been proposed that apparent similarities between phylogeny of hantaviruses and that of their mammalian hosts are the result of a more recent history of preferential host switching and local adaptation (Ramsden et al., 2009). To better understand the origin and the dissemination process of rodent-borne hantaviruses, we have analyzed a comprehensive data set including 252 S gene sequences of hantaviruses detected in humans and rodents worldwide. Spatial and temporal information of sequences were analyzed by a Bayesian method allowing
1567-1348/$ - see front matter Ó 2013 Published by Elsevier B.V. http://dx.doi.org/10.1016/j.meegid.2013.11.015
Please cite this article in press as: Souza, W.M., et al. Phylogeography and evolutionary history of rodent-borne hantaviruses. Infect. Genet. Evol. (2013), http://dx.doi.org/10.1016/j.meegid.2013.11.015
62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86
MEEGID 1806
No. of Pages 7, Model 5G
27 November 2013 2
W.M. Souza et al. / Infection, Genetics and Evolution xxx (2013) xxx–xxx
89
the reconstruct a time-scale and migration routes of Hantavirus infecting Murinae, Arvicolinae, Neotominae and Sigmodontinae subfamilies of rodents.
90
2. Materials and methods
87 88
91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108
2.1. Sequence dataset Complete S gene sequences (1319 bp) of rodent-borne hantaviruses deposited until November 2012 were retrieved from GenBank (www.ncbi.nlm.nih.gov). Two unpublished sequences of Araraquara virus isolated in Brazil were also included in the study (Supporting Figure 1). Known recombinant sequences were excluded from the analysis. In our initial data set, samples from China were overrepresented (n = 86, 34%) when compared to those from other countries (n 6 21). To avoid potential biases in the phylogeographic reconstructions (ancestral root location and viral gene flow estimates) due to sampling heterogeneity (Faria et al., 2012; Salemi et al., 2005), we obtained a ‘‘non-redundant’’ representative Chinese subset. Highly similar (identity P 97%) sequences from China were clustered with the CD-HIT program (Li and Godzik, 2006) using an online web server (Huang et al., 2010) and only one sequence per cluster was selected. It was obtained a final data set of 190 N gene sequences identified from 30 countries over the past 25 years (Table 1).
109
2.2. Evolutionary and phylogeographic analyses
110
Nucleotide sequences were aligned using the CLUSTAL W program (Thompson et al., 1994) and hand edited. Alignment is available from the authors upon request. Based on this alignment, the spatial–temporal and demographic dynamics of dissemination of
111 112 113
Table 1 Nucleotide sequences of rodent-borne hantavirus analyzed in the study. Region
Country
N
Sampling dates
South America
Argentina Bolivia Brazil Chile Paraguay Peru Venezuela
11 4 15 4 4 1 1
1997–1999 1992–2008 2001–2006 1997–1999 1995–2000 1996 1994
Costa Rica Panama Mexico USA
1 1 8 11
1989 2000 2006 1985–2006
Croatia Czech Republic Denmark Finland Germany Greece Poland Latvia Serbia Slovakia Sweden Russia
1 1 1 3 15 3 2 5 1 6 16 21
2000 1995 2000 1991–2000 1997–2008 1999 1995 2000–2008 1997 2001–2004 2004–2005 1993–2005
China Kazakhstan Japan Russia South Korea Singapore Thailand
25 1 10 21 10 4 2
1999–2007 1995 1995–2010 1993–2005 1997–2009 2006 1998–2004
Guinea 30
2 190
2004 1985–2010
Central and North America
Europe
Asia
Africa 4
rodent-borne hantavirus was reconstructed using the Bayesian Markov Chain Monte Carlo (MCMC) approach using the BEAST 1.7.4 program (Drummond et al., 2012). For these analysis, use the general time reversible GTR + I + G nucleotide substitution model as determined by jModeltest (Posada, 2008), an uncorrelated Lognormal relaxed molecular clock model (Drummond et al., 2006) and a Bayesian skyline coalescent model (Drummond et al., 2005), as previously described (Ramsden et al., 2009). Time-scale was inferred using an informative substitution rate interval (1.0 10 4 to 1.0 10 3 substitutions/site/year) previously estimated for the N gene of rodent-borne hantavirus (Ramsden et al., 2009; Ramsden et al., 2008). Sequences were assigned to 15 geographic locations: China, Japan, South Korea, Southeast Asia (Thailand and Singapore), former URSS (Kazakhstan, Latvia and Russia), Central/Eastern Europe (Croatia, Czech Republic, Germany, Greece, Poland, Serbia and Slovakia), Northern Europe (Denmark, Finland and Sweden), USA, Mexico/Central America (Costa Rica and Panama), Argentina, Brazil, Chile, Bolivia/Paraguay/Peru Venezuela and Guine. Migration events between discrete locations were reconstructed by applying a Bayesian phylogeographic approach that models the unobserved diffusion process as a reversible continuous-time Markov chain process (Lemey et al., 2009). MCMC chain was run for 1 108 generations and adequate chain mixing was checked, after excluding an initial 10%, by calculating the effective sample size (ESS) using TRACER v1.4 program (http://www.beast.bio.ed.ac.uk/Tracer). Maximum clade credibility (MCC) trees were summarized from the distribution of trees with TreeAnnotator and were visualized with FigTree v1.4.0 (http://tree.bio.ed.ac.uk/software/figtree).
114
3. Results
143
The Bayesian phylogenetic analysis of 190 hantavirus S gene sequences confirmed the existence of two highly supported (Posterior Probability [PP] = 1) monophyletic clades associated with the rodent host families Muridae (subfamily Murinae) and Cricetidae (subfamilies Arvicolinae, Neotominae and Sigmodontinae) (Fig. 1A). Viruses included in the Cricetidae family were subdivided in two reciprocally monophyletic clades (PP = 1) related to Arvicolinae and Neotominae/Sigmodontinae subfamilies. The Sigmodontinae hantaviruses branched in a well-supported (PP = 1) monophyletic subcluster that was nested within the paraphyletic group of Neotominae hantaviruses. The analysis also suggest a subdivision of hantaviruses into genus or tribe of their rodent hosts (Fig. 1B). Muridae-borne hantaviruses adapted to rodents of genus Apodemus and Rattus. The Arvicolinae-associated viruses were mostly found in hosts of the genus Myodes or Microtus. Neotominae-associated hantaviruses adapted to genus Peromyscus and Reithrodontomys (both belong to Reithrodontomyini tribe). The Sigmodontinae hantaviruses were found principally in Oryzomyini and Akodontini tribes. The estimated rate of nucleotide substitutions per site per year for the N gene of hantavirus was 6.8 10 4. The 95% HPD interval of such estimate (2.5 10 4 to 1 10 3 subst./site/year) almost coincided with the informative prior interval (1.0 10 4 to 1.0 10 3 subst./site/year), thus indicating a correlation between both data. According to this estimated rate, the most recent common ancestor (TMRCA) for all rodent-borne hantaviruses occurred 1915 years before present (ybp) (95% HPD: 5541–922 ybp); whereas the major hantaviruses subfamily clades emergerded around 500–600 ybp: Murinae (573 ybp, 95% HPD 1644–339 ybp), Arvicolinae (628 ybp, 95% HPD 1782–384 ybp) and Neotominae/Sigmodontinae (549 ybp, 95% HPD 1555–341 ybp) (Fig. 1A). The posterior root state probability (PRSP) distributions at the nodes of the rodent subfamilies clades in the Bayesian tree, allowed to infer on the spreading of hantaviruses around the world
144
Please cite this article in press as: Souza, W.M., et al. Phylogeography and evolutionary history of rodent-borne hantaviruses. Infect. Genet. Evol. (2013), http://dx.doi.org/10.1016/j.meegid.2013.11.015
115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130 131 132 133 134 135 136 137 138 139 140 141 142
145 146 147 148 149 150 151 152 153 154 155 156 157 158 159 160 161 162 163 164 165 166 167 168 169 170 171 172 173 174 175 176
MEEGID 1806
No. of Pages 7, Model 5G
27 November 2013 W.M. Souza et al. / Infection, Genetics and Evolution xxx (2013) xxx–xxx
3
Fig. 1. Time-scaled Bayesian Maximum Clade Credibility tree for hantavirus based on the S segment of their genomes. (A) Branches are colored according to the most probable location state (geographic position) of their descendent nodes. Branches with undefined location states (PSRP < 0.6) are colored in gray. (B) Branches are colored according to genus or tribe of rodent hosts. The legends for the colors are shown on the left. The asterisk denotes Caño Delgadito virus found in the Tribe Sigmodontini (Sigmodontiane subfamily). The median age (with 95% HPD interval in parentheses) and the PP support of those monophyletic clades associated with different families and subfamilies of rodents are indicated. Horizontal branch lengths are drawn to scale with the bar at the bottom indicating years. The tree was automatically rooted under the assumption of a relaxed molecular clock.
177 178 179 180
(Figs. 2 and 3). The Murinae clade displayed the best defined root location. Our analysis placed the majority of the PRSP mass of this clade in China (PRSP = 0.68) (Fig. 2). This country was the most probable epicenter from where the virus was disseminated to
South Korea, Southeast Asia (Thailand and Singapore) Russia, Europe (Denmark. Germany, Greece, Slovakia, and Slovenia) and Africa (Guinea Conakry) (Figs. 1A and 3). Secondary migrations of Murinae hantaviruses from Europe to Russia were also detected
Please cite this article in press as: Souza, W.M., et al. Phylogeography and evolutionary history of rodent-borne hantaviruses. Infect. Genet. Evol. (2013), http://dx.doi.org/10.1016/j.meegid.2013.11.015
181 182 183 184
MEEGID 1806
No. of Pages 7, Model 5G
27 November 2013 4
W.M. Souza et al. / Infection, Genetics and Evolution xxx (2013) xxx–xxx
Fig. 2. Geographic location of hantavirus ancestors of the principal clades (named based on their subfamilies of rodent-reservoirs). Graphics depict the posterior probability distributions of location state at the first ancestral nodes of major hantaviruses lineages at the Bayesian MCC tree.
185 186 187 188 189 190 191 192 193 194 195 196 197 198 199 200
(Figs. 1A and 3). The PRSP mass for the Arvicolinae viruses was mainly placed in Asia (PRSP = 0.39) and the former URSS (PRSP = 0.27) (Fig. 3). Countries from the former URSS (Russia and Latvia) seems to have been an important source of Arvicolinae hantaviruses introduced in Japan and Europe (Finland, Germany, Slovenia and Sweden) (Fig. 1A). In the New World, the hantaviruses are mainly associated to rodents subfamilies Neotominae and Sigmodontinae. The root location of the Cricetidae clade (from which Neotominae and Sigmodontinae viruses originated) was traced with quite similar probability to the Old (PRSP = 0.53) and New (PRSP = 0.47) World (Fig. 2). Irrespective of the precise origin, our analysis suggests that modern populations of hantaviruses circulating in the Americas evolved from a single founder strain introduced in rodents of Central America or Mexico (PRSP = 0.48) (Fig. 2). From there, the hantaviruses first disseminate to other Neotominae populations of North America
and then to Sigmodontinae populations in South America (Figs. 1A and 3). Brazil was the most probable location at the root of the Sigmodontinae viruses (PRSP = 0.51) (Fig. 3) and is an important hub of dissemination of viruses to Argentina, Bolivia, Paraguay and Peru (Fig. 1A). Viral migrations from Argentina back to Brazil and to Bolivia, Chile and Panama were also evident (Fig. 1A).
201
4. Discussion
207
In Hantavirus genus, for a long time, it was believed that rodents were the primordial resevoirs hosts of ancestral hantaviruses. However, a recent study suggests that hantaviruses first appeared in Chiroptera (bats) or Soricomorpha (moles and shrews), before emerging in rodents. Bat-borne and shrew/mole-borne hantaviruses are not associated with human disease (Guo et al., 2013).
208
Please cite this article in press as: Souza, W.M., et al. Phylogeography and evolutionary history of rodent-borne hantaviruses. Infect. Genet. Evol. (2013), http://dx.doi.org/10.1016/j.meegid.2013.11.015
202 203 204 205 206
209 210 211 212 213
MEEGID 1806
No. of Pages 7, Model 5G
27 November 2013 W.M. Souza et al. / Infection, Genetics and Evolution xxx (2013) xxx–xxx
5
Fig. 3. World map showing probable origin and migratory routes of rodent-borne hantavirus. Point lines represent supposed spreading routes based on the Bayesian MCC tree and the PRSP analysis. The lines including question marks represent migratory routes without statistical support in the MCC tree. 214 215 216 217 218 219 220 221 222 223 224 225 226 227 228 229 230 231 232 233 234 235 236 237 238 239 240 241 242 243
For the rodent-borne it has been observed a codivergence between hantaviruses and their hosts for decades. Therefore, there is a phylogenetic congruence between main hantaviruses clades and subfamilies of rodent natural hosts (Hughes and Friedman, 2000; Hugot et al., 2006; Nemirov et al., 2002). However, recent studies showed that hantaviruses exhibit fast short-term evolutionary rates (1 10 4–1 0 3 subst./site/year) and relatively recent TMRCA estimates (<1000 ypb) that were not compatible with a codivergence with their rodents hosts (Ramsden et al., 2009; Ramsden et al., 2008). In the present study, the TMRCA estimations for all rodent-borne hantaviruses (1500 ybp) and for major subfamily clades (500–600 ybp) are quite older than those previously reported (850 ybp; 200–250 ybp), but still much more recent than the estimated origin of rodent’s subfamilies (10– 20 Mybp) (Ramsden et al., 2009; Steppan et al., 2004). We show here that all major clades of hantaviruses probably arose between 500 and 600 ybp. This relatively recent origin of major hantavirus clades apparently contradicts the viral-host codivergence. However, some caution must be taken when interpreting our results because we have estimated the genetic diversity age based only on N nucleotide sequences current. Therefore, the Bayesian method is extremely sensitive excluding extant or extinct basal viral lineages in the data set (Duffy et al., 2008; Holmes, 2008; Ramsden et al., 2009). A recent study using this method, showed that molecular clock analyses calibrated by modern sequences may produce quite accurate inferences over short-term scales, but errors could arise at larger time scales for fast evolving RNA viruses due to stringent evolutionary constraints and saturation by nucleotide substitutions in the same site (Worobey et al., 2010). As a consequence, it would be possible to obtain relatively
recent TMRCAs estimates for viral lineages that diverged many years ago. Our phylogeographic study suggests that the Murinae-associated hantaviruses probably originated in China, being the ancestors of Hantaan virus, the prototype of Hantavirus genus, from striped field mouse (Apodemus agrarius) and a causative of HFRS (Lee et al., 1978). The geographical position of China and the presence of both Rattus and Apodemus genera, probably, played a key role in virus dissemination to other countries (Fig. 3). Once well adapted to the Chinese population of Rattus, ancestral hantaviruses probably moved from China to South Korea originating the modern Seoul virus, the probable causative of a HFRS outbreak that affected more than 3000 United Nations soldiers during the Korean War (1950–1953) (Lee et al., 1982). Probably, these viruses also moved from China to Southeast Asia originating Thailand and Jurong viruses, both well adapted to rodents of Rattus genus (Hugot et al., 2006; Johansson et al., 2010). Murinae hantaviruses, probably carried by Apodemus rodents, also arrived to Siberia and Europe originating Dobrava virus and their variations, that are cause of HFRS in that regions (Papa, 2012). Finally, Murinae hantaviruses moved from Asia into Africa, probably crossing through the Middle East; although this route is largely speculative due to the paucity of hantaviruses described in those regions. Until now, only one specie of rodent-borne hantavirus was reported in Africa (Guinea Conakry), in Hylomyscus simus rodents (Klempa et al., 2012). Hantaviruses related to the Arvicolinae rodent subfamily probably emerged in China or Siberia (Fig. 3). Most of these Asian Arvicolinae hantaviruses adapted to genus Myodes and gave rise to different species, such as Puumala, Khabarovsk and Ussuri viruses in Russia, and Shenyang and Yuanjiang viruses in China (Jonsson
Please cite this article in press as: Souza, W.M., et al. Phylogeography and evolutionary history of rodent-borne hantaviruses. Infect. Genet. Evol. (2013), http://dx.doi.org/10.1016/j.meegid.2013.11.015
244 245 246 247 248 249 250 251 252 253 254 255 256 257 258 259 260 261 262 263 264 265 266 267 268 269 270 271 272 273
MEEGID 1806
No. of Pages 7, Model 5G
27 November 2013 6
W.M. Souza et al. / Infection, Genetics and Evolution xxx (2013) xxx–xxx
327
et al., 2010). The lineage related to Arvicolinae probably spread from Siberia to Japan, originating Hokkaido virus (Kariwa et al., 1999) and from Russia to Scandinavia adapting to Myodes rodents (previously known as Clethrionomys). This initial lineage migrated and adapted in Myodes giving rise to Puumala virus and their variations, responsible for nephropathia epidemica (NE) in Scandinavia (Jonsson et al., 2010). Simultaneously, Arvicolinae hantavirus adapted to Microtus genus hosts and spread toward Asia (Kazakhstan), Europe and North America. In Asia and Europe, an ancestral Arvicolinae hantaviruses originated Tula virus which is, probably, non-pathogenic to humans (Schlegel et al., 2012). In North America Arvicolinae hantaviruses originated Isla Vista and Prospect Hill virus (Jonsson et al., 2010). The exact migration route of these viruses from Asia/Europe to North America is unknown. Hantavirus associated to Neotominae (genus Peromyscus and Reithrodontomy) probably emerged in Central America or Mexico and evolved to originate Carrizal virus, Huitzilac virus (Mexico), and Rio Segundo virus (Costa Rica) (Kariwa et al., 2012). Hantavirus from Central America and/or Mexico spread northward and probably gave rise to Sin Nombre virus that was responsible for the first outbreak of HPS, in 1993 (Nichol et al., 1993) (Fig. 3). There was also a Neotominae hantavirus that migrated southward and originated Caño Delgadito virus in Venezuela, related to Sigmodon alstoni. Notably, Caño Delgadito virus branched between Neotominae hantaviruses from Central America and Sigmodontinae hantaviruses from South America (Fig. 1), thus, suggesting an evolutionary link between these two viral clades. Most South American Sigmodontinae hantaviruses are adapted to rodents of Oryzomyini and Akodontini tribes (Parada et al., 2013). Sigmodontinae hantaviruses were also reported in Central America, Choclo virus was described in Panama associated to Oligoryzomys fulvescens (Vincent et al., 2000). The origin of Sigmodontinae clade of Hantavirus was traced to Brazil were originated Juquitiba, the first hantavirus causing HPS reported in Brazil, and Araraquara virus that produces HPS with the highest case fatality ratio in the world (Figueiredo et al., 2009). From Brazil, probably, Sigmodontinae hantaviruses were exported to Bolivia, Peru and Paraguay originating Rio Mamore virus and Laguna Negra virus (Bharadwaj et al., 1997; Chu et al., 2006; Johnson et al., 1997; Powers et al., 1999; Richter et al., 2010) and to Argentina originating Andes virus, the first hantaviruses identified in South America, in 1993 (Lopez et al., 1996) (Fig. 3). The Sigmodontinae hantaviruses probably spread from Argentina to Chile and back to north reaching Brazil, Bolivia and Panama. In conclusion, our study supports a relatively recent origin for the rodent-borne hantavirus (2000 ybp) and hantaviruses associated with major rodent subfamilies (500 ybp). The phylogeographic analysis also suggests that Asia was the most probable epicenter of dissemination of both the Murinae and the Arvicolinae subfamilies, meanwhile Central America and Brazil were traced as the most probable places of origin of Neotominae and Sigmodontinae subclades, respectively. These data provide important insights for better understanding the spatio-temporal dynamics of spreading of the rodent-born hantaviruses.
328
5. Uncited reference
274 275 276 277 278 279 280 281 282 283 284 285 286 287 288 289 290 291 292 293 294 295 296 297 298 299 300 301 302 303 304 305 306 307 308 309 310 311 312 313 314 315 316 317 318 319 320 321 322 323 324 325 326
329
Q3
Firth et al. (2012).
330
Appendix A. Supplementary data
331
Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/ j.meegid.2013.11.015.
332 333
References
334
Arai, S., Ohdachi, S.D., Asakawa, M., Kang, H.J., Mocz, G., Arikawa, J., Okabe, N., Yanagihara, R., 2008. Molecular phylogeny of a newfound hantavirus in the Japanese shrew mole (Urotrichus talpoides). Proc. Nat. Acad. Sci. U.S.A. 105, 16296–16301. Bharadwaj, M., Botten, J., Torrez-Martinez, N., Hjelle, B., 1997. Rio Mamore virus: genetic characterization of a newly recognized hantavirus of the pygmy rice rat, Oligoryzomys microtis, from Bolivia. Am. J. Trop. Med. Hyg. 57, 368–374. Chu, Y.K., Milligan, B., Owen, R.D., Goodin, D.G., Jonsson, C.B., 2006. Phylogenetic and geographical relationships of hantavirus strains in eastern and western Paraguay. Am. J. Trop. Med. Hyg. 75, 1127–1134. Drummond, A.J., Ho, S.Y., Phillips, M.J., Rambaut, A., 2006. Relaxed phylogenetics and dating with confidence. PLoS Biol. 4, e88. Drummond, A.J., Rambaut, A., Shapiro, B., Pybus, O.G., 2005. Bayesian coalescent inference of past population dynamics from molecular sequences. Mol. Biol. Evol. 22, 1185–1192. Drummond, A.J., Suchard, M.A., Xie, D., Rambaut, A., 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969–1973. Duffy, S., Shackelton, L.A., Holmes, E.C., 2008. Rates of evolutionary change in viruses: patterns and determinants. Nat. Rev. Genet. 9, 267–276. Faria, N.R., Hodges-Mameletzis, I., Silva, J.C., Rodes, B., Erasmus, S., Paolucci, S., Ruelle, J., Pieniazek, D., Taveira, N., Trevino, A., Goncalves, M.F., Jallow, S., Xu, L., Camacho, R.J., Soriano, V., Goubau, P., de Sousa, J.D., Vandamme, A.M., Suchard, M.A., Lemey, P., 2012. Phylogeographical footprint of colonial history in the global dispersal of human immunodeficiency virus type 2 group A. J. Gen. Virol. 93, 889–899. Figueiredo, L.T., Moreli, M.L., de-Sousa, R.L., Borges, A.A., de-Figueiredo, G.G., Machado, A.M., Bisordi, I., Nagasse-Sugahara, T.K., Suzuki, A., Pereira, L.E., deSouza, R.P., de-Souza, L.T., Braconi, C.T., Harsi, C.M., de-Andrade-Zanotto, P.M., Viral Diversity Genetic Network, C., 2009. Hantavirus pulmonary syndrome, central plateau, southeastern, and southern Brazil. Emerg. Infect. Dis. 15, 561– 567. Firth, C., Tokarz, R., Simith, D.B., Nunes, M.R., Bhat, M., Rosa, E.S., Medeiros, D.B., Palacios, G., Vasconcelos, P.F., Lipkin, W.I., 2012. Diversity and distribution of hantaviruses in South America. J. Virol. 86, 13756–13766. Guo, W.P., Lin, X.D., Wang, W., Tian, J.H., Cong, M.L., Zhang, H.L., Wang, M.R., Zhou, R.H., Wang, J.B., Li, M.H., Xu, J., Holmes, E.C., Zhang, Y.Z., 2013. Phylogeny and origins of hantaviruses harbored by bats, insectivores, and rodents. PLoS Pathog. 9, e1003159. Holmes, E.C., 2008. Evolutionary history and phylogeography of human viruses. Annu. Rev. Microbiol. 62, 307–328. Huang, Y., Niu, B., Gao, Y., Fu, L., Li, W., 2010. CD-HIT Suite: a web server for clustering and comparing biological sequences. Bioinformatics 26, 680–682. Hughes, A.L., Friedman, R., 2000. Evolutionary diversification of protein-coding genes of hantaviruses. Mol. Biol. Evol. 17, 1558–1568. Hugot, J.P., Plyusnina, A., Herbreteau, V., Nemirov, K., Laakkonen, J., Lundkvist, A., Supputamongkol, Y., Henttonen, H., Plyusnin, A., 2006. Genetic analysis of Thailand hantavirus in Bandicota indica trapped in Thailand. Virol. J. 3, 72. Jaaskelainen, K.M., Kaukinen, P., Minskaya, E.S., Plyusnina, A., Vapalahti, O., Elliott, R.M., Weber, F., Vaheri, A., Plyusnin, A., 2007. Tula and Puumala hantavirus NSs ORFs are functional and the products inhibit activation of the interferon-beta promoter. J. Med. Virol. 79, 1527–1536. Johansson, P., Yap, G., Low, H.T., Siew, C.C., Kek, R., Ng, L.C., Bucht, G., 2010. Molecular characterization of two hantavirus strains from different rattus species in Singapore. Virol. J. 7, 15. Johnson, A.M., Bowen, M.D., Ksiazek, T.G., Williams, R.J., Bryan, R.T., Mills, J.N., Peters, C.J., Nichol, S.T., 1997. Laguna Negra virus associated with HPS in western Paraguay and Bolivia. Virology 238, 115–127. Jonsson, C.B., Figueiredo, L.T., Vapalahti, O., 2010. A global perspective on hantavirus ecology, epidemiology, and disease. Clin. Microbiol. Rev. 23, 412–441. Kariwa, H., Yoshida, H., Sanchez-Hernandez, C., Romero-Almaraz Mde, L., Almazan-Catalan, J.A., Ramos, C., Miyashita, D., Seto, T., Takano, A., Totani, M., Murata, R., Saasa, N., Ishizuka, M., Sanada, T., Yoshii, K., Yoshimatsu, K., Arikawa, J., Takashima, I., 2012. Genetic diversity of hantaviruses in Mexico: identification of three novel hantaviruses from Neotominae rodents. Virus Res. 163, 486–494. Kariwa, H., Yoshimatsu, K., Sawabe, J., Yokota, E., Arikawa, J., Takashima, I., Fukushima, H., Lundkvist, A., Shubin, F.N., Isachkova, L.M., Slonova, R.A., Leonova, G.N., Hashimoto, N., 1999. Genetic diversities of hantaviruses among rodents in Hokkaido, Japan and Far East Russia. Virus Res. 59, 219–228. Klempa, B., Witkowski, P.T., Popugaeva, E., Auste, B., Koivogui, L., Fichet-Calvet, E., Strecker, T., Ter Meulen, J., Kruger, D.H., 2012. Sangassou virus, the first hantavirus isolate from Africa, displays genetic and functional properties distinct from those of other murinae-associated hantaviruses. J. Virol. 86, 3819– 3827. Lee, H.W., Baek, L.J., Johnson, K.M., 1982. Isolation of Hantaan virus, the etiologic agent of Korean hemorrhagic fever, from wild urban rats. J. Infect. Dis. 146, 638– 644. Lee, H.W., Lee, P.W., Johnson, K.M., 1978. Isolation of the etiologic agent of Korean Hemorrhagic fever. J. Infect. Dis. 137, 298–308. Lemey, P., Rambaut, A., Drummond, A.J., Suchard, M.A., 2009. Bayesian phylogeography finds its roots. PLoS Comput. Biol. 5, e1000520. Li, W., Godzik, A., 2006. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22, 1658–1659.
335 336 337 338 339 340 341 342 343 344 345 346 347 348 349 350 351 352 353 354 355 356 357 358 359 360 361 362 363 364 365 366 367 368 369 370 371 372 373 374 375 376 377 378 379 380 381 382 383 384 385 386 387 388 389 390 391 392 393 394 395 396 397 398 399 400 401 402 403 404 405 406 407 408 409 410 411 412 413 414 415 416 417
Please cite this article in press as: Souza, W.M., et al. Phylogeography and evolutionary history of rodent-borne hantaviruses. Infect. Genet. Evol. (2013), http://dx.doi.org/10.1016/j.meegid.2013.11.015
MEEGID 1806
No. of Pages 7, Model 5G
27 November 2013 W.M. Souza et al. / Infection, Genetics and Evolution xxx (2013) xxx–xxx 418 419 420 421 422 423 424 425 426 427 428 429 430 431 432 433 434 435 436 437 438 439 440 441 442 443 444 445 446 447 448 449 450
Lopez, N., Padula, P., Rossi, C., Lazaro, M.E., Franze-Fernandez, M.T., 1996. Genetic identification of a new hantavirus causing severe pulmonary syndrome in Argentina. Virology 220, 223–226. Morzunov, S.P., Rowe, J.E., Ksiazek, T.G., Peters, C.J., St Jeor, S.C., Nichol, S.T., 1998. Genetic analysis of the diversity and origin of hantaviruses in Peromyscus leucopus mice in North America. J. Virol. 72, 57–64. Nemirov, K., Henttonen, H., Vaheri, A., Plyusnin, A., 2002. Phylogenetic evidence for host switching in the evolution of hantaviruses carried by Apodemus mice. Virus Res. 90, 207–215. Nichol, S.T., Spiropoulou, C.F., Morzunov, S., Rollin, P.E., Ksiazek, T.G., Feldmann, H., Sanchez, A., Childs, J., Zaki, S., Peters, C.J., 1993. Genetic identification of a hantavirus associated with an outbreak of acute respiratory illness. Science 262, 914–917. Papa, A., 2012. Dobrava-Belgrade virus: phylogeny, epidemiology, disease. Antiviral Res. 95, 104–117. Parada, A., Pardinas, U.F., Salazar-Bravo, J., D’Elia, G., Palma, R.E., 2013. Dating an impressive Neotropical radiation: Molecular time estimates for the Sigmodontinae (Rodentia) provide insights into its historical biogeography. Mol. Phylogenet. Evol. 66, 960–968. Posada, D., 2008. jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 25, 1253–1256. Powers, A.M., Mercer, D.R., Watts, D.M., Guzman, H., Fulhorst, C.F., Popov, V.L., Tesh, R.B., 1999. Isolation and genetic characterization of a hantavirus (Bunyaviridae: Hantavirus) from a rodent, Oligoryzomys microtis (Muridae), collected in northeastern Peru. Am. J. Trop. Med. Hyg. 61, 92–98. Ramsden, C., Holmes, E.C., Charleston, M.A., 2009. Hantavirus evolution in relation to its rodent and insectivore hosts: no evidence for codivergence. Mol. Biol. Evol. 26, 143–153. Ramsden, C., Melo, F.L., Figueiredo, L.M., Holmes, E.C., Zanotto, P.M., Consortium, V., 2008. High rates of molecular evolution in hantaviruses. Mol. Biol. Evol. 25, 1488–1492. Richter, M.H., Hanson, J.D., Cajimat, M.N., Milazzo, M.L., Fulhorst, C.F., 2010. Geographical range of Rio Mamore virus (family Bunyaviridae, genus
7
Hantavirus) in association with the small-eared pygmy rice rat (Oligoryzomys microtis). Vector Borne Zoonotic Dis. 10, 613–620. Salemi, M., Lamers, S.L., Yu, S., de Oliveira, T., Fitch, W.M., McGrath, M.S., 2005. Phylodynamic analysis of human immunodeficiency virus type 1 in distinct brain compartments provides a model for the neuropathogenesis of AIDS. J. Virol. 79, 11343–11352. Schlegel, M., Kindler, E., Essbauer, S.S., Wolf, R., Thiel, J., Groschup, M.H., Heckel, G., Oehme, R.M., Ulrich, R.G., 2012. Tula virus infections in the Eurasian water vole in Central Europe. Vector borne and zoonotic diseases 12, 503–513. Steppan, S., Adkins, R., Anderson, J., 2004. Phylogeny and divergence-date estimates of rapid radiations in muroid rodents based on multiple nuclear genes. Syst. Biol. 53, 533–553. Thompson, J.D., Higgins, D.G., Gibson, T.J., 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680. Vaheri, A., Strandin, T., Hepojoki, J., Sironen, T., Henttonen, H., Makela, S., Mustonen, J., 2013. Uncovering the mysteries of hantavirus infections. Nat. Rev. Microbiol. 11, 539–550. Vera-Otarola, J., Solis, L., Soto-Rifo, R., Ricci, E.P., Pino, K., Tischler, N.D., Ohlmann, T., Darlix, J.L., Lopez-Lastra, M., 2012. The Andes hantavirus NSs protein is expressed from the viral small mRNA by a leaky scanning mechanism. J. Virol. 86, 2176–2187. Vincent, M.J., Quiroz, E., Gracia, F., Sanchez, A.J., Ksiazek, T.G., Kitsutani, P.T., Ruedas, L.A., Tinnin, D.S., Caceres, L., Garcia, A., Rollin, P.E., Mills, J.N., Peters, C.J., Nichol, S.T., 2000. Hantavirus pulmonary syndrome in Panama: identification of novel hantaviruses and their likely reservoirs. Virology 277, 14–19. Weiss, S., Witkowski, P.T., Auste, B., Nowak, K., Weber, N., Fahr, J., Mombouli, J.V., Wolfe, N.D., Drexler, J.F., Drosten, C., Klempa, B., Leendertz, F.H., Kruger, D.H., 2012. Hantavirus in bat, Sierra Leone. Emerg. Infect. Dis. 18, 159–161. Worobey, M., Telfer, P., Souquiere, S., Hunter, M., Coleman, C.A., Metzger, M.J., Reed, P., Makuwa, M., Hearn, G., Honarvar, S., Roques, P., Apetrei, C., Kazanji, M., Marx, P.A., 2010. Island biogeography reveals the deep history of SIV. Science 329, 1487.
451 452 453 454 455 456 457 458 459 460 461 462 463 464 465 466 467 468 469 470 471 472 473 474 475 476 477 478 479 480 481 482 483 484 485
Please cite this article in press as: Souza, W.M., et al. Phylogeography and evolutionary history of rodent-borne hantaviruses. Infect. Genet. Evol. (2013), http://dx.doi.org/10.1016/j.meegid.2013.11.015