Hostname: page-component-848d4c4894-pftt2 Total loading time: 0 Render date: 2024-05-28T14:39:35.427Z Has data issue: false hasContentIssue false
  • English
  • Français

The global biogeography of avian haemosporidian parasites is characterized by local diversification and intercontinental dispersal

Published online by Cambridge University Press:  16 July 2018

Vincenzo A. Ellis Open the ORCID record for Vincenzo A. Ellis [Opens in a new window] ,
Eloisa H. R. Sari ,
Dustin R. Rubenstein ,
Rebecca C. Dickerson ,
Staffan Bensch  and
Robert E. Ricklefs
Vincenzo A. Ellis*
Affiliation:
Department of Biology, Molecular Ecology and Evolution Lab, Lund University, Lund, Sweden
Eloisa H. R. Sari
Affiliation:
Department of Biology, Molecular Ecology and Evolution Lab, Lund University, Lund, Sweden
Dustin R. Rubenstein
Affiliation:
Department of Ecology, Evolution and Environmental Biology, Columbia University, New York, NY 10027, USA
Rebecca C. Dickerson
Affiliation:
College of Veterinary Medicine, University of Missouri, Columbia, MO 65211, USA
Staffan Bensch
Affiliation:
Department of Biology, Molecular Ecology and Evolution Lab, Lund University, Lund, Sweden
Robert E. Ricklefs
Affiliation:
Department of Biology, University of Missouri-St. Louis, St. Louis, MO 63121, USA
*
Author for correspondence: Vincenzo A. Ellis, E-mail: vincenzoaellis@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

The biogeographic histories of parasites and pathogens are infrequently compared with those of free-living species, including their hosts. Documenting the frequency with which parasites and pathogens disperse across geographic regions contributes to understanding not only their evolution, but also the likelihood that they may become emerging infectious diseases. Haemosporidian parasites of birds (parasite genera Plasmodium, Haemoproteus and Leucocytozoon) are globally distributed, dipteran-vectored parasites. To date, over 2000 avian haemosporidian lineages have been designated by molecular barcoding methods. To achieve their current distributions, some lineages must have dispersed long distances, often over water. Here we quantify such events using the global avian haemosporidian database MalAvi and additional records primarily from the Americas. We scored lineages as belonging to one or more global biogeographic regions based on infection records. Most lineages were restricted to a single region but some were globally distributed. We also used part of the cytochrome b gene to create genus-level parasite phylogenies and scored well-supported nodes as having descendant lineages in regional sympatry or allopatry. Descendant sister lineages of Plasmodium, Haemoproteus and Leucocytozoon were distributed in allopatry in 11, 16 and 15% of investigated nodes, respectively. Although a small but significant fraction of the molecular variance in cytochrome b of all three genera could be explained by biogeographic region, global parasite dispersal likely contributed to the majority of the unexplained variance. Our results suggest that avian haemosporidian parasites have faced few geographic barriers to dispersal over their evolutionary history.

Keywords

Avian malariabiogeographyemerging infectious diseaseHaemosporidaparasite dispersalpathogens
Type
Research Article
Information
Parasitology , Volume 146 , Issue 2 , February 2019 , pp. 213 - 219
Check for updates
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alcala, N, Jenkins, T, Christe, P and Vuilleumier, S (2017) Host shift and cospeciation rate estimation from co-phylogenies. Ecology Letters 20, 1014–1024.Google Scholar
Asahina, S (1970) Transoceanic flight of mosquitoes on the northwest Pacific. Japanese Journal of Medical Science & Biology 23, 255–258.Google Scholar
Bairlein, F, Norris, DR, Nagel, R, Bulte, M, Voigt, CC, Fox, JW, Hussell, DJT and Schmaljohann, H (2012) Cross-hemisphere migration of a 25 g songbird. Biology Letters 8, 505–507.Google Scholar
Beadell, JS, Ishtiaq, F, Covas, R, Melo, M, Warren, BH, Atkinson, CT, Bensch, S, Graves, GR, Jhala, YV, Peirce, MA, Rahmani, AR, Fonseca, DM and Fleischer, RC (2006) Global phylogeographic limits of Hawaii's avian malaria. Proceedings of the Royal Society B: Biological Sciences 273, 2935–2944.Google Scholar
Bensch, S, Pérez-Tris, J, Waldenström, J and Hellgren, O (2004) Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: multiple cases of cryptic speciation? Evolution 58, 1617–1621.Google Scholar
Bensch, S, Hellgren, O and Pérez-Tris, J (2009) Malavi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Molecular Ecology Resources 9, 1353–1358.Google Scholar
Bensch, S, Hellgren, O, Križanauskienė, A, Palinauskas, V, Valkiūnas, G, Outlaw, D and Ricklefs, RE (2013) How can we determine the molecular clock of malaria parasites? Trends in Parasitology 29, 363–369.Google Scholar
Bensch, S, Canbäck, B, DeBarry, JD, Johansson, T, Hellgren, O, Kissinger, JC, Palinauskas, V, Videvall, E and Valkiūnas, G (2016) The genome of Haemoproteus tartakovskyi and its relationship to human malaria parasites. Genome Biology and Evolution 8, 1361–1373.Google Scholar
Burgin, LE, Gloster, J, Sanders, C, Mellor, PS, Gubbins, S and Carpenter, S (2013) Investigating incursions of Bluetongue Virus using a model of long-distance Culicoides biting midge dispersal. Transboundary and Emerging Diseases 60, 263–272.Google Scholar
Clark, NJ, Clegg, SM and Lima, MR (2014) A review of global diversity in avian haemosporidians (Plasmodium and Haemoproteus: Haemosporida): new insights from molecular data. International Journal for Parasitology 44, 329–338.Google Scholar
Cornuault, J, Warren, BH, Bertrand, JAM, Milá, B, Thébaud, C and Heeb, P (2013) Timing and number of colonizations but not diversification rates affect diversity patterns in hemosporidian lineages on a remote oceanic archipelago. The American Naturalist 182, 820–833.Google Scholar
Daszak, P, Cunningham, AA and Hyatt, AD (2000) Emerging infectious diseases of wildlife – threats to biodiversity and human health. Science 287, 443–449.Google Scholar
Ellis, VA, Collins, MD, Medeiros, MCI, Sari, EHR, Coffey, ED, Dickerson, RC, Lugarini, C, Stratford, JA, Henry, DR, Merrill, L, Matthews, AE, Hanson, AA, Roberts, JR, Joyce, M, Kunkel, MR and Ricklefs, RE (2015) Local host specialization, host-switching, and dispersal shape the regional distributions of avian haemosporidian parasites. Proceedings of the National Academy of Sciences 112, 11294–11299.Google Scholar
Ellis, VA, Bensch, S and Canbäck, B (2017) MalaviR: an R interface to MalAvi. R package version 0.1.0. Available at https://github.com/vincenzoaellis/malaviR.Google Scholar
Escalante, AA, Cornejo, OE, Freeland, DE, Poe, AC, Durrego, E, Collins, WE and Lal, AA (2005) A monkey's tale: the origin of Plasmodium vivax as a human malaria parasite. Proceedings of the National Academy of Sciences of the USA 102, 1980–1985.Google Scholar
Ewen, JG, Bensch, S, Blackburn, TM, Bonneaud, C, Brown, R, Cassey, P, Clarke, RH and Pérez-Tris, J (2012) Establishment of exotic parasites: the origins and characteristics of an avian malaria community in an isolated island avifauna. Ecology Letters 15, 1112–1119.Google Scholar
Excoffier, L, Smouse, PE and Quattro, JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479–491.Google Scholar
Fallon, SM, Bermingham, E and Ricklefs, RE (2005) Host specialization and geographic localization of avian malaria parasites: a regional analysis in the Lesser Antilles. The American Naturalist 165, 466–480.Google Scholar
Frick, WF, Pollock, JF, Hicks, AC, Langwing, KE, Reynolds, DS, Turner, GG, Butchkoski, CM and Kunz, TH (2010) An emerging disease causes regional population collapse of a common North American bat species. Science 329, 679–682.Google Scholar
Frick, WF, Puechmaille, SJ, Hoyt, JR, Nickel, BA, Langwig, KE, Foster, JT, Barlow, KE, Bartonička, T, Feller, D, Haarsma, A-J, Herzog, C, Horáček, I, van der Kooij, J, Mulkens, B, Petrov, B, Reynolds, R, Rodrigues, L, Stihler, CW, Turner, GG and Kilpatrick, AM (2015) Disease alters macroecological patterns of North American bats. Global Ecology and Biogeography 24, 741–749.Google Scholar
Gaunt, MW, Sall, AA, de Lamballerie, X, Falconar, AK, Dzhivanian, TI and Gould, EA (2001) Phylogenetic relationships of flaviviruses correlate with their epidemiology, disease association and biogeography. Journal of General Virology 82, 1867–1876.Google Scholar
Hellgren, O, Waldenström, J, Peréz-Tris, J, Ösi, ES, Hasselquist, D, Krizanauskiene, A, Ottosson, U and Bensch, S (2007) Detecting shifts of transmission areas in avian blood parasites – a phylogenetic approach. Molecular Ecology 16, 1281–1290.Google Scholar
Hellgren, O, Perez-Tris, J and Bensch, S (2009) A jack-of-all-trades and still a master of some: prevalence and host range in avian malaria and related blood parasites. Ecology 90, 2840–2849.Google Scholar
Hellgren, O, Atkinson, CT, Bensch, S, Albayrak, T, Dimitrov, D, Ewen, JG, Kim, KS, Lima, MR, Martin, L, Palinauskas, V, Ricklefs, R, Sehgal, RNM, Valkiūnas, G, Tsuda, Y and Marzal, A (2015) Global phylogeography of the avian malaria pathogen Plasmodium relictum based on MSP1 allelic diversity. Ecography 38, 842–850.Google Scholar
James, TY, Toledo, LF, Rödder, D, Silva Leite, D, Belasen, AM, Betancourt-Román, CM, Jenkinson, TS, Soto-Azat, C, Lambertini, C, Longo, AV, Ruggeri, J, Collins, JP, Burrowes, PA, Lips, KR, Zamudio, KR and Longcore, JE (2015) Disentangling host, pathogen, and environmental determinants of a recently emerged wildlife disease: lessons from the first 15 years of amphibian chytridiomycosis research. Ecology and Evolution 5, 4079–4097.Google Scholar
Kay, BH and Farrow, RA (2000) Mosquito (Diptera: Culicidae) dispersal: implications for the epidemiology of Japanese and Murray Valley Encephalitis Viruses in Australia. Journal of Medical Entomology 37, 797–801.Google Scholar
Kilpatrick, AM, Chmura, AA, Gibbons, DW, Fleischer, RC, Marra, PP and Daszak, P (2006) Predicting the global spread of H5N1 avian influenza. Proceedings of the National Academy of Sciences 103, 19368–19373.Google Scholar
LaDeau, SL, Kilpatrick, AM and Marra, PP (2007) West Nile virus emergence and large-scale declines of North American bird populations. Nature 447, 710–713.Google Scholar
Levin, II and Parker, PG (2014) Infection with Haemoproteus iwa affects vector movement in a hippoboscid fly-frigatebird system. Molecular Ecology 23, 947–953.Google Scholar
Levin, II, Zwiers, P, Deem, SL, Geest, EA, Higashiguchi, JM, Iezhova, TA, JiméNez-UzcáTegui, G, Kim, DH, Morton, JP, Perlut, NG, Renfrew, RB, Sari, EHR, Valkiunas, G and Parker, PG (2013) Multiple lineages of avian malaria parasites (Plasmodium) in the Galapagos Islands and evidence for arrival via migratory birds. Conservation Biology 27, 1366–1377.Google Scholar
Levin, II, Colborn, RE, Kim, D, Perlut, NG, Renfrew, RB and Parker, PG (2016) Local parasite lineage sharing in temperate grassland birds provides clues about potential origins of Galapagos avian Plasmodium. Ecology and Evolution 6, 716–726.Google Scholar
Mendes, L, Pardal, S, Morais, J, Antunes, S, Ramos, JA, Perez-Tris, J and Piersma, T (2013) Hidden haemosporidian infections in Ruffs (Philomachus pugnax) staging in Northwest Europe en route from Africa to Arctic Europe. Parasitology Research 112, 2037–2043.Google Scholar
Morand, S and Krasnov, BR (eds) (2010) The Biogeography of Host-Parasite Interactions. New York: Oxford University Press.Google Scholar
Murdock, CC, Adler, PH, Frank, J and Perkins, SL (2015) Molecular analyses on host-seeking black flies (Diptera: Simuliidae) reveal a diverse assemblage of Leucocytozoon (Apicomplexa: Haemospororida) parasites in an alpine ecosystem. Parasites & Vectors 8, 1–7. doi: 10.1186/s13071-015-0952-9Google Scholar
Newton, I (2007) The Migration Ecology of Birds. New York: Academic Press.Google Scholar
Oksanen, J, Blanchet, FG, Friendly, M, Kindt, R, Legendre, P, McGlinn, D, Minchin, PR, O'Hara, RB, Simpson, GL, Solymos, P, Stevens, MHH, Szoecs, E and Wagner, H (2017) Vegan: community ecology package. R package version 2.4-3. Available at https://CRAN.R-project.org/package=vegan.Google Scholar
Outlaw, DC and Ricklefs, RE (2014) Species limits in avian malaria parasites (Haemosporida): how to move forward in the molecular era. Parasitology 141, 1223–1232.Google Scholar
Pacheco, MA, Battistuzzi, FU, Junge, RE, Cornejo, OE, Williams, CV, Landau, I, Rabetafika, L, Snounou, G, Jones-Engel, L and Escalante, AA (2011) Timing the origin of human malarias: the lemur puzzle. BMC Evolutionary Biology 11, 299.Google Scholar
Pacheco, MA, Matta, NE, Valkiūnas, G, Parker, PG, Mello, B, Stanley, CE, Lentino, M, Garcia-Amado, MA, Cranfield, M, Kosakovsky Pond, SL and Escalante, AA (2018) Mode and rate of evolution of haemosporidian mitochondrial genomes: timing the radiation of avian parasites. Molecular Biology and Evolution 35, 383–403.Google Scholar
Pagenkopp Lohan, KM, Fleischer, RC, Carney, KJ, Holzer, KK and Ruiz, GM (2016) Amplicon-based pyrosequencing reveals high diversity of protistan parasites in ships’ ballast water: implications for biogeography and infectious diseases. Microbial Ecology 71, 530–542.Google Scholar
Paradis, E, Claude, J and Strimmer, K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics (Oxford, England) 20, 289–290.Google Scholar
Pérez-Tris, J and Bensch, S (2005) Dispersal increases local transmission of avian malarial parasites. Ecology Letters 8, 838–845.Google Scholar
Peterson, AT (2008) Biogeography of diseases: a framework for analysis. Naturwissenschaften 95, 483–491.Google Scholar
Pettersson, E, Bensch, S, Ander, M, Chirico, J, Sigvald, R and Ignell, R (2013) Molecular identification of bloodmeals and species composition in Culicoides biting midges. Medical and Veterinary Entomology 27, 104–112.Google Scholar
R Core Team (2017) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
Rappole, JH, Derrickson, SR and Hubálek, Z (2000) Migratory birds and spread of West Nile virus in the Western Hemisphere. Emerging Infectious Diseases 6, 319.Google Scholar
Revell, LJ (2012) Phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution 3, 217–223.Google Scholar
Ricklefs, RE and Fallon, SM (2002) Diversification and host switching in avian malaria parasites. Proceedings of the Royal Society of London B: Biological Sciences 269, 885–892.Google Scholar
Ricklefs, RE and Outlaw, DC (2010) A molecular clock for malaria parasites. Science 329, 226–229.Google Scholar
Ricklefs, R, Fallon, S and Bermingham, E (2004) Evolutionary relationships, cospeciation, and host switching in avian malaria parasites. Systematic Biology 53, 111–119.Google Scholar
Ricklefs, RE, Outlaw, DC, Svensson-Coelho, M, Medeiros, MCI, Ellis, VA and Latta, S (2014) Species formation by host shifting in avian malaria parasites. Proceedings of the National Academy of Sciences 111, 14816–14821.Google Scholar
Ricklefs, RE, Medeiros, M, Ellis, VA, Svensson-Coelho, M, Blake, JG, Loiselle, BA, Soares, L, Fecchio, A, Outlaw, D, Marra, PP, Latta, SC, Valkiūnas, G, Hellgren, O and Bensch, S (2017) Avian migration and the distribution of malaria parasites in New World passerine birds. Journal of Biogeography 44, 1113–1123.Google Scholar
Soares, L, Marra, P, Gray, L and Ricklefs, RE (2017) The malaria parasite Plasmodium relictum in the endemic avifauna of eastern Cuba: Malaria in Cuban avifauna. Conservation Biology 31, 1477–1482.Google Scholar
Stamatakis, A, Hoover, P and Rougemont, J (2008) A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology 57, 758–771.Google Scholar
Summerell, BA, Laurence, MH, Liew, ECY and Leslie, JF (2010) Biogeography and phylogeography of Fusarium: a review. Fungal Diversity 44, 3–13.Google Scholar
Valkiūnas, G (2005) Avian Malaria Parasites and Other Haemosporidia. Boca Raton, FL, USA: CRC Press.Google Scholar
van Riper, C III, Sandra, G, van Riper, M, Lee, Goff and Marshal, Laird (1986) The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecological Monographs 56, 327–344.Google Scholar
Videvall, E, Cornwallis, CK, Ahrén, D, Palinauskas, V, Valkiūnas, G and Hellgren, O (2017) The transcriptome of the avian malaria parasite Plasmodium ashfordi displays host-specific gene expression. Molecular Ecology 26, 2939–2958.Google Scholar
Waldenström, J, Bensch, S, Kiboi, S, Hasselquist, D and Ottosson, U (2002) Cross-species infection of blood parasites between resident and migratory songbirds in Africa. Molecular Ecology 11, 1545–1554.Google Scholar
Wickham, H (2009) ggplot2: Elegant Graphics for Data Analysis. New York: Springer-VerlagGoogle Scholar
Supplementary material: File

Ellis et al. supplementary material

Ellis et al. supplementary material 1

Download Ellis et al. supplementary material(File)
File 387.2 KB