Skip to main content
PMC home page
Springer Nature - PMC COVID-19 Collection logoLink to Springer Nature - PMC COVID-19 Collection
. 2018 Dec 30;19(2):168–175. doi: 10.1556/168.2018.19.2.9

Viral metacommunities associated to bats and rodents at different spatial scales

F Nieto-Rabiela 1, G Suzán 1, A Wiratsudakul 2, O Rico-Chávez 1,✉
PMCID: PMC7091747  PMID: 32218712

Abstract

One of the main goals of community ecology is to measure the relative importance of environmental filters to understand patterns of species distribution at different temporal and spatial scales. Likewise, the identification of factors that shape symbiont metacommunity structures is important in disease ecology because resulting structures drive disease transmission. We tested the hypothesis that distributions of virus species and viral families from rodents and bats are defined by shared responses to host phylogeny and host functional characteristics, shaping the viral metacommunity structures at four spatial scales (Continental, Biogeographical, Zoogeographical, and Regional). The contribution of host phylogeny and host traits to the metacommunity of viruses at each spatial scale was calculated using a redundant analysis of canonical ordering (RDA). For rodents, at American Continental scale the coherence of viral species metacommunity increased while the spatial scale decreased and Quasi-Clementsian structures were observed. This pattern suggests a restricted distribution of viruses through their hosts, while in the Big Mass (Europe, Africa, and Asia), the coherence decreased as spatial scale decreased. Viral species metacommunities associated with bats was dominated by random structures along all spatial scales. We suggest that this random pattern is a result of the presence of viruses with high occupancy range such as rabies (73%) and coronavirus (27%), that disrupt such structures. At viral family scale, viral metacommunities associated with bats showed coherent structures, with the emergence of Quasi- Clementsian and Checkerboard structures. RDA analysis indicates that the assemblage of viral diversity associated with rodents and bats responds to phylogenetic and functional characteristics, which alternate between spatial scales. Several of these variations could be subject to the spatial scale, in spite of this, we could identify patterns at macro ecological scale. The application of metacommunity theory at symbiont scales is particularly useful for large-scale ecological analysis. Understanding the rules of host-virus association can be useful to take better decisions in epidemiological surveillance, control and even predictions of viral distribution and dissemination.

Electronic Supplementary Material

Supplementary material is available for this article at 10.1556/168.2018.19.2.9 and is accessible for authorized users.

Keywords: Biogeographic scale, Disease ecology, Host environmental filtering, Niche theory, Zoogeographic scale

Electronic supplementary material

42974_2018_19020168_MOESM1_ESM.pdf (20.2KB, pdf)

Supplementary material, approximately 21 KB.

Acknowledgments

We are very grateful to PAPIIT (Project IA206416), Programa de Apoyo de los Estudios de Posgrado, UNAM, CONACYT, and Laboratorio de Ecología de Enfermedades y Una Salud, FMVZ, UNAM, especially to M. López Santana and D. Mendizabal Castillo for their contribution in databases construction.

References

  1. Bininda-Emonds ORP, Cardillo M, Jones KE, Macphee RDE, Beck RMD, Grenyer R, Price SA, Vos RA, Gittleman JL, Purvis A. The delayed rise of present-day mammals. Nature. 2007;446:507–512. doi: 10.1038/nature05634. [DOI] [PubMed] [Google Scholar]
  2. Buckley, L.B., T.J. Davies, D.D. Ackerly, N.J.B. Kraft, P. Susan, B.L. Anacker, H.V Cornell, E.I. Damschen, J. Grytnes, B.A. Hawkins, C.M. Mccain, P.R. Stephens and J.J. Wiens. 2010. Phylogeny, niche conservatism and the latitudinal diversity gradient in mammals. Proc. Roy. Soc. Lond. B. Biol. Sci. 277:rspb20100179. [DOI] [PMC free article] [PubMed]
  3. Chase JM, Myers JA. Disentangling the importance of ecological niches from stochastic processes across scales. Phil. Trans. Royal Soc. B: Biol. Sci. 2011;366:2351–2363. doi: 10.1098/rstb.2011.0063. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chave J. Neutral theory and community ecology. Ecol. Lett. 2004;7:241–253. doi: 10.1111/j.1461-0248.2003.00566.x. [DOI] [Google Scholar]
  5. Córdova-Tapia F, Zambrano L. La diversidad funcional en la ecología de comunidades. Revista Ecosistemas. 2015;24:78–87. doi: 10.7818/ECOS.2015.24-3.10. [DOI] [Google Scholar]
  6. Cox B. The biogeographic regions reconsidered. J. Biogeogr. 2001;28:511–523. doi: 10.1046/j.1365-2699.2001.00566.x. [DOI] [Google Scholar]
  7. Dallas T. Metacom: An R package for the analysis of metacommunity structure. Ecography. 2014;37:402–405. doi: 10.1111/j.1600-0587.2013.00695.x. [DOI] [Google Scholar]
  8. Dallas T, Presley SJ. Relative importance of host environment, transmission potential and host phylogeny to the structure of parasite metacommunities. Oikos. 2014;123:866–874. doi: 10.1111/oik.00707. [DOI] [Google Scholar]
  9. Davies TJ, Pedersen AB. Phylogeny and geography predict pathogen community similarity in wild primates and humans. Proc. Royal Soc. B: Biol. Sci. 2008;275:1695–1701. doi: 10.1098/rspb.2008.0284. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Drexler JF, Gloza-Rausch F, Glende J, Corman VM, Muth D, Goettsche M, Seebens A, Niedrig M, Pfefferle S, Yordanov S, Zhelyazkov L, Hermanns U, Vallo P, Lukashev A, Muller MA, Deng H, Herrler G, Drosten C. Genomic characterization of severe acute respiratory syndrome-related coronavirus in European bats and classification of coronaviruses based on partial RNA-dependent RNA polymerase gene sequences. J. Virology. 2010;84:11336–11349. doi: 10.1128/JVI.00650-10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gaston KJ. Global patterns in biodiversity. Nature. 2000;405:220–227. doi: 10.1038/35012228. [DOI] [PubMed] [Google Scholar]
  12. Gonzalez, A. 2009. Metacommunities: Spatial Community Ecology. Encyclopedia of Life Sciences:1–8.
  13. Gorman OT, Bean WJ, Webster RG. Evolutionary processes in influenza viruses: divergence, rapid evolution, and stasis. In: Holland JJ, editor. Genetic Diversity of RNA Viruses. Berlin: Springer; 1992. pp. 75–97. [DOI] [PubMed] [Google Scholar]
  14. Guernier V, Hochberg ME, Guégan JF. Ecology drives the worldwide distribution of human diseases. PLoS Biology. 2004;2:e141. doi: 10.1371/journal.pbio.0020141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD. Climate warming and disease risks for terrestrial and marine biota. Science. 2002;296:2158–2162. doi: 10.1126/science.1063699. [DOI] [PubMed] [Google Scholar]
  16. Holt BG, Lessard JP, Borregaard MK, Fritz SA, Araujo MB, Dimitrov D, Fabre PH, Graham CH, Graves GR, Jonsson KA, Nogues-Bravo D, Wang Z, Whittaker RJ, Fjeldsa J, Rahbek C. Response to comment on “An Update of Wallace’s Zoogeographic Regions of the World.”. Science. 2013;341:343–343. doi: 10.1126/science.1237541. [DOI] [PubMed] [Google Scholar]
  17. Hubbell SP. Neutral theory in community ecology and the hypothesis of functional equivalence. Funct. Ecol. 2005;19:166–172. doi: 10.1111/j.0269-8463.2005.00965.x. [DOI] [Google Scholar]
  18. Jaisson, P.C. 2000. La hormiga y el sociobiólogo. (No. 304.5 J3). México.
  19. Johnson PTJ, De Roode JC, Fenton A. Why infectious disease research needs community ecology. Science. 2016;349:1259504. doi: 10.1126/science.1259504. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Jones KE, Bielby J, Cardillo M, Fritz S, O’Dell J, Orme CDL, Safi K, Sechrest W, Boakes EH, Carbone C, Connolly C, Cutts MJ, Foster JK, Grenyer R, Habib M, Plaster C, Price S, Rigby E, Rist J, Teacher A, Bininda-Emonds ORP, Gittleman JL, Mace GM, Purvis A. PanTHERIA: a species-level database of life history, ecology, and geography of extant and recently extinct mammals. Ecology. 2009;90:2648–2648. doi: 10.1890/08-1494.1. [DOI] [Google Scholar]
  21. Kaufman DM. Diversity of new world mammals: universality of the latitudinal gradients of species and bauplans. J. Mammal. 1995;76:322–334. doi: 10.2307/1382344. [DOI] [Google Scholar]
  22. Krasnov BR, Pilosof S, Stanko M, Morand S, Korallo-Vinarskaya NP, Vinarski MV, Poulin R. Co-occurrence and phylogenetic distance in communities of mammalian ectoparasites: Limiting similarity versus environmental filtering. Oikos. 2014;123:63–70. doi: 10.1111/j.1600-0706.2013.00646.x. [DOI] [Google Scholar]
  23. Leibold MA, Holyoak M, Mouquet N, Amarasekare P, Chase JM, Hoopes MF, Holt RD, Shurin JB, Law R, Tilman D, Loreau M, Gonzalez A. The metacommunity concept: A framework for multi-scale community ecology. Ecol. Lett. 2004;7:601–613. doi: 10.1111/j.1461-0248.2004.00608.x. [DOI] [Google Scholar]
  24. Leibold MA, Mikkelson GM. Coherence, species turnover, and boundary clumping: elements of meta-community structure. Oikos. 2002;97:237–250. doi: 10.1034/j.1600-0706.2002.970210.x. [DOI] [Google Scholar]
  25. Lorencio, C.G. 2007. Avances en ecología: hacia un mejor conocimiento de la naturaleza. Secretariado de Publicaciones de la Universidad de Sevilla.
  26. Lovejoy TE, Bierregaard RO, Rylands AB. Edge and other effects of isolation on Amazon forest fragments. In: Solé ME, editor. The Science of Scarcity and Diversity. Sunderland, Massachusetts: Sinauer; 1986. pp. 257–284. [Google Scholar]
  27. Luis AD, Hayman DTS, O’Shea TJ, Cryan PM, Gilbert AT, Pulliam JRC, Mills JN, Timonin ME, Willis CKR, Cunningham AA, Fooks AR, Rupprecht CE, Wood JLN, Webb CT. A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special? Proc. Royal Soc.B: Biol. Sci. 2013;280:2012–2753. doi: 10.1098/rspb.2012.2753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Luis AD, O’Shea TJ, Hayman DTS, Wood JLN, Cunningham AA, Gilbert AT, Mills JN, Webb CT. Network analysis of host-virus communities in bats and rodents reveals determinants of cross-species transmission. Ecol. Lett. 2015;18:1153–1162. doi: 10.1111/ele.12491. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Mihaljevic JR. Linking metacommunity theory and symbiont evolutionary ecology. Trends Ecol. Evol. 2012;27:323–329. doi: 10.1016/j.tree.2012.01.011. [DOI] [PubMed] [Google Scholar]
  30. Morand S, Krasnov BR. The Biogeography of Host–Parasite Interactions. Oxford: Oxford University Press; 2010. [Google Scholar]
  31. Oksanen, A.J., F.G. Blanchet, M. Friendly, R. Kindt, P. Legendre, D. Mcglinn, P.R. Minchin, R.B.O. Hara, G.L. Simpson, P. Solymos, M.H.H. Stevens and E. Szoecs. 2016. Package “vegan” (Version 2.4-0). URL https://cran.r-project.org, https://github.com/vegandevs/vegan.
  32. Peres-Neto PR, Legendre P, Dray S, Borcard D. Variation partitioning of species data matrices: estimation and comparison of fractions. Ecology. 2006;87:2614–2625. doi: 10.1890/0012-9658(2006)87[2614:VPOSDM]2.0.CO;2. [DOI] [PubMed] [Google Scholar]
  33. Presley SJ, Higgins CL, Willig MR. A comprehensive framework for the evaluation of metacommunity structure. Oikos. 2010;119:908–917. doi: 10.1111/j.1600-0706.2010.18544.x. [DOI] [Google Scholar]
  34. R Core Team. R: A language and environment for statistical computing. Boston, MA: RStudio, Inc.; 2017. [Google Scholar]
  35. Rahbek C, Graves GR. Multiscale assessment of patterns of avian species richness. Proc. Nat. Acad. Sci. 2001;98:4534–4539. doi: 10.1073/pnas.071034898. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Streicker DG, Turmelle S, Vonhof MJ, Kuzmin IV, McCracken GF, Rupprecht CE. Host phylogeny constrains cross-species emergence and establishment of rabies virus in bats. Science. 2010;329:676–679. doi: 10.1126/science.1188836. [DOI] [PubMed] [Google Scholar]
  37. Suzán G, García-Peña GE, Castro-Arellano I, Rico O, Rubio AV, Tolsá MJ, Roche B, Hosseini PR, Rizzoli A, Murray KA, Zambrana-Torrelio C, Vittecoq M, Bailly X, Aguirre AA, Daszak P, Prieur-Richard AH, Mills JN, Guégan JF. Metacommunity and phylogenetic structure determine wildlife and zoonotic infectious disease patterns in time and space. Ecol. Evol. 2015;5:865–873. doi: 10.1002/ece3.1404. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Urteaga, L. 1993. La Teoría De Los Climas Y Los Orígenes Del Ambientalismo. Cuadernos criticos de geografia humana XVIII:1–36.
  39. Woolhouse MEJ. Population biology of multihost pathogens. Science. 2001;292:1109–1112. doi: 10.1126/science.1059026. [DOI] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

42974_2018_19020168_MOESM1_ESM.pdf (20.2KB, pdf)

Supplementary material, approximately 21 KB.

Articles from Community Ecology are provided here courtesy of Nature Publishing Group

RESOURCES