Data-driven identification of potential Zika virus vectors

  1. Michelle V Evans  Is a corresponding author
  2. Tad A Dallas
  3. Barbara A Han
  4. Courtney C Murdock
  5. John M Drake
  1. University of Georgia, United States
  2. Center for the Ecology of Infectious Diseases, University of Georgia, United States
  3. University of California-Davis, United States
  4. Cary Institute of Ecosystem Studies, United States
  5. Center for Tropical Emerging Global Diseases, University of Georgia, United States
  6. Center for Vaccines and Immunology, University of Georgia, United States
  7. River Basin Center, University of Georgia, United States
5 figures and 6 tables

Figures

A network diagram of mosquito vectors (circles) and their flavivirus pairs (rectangles).

The Culex mosquitoes (light blue) and primarily encephalitic viruses (blue) are more clustered than the Aedes (orange) and hemmorhagic viruses (red). Notably, West Nile Virus is vectored by both Aedes and Culex species. Predicted vectors of Zika are shown by bolded links in black. The inset shows predicted vectors of Zika and species names, ordered by the model’s propensity scores. Included flaviviruses are Banzi virus (BANV), Bouboui virus (BOUV), dengue virus strains 1, 2, 3 and 4 (DENV-1,2,3,4), Edge Hill virus (EHV), Ilheus virus (ILHV), Israel turkey meningoencephalomyelitis virus (ITV), Japanese encephalitis virus (JEV), Kedougou virus (KEDV), Kokobera virus (KOKV), Kunjin virus (KUNV), Murray Valley encephalitis virus (MVEV), Rocio virus (ROCV), St. Louis encephalitis virus (SLEV), Spondwendi virus (SPOV), Stratford virus (STRV), Uganda S virus (UGSV), Wesselsbron virus (WESSV), West Nile Virus (WNV), yellow fever virus (YFV), and Zika virus (ZIKV).

https://doi.org/10.7554/eLife.22053.003
Variable importance by permutation, averaged over 25 models.

Because some categorical variables were treated as binary by our model (i.e. continental range), the relative importance of each binary variable was summed to result in the overall importance of the categorical variable. Mosquito and virus traits are shown in blue and maroon, respectively. Error bars represent the standard error from 25 models.

https://doi.org/10.7554/eLife.22053.004
Distribution maps of predicted vectors of Zika virus in the continental US.

Maps of Aedes species are based on Centers for disease control and prevention (2016). All other species’ distributions are georectified maps from Darsie and Ward (2005).

https://doi.org/10.7554/eLife.22053.005
Appendix 1—figure 1
Propensity values of the main and supplementary models.

Dashed lines represent corresponding threshold values for each model based on lowest ranked known vector propensities.

https://doi.org/10.7554/eLife.22053.008
Appendix 1—figure 2
Distribution of propensity values for the main and supplementary models.

Dashed lines represent corresponding threshold values for each model based on lowest ranked known vector propensities.

https://doi.org/10.7554/eLife.22053.009

Tables

Table 1

Predicted vectors of Zika virus, as reported by our model. Mosquito species endemic to the continental United States are bolded. A species is defined as a known vector of Zika virus if a full transmission cycle (see main text) has been observed.

https://doi.org/10.7554/eLife.22053.006
SpeciesGBM prediction ±SDKnown vector?
Aedes aegypti0.81 ± 0.12Yes
Ae. albopictus0.54 ± 0.14Yes
Culex quinquefasciatus0.38 ± 0.14No
Ae. polynesiensis0.36 ± 0.13No
Ae. scutellaris0.33 ± 0.13No
Ae. africanus0.32 ± 0.11No
Ae. furcifer0.31 ± 0.16Yes
Ae. vittatus0.30 ± 0.20Yes
Ae. taylori0.30 ± 0.16Yes
Ae. luteocephalus0.25 ± 0.12Yes
Ae. tarsalis0.18 ± 0.11Yes
Ae. metallicus0.16 ± 0.08No
Ae. minutus0.16 ±0.09No
Ae. opok0.14 ± 0.06No
Ae. bromeliae0.11 ± 0.06No
Ae. scapularis0.10 ± 0.04No
Cx. pipiens0.10 ± 0.04No
Ae. hensilli0.10 ± 0.06Yes
Ae. vigilax0.10 ± 0.05No
Cx. annulirostrix0.08 ± 0.03No
Psorophora ferox0.08 ± 0.05No
Cx. rubinotus0.08 ± 0.07No
Cx. tarsalis0.08 ± 0.03No
Ae. occidentalis0.08 ± 0.05No
Ae. flavicolis0.07 ± 0.04No
Ae. serratus0.07 ± 0.04No
Cx. p. molestus0.07 ± 0.04No
Ae. vexans0.06 ± 0.04No
Cx. neavei0.06 ± 0.02No
Runchomyia frontosa0.06 ± 0.04No
Ae. neoafricanus0.06 ± 0.03No
Ae. chemulpoensis0.06 ± 0.03No
Cx. vishnui0.05 ± 0.01No
Cx. tritaeniorhynchus0.05 ± 0.01No
Ae. fowleri0.04 ± 0.03Yes
Appendix 1—table 1

Vector predictions by the supplementary model.

https://doi.org/10.7554/eLife.22053.007
Vector
GBM PredictionSD
Aedes aegypti0.840.06
Aedes albopictus0.810.07
Aedes vittatus0.760.10
Aedes africanus0.700.11
Aedes taylori0.650.14
Aedes furcifer0.650.14
Aedes luteocephalus0.590.12
Aedes metallicus0.590.13
Aedes opok0.580.13
Culex quinquefasciatus0.560.13
Aedes tarsalis0.560.12
Aedes scutellaris0.560.11
Aedes minutus0.550.12
Aedes polynesiensis0.530.11
Mansonia uniformis0.520.12
Aedes fowleri0.480.14
Aedes vexans0.460.11
Aedes dalzieli0.450.13
Culex annulirostris0.450.08
Mansonia africana0.420.12
Psorophora ferox0.390.14
Culex tarsalis0.380.09
Culex tritaeniorhynchus0.370.08
Culex pipiens0.370.13
Culex neavei0.340.06
Aedes vigilax0.340.07
Aedes flavicollis0.330.14
Aedes scapularis0.310.07
Aedes taeniarostris0.310.13
Aedes jamoti0.310.13
Aedes circumluteolus0.300.13
Eretmapodites inornatus0.300.15
Aedes cumminsii0.290.11
Culex vishnui0.280.05
Aedes lineatopennis0.280.11
Aedes neoafricanus0.270.11
Aedes bromeliae0.260.10
Culex guiarti0.260.06
Culex perfuscus0.260.06
Aedes stokesi0.260.12
Culex telesilla0.250.06
Anopheles gambiae0.240.11
Sabethes chloropterus0.240.11
Aedes hensilli0.240.09
Aedes serratus0.230.06
Aedes chemulpoensis0.230.08
Aedes normanensis0.230.06
Culex bitaeniorhynchus0.220.09
Culex pseudovishnui0.220.05
Aedes argenteopunctatus0.210.06
Wyeomyia vanduzeei0.210.15
Culex p. molestus0.210.06
Culex salinarius0.200.04
Aedes grahami0.190.15
Anopheles coustani0.190.08
Aedes longipalpis0.180.18
Uranotaenia sapphirina0.170.08
Aedes domesticus0.170.06
Aedes abnormalis0.170.06
Aedes natronius0.170.06
Eretmapodites chrysogaster0.170.08
Aedes mcintoshi0.170.06
Aedes ochraceus0.160.06
Culex fatigans0.160.07
Anopheles amictus0.160.06
Eretmapodites quinquevittatus0.160.08
Appendix 2—table 1

Table of mosquito traits used in model.

https://doi.org/10.7554/eLife.22053.010
TraitTypeSubcategories
AnthropophilybinaryNA
SubgenusfactorNA
Host breadthnumericNA
Host rangebinary (x4)Primate, Non-Primate Mammal, Bird, Cold-Blooded Vertebrate
Geographic areanumericNA
Continental rangebinary (x8)Africa, Middle East, Australia, Pacific, Asia, Europe, North America, South America
Biting timebinary (x4)Dawn, Day, Dusk, Night
Artificia container breederbinaryNA
Oviposition sitebinary (x8)Treehole, Natural Container, Permanent Fresh Water, Rockhole, Marsh, Swamp, Temporary Ground Pools, Rice Paddy
Habitat discriminationnumericNA
Salinity tolerancebinaryNA
Habitat permanencebinaryNA
Urban preferencebinaryNA
EndophilybinaryNA
No. of flaviviruses vectorednumericNA
Appendix 2—table 2

Table of virus traits used in model.

https://doi.org/10.7554/eLife.22053.011
TraitTypeSubcategories
GroupfactorJapanese Encephalitis, Ntaya, Yellow Fever, Aroa, Dengue, Kokobera, Spondweni
Continental rangebinary(x8)Africa, Middle East, Australia, Pacific, Asia, Europe, North America, South America
CladefactorVI, VII, IX, X, XI, XII, XIV,
Year isolatednumericNA
Mutated envelopebinaryNA
Host breadthnumericNA
Host Rangebinary(x6)Human, Non-Human Primate, Rodent, Other Mammal, Bird, Marsupial
Mosquito vector breadthnumericNA
Vectored by other arthropodsbinaryNA
Disease symptomsbinary (x2)Encephalitis, Fever
Disease severitynumericNA
Genome lengthnumericNA
Appendix 3—table 1

Primary sources for mosquito traits.

https://doi.org/10.7554/eLife.22053.012
Mosquito speciesSources
Aedeomyia africanaRobert et al. (1998), Harbach (2015), Omondi et al. (2015)
Aedeomyia catastictaHarbach (2015), Jansen et al. (2009), Wright et al. (1981)
Aedes abnormalisIwuala (1981)
Aedes aegyptiHalstead (2008), Ramasamy et al. (2011)
Aedes africanusHaddow (1961)
Aedes albopictusRamasamy et al. (2011)
Aedes alternansNSW Health (2016), Russell et al. (2013), Knight et al. (2012)
Aedes argenteopunctatusHarbach (2015), Fontenille et al. (1998)
Aedes bancroftianusNSW Health (2016), Russell (1986), Harbach (2015)
Aedes bromeliaeBennett et al. (2015), Beran (1994), Digoutte (1999)
Aedes caballusHarbach (2015), Steyn and Schulz (1955)
Aedes canadensisCarpenter and LaCasse (1974), Andreadis et al. (2004)
Aedes cantansRenshaw et al. (1994, 1995), Service (1993)
Aedes cantatorGiberson et al. (2007)
Aedes chemulpoensisFeng (1983)
Aedes cinereusMorrison and Andreadis (1992), Anderson et al. (2007), Becker and Neumann (1983), Molaei et al. (2008)
Aedes circumluteolusJupp and McIntosh (1987), Paterson et al. (1964), Chandler et al. (1975)
Aedes cumminsiLane and Crosskey (2012)
Aedes curtipesHarbach (2015), MacDonald et al. (1965), Knight and Hull (1953)
Aedes dalzieliFontenille et al. (1998)
Aedes domesticusHarbach (2015), Lane and Crosskey (2012), Geoffroy (1987)
Aedes dorsalisAldemir et al. (2010), Wang et al. (2012)
Aedes flavicolisReinert (1970)
Aedes fluviatilisMultini et al. (2015), Baton et al. (2013), Reinert et al. (2008)
Aedes fowleri(Boussès et al., 2013)
Aedes furciferBeran (1994), Hopkins (1952)
Aedes grahamiHarbach (2015)
Aedes hensilliLedermann et al. (2014), Bohart and Ingram (1946)
Aedes ingramiLane and Crosskey (2012), Haddow (1946b, 1964, 1942)
Aedes jamotiHarbach (2015), Le Berre and Hamon (1961)
Aedes japonicusKaufman and Fonseca (2014), Kampen and Werner (2014)
Aedes juppiHarbach (2015), Jupp and Kemp (1998)
Aedes koreicusHarbach (2015), Montarsi et al. (2013), Medlock et al. (2015)
Aedes lineatopennisHarbach (2015), Amerasinghe and Indrajith (1995), Jupp (1967), Linthicum et al. (1985)
Aedes longipalpisHarbach (2015)
Aedes luteocephalusDiallo et al. (2012a), Service (1965b), Boorman (1961)
Aedes mcintoshiWalter Reed Biosystematics Unit (2016), Harbach (2015)
Aedes mediolineatusHarbach (2015)
Aedes melanimonWalter Reed Biosystematics Unit (2016), Barker et al. (2009), Chapman (1960)
Aedes metallicusHarbach (2015), Beran (1994)
Aedes minutusHarbach (2015), Diallo et al. (2012b)
Aedes natroniusHarbach (2015)
Aedes neoafricanusHarbach (2015), Diallo et al. (2012b), Hervy et al. (1986)
Aedes normanensisNSW Health (2016), Hearnden and Kay (1995)
Aedes notoscriptusNSW Health (2016), Jansen et al. (2015), Nicholson et al. (2015), Derraik et al. (2007), Frances et al. (2002)
Aedes occidentalisHarbach (2015), Evans (1926)
Aedes ochraceusCorbet (1962), Lutomiah et al. (2014)
Aedes opokBeran (1994), Herve et al. (1975), Germain et al. (1976)
Aedes polynesiensisYoung (2007)
Aedes procaxNSW Health (2016), Ryan and Kay (2000)
Aedes scapularisForattini et al. (1988)
Aedes scutellarisPenn (1947)
Aedes serratusGuimarães et al. (2000), Cardoso et al. (2010)
Aedes simulansHarbach (2015)
Aedes sollicitansGiberson et al. (2007), Carpenter and LaCasse (1974), Crans and Sprenger (1996), Crans et al. (1996)
Aedes stokesiHarbach (2015), Reinert (1986)
Aedes taeniarostrisEastwood et al. (2013)
Aedes tarsalisEllis et al. (2007)
Aedes tayloriWalter Reed Biosystematics Unit (2016)
Aedes togoiTsunoda et al. (2012), Lee and Hong (1995)
Aedes tremulusKay et al. (2000), Webb et al. (2016)
Aedes trivittatusCarpenter and LaCasse (1974), Andreadis et al. (2004)
Aedes vexansBoxmeyer and Palchick (1999), Aldemir et al. (2010)
Aedes vigilaxNSW Health (2016), Chapman et al. (1999)
Aedes vittatusBoorman (1961), Selvaraj and Dwarakanath (1992)
Anopheles amictusHearnden and Kay (1995)
Anopheles barbirostrisSriwichai et al. (2016), Amerasinghe and Indrajith (1995), Bashar et al. (2012)
Anopheles coustaniFornadel et al. (2011), Mwangangi et al. (2013), Muriu et al. (2008), Mwangangi et al. (2007)
Anopheles cruciansGrieco et al. (2006), Qualls et al. (2012)
Anopheles domicolaDiagne et al. (1994)
Anopheles funestusGillies et al. (1968), Githeko et al. (1996)
Anopheles gambiaeCoggeshall (1944), Gillies et al. (1968), Huho et al. (2013)
Anopheles hyrcanusRueda et al. (2006, 2005), Ponçon et al., 2007), Aldemir et al. (2010)
Anopheles maculipennisAldemir et al. (2010), Brugman et al. (2015), Gordeev et al. (2005)
Anopheles meraukensisCooper et al. (2006), NSW Health (2016)
Anopheles paludisKarch and Mouchet (1992), Mouchet (1957)
Anopheles pharoensisGillies et al. (1968), Taye et al. (2006)
Anopheles philippinensisToma et al. (2002), Silver (2007), Bashar et al. (2012)
Anopheles pretoriensisAl-Sheik (2011), Shililu et al. (2003)
Anopheles punctipennisCarpenter and LaCasse (1974)
Anopheles quadrimaculatusCarpenter and LaCasse (1974)
Anopheles subpictusSinka et al. (2011)
Anopheles tesselatusMiyagi et al. (1983), Paramasivan et al. (2015)
Armigeres obturbansHarbach (2015)
Coquillettidia auritesSchwetz (1930), Njabo et al. (2009)
Coquillettidia linealisRussell et al. (2013), Williams (2005), Webb et al. (2016)
Coquillettidia metallicaNjabo et al. (2009), Mcclelland ga et al. (1960)
Coquillettidia perturbansCarpenter and LaCasse (1974), Anderson et al. (2007), Bosak et al. (2001), Callahan and Morris (1987)
Coquillettidia richiardiiVentim et al. (2012), Serandour et al. (2006), Versteirt et al. (2013)
Coquillettidia venezuelensisGuimarães et al. (2000), Degallier et al. (1978)
Culex adamesiSirivanakarn and Galindo (1980)
Culex annulirostrisNSW Health (2016), Hall-Mendelin et al. (2012), Williams and Kokkinn (2005)
Culex antennatusGad et al. (1995), Karch et al. (1993), Morsy et al. (1990), Kenawy et al. (1998)
Culex australicusNSW Health (2016), Russell (2012)
Culex bahamensisLopes (1997)
Culex bitaeniorhynchusKulkarni and Rajput (1988), Fakoorziba and Vijayan (2008), Harbach (1988)
Culex caudelliAlfonzo et al. (2005), Chadee and Tikasingh (1989)
Culex coronatorYee and Skiff (2014), de Oliveria et al. (1985)
Culex crybdade Oliveria et al. (1985)
Culex duttoniMwangangi et al. (2009)
Culex epidesmusKanojia (2003), Reisen et al. (1976)
Culex fatigansFlordia Medical Entomology Laboratory (2016), Liu et al. (1960), Robinson (2005)
Culex fuscocephalaOhba et al. (2015), Kulkarni and Rajput (1988), Amerasinghe and Munasingha (1994), Wang (1975)
Culex gelidusWilliams (2005), Sudeep (2014)
Culex guiartiLogan et al. (1991)
Culex modestusVeronesi et al. (2012), Radrova et al. (2013), Muñoz et al. (2012), Chalvet-Monfray et al. (2007), Fyodorova et al. (2006)
Culex nakuruensisSomeren (1967)
Culex neaveiDiallo et al. (2012a), Nikolay et al. (2012), Fall et al. (2013, 2011)
Culex nebulosusAdebote et al. (2006), Okorie (1978), Davis and Philip (1931)
Culex nigripalpusLaporta et al. (2008), Carpenter and LaCasse (1974), Flordia Medical Entomology Laboratory. (2016)
Culex p. molestusRobinson (2005), Gomes et al. (2013)
Culex perexiguusMuñoz et al. (2012), Ammar et al. (2012)
Culex perfuscusHopkins (1952), Diallo et al. (2014), Service (1993)
Culex pipiensHarbach (1988), Anderson et al. (2007)
Culex poicilipesMuturi et al. (2008), Yamar et al. (2005), Chevalier et al. (2004)
Culex pruinaWanson and Lebred (1946)
Culex pseudovishnuiFakoorziba and Vijayan (2008), Reisen et al. (1976), Amerasinghe and Indrajith (1995), Reuben et al. (1992)
Culex pullusJohansen et al. (2009), Webb et al. (2016)
Culex quinquefasciatusFlordia Medical Entomology Laboratory (2016), DeGroote and Sugumaran (2012)
Culex restuansApperson et al. (2002), Ebel et al. (2005), Kilpatrick et al. (2005), Molaei et al. (2008)
Culex rubinotusJupp et al. (1976)
Culex salinariusRochlin et al. (2008), Mackay et al. (2010), Rey et al. (2006)
Culex sitiensNSW Health (2016), Prummongkol et al. (2012)
Culex spissipesTakahashi (1968), Degallier et al. (1978)
Culex squamosesNSW Health (2016), Jansen et al. (2009)
Culex taeniopusDavies (1978), 1975), Lopes (1996)
Culex tarsalisReisen (1993), Rueger et al. (1964)
Culex telesillaNjogu and Kinoti (1971)
Culex thalassiusKerr (1932), Snow and Boreham (1978), Service (1993), Kirby et al. (2008)
Culex theileriAldemir et al. (2010), Muñoz et al. (2012), Simsek (2004)
Culex tritaeniorhynchusKanojia and Geevarghese (2004), Fakoorziba and Vijayan (2008), Flemings (1959), Amerasinghe and Munasingha (1994), Mwandawiro et al. (1999), Bhattacharyya et al. (1994), Reuben (1971)
Culex univittatusJupp (1967), Chandler et al. (1975), Jupp and Brown (1967)
Culex virgultusCarpenter and LaCasse (1974)
Culex vishnuiChen et al. (2014), Bhattacharyya et al. (1994), Ohba et al. (2015)
Culex vomeriferFerro et al. (2003), Natal et al. (1998), Suárez-Mutis et al. (2009), Sallum and Forattini (1996)
Culex wescheiSnow and Boreham (1973), Lane and Crosskey (2012)
Culex whitmoreiBegum et al. (1986), Reisen et al. (1976), Peiris et al. (1992)
Culex zombaensisLane and Crosskey (2012), Logan et al. (1991)
Culiseta alaskensisFrohne (1953)
Culiseta impatiensSommerman (1964), Frohne (1953), Murdock et al. (2010), Smith (1966)
Culiseta inornataCarpenter and LaCasse (1974), Smith (1966), Belton (1979)
Culiseta melanuraMolaei et al. (2006), Mahmood and Crans (1998), Flordia Medical Entomology Laboratory (2016), Hickman and Brown (2013)
Deinocerites pseudesMartin et al. (1973), Peyton et al. (1964)
Eretmapodites chrysogasterDoucet and Cachan (1961), Sylla et al. (2013), Service (1965a), Haddow (1946b)
Eretmapodites inornatusHaddow (1946a)
Eretmapodites oedipodeios (oedipodius)Haddow (1946a), de Cunha Ramos and Ribeiro (1990)
Eretmapodites quinquevittatusBohart and Ingram (1946), Jupp and Kemp (2002), Lounibos (1980)
Eretmapodites silvestrisLounibos (1980), Hoogstraal and Knight (1951)
Ficalbia flavensKing and Hoogstraal (1946)
Haemagogus anastasionisVan der Kuyp (1949), Bueno-Marà etal. (2015), Maestre-Serrano et al. (2013)
Haemagogus celesteBueno-Marà etal., 2015, Maestre-Serrano et al. (2013), Beran (1994), Chadee et al. (1985)
Haemagogus equinusChadee et al. (1985, 1993), Waddell and Taylor (1945)
Haemagogus janthinomysArnell (1973), Alencar et al. (2005), Chadee et al. (1992)
Haemagogus leucocelaenusAlencar et al. (2008), Pinto et al. (2009)
Haemagogus spegazziniiArnell (1973), Galindo et al. (1951, 1950)
Mansonia africanaKarch et al. (1993), Chandler et al. (1975), Hopkins (1952)
Mansonia septempunctataNSW Health (2016), Harbach (2015)
Mansonia titillansCarpenter and LaCasse (1974), Viana et al. (2010), Stein et al. (2013)
Mansonia uniformisSabesan et al. (1991), Kumar et al. (1989), Wharton (1962)
Mimomyia hispidaBoreham et al. (1975), Harbach (2015)
Mimomyia lacustrisHarbach (2015)
Mimomyia splendensBoreham et al. (1975), Robert et al. (1998)
Orthopodomyia signiferaHanson et al. (1995), Burkett-Cadena (2013)
Psorophora albipesAlfonzo et al. (2005), dos Santos Silva et al. (2012), Guimarães et al. (2000)
Psorophora columbiaeCarpenter and LaCasse (1974)
Psorophora feroxCarpenter and LaCasse (1974), Flordia Medical Entomology Laboratory (2016), Degallier et al. (1978), Molaei et al. (2008)
Runchomyia frontosaCardoso et al. (2015), Heinemann et al. (1980)
Sabethes albiprivusGomes et al. (2010), Pedro et al. (2008)
Sabethes belisarioiPinto et al. (2009)
Sabethes chloropterusBeran (1994), Pinto et al. (2009), Galindo (1958)
Sabethes soperiNavarro et al. (2015), Harbach (2015)
Uranotaenia mashonaensisHarbach and Schnur (2007)
Uranotaenia sapphirinaCupp et al. (2003), Crans (2016)
Uranotaenia unguiculataKhoshdel-Nezamiha et al. (2014), Ramsdale and Snow (2001), Sebesta et al. (2010), Bagirov et al. (1994), Kenawy et al. (1987)
Appendix 3—table 2

Primary sources for virus traits.

https://doi.org/10.7554/eLife.22053.013
VirusSources
Alfuy VirusMackenzie et al. (2012)
Bagaza virusMahy (2009), Llorente et al. (2015), Gamino et al. (2012)
Banzi virusGrard et al. (2010), Karabatsos (1985)
Bouboui virusGrard et al. (2010), Cook and Zumla (2009)
Bussuquara virusBeran (1994)
Dengue type 1Cook and Zumla (2009)
Dengue type 2Cook and Zumla (2009)
Dengue type 3Cook and Zumla (2009)
Dengue type 4Cook and Zumla (2009)
Edge Hill virusMackenzie et al. (2012), Doherty et al. (1964)
Iguape VirusCoimbra et al. (1993), Mahy (2009)
Ilheus virusMahy (2009), Chambers and Monath (2003), Laemmert and Hughes (1947), Aitken and Anderson (1959)
Israel turkey meningoencephalomyelitis virusMahy (2009), Nir (1972)
Japanese encephalitis virusMahy (2009), Burke and Leake (1988), Gresser et al. (1958)
Jugra virusNone
Kedougou virusCook and Zumla (2009), Diagne et al. (2015a)
Kokobera virusCook and Zumla (2009), Lequime and Lambrechts (2014)
Koutango virusChambers and Monath (2003), Cook and Zumla (2009)
Kunjin virusMahy (2009), Mackenzie et al. (2012)
Murray Valley encephalitis virusCook and Zumla (2009), Mackenzie et al. (2012)
Naranjal virusMahy (2009)
New Mapoon virusNisbet et al. (2005), Mahy (2009)
Ntaya virusMahy (2009)
Rocio virusMahy (2009), Cook and Zumla (2009)
Saboya virusMahy (2009), Traoré-Lamizana et al. (2001)
Sepik virusMackenzie et al. (2012), Cook and Zumla (2009)
Spondweni virusChambers and Monath (2003), Cook and Zumla (2009)
St. Louis encephalitis virusMackenzie et al. (2012), Cook and Zumla (2009)
Stratford virusMackenzie et al. (2012)
Tembusu virusMahy (2009), Tang et al. (2015)
Uganda S virusMahy (2009)
Usutu virusMahy (2009), Chambers and Monath (2003), Cook and Zumla (2009)
WesselbronMahy (2009), Chambers and Monath (2003), Cook and Zumla (2009)
West Nile virusMackenzie et al. (2012), Cook and Zumla (2009a), Mores et al. (2007), Turell et al. (2001)
Yaounde virusMackenzie et al. (2012)
Yellow fever virusMahy (2009)
Zika virusChambers and Monath (2003), Cook and Zumla (2009)

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Michelle V Evans
  2. Tad A Dallas
  3. Barbara A Han
  4. Courtney C Murdock
  5. John M Drake
(2017)
Data-driven identification of potential Zika virus vectors
eLife 6:e22053.
https://doi.org/10.7554/eLife.22053