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Coevolutionary patterns and diversification of avian malaria parasites in African sunbirds (Family Nectariniidae)



The coevolutionary relationships between avian malaria parasites and their hosts influence the host specificity, geographical distribution and pathogenicity of these parasites. However, to understand fine scale coevolutionary host–parasite relationships, robust and widespread sampling from closely related hosts is needed. We thus sought to explore the coevolutionary history of avian Plasmodium and the widespread African sunbirds, family Nectariniidae. These birds are distributed throughout Africa and occupy a variety of habitats. Considering the role that habitat plays in influencing host-specificity and the role that host-specificity plays in coevolutionary relationships, African sunbirds provide an exceptional model system to study the processes that govern the distribution and diversity of avian malaria. Here we evaluated the coevolutionary histories using a multi-gene phylogeny for Nectariniidae and avian Plasmodium found in Nectariniidae. We then assessed the host–parasite biogeography and the structuring of parasite assemblages. We recovered Plasmodium lineages concurrently in East, West, South and Island regions of Africa. However, several Plasmodium lineages were recovered exclusively within one respective region, despite being found in widely distributed hosts. In addition, we inferred the biogeographic history of these parasites and provide evidence supporting a model of biotic diversification in avian Plasmodium of African sunbirds.


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* Corresponding author. Department of Biology San Francisco State University, 1600 Holloway Avenue, San Francisco, California 94132, USA. E-mail:


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Afrane, Y. A., Little, T. J., Lawson, B. W., Githeko, A. K. and Yan, G. (2008). Deforestation and vectorial capacity of Anopheles gambiae Giles mosquitoes in malaria transmission, Kenya. Emerging Infectious Diseases 14, 15331538.
Agosta, S. J., Janz, N. and Brooks, D. R. (2010). How specialists can be generalists: resolving the ‘parasite paradox’ and implications for emerging infectious disease. Zoologia 27, 151162.
Ali, S. S., Yu, Y., Pfosser, M. and Wetschnig, W. (2011). Inferences of biogeographical histories within subfamily Hyacinthoideae using S-DIVA and Bayesian binary MCMC analysis implemented in RASP (Reconstruct Ancestral State in Phylogenies). Annals of Botany 109, 95107.
Balbuena, J. A., Míguez-Lozano, R. and Blasco-Costa, I. (2013). PACo: a novel procrustes application to cophylogenetic analysis. PLoS ONE 8, e61048.
Bensch, S., Stjernman, M., Hasselquist, D., Ostman, O., Hansson, B., Westerdahl, H. and Pinheiro, R. T. (2000). Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proceedings of the Royal Society B: Biological Sciences 267, 15831589.
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 Resource 9, 13531358.
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, 16171621.
Bowie, R. C. K. (2003). Birds, molecules, and evolutionary patterns among Africa's islands in the sky. Ph.D. Thesis. University of Cape Town, South Africa.
Bowie, R. C. K., Fjeldså, J., Hackett, S. J. and Crowe, T. M. (2004). Molecular evolution in space and through time: mtDNA phylogeography of the Olive Sunbird (Nectarinia olivacea/obscura) throughout continental Africa. Molecular Phylogenetics and Evolution 33, 5674.
Brodie, E. D. III and Brodie, E. D. Jr. (1999). Predator–prey arms race and dangerous prey. Biosciences 49, 557568.
Clark, M. A., Moran, N. A., Baumann, P. and Wernegreen, J. J. (2000). Cospeciation between bacterial endosymbionts (Buchnera) and a recent radiation of aphids (Uroleucon) and pitfalls of testing for phylogenetic congruence. Evolution 54, 517525.
Chasar, A., Loiseau, C., Valkiūnas, G., Iezhova, T., Smith, T. B. and Sehgal, R N M. (2009). Prevalence and diversity patterns of avian blood parasites in degraded African rainforest habitats. Molecular Ecology 18, 41214133.
Chaves, L. F. and Koenraadt, C. J. M. (2010). Climate change and highland malaria: fresh air for a hot debate. Quarterly Review of Biology 85, 2755.
Cheke, R. S., Clive, M. F. and Allen, R. (2001). Sunbirds. Yale University Press, New Haven and London.
Conow, C., Fielder, D., Ovadia, Y. and Libeskind-Hadas, R. (2010). Jane: a new tool for the cophylogeny reconstruction problem. Algorithms for Molecular Biology 5, 16.
Cooper, N., Griffin, R., Franz, M., Omotayo, M., Nunn, C. L. and Fryxell, J. (2012). Phylogenetic host specificity and understanding parasite sharing in primates. Ecology Letters 15, 13701377.
Demastes, J. W. and Hafner, M. S. (1993). Cospeciation of pocket gophers (Geomys) and their chewing lice (Geomydoecus). Journal of Mammalogy 74, 521.
De Roode, J. C., Pansini, R., Cheesman, S. J., Helinski, M. E. H., Huijben, S., Wargo, A. R., Bell, A. S., Chan, B. H. K., Walliker, D. and Read, A. F. (2005). Virulence and competitive ability in genetically diverse malaria infections. Proceedings of the National Academy of Sciences of the USA 102, 76247628.
Drummond, A. J., Suchard, M. A., Xie, D. and Rambaut, A. (2012). Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29, 19691973.
Ehrnsberger, R. (2001). A preliminary analysis of phylogenetic relationships of the feather mite family Freyanidae Dubinin, 1953 (Acari: Astigmata). Biological Bulletin of Poznań 38, 181201.
Excoffier, L. and Lischer, H. E. L. (2010). Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564567.
Fallon, S. M., Bermingham, E. and Ricklefs, R. E. (2003). Island and taxon effects in parasitism revisited: avian malaria in the Lesser Antilles. Evolution 57, 606615.
Fallon, S. M., Bermingham, E. and Ricklefs, R. E. (2005). Host specialization and geographic localization of avian malaria parasites: a regional analysis in the Lesser Antilles. American Naturalist 165, 466480.
Fallon, S. M., Fleischer, R. C. and Graves, G. R. (2006). Malarial parasites as geographical markers in migratory birds? Biology Letters 2, 213216.
Figuerola, J. and Green, A. J. (2000). Haematozoan parasites and migratory behaviour in waterfowl.
Galtier, N., Gouy, M. and Gautier, C. (1996). SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Computer Applications in the Biosciences: CABIOS 12, 543548.
Garamszegi, L. Z. (2006). The evolution of virulence and host specialization in malaria parasites of primates. Ecology Letters 9, 933940.
Garamszegi, L. Z. (2009). Patterns of co-speciation and host switching in primate malaria parasites. Malaria Journal 8, 110.
Graham, A. L. (2008). Ecological rules governing helminth–microparasite coinfection. Proceedings of the National Academy of Sciences 105, 566570.
Hagner, S. C., Misof, B., Maier, W. A. and Kampen, H. (2007). Bayesian analysis of new and old malaria parasite DNA sequence data demonstrates the need for more phylogenetic signal to clarify the descent of Plasmodium falciparum . Parasitology Research 101, 493503.
Hamer, G. L., Kitron, U. D., Goldberg, T. L., Brawn, J. D., Loss, S. R., Ruiz, M. O., Hayes, G. L. and Walker, E. D. (2009). Host selection by Culex pipiens mosquitoes and West Nile virus amplification. American Journal of Tropical Medicine and Hygiene 80, 268278.
Hellgren, O., Waldenström, J. and Bensch, S. (2004). A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. Journal of Parasitology 90, 797802.
Hellgren, O., Krizanauskiene, A., Valkĭunas, G. and Bensch, S. (2007 a). Diversity and phylogeny of mitochondrial cytochrome B lineages from six morphospecies of avian Haemoproteus (Haemosporida: Haemoproteidae). Journal of Parasitology 93, 889896.
Hellgren, O., Waldenström, J., Peréz-Tris, J., Szöll, E., Si, O., Hasselquist, D., Krizanauskiene, A., Ottosson, U. and Bensch, S. (2007 b). Detecting shifts of transmission areas in avian blood parasites: a phylogenetic approach. Molecular Ecology 16, 12811290.
Hellgren, O., Pérez-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, 28402849.
Hendricks, S., Flannery, M. E. and Spicer, G. S. (2013). Cophylogeny of quill mites from the genus Syringophilopsis (Acari: Syringophilidae) and their North American passerine hosts. Journal of Parasitology 99, 827834.
Hoberg, E. P. and Brooks, D. R. (2008). A macroevolutionary mosaic: episodic host-switching, geographical colonization and diversification in complex host–parasite systems. Journal of Biogeography 35, 15331550.
Hubálek, Z. (2004). An annotated checklist of pathogenic microorganisms associated with migratory birds. Journal of Wildlife Diseases 40, 639659.
Hughes, A. L. and Verra, F. (2010). Malaria parasite sequences from chimpanzee support the co-speciation hypothesis for the origin of virulent human malaria (Plasmodium falciparum). Molecular Phylogenetics and Evolution 57, 135143.
Hunt, J. S., Bermingham, E. and Ricklefs, R. E. (2001). Molecular systematics and biogeography of antillean thrashers, tremblers, and mockingbirds (Aves: Mimidae). Auk 118, 3555.
Janz, N. and Nylin, S. (2007). The oscillation hypothesis of host plant-range and speciation. In Specialization, Speciation and Radiation: the Evolutionary Biology of Herbivorus Insects (ed. Tilman, J. T.), pp. 203215. University of California Press, Berkeley, CA.
Jenkins, T. and Owens, I. P. F. (2011). Biogeography of avian blood parasites (Leucocytozoon spp.) in two resident hosts across Europe: phylogeographic structuring or the abundance occupancy relationship? Molecular Ecology 20, 39103920.
Jenkins, T., Thomas, G. H., Hellgren, O. and Owens, I. P. F. (2012). Migratory behavior of birds affects their coevolutionary relationship with blood parasites. Evolution 66, 740751.
Kamdem, C., Tene Fossog, B., Simard, F., Etouna, J., Ndo, C., Kengne, P., Boussès, P., Etoa, F.-X., Awono-Ambene, P., Fontenille, D., Antonio-Nkondjio, C., Besansky, N. J. and Costantini, C. (2012). Anthropogenic habitat disturbance and ecological divergence between incipient species of the malaria mosquito Anopheles gambiae . PLoS ONE 7, e39453.
Kawecki, T. J. (1998). Red queen meets Santa Rosalia: arms races and the evolution of host specialization in organisms with parasitic lifestyles. American Naturalist 152, 635651.
Kim, K. S. and Tsuda, Y. (2012). Avian Plasmodium lineages found in spot surveys of mosquitoes from 2007 to 2010 at Sakata wetland, Japan: do dominant lineages persist for multiple years? Molecular Ecology 21, 53745385.
King, K. C., Delph, L. F., Jokela, J. and Lively, C. M. (2009). The geographic mosaic of sex and the Red Queen. Current Biology 19, 14381441.
Koenraadt, C. J. M., Paaijmans, K. P., Schneider, P., Githeko, A. K. and Takken, W. (2006). Low larval vector survival explains unstable malaria in the western Kenya highlands. Tropical Medicine and International Health 11, 11951205.
LaPointe, D. A., Goff, M. L. and Atkinson, C. T. (2010). Thermal constraints to the sporogonic development and altitudinal distribution of avian malaria Plasmodium relictum in Hawai'i. Journal of Parasitology 96, 318324.
Legendre, P., Desdevises, Y. and Bazin, E. (2002). A statistical test for host–parasite coevolution. Systematic Biology 51, 217234.
Levine, N. D. (1988). The Protozoan Phylum Apicomplexa. CRC Press, Baca Raton.
Levins, R. (1968). Evolution in Changing Environments. Princeton University Press, New Jersey.
Lively, C. M. (1999). Migration, virulence, and the geographic mosaic of adaptation by parasites. American Naturalist 153, S34S47.
Loiseau, C., Harrigan, R. J., Robert, A., Bowie, R. C. K., Henri, A. T., Smith, T. B. and Sehgal, R. N. M. (2012). Host and habitat specialization of avian malaria in Africa. Molecular Ecology 21, 431441.
Martinsen, E. S., Perkins, S. L. and Schall, J. J. (2008). A three-genome phylogeny of malaria parasites (Plasmodium and closely related genera): evolution of life-history traits and host switches. Molecular Phylogenetics and Evolution 47, 261273.
Medeiros, M. C. I., Hamer, G. L. and Ricklefs, R. E. (2013). Host compatibility rather than vector-host encounter rate determines the host range of avian Plasmodium parasites. Proceedings of the Royal Society B: Biological Sciences 280, 20122947.
Merkle, D., Middendorf, M. and Wieseke, N. (2010). A parameter-adaptive dynamic programming approach for inferring cophylogenies. BMC Bioinformatics 11, S60.
Mideo, N. (2009). Parasite adaptations to within-host competition. Trends in Parasitology 25, 261268.
Mideo, N., Alizon, S. and Day, T. (2008). Linking within- and between-host dynamics in the evolutionary epidemiology of infectious diseases. Trends in Ecology and Evolution 23, 511517.
Minakawa, N., Omukunda, E., Zhou, G., Githeko, A. and Yan, G. (2006). Malaria vector productivity in relation to the highland environment in Kenya. American Journal of Tropical Medicine and Hygiene 75, 448453.
Morelli, M. and Spicer, G. (2007). Cospeciation between the nasal mite Ptilonyssus sairae (Acari: Rhinonyssidae) and its bird hosts. Systematic and Applied Acarology 12, 179188.
Njabo, K. Y., Cornel, A. J., Bonneaud, C., Toffelmier, E., Sehgal, R. N. M., Valkiūnas, G., Russell, A. F. and Smith, T. B. (2011). Nonspecific patterns of vector, host and avian malaria parasite associations in a central African rainforest. Molecular Ecology 20, 10491061.
Paaijmans, K. P., Read, A. F. and Thomas, M. B. (2009). Understanding the link between malaria risk and climate. PNAS 106, 1384413849.
Paaijmans, K. P., Blanford, S., Bell, A. S., Blanford, J. I., Read, A. F. and Thomas, M. B. (2010). Influence of climate on malaria transmission depends on daily temperature variation. Proceedings of the National Academy of Sciences 107, 1513515139.
Page, R. D. M. (1994). Parallel phylogenies: reconstructing the history of host-parasite assemblages. Cladistics 10, 155173.
Pagenkopp, K., Klicka, J., Durrant, K., Garvin, J. and Fleischer, R. (2008). Geographic variation in malarial parasite lineages in the Common Yellowthroat (Geothylpis trichas). Conservation Genetics 15771588.
Palinauskas, V., Valkiūnas, G., Bolshakov, C. V. and Bensch, S. (2011). Plasmodium relictum (lineage SGS1) and Plasmodium ashfordi (lineage GRW2): the effects of the co-infection on experimentally infected passerine birds. Experimental Parasitology 127, 527533.
Pavlacky, D. C., Possingham, H. P., Lowe, A. J., Prentis, P. J., Green, D. J. and Goldizen, A. W. (2012). Anthropogenic landscape change promotes asymmetric dispersal and limits regional patch occupancy in a spatially structured bird population. Journal of Animal Ecology 81, 940952.
Pérez-Tris, J. and Bensch, S. (2005). Dispersal increases local transmission of avian malarial parasites. Ecology Letters 8, 838845.
Pérez-Tris, J., Hellgren, O., Križanauskienė, A., Waldenström, J., Secondi, J., Bonneaud, C., Fjeldså, J., Hasselquist, D. and Bensch, S. (2007). Within-host speciation of malaria parasites. PLoS ONE 2, e235.
Posada, D. and Crandall, K. A. (1998). MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817818.
Primmer, C. R., Borge, T., Lindell, J. and Saetre, G.-P. (2002). Single-nucleotide polymorphism characterization in species with limited available sequence information: high nucleotide diversity revealed in the avian genome. Molecular Ecology 11, 603612.
Rathore, D., Wahl, A. M., Sullivan, M. and McCutchan, T. F. (2001). A phylogenetic comparison of gene trees constructed from plastid, mitochondrial and genomic DNA of Plasmodium species. Molecular and Biochemical Parasitology 114, 8994.
R Core Team. (2012). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
Read, A. F. and Taylor, L. H. (2001). The ecology of genetically diverse infections. Science 292, 10991102.
Ricklefs, R. E. and Fallon, S. M. (2002). Diversification and host switching in avian malaria parasites. Proceedings of the Royal Society B: Biological Sciences 269, 885892.
Ricklefs, R. E., Fallon, S. M. and Bermingham, E. (2004). Evolutionary relationships, cospeciation, and host switching in avian malaria parasites. Systematic Biology 53, 111119.
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19, 15721574.
Sehgal, R. N. M. and Lovette, I. J. (2003). Molecular evolution of three avian neurotrophin genes: implications for proregion functional constraints. Journal of Molecular Evolution 57, 335342.
Sehgal, R. N. M., Buermann, W., Harrigan, R. J., Bonneaud, C., Loiseau, C., Chasar, A., Sepil, I., Valkiūnas, G., Iezhova, T., Saatchi, S. and Smith, T. B. (2011). Spatially explicit predictions of blood parasites in a widely distributed African rainforest bird. Proceedings of the Royal Society B: Biological Sciences 278, 10251033.
Smith, T. B., Thomassen, H. A., Freedman, A. H., Sehgal, R. N. M., Buermann, W., Saatchi, S., Pollinger, J., Milá, B., Pires, D., Valkiūnas, G. and Wayne, R. K. (2011). Patterns of divergence in the olive sunbird Cyanomitra olivacea (Aves: Nectariniidae) across the African rainforest–savanna ecotone. Biological Journal of the Linnean Society 103, 821835.
Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 26882690.
Svensson-Coelho, M., Blake, J. G., Loiselle, B. A., Penrose, A. S., Parker, P. G. and Ricklefs, R. E. (2013). Diversity, prevalence, and host specificity of avian Plasmodium and Haemoproteus in a western amazon assemblage. Ornithological Monographs No. 76 No. 76, 1–47 (American Ornithologists’ Union).
Swei, A., Rowley, J. J. L., Rödder, D., Diesmos, M. L. L., Diesmos, A. C., Briggs, C. J., Brown, R., Cao, T. T., Cheng, T. L., Chong, R. A., Han, B., Hero, J., Hoang, H. D., Kusrini, M. D., Le, D. T. T., McGuire, J. A., Meegaskumbura, M., Min, M., Mulcahy, D. G., Neang, T., Phimmachak, S., Rao, D., Schoville, S. D., Sivongxay, N., Srei, N., Stöck, M., Stuart, B. L., Torres, L. S., Tran, D. T. A., Tunstall, T. S., Vieites, D. and Vredenburg, V. T. (2011). Is chytridiomycosis an emerging infectious disease in Asia? PLoS ONE 6, e23179.
Swofford, D. (2001). PAUP* 4.0. Sinauer Associates.
Szymanski, M. M. and Lovette, I. J. (2005). High lineage diversity and host sharing of malarial parasites in a local avian assemblage. Journal of Parasitology 91, 768774.
Thompson, J. N. (1994). The Coevolutionary Process. The University of Chicago Press, Chicago, USA.
Valkiunas, G. (2005). Avian Malaria Parasite and other Haemosporidia. CRC Press, Boca Raton, FL, USA.
Van Riper, C. III, van Riper, S. G., Goff, M. L. and Laird, M. (1986). The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecological Monographs 56, 327.
van Rooyen, J., Lalubin, F., Glaizot, O. and Christe, P. (2013). Altitudinal variation in haemosporidian parasite distribution in great tit populations. Parasites and Vectors 6, 139.
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, 15451554.
Waldenström, J., Bensch, S., Hasselquist, D. and Ostman, O. (2004). A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood. Journal of Parasitology 90, 191194.
Waltari, E., Hoberg, E. P., Lessa, E. P. and Cook, J. A. (2007). Eastward Ho: phylogeographical perspectives on colonization of hosts and parasites across the Beringian nexus. Journal of Biogeography 34, 561574.
Yu, Y., Harris, A. J. and He, X. (2010). S-DIVA (Statistical Dispersal-Vicariance Analysis): a tool for inferring biogeographic histories. Molecular Phylogenetics and Evolution 56, 848850.
Yu, Y., Harris, A. J. and He, X. (2013). RASP (Reconstruct Ancestral State in Phylogenies). 2.1 beta. Available at
Zarlenga, D. S., Rosenthal, B. M., La Rosa, G., Pozio, E. and Hoberg, E. P. (2006). Post-miocene expansion, colonization, and host switching drove speciation among extant nematodes of the archaic genus Trichinella . Proceedings of the National Academy of Sciences of the USA 103, 73547359.


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