Advertisement

EcoHealth

pp 1–8 | Cite as

Insights into the Host Specificity of Mosquito-Borne Flaviviruses Infecting Wild Mammals

  • Jesús Sotomayor-Bonilla
  • María José Tolsá-GarcíaEmail author
  • Gabriel E. García-Peña
  • Diego Santiago-Alarcon
  • Hugo Mendoza
  • Paulina Alvarez-Mendizabal
  • Oscar Rico-Chávez
  • Rosa Elena Sarmiento-Silva
  • Gerardo Suzán
Original Contribution

Abstract

Mosquito-borne flaviviruses (MBFVs) are of public and animal health concern because they cause millions of human deaths annually and impact domestic animals and wildlife globally. MBFVs are phylogenetically divided into two clades, one is transmitted by Aedes mosquitoes (Ae-MBFVs) associated with mammals and the other by Culex mosquitoes (Cx-MBFVs) associated with birds. However, this assumption has not been evaluated. Here, we synthesized 79 published reports of MBFVs from wild mammals, estimating their host. Then, we tested whether the host specificity was biased to sampling and investigation efforts or to phylogenetic relationships using a viral phylogenetic tree drawn from analyzing whole flavivirus genomes obtained in GenBank. We found in total 18 flaviviruses, nine related to Aedes spp. and nine to Culex spp. infecting 129 mammal species. Thus, this supports that vectors are transmitting MBFV across available host clades and that ornithophilic mosquitoes are readily infecting mammals. Although most of the mosquito species are generalists in their host-feeding preferences, we also found a certain degree of MBFV’s specificity, as most of them infect closely related mammal species. The present study integrates knowledge regarding MBFVs, and it may help to understand their transmission dynamics between viruses, vectors, and mammal hosts.

Keywords

Mammals Flaviviridae Mosquitoes Virus–host association West Nile virus Dengue 

Notes

Acknowledgements

We acknowledge the Posgrado en Ciencias de la Producción y Salud Animal, UNAM, PAPIIT Project IN221715, and CONACYT PhD grant for JSB.

Funding

This study was funded by the CONACYT PhD grant for JSB.

Compliance with Ethical Standards

Conflict of interest

The authors have no competing interests.

Ethical statement

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

10393_2019_1442_MOESM1_ESM.xlsx (115 kb)
Supplementary material 1 (XLSX 115 kb)
10393_2019_1442_MOESM2_ESM.docx (24 kb)
Supplementary material 2 (DOCX 24 kb)
10393_2019_1442_MOESM3_ESM.nex (3 kb)
Supplementary material 3 (NEX 3 kb)
10393_2019_1442_MOESM4_ESM.xlsx (21 kb)
Supplementary material 4 (XLSX 20 kb)

References

  1. Abella-Medrano CA, Ibáñez-Bernal S, Carbó-Ramírez P, Santiago-Alarcon D (2018) Blood-meal preferences and avian malaria detection in mosquitoes (Diptera: Culicidae) captured at different land use types within a neotropical montane cloud forest matrix. Parasitology International 67(3):313–20.  https://doi.org/10.1016/j.parint.2018.01.006 PubMedCrossRefGoogle Scholar
  2. Aguilar-Setién A, Romero-Almaraz ML, Sánchez-Hernández C, Figueroa R, Juárez-Palma LP, García-Flores MM, Vázquez-Salinas C, Salas-Rojas M, Hidalgo-Martínes AC, Aguilar-Pierlé S, García-Estrada C, Ramos C (2008) Dengue virus in Mexican bats. Epidemiology and Infection 136: 1678–83.  https://doi.org/10.1017/s0950268808000460 PubMedPubMedCentralCrossRefGoogle Scholar
  3. Bininda-Emonds ORP, Cardillo M, Jones KE, Macphee RDE, Beck RMD, Grenyer R, Price SA, Vos RA, Gittleman JL, Purvis A (2007) The delayed rise of present-day mammals. Nature 446:507–12.  https://doi.org/10.1038/nature05634 PubMedCrossRefGoogle Scholar
  4. Calistri P, Giovannini A, Savini G, Bonfanti L, Ceolin C, Terregino C, Tamba M. 2010 West Nile Virus transmission in 2008 in North-Eastern Italy. Zoonoses Public Health 57: 211–219.  https://doi.org/10.1111/j.1863-2378.2009.01303.x PubMedCrossRefGoogle Scholar
  5. Esser HJ, Mögling R, Cleton N. B., Henk van der Jeugd, Hein Sprong, Arjan Stroo, Marion P. G. Koopmans, Willem F. de Boer and Chantal B. E. M. Reusken. 2019. Risk factors associated with sustained circulation of six zoonotic arboviruses: a systematic review for selection of surveillance sites in non-endemic areas. Parasites Vectors  https://doi.org/10.1186/s13071-019-3515-7 PubMedPubMedCentralCrossRefGoogle Scholar
  6. Freckleton RP, Harvey PH, Pagel M (2002) Phylogenetic analysis and comparative data: a test and review of evidence. The American Naturalist 160:712–26.  https://doi.org/10.1086/343873 PubMedCrossRefGoogle Scholar
  7. Gould EA, Pettersson J, Higgs S, Charrel R, de Lamballerie X (2017) Emerging arboviruses: Why today? One Health.  https://doi.org/10.1016/j.onehlt.2017.06.001 PubMedPubMedCentralCrossRefGoogle Scholar
  8. Grubaugh ND, Ebel GD (2016) Dynamics of West Nile virus evolution in mosquito vectors. Current Opinion in Virology 21:132–38.  https://doi.org/10.1016/j.coviro.2016.09.007 PubMedPubMedCentralCrossRefGoogle Scholar
  9. Gupta SK, Singh S, Nischal A, Pant KK, Seth PK (2014). Molecular-based identification and phylogeny of genomic and proteomic sequences of mosquito-borne flavivirus. Genes and Genomics 36: 31–43.  https://doi.org/10.1007/s13258-013-0137-x CrossRefGoogle Scholar
  10. Guy C, Thiagavel J, Mideo N, Ratcliffe JM. (2019). Phylogeny matters: revisiting ‘a comparison of bats and rodents as reservoirs of zoonotic viruses’. Royal Society Open Science 6: 181182.  https://doi.org/10.1098/rsos.181182 PubMedPubMedCentralCrossRefGoogle Scholar
  11. Holzmann I, Agostini I, Areta JI, Ferreyra H, Beldomenico P, di Bitetti MS (2010) Impact of yellow fever outbreaks on two howler monkey species (Alouatta guariba clamitans and A. caraya) in Misiones, Argentina. American Journal of Primatology 72:475–80.  https://doi.org/10.1002/ajp.20796 PubMedCrossRefGoogle Scholar
  12. Huelsenbeck JP, Ronquist F. 2001. MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–55.  https://doi.org/10.1093/bioinformatics/17.8.754 CrossRefGoogle Scholar
  13. Jansen CC, Prow NA, Webb CE, Hall RA, Pyke AT, Harrower BJ, Pritchard IL, Zborowski P, Ritchie SA, Russell RC, Van den Hurk AF (2009) Arboviruses isolated from mosquitoes collected from urban and peri-urban areas of Eastern Australia. Journal of the American Mosquito Control Association 25(3):272–78.  https://doi.org/10.2987/09-5908.1 PubMedCrossRefGoogle Scholar
  14. Katoh K, Standley DM (2013) MAFFT Multiple Sequence Alignment Software Version 7: improvements in performance and usability. Molecular Biology and Evolution 30:772–80.  https://doi.org/10.1093/molbev/mst010 PubMedPubMedCentralCrossRefGoogle Scholar
  15. Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464.  https://doi.org/10.1093/bioinformatics/btq166 PubMedCrossRefGoogle Scholar
  16. Kilpatrick AM, Peters RJ, Dupuis AP, Jones MJ, Daszak P, Marra PP, Kramer LD (2013) Predicted and observed mortality from vector-borne disease in wildlife: West Nile virus and small songbirds. Biological Conservation 165:79–85.  https://doi.org/10.1016/j.biocon.2013.05.015 PubMedPubMedCentralCrossRefGoogle Scholar
  17. Kyle JL, Eva Harris (2008) Global spread and persistence of dengue. Annual Review of Microbiology 62:71–92  https://doi.org/10.1146/annurev.micro.62.081307.163005 PubMedCrossRefGoogle Scholar
  18. Lobo FP, Mota BEF, Pena SDJ, Azevedo V, Macedo AM, et al. (2009) Virus-host coevolution: common patterns of nucleotide motif usage in flaviviridae and their hosts. PLoS ONE 4(7): e6282.  https://doi.org/10.1371/journal.pone.0006282 PubMedPubMedCentralCrossRefGoogle Scholar
  19. Machain-Williams C, López-Uribe M, Talavera-Aguilar L, Vera-Escalante L, Puerto-Manzano F, Ulloa A, Farfán-Ale JA, Garcia-Rejon J, Blitvich BJ, Loroño-Pino MA (2013) Selogic Evidence of flavivirus infection in bats in the Yucatan Peninsula of Mexico. Journal of Wildlife Diseases 49:1–8.  https://doi.org/10.7589/2012-12-318.serologic CrossRefGoogle Scholar
  20. Pagel M (1999) Inferring the historical patterns of biological evolution. Nature 401:877–84.  https://doi.org/10.1038/44766 PubMedCrossRefGoogle Scholar
  21. Plourde BT, Burgess TL, Eskew EA, Roth TM, Stephenson N, Foley JE (2017) Are disease reservoirs special? Taxonomic and life history characteristics. PLoS ONE 12(7): e0180716.  https://doi.org/10.1371/journal.pone.0180716 PubMedPubMedCentralCrossRefGoogle Scholar
  22. Ragan IK, Blizzard EL, Gordy P, Bowen RA (2017) Investigating the potential role of North American animals as hosts for Zika virus. Vector-Borne and Zoonotic Diseases 17:161–64.  https://doi.org/10.1089/vbz.2016.2099 PubMedCrossRefGoogle Scholar
  23. Reisen, WK (2003) Epidemiology of St. Louis encephalitis virus. Advances in Virus Research 61:139–84PubMedCrossRefGoogle Scholar
  24. Stephens CR, Heau JG, Gonza´lez C, Ibarra-Cerdeñaa CN, Sánchez-Cordero V, et al. (2009). Using biotic interaction networks for prediction in biodiversity and emerging diseases. PLoS ONE 4(5): e5725.  https://doi.org/10.1371/journal.pone.0005725 PubMedPubMedCentralCrossRefGoogle Scholar
  25. Takken W, Verhulst NO (2013) Host Preferences of blood-feeding mosquitoes. Annual Review of Entomology 58:433–53.  https://doi.org/10.1146/annurev-ento-120811-153618 PubMedCrossRefGoogle Scholar
  26. Thompson-Reuters (2017) Web of Science. https://www.webofknowledge.com/
  27. Vicente-Santos A, Moreira-Soto A, Soto-Garita C, Chaverri LG, Chaves A, Drexler JF, Morales JA, Alfaro-Alarcón A, Rodríguez-Herrera B, Corrales-Aguilar E (2017) Neotropical bats that co-habit with humans function as dead-end hosts for dengue virus. PLoS Neglected Tropical Diseases 11:e0005537.  https://doi.org/10.1371/journal.pntd.0005537 PubMedPubMedCentralCrossRefGoogle Scholar
  28. Tolsá MJ, Garcìa-Peña GE, Rico-Chávez O, Roche B, Suzán G. (2018). Macroecology of birds potentially susceptible to West Nile virus. Proceedings of the Royal Society B 285: 20182178. https://doi.org/10.1098/rspb.2018.2178 PubMedCrossRefGoogle Scholar
  29. Valiakos G, Athanasiou LV, Touloudi A, Papatsiros V, Spyrou V, Petrovska L, Billinis C (2013) West Nile Virus: basic principles, replication and important genetic determinants of virulence. In Viral replication (ed. G Rosas-Acosta), pp. 43–68. London, UK: IntechGoogle Scholar

Copyright information

© EcoHealth Alliance 2019

Authors and Affiliations

  • Jesús Sotomayor-Bonilla
    • 1
    • 2
  • María José Tolsá-García
    • 1
    • 2
    Email author
  • Gabriel E. García-Peña
    • 1
    • 2
    • 3
  • Diego Santiago-Alarcon
    • 4
  • Hugo Mendoza
    • 1
    • 2
  • Paulina Alvarez-Mendizabal
    • 1
    • 2
  • Oscar Rico-Chávez
    • 1
    • 2
  • Rosa Elena Sarmiento-Silva
    • 5
  • Gerardo Suzán
    • 1
    • 2
  1. 1.Laboratorio de Ecología de Enfermedades y Una Salud, Departamento de Etología, Fauna Silvestre y Animales de Laboratorio, Facultad de Medicina Veterinaria y ZootecniaUniversidad Nacional Autónoma de MéxicoCiudad de MéxicoMexico
  2. 2.Asociación Mexicana de Medicina de la Conservación Kalaan Kab ACCiudad de MexicoMexico
  3. 3.Centro de Ciencias de la ComplejidadUniversidad Nacional Autónoma de MéxicoCiudad de MéxicoMexico
  4. 4.Red de Biología y Conservación de VertebradosInstituto de Ecología ACXalapaMexico
  5. 5.Departamento de Microbiología e Inmunología, Facultad de Medicina Veterinaria y ZootecniaUniversidad Nacional Autónoma de MéxicoCiudad de MéxicoMexico

Personalised recommendations