Spatiotemporal patterns of avian host-parasite interactions in the face of biogeographical range expansions

. 2020 Jul ; 29 (13) : 2431-2448. [epub] 20200617

Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid32470165

Exploration of interactions between hosts and parasitic symbionts is important for our understanding of the temporal and spatial distribution of organisms. For example, host colonization of new geographical regions may alter levels of infections and parasite specificity, and even allow hosts to escape from co-evolved parasites, consequently shaping spatial distributions and community structure of both host and parasite. Here we investigate the effect of host colonization of new regions and the elevational distribution of host-parasite associations between birds and their vector-transmitted haemosporidian blood parasites in two geological and geographical settings: mountains of New Guinea and the Canary Islands. Our results demonstrate that bird communities in younger regions have significantly lower levels of parasitism compared to those of older regions. Furthermore, host-parasite network analyses demonstrate that blood parasites may respond differently after arriving to a new region, through adaptations that allow for either expanding (Canary Islands) or retaining (New Guinea) their host niches. The spatial prevalence patterns along elevational gradients differed in the two regions, suggesting that region-specific biotic (e.g., host community) and abiotic factors (e.g., temperature) govern prevalence patterns. Our findings suggest that the spatiotemporal range dynamics in host-parasite systems are driven by multiple factors, but that host and parasite community compositions and colonization histories are of particular importance.

Zobrazit více v PubMed

Altizer, S. M., Oberhauser, K. S., & Brower, L. P. (2000). Associations between host migration and the prevalence of a protozoan parasite in natural populations of adult monarch butterflies. Ecological Entomology, 25(2), 125-139. https://doi.org/10.1046/j.1365-2311.2000.00246.x

Atkinson, C. T., & Vanriper, C. (1991). Pathogenicity and epizootiology of avian haematozoa: Plasmodium, Leucocytozoon, and Haemoproteus. In J. E. Loye, & M. Zuk (Eds.), Bird-parasite interactions: Ecology, evolution and behavior (Vol. 1, pp. 21-48). Oxford, UK: Oxford Press.

Baldwin, S. L., Fitzgerald, P. G., & Webb, L. E. (2012). Tectonics of the New Guinea Region. Annual Review of Earth and Planetary Sciences, 40, 495-520. https://doi.org/10.1146/annurev-earth-040809-152540

Bayoh, M. N., & Lindsay, S. W. (2004). Temperature-related duration of aquatic stages of the Afrotropical malaria vector mosquito Anopheles gambiae in the laboratory. Medical and Veterinary Entomology, 18(2), 174-179. https://doi.org/10.1111/j.0269-283X.2004.00495.x

Beadell, J. S., Atkins, C., Cashion, E., Jonker, M., & Fleischer, R. C. (2007). Immunological change in a parasite-impoverished environment: Divergent signals from four island taxa. PLoS One, 2(9), e896. https://doi.org/10.1371/journal.pone.0000896

Beck-Johnson, L. M., Nelson, W. A., Paaijmans, K. P., Read, A. F., Thomas, M. B., & Bjornstad, O. N. (2013). The effect of temperature on Anopheles mosquito population dynamics and the potential for malaria transmission. PLoS One, 8(11), e79276. https://doi.org/10.1371/journal.pone.0079276

Bensch, S., Hellgren, O., & Perez-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(5), 1353-1358. https://doi.org/10.1111/j.1755-0998.2009.02692.x

Bluthgen, N., Menzel, F., & Bluthgen, N. (2006). Measuring specialization in species interaction networks. BMC Ecology, 6, 9. https://doi.org/10.1186/1472-6785-6-9

Clark, N. J., & Clegg, S. M. (2015). The influence of vagrant hosts and weather patterns on the colonization and persistence of blood parasites in an island bird. Journal of Biogeography, 42(4), 641-651. https://doi.org/10.1111/jbi.12454

Clark, N. J., Clegg, S. M., & Lima, M. R. (2014). A review of global diversity in avian haemosporidians (Plasmodium and Haemoproteus: Haemosporida): New insights from molecular data. International Journal for Parasitology, 44(5), 329-338. https://doi.org/10.1016/j.ijpara.2014.01.004

Clark, N. J., Clegg, S. M., Sam, K., Goulding, W., Koane, B., & Wells, K. (2018). Climate, host phylogeny and the connectivity of host communities govern regional parasite assembly. Diversity and Distributions, 24(1), 13-23. https://doi.org/10.1111/ddi.12661

Clark, N. J., Olsson-Pons, S., Ishtiaq, F., & Clegg, S. M. (2015). Specialist enemies, generalist weapons and the potential spread of exotic pathogens: Malaria parasites in a highly invasive bird. International Journal for Parasitology, 45(14), 891-899. https://doi.org/10.1016/j.ijpara.2015.08.008

Cornuault, J., Bataillard, A., Warren, B. H., Lootvoet, A., Mirleau, P., Duval, T., … Heeb, P. (2012). The role of immigration and in-situ radiation in explaining blood parasite assemblages in an island bird clade. Molecular Ecology, 21(6), 1438-1452. https://doi.org/10.1111/j.1365-294X.2012.05483.x

Cosgrove, C. L., Wood, M. J., Day, K. P., & Sheldon, B. C. (2008). Seasonal variation in Plasmodium prevalence in a population of blue tits Cyanistes caeruleus. Journal of Animal Ecology, 77(3), 540-548. https://doi.org/10.1111/j.1365-2656.2008.01370.x

Cozzarolo, C. S., Jenkins, T., Toews, D. P. L., Brelsford, A., & Christe, P. (2018). Prevalence and diversity of haemosporidian parasites in the yellow-rumped warbler hybrid zone. Ecology and Evolution, 8(19), 9834-9847. https://doi.org/10.1002/ece3.4469

del-Arco, M., Acebes, J. R., Pérez-De-Paz, P. L., & Marrero, M. D. (1999). Bioclimatology and climatophilous vegetation of Heirro (part 2) and La Palma (Canary Islands). Phytocoenologia, 29(2), 253-290.

del-Arco, M., & Delgado, O. R. (2018). Vegetation of the Canary Islands, Vol. 16. Cham, Switzerland: Springer International Publishing AG.

del-Arco, M., Pérez-de-Paz, P. L., Acebes, J. R., González-Mancebo, J. M., Reyes-Betancort, J. A., Bermejo, J. A., … González-González, R. (2006). Bioclimatology and climatophilous vegetation of Tenerife (Canary Islands). Annales Botanici Fennici, 43(3), 167-192.

del-Arco, M. J., Rodríguez-Delgado, O., Acebes, J. R., García-Gallo, A., Pérez-de-Paz, P. L., González-Mancebo, J. M., … Garzón-Machado, V. (2009). Bioclimatology and climatophilous vegetation of Gomera (Canary Islands). Annales Botanici Fennici, 46(3), 161-191. https://doi.org/10.5735/085.046.0301

del-Arco, M., Salas, M., Acebes, J. R., Marrero, M. D., Reyes-Betancort, J. A., & Pérez-de-Paz, P. L. (2002). Bioclimatology and climatophilous vegetation of Gran Canaria (Canary Islands). Annales Botanici Fennici, 39(1), 15-41.

Diamond, J. M. (1972). Avifauna of the Eastern Highlands of New Guinea. Cambridge, MA: Nuttall Ornithological Club.

Dormann, C. F., Gruber, B., & Fründ, J. (2008). Introducing the bipartite package: Analysing ecological networks. R News, 8(2), 8-11.

Eggert, L. S., Terwilliger, L. A., Woodworth, B. L., Hart, P. J., Palmer, D., & Fleischer, R. C. (2008). Genetic structure along an elevational gradient in Hawaiian honeycreepers reveals contrasting evolutionary responses to avian malaria. Bmc Evolutionary Biology, 8, 315. https://doi.org/10.1186/1471-2148-8-315

Ewen, J. G., Bensch, S., Blackburn, T. M., Bonneaud, C., Brown, R., Cassey, P., … 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(10), 1112-1119. https://doi.org/10.1111/j.1461-0248.2012.01833.x

Expósito, F. J., González, A., Pérez, J. C., Díaz, J. P., & Taima, D. (2015). High-resolution future projections of temperature and precipitation in the Canary Islands. Journal of Climate, 28(19), 7846-7856. https://doi.org/10.1175/Jcli-D-15-0030.1

Fallon, S. M., Ricklefs, R. E., Latta, S. C., & Bermingham, E. (2004). Temporal stability of insular avian malarial parasite communities. Proceedings of the Royal Society B-Biological Sciences, 271(1538), 493-500. https://doi.org/10.1098/rspb.2003.2621

Fecchio, A., Wells, K., Bell, J. A., Tkach, V. V., Lutz, H. L., Weckstein, J. D., … Clark, N. J. (2019). Climate variation influences host specificity in avian malaria parasites. Ecology Letters, 22(3), 547-557. https://doi.org/10.1111/ele.13215

Fernandez-Palacios, J. M., & Whittaker, R. J. (2008). The Canaries: An important biogeographical meeting place. Journal of Biogeography, 35(3), 379-387. https://doi.org/10.1111/j.1365-2699.2008.01890.x

Fox, J., & Weisberg, S. (2019). An R companion to applied regression 3rd ed. Thousand Oaks, CA: Sage Publications.

Gandon, S., & Michalakis, Y. (2002). Local adaptation, evolutionary potential and host-parasite coevolution: Interactions between migration, mutation, population size and generation time. Journal of Evolutionary Biology, 15(3), 451-462. https://doi.org/10.1046/j.1420-9101.2002.00402.x

Gohli, J., Leder, E. H., Garcia-del-Rey, E., Johannessen, L. E., Johnsen, A., Laskemoen, T., … Lifjeld, J. T. (2015). The evolutionary history of Afrocanarian blue tits inferred from genomewide SNPs. Molecular Ecology, 24(1), 180-191. https://doi.org/10.1111/mec.13008

Gonzalez-Quevedo, C., Davies, R. G., & Richardson, D. S. (2014). Predictors of malaria infection in a wild bird population: Landscape-level analyses reveal climatic and anthropogenic factors. Journal of Animal Ecology, 83(5), 1091-1102. https://doi.org/10.1111/1365-2656.12214

Harvell, C. D., Mitchell, C. E., Ward, J. R., Altizer, S., Dobson, A. P., Ostfeld, R. S., & Samuel, M. D. (2002). Ecology - Climate warming and disease risks for terrestrial and marine biota. Science, 296(5576), 2158-2162. https://doi.org/10.1126/science.1063699

Hellgren, O., Waldenstrom, J., & Bensch, S. (2004). A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. Journal of Parasitology, 90(4), 797-802. https://doi.org/10.1645/Ge-184r1

Hoberg, E. P., & Brooks, D. R. (2008). A macroevolutionary mosaic: Episodic host-switching, geographical colonization and diversification in complex host-parasite systems. Journal of Biogeography, 35(9), 1533-1550. https://doi.org/10.1111/j.1365-2699.2008.01951.x

Illera, J. C., López, G., García-Padilla, L., & Moreno, A. (2017). Factors governing the prevalence and richness of avian haemosporidian communities within and between temperate mountains. PLoS One, 12(9), e0184587. https://doi.org/10.1371/journal.pone.0184587

Ishtiaq, F., & Barve, S. (2018). Do avian blood parasites influence hypoxia physiology in a high elevation environment? Bmc Ecology, 18, 15. https://doi.org/10.1186/s12898-018-0171-2

Jones, M. R., Cheviron, Z. A., & Carling, M. D. (2013). Spatial patterns of avian malaria prevalence in Zonotrichia capensis on the western slope of the Peruvian Andes. Journal of Parasitology, 99(5), 903-905. https://doi.org/10.1645/12-147.1

Juan, C., Emerson, B. C., Oromi, P., & Hewitt, G. M. (2000). Colonization and diversification: Towards a phylogeographic synthesis for the Canary Islands. Trends in Ecology & Evolution, 15(3), 104-109. https://doi.org/10.1016/S0169-5347(99)01776-0

LaPointe, D. A., Atkinson, C. T., & Samuel, M. D. (2012). Ecology and conservation biology of avian malaria. Year in Ecology and Conservation Biology, 1249, 211-226. https://doi.org/10.1111/j.1749-6632.2011.06431.x

Levin, I. I., Zwiers, P., Deem, S. L., Geest, E. A., Higashiguchi, J. M., Iezhova, T. A., … Parker, P. G. (2013). Multiple lineages of avian malaria parasites (Plasmodium) in the Galapagos Islands and evidence for arrival via migratory birds. Conservation Biology, 27(6), 1366-1377. https://doi.org/10.1111/cobi.12127

Loiseau, C., Iezhova, T., Valkiūnas, G., Chasar, A., Hutchinson, A., Buermann, W., … Sehgal, R. N. M. (2010). Spatial variation of haemosporidian parasite infection in African rainforest bird species. Journal of Parasitology, 96(1), 21-29. https://doi.org/10.1645/Ge-2123.1

Loiseau, C., Melo, M., Lobato, E., Beadell, J. S., Fleischer, R. C., Reis, S., … Covas, R. (2017). Insularity effects on the assemblage of the blood parasite community of the birds from the Gulf of Guinea. Journal of Biogeography, 44(11), 2607-2617. https://doi.org/10.1111/jbi.13060

Marzal, A., de Lope, F., Navarro, C., & Møller, A. P. (2005). Malarial parasites decrease reproductive success: An experimental study in a passerine bird. Oecologia, 142(4), 541-545. https://doi.org/10.1007/s00442-004-1757-2

Marzal, A., Ricklefs, R. E., Valkiūnas, G., Albayrak, T., Arriero, E., Bonneaud, C., … Bensch, S. (2011). Diversity, loss, and gain of malaria parasites in a globally invasive bird. PLoS One, 6(7), e21905. https://doi.org/10.1371/journal.pone.0021905

Mata, V. A., da Silva, L. P., Lopes, R. J., & Drovetski, S. V. (2015). The Strait of Gibraltar poses an effective barrier to host-specialised but not to host-generalised lineages of avian Haemosporidia. International Journal for Parasitology, 45(11), 711-719. https://doi.org/10.1016/j.ijpara.2015.04.006

Menéndez, R., González-Megías, A., Lewis, O. T., Shaw, M. R., & Thomas, C. D. (2008). Escape from natural enemies during climate-driven range expansion: A case study. Ecological Entomology, 33(3), 413-421. https://doi.org/10.1111/j.1365-2311.2008.00985.x

Meyer, D., Zeileis, A., & Hornik, K. (2017). vcd: Visualizing Categorical Data. Retrieved from https://rdrr.io/cran/vcd/ (November 2019)

Minakawa, N., Sonye, G., Mogi, M., Githeko, A., & Yan, G. Y. (2002). The effects of climatic factors on the distribution and abundance of malaria vectors in Kenya. Journal of Medical Entomology, 39(6), 833-841. https://doi.org/10.1603/0022-2585-39.6.833

Nieberding, C., Morand, S., Libois, R., & Michaux, J. R. (2006). Parasites and the island syndrome: The colonization of the western Mediterranean islands by Heligmosomoides polygyrus (Dujardin, 1845). Journal of Biogeography, 33(7), 1212-1222. https://doi.org/10.1111/j.1365-2699.2006.01503.x

Njabo, K. Y., Cornel, A. J., Bonneaud, C., Toffelmier, E., Sehgal, R. N. M., Valkiūnas, G., … Smith, T. B. (2011). Nonspecific patterns of vector, host and avian malaria parasite associations in a central African rainforest. Molecular Ecology, 20(5), 1049-1061. https://doi.org/10.1111/j.1365-294X.2010.04904.x

Oksanen, J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., … Wagner, H. (2019). vegan: Community Ecology Package. R package version 2.5-4. Retrieved from https://CRAN.R-project.org/package=vegan

Ortego, J., Calabuig, G., Cordero, P. J., & Aparicio, J. M. (2007). Genetic characterization of avian malaria (Protozoa) in the endangered lesser kestrel, Falco naumanni. Parasitology Research, 101(4), 1153-1156. https://doi.org/10.1007/s00436-007-0575-y

Pacheco, M. A., Matta, N. E., Valkiūnas, G., Parker, P. G., Mello, B., Stanley, C. E., … Escalante, A. A. (2018). Mode and rate of evolution of haemosporidian mitochondrial genomes: Timing the radiation of avian parasites. Molecular Biology and Evolution, 35(2), 383-403. https://doi.org/10.1093/molbev/msx285

Padilla, D. P., Illera, J. C., Gonzalez-Quevedo, C., Villalba, M., & Richardson, D. S. (2017). Factors affecting the distribution of haemosporidian parasites within an oceanic island. International Journal for Parasitology, 47(4), 225-235. https://doi.org/10.1016/j.fipara.2016.11.008

Pérez-Rodríguez, Á., Ramírez, A., Richardson, D. S., & Pérez-Tris, J. (2013). Evolution of parasite island syndromes without long-term host population isolation: Parasite dynamics in Macaronesian blackcaps Sylvia atricapilla. Global Ecology and Biogeography, 22(12), 1272-1281. https://doi.org/10.1111/geb.12084

Prenter, J., MacNeil, C., Dick, J. T. A., & Dunn, A. M. (2004). Roles of parasites in animal invasions. Trends in Ecology & Evolution, 19(7), 385-390. https://doi.org/10.1016/j.tree.2004.05.002

Pulgarín, R. P., Gómez, J. P., Robinson, S., Ricklefs, R. E., & Cadena, C. D. (2018). Host species, and not environment, predicts variation in blood parasite prevalence, distribution, and diversity along a humidity gradient in northern South America. Ecology and Evolution, 8(8), 3800-3814. https://doi.org/10.1002/ece3.3785

R Core Team (2019). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Retrieved from https://www.R-project.org/

Reiter, M. E., & LaPointe, D. A. (2009). Larval habitat for the avian malaria vector Culex quinquefasciatus (Diptera: Culicidae) in altered mid-elevation mesic-dry forests in Hawai'i. Journal of Vector Ecology, 34(2), 208-216. https://doi.org/10.1111/j.1948-7134.2009.00028.x

Ricklefs, R. E. (2011). A biogeographical perspective on ecological systems: Some personal reflections. Journal of Biogeography, 38(11), 2045-2056. https://doi.org/10.1111/j.1365-2699.2011.02520.x

Ricklefs, R. E. (2015). Intrinsic dynamics of the regional community. Ecology Letters, 18(6), 497-503. https://doi.org/10.1111/ele.12431

Ricklefs, R. E., & Fallon, S. M. (2002). Diversification and host switching in avian malaria parasites. Proceedings of the Royal Society of London. Series B: Biological Sciences, 269(1494), 885-892. https://doi.org/10.1098/rspb.2001.1940

Ricklefs, R. E., Medeiros, M., Ellis, V. A., Svensson-Coelho, M., Blake, J. G., Loiselle, B. A., … Bensch, S. (2017). Avian migration and the distribution of malaria parasites in New World passerine birds. Journal of Biogeography, 44(5), 1113-1123. https://doi.org/10.1111/jbi.12928

Ricklefs, R. E., & Outlaw, D. C. (2010). A molecular clock for malaria parasites. Science, 329(5988), 226-229. https://doi.org/10.1126/science.1188954

Ricklefs, R. E., Swanson, B. L., Fallon, S. M., Martínez-Abraín, A., Scheuerlein, A., Gray, J., & Latta, S. C. (2005). Community relationships of avian malaria parasites in southern missouri. Ecological Monographs, 75(4), 543-559. https://doi.org/10.1890/04-1820

Sam, K., & Koane, B. (2014). New avian records along the elevational gradient of Mt. Wilhelm, Papua New Guinea. Bulletin of the British Ornithologists’ Club, 134(2), 116-133.

Sam, K., Koane, B., Bardos, D. C., Jeppy, S., & Novotny, V. (2019). Species richness of birds along a complete rain forest elevational gradient in the tropics: Habitat complexity and food resources matter. Journal of Biogeography, 46(2), 279-290. https://doi.org/10.1111/jbi.13482

Sehgal, R. N. M. (2015). Manifold habitat effects on the prevalence and diversity of avian blood parasites. International Journal for Parasitology-Parasites and Wildlife, 4(3), 421-430. https://doi.org/10.1016/j.ijppaw.2015.09.001

Sheldon, B. C., & Verhulst, S. (1996). Ecological immunology: Costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology & Evolution, 11(8), 317-321. https://doi.org/10.1016/0169-5347(96)10039-2

Sinorell, A. (2019). DescTools: Tools for descriptive statistics. Retrieved from https://rdrr.io/cran/DescTools/

Stone, G. N., Lohse, K., Nicholls, J. A., Fuentes-Utrilla, P., Sinclair, F., Schönrogge, K., … Hickerson, M. J. (2012). Reconstructing community assembly in time and space reveals Enemy escape in a western Palearctic insect community. Current Biology, 22(6), 532-537. https://doi.org/10.1016/j.cub.2012.01.059

Svensson-Coelho, M., Ellis, V. A., Loiselle, B. A., Blake, J. G., & Ricklefs, R. E. (2014). Reciprocal specialization in multihost malaria parasite communities of Birds: A Temperate-Tropical comparison. American Naturalist, 184(5), 624-635. https://doi.org/10.1086/678126

Thrall, P. H., Hochberg, M. E., Burdon, J. J., & Bever, J. D. (2007). Coevolution of symbiotic mutualists and parasites in a community context. Trends in Ecology & Evolution, 22(3), 120-126. https://doi.org/10.1016/j.tree.2006.11.007

Torchin, M. E., Lafferty, K. D., Dobson, A. P., McKenzie, V. J., & Kuris, A. M. (2003). Introduced species and their missing parasites. Nature, 421(6923), 628-630. https://doi.org/10.1038/nature01346

Valente, L., Illera, J. C., Havenstein, K., Pallien, T., Etienne, R. S., & Tiedemann, R. (2017). Equilibrium bird species diversity in Atlantic Islands. Current Biology, 27(11), 1660-1666. https://doi.org/10.1016/j.cub.2017.04.053

van Riper, C., van Riper, S. G., Goff, M. L., & Laird, M. (1986). The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecological Monographs, 56(4), 327-344. https://doi.org/10.2307/1942550

van Rooyen, J., Lalubin, F., Glaizot, O., & Christe, P. (2013). Altitudinal variation in haemosporidian parasite distribution in great tit populations. Parasites & Vectors, 6, 139. https://doi.org/10.1186/1756-3305-6-139

van Ufford, A. Q., & Cloos, M. (2005). Cenozoic tectonics of New Guinea. AAPG Bulletin, 89(1), 119-140. https://doi.org/10.1306/08300403073

Videvall, E. (2019). Genomic advances in avian aalaria research. Trends in Parasitology, 35(3), 254-266. https://doi.org/10.1016/j.pt.2018.12.005

Wickham, H., François, R., Henry, L., & Müller, K. (2019). dplyr: A grammar of data manipulation. R package version 0.8.3. Retrieved from https://CRAN.R-project.org/package=dplyr

Wolinska, J., & King, K. C. (2009). Environment can alter selection in host-parasite interactions. Trends in Parasitology, 25(5), 236-244. https://doi.org/10.1016/j.pt.2009.02.004

Zamora-Vilchis, I., Williams, S. E., & Johnson, C. N. (2012). Environmental temperature affects prevalence of blood Parasites of birds on an elevation gradient: Implications for disease in a warming climate. PLoS One, 7(6), e39208. https://doi.org/10.1371/journal.pone.0039208

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...