Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-28T18:01:19.730Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  29 October 2014

ELVIN J. LAURON ,
CLAIRE LOISEAU ,
RAURI C. K. BOWIE ,
GREG S. SPICER ,
THOMAS B. SMITH ,
MARTIM MELO  and
RAVINDER N. M. SEHGAL
ELVIN J. LAURON*
Affiliation:
Department of Biology, San Francisco State University, San Francisco, California 94132, USA
CLAIRE LOISEAU
Affiliation:
Department of Biology, San Francisco State University, San Francisco, California 94132, USA
RAURI C. K. BOWIE
Affiliation:
Museum of Vertebrate Zoology and Department of Integrative Biology, University of California at Berkeley, Berkeley, California 94720, USA
GREG S. SPICER
Affiliation:
Department of Biology, San Francisco State University, San Francisco, California 94132, USA
THOMAS B. SMITH
Affiliation:
Center for Tropical Research, University of California at Los Angeles, Los Angeles, California 90095, USA
MARTIM MELO
Affiliation:
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBio, Universidade do Porto, Campus Agrário de Vairão, 4485-661 Vairão, Portugal
RAVINDER N. M. SEHGAL
Affiliation:
Department of Biology, San Francisco State University, San Francisco, California 94132, USA
*
*Corresponding author. Department of Biology San Francisco State University, 1600 Holloway Avenue, San Francisco, California 94132, USA. E-mail: elauron@mail.sfsu.edu
Get access Rights & Permissions [Opens in a new window]

Summary

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.

Keywords

PlasmodiumnectariniidaecospeciationAfrican sunbirdavian malariahost switching
Type
Research Article
Information
Parasitology , Volume 142 , Issue 5 , April 2015 , pp. 635 - 647
Check for updates
Copyright
Copyright © Cambridge University Press 2014 

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

REFERENCES

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, 1533–1538.CrossRefGoogle ScholarPubMed
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, 151–162.CrossRefGoogle Scholar
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, 95–107.Google Scholar
Balbuena, J. A., Míguez-Lozano, R. and Blasco-Costa, I. (2013). PACo: a novel procrustes application to cophylogenetic analysis. PLoS ONE 8, e61048.CrossRefGoogle Scholar
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, 1583–1589.CrossRefGoogle ScholarPubMed
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, 1353–1358.CrossRefGoogle ScholarPubMed
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
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.Google Scholar
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, 56–74.CrossRefGoogle ScholarPubMed
Brodie, E. D. III and Brodie, E. D. Jr. (1999). Predator–prey arms race and dangerous prey. Biosciences 49, 557–568.CrossRefGoogle Scholar
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, 517–525.Google Scholar
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, 4121–4133.Google Scholar
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, 27–55.Google Scholar
Cheke, R. S., Clive, M. F. and Allen, R. (2001). Sunbirds. Yale University Press, New Haven and London.Google Scholar
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.Google Scholar
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, 1370–1377.CrossRefGoogle ScholarPubMed
Demastes, J. W. and Hafner, M. S. (1993). Cospeciation of pocket gophers (Geomys) and their chewing lice (Geomydoecus). Journal of Mammalogy 74, 521.CrossRefGoogle Scholar
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, 7624–7628.Google Scholar
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, 1969–1973.CrossRefGoogle ScholarPubMed
Ehrnsberger, R. (2001). A preliminary analysis of phylogenetic relationships of the feather mite family Freyanidae Dubinin, 1953 (Acari: Astigmata). Biological Bulletin of Poznań 38, 181–201.Google Scholar
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, 564–567.Google Scholar
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, 606–615.Google Scholar
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, 466–480.Google Scholar
Fallon, S. M., Fleischer, R. C. and Graves, G. R. (2006). Malarial parasites as geographical markers in migratory birds? Biology Letters 2, 213–216.Google Scholar
Figuerola, J. and Green, A. J. (2000). Haematozoan parasites and migratory behaviour in waterfowl. http://digital.csic.es/handle/10261/43207.Google Scholar
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, 543–548.Google Scholar
Garamszegi, L. Z. (2006). The evolution of virulence and host specialization in malaria parasites of primates. Ecology Letters 9, 933–940.Google Scholar
Garamszegi, L. Z. (2009). Patterns of co-speciation and host switching in primate malaria parasites. Malaria Journal 8, 110.CrossRefGoogle ScholarPubMed
Graham, A. L. (2008). Ecological rules governing helminth–microparasite coinfection. Proceedings of the National Academy of Sciences 105, 566–570.CrossRefGoogle ScholarPubMed
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, 493–503.CrossRefGoogle ScholarPubMed
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, 268–278.Google Scholar
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, 797–802.Google Scholar
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, 889–896.Google Scholar
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, 1281–1290.CrossRefGoogle ScholarPubMed
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, 2840–2849.CrossRefGoogle Scholar
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, 827–834.Google Scholar
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, 1533–1550.Google Scholar
Hubálek, Z. (2004). An annotated checklist of pathogenic microorganisms associated with migratory birds. Journal of Wildlife Diseases 40, 639–659.CrossRefGoogle ScholarPubMed
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, 135–143.CrossRefGoogle ScholarPubMed
Hunt, J. S., Bermingham, E. and Ricklefs, R. E. (2001). Molecular systematics and biogeography of antillean thrashers, tremblers, and mockingbirds (Aves: Mimidae). Auk 118, 35–55.Google Scholar
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. 203–215. University of California Press, Berkeley, CA.Google Scholar
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, 3910–3920.Google Scholar
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, 740–751.Google Scholar
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.Google Scholar
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, 635–651.CrossRefGoogle ScholarPubMed
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, 5374–5385.Google Scholar
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, 1438–1441.CrossRefGoogle ScholarPubMed
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, 1195–1205.Google Scholar
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, 318–324.Google Scholar
Legendre, P., Desdevises, Y. and Bazin, E. (2002). A statistical test for host–parasite coevolution. Systematic Biology 51, 217–234.Google Scholar
Levine, N. D. (1988). The Protozoan Phylum Apicomplexa. CRC Press, Baca Raton.Google Scholar
Levins, R. (1968). Evolution in Changing Environments. Princeton University Press, New Jersey.Google Scholar
Lively, C. M. (1999). Migration, virulence, and the geographic mosaic of adaptation by parasites. American Naturalist 153, S34–S47.Google Scholar
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, 431–441.Google Scholar
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, 261–273.Google Scholar
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.Google Scholar
Merkle, D., Middendorf, M. and Wieseke, N. (2010). A parameter-adaptive dynamic programming approach for inferring cophylogenies. BMC Bioinformatics 11, S60.Google Scholar
Mideo, N. (2009). Parasite adaptations to within-host competition. Trends in Parasitology 25, 261–268.Google Scholar
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, 511–517.Google Scholar
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, 448–453.Google Scholar
Morelli, M. and Spicer, G. (2007). Cospeciation between the nasal mite Ptilonyssus sairae (Acari: Rhinonyssidae) and its bird hosts. Systematic and Applied Acarology 12, 179–188.Google Scholar
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, 1049–1061.Google Scholar
Paaijmans, K. P., Read, A. F. and Thomas, M. B. (2009). Understanding the link between malaria risk and climate. PNAS 106, 13844–13849.Google Scholar
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, 15135–15139.Google Scholar
Page, R. D. M. (1994). Parallel phylogenies: reconstructing the history of host-parasite assemblages. Cladistics 10, 155–173.Google Scholar
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 1577–1588.Google Scholar
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, 527–533.Google Scholar
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, 940–952.Google Scholar
Pérez-Tris, J. and Bensch, S. (2005). Dispersal increases local transmission of avian malarial parasites. Ecology Letters 8, 838–845.Google Scholar
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.Google Scholar
Posada, D. and Crandall, K. A. (1998). MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817–818.Google Scholar
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, 603–612.Google Scholar
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, 89–94.Google Scholar
R Core Team. (2012). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Read, A. F. and Taylor, L. H. (2001). The ecology of genetically diverse infections. Science 292, 1099–1102.Google Scholar
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, 885–892.Google Scholar
Ricklefs, R. E., Fallon, S. M. and Bermingham, E. (2004). Evolutionary relationships, cospeciation, and host switching in avian malaria parasites. Systematic Biology 53, 111–119.Google Scholar
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.Google Scholar
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, 335–342.Google Scholar
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, 1025–1033.Google Scholar
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, 821–835.Google Scholar
Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690.Google Scholar
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).Google Scholar
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.Google Scholar
Swofford, D. (2001). PAUP* 4.0. Sinauer Associates.Google Scholar
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, 768–774.Google Scholar
Thompson, J. N. (1994). The Coevolutionary Process. The University of Chicago Press, Chicago, USA.Google Scholar
Valkiunas, G. (2005). Avian Malaria Parasite and other Haemosporidia. CRC Press, Boca Raton, FL, USA.Google Scholar
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.Google Scholar
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.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
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, 191–194.Google Scholar
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, 561–574.Google Scholar
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, 848–850.Google Scholar
Yu, Y., Harris, A. J. and He, X. (2013). RASP (Reconstruct Ancestral State in Phylogenies). 2.1 beta. Available at http://mnh.scu.edu.cn/soft/blog/RASP Google Scholar
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, 7354–7359.Google Scholar
Supplementary material: Image

Lauron Supplementary Material

Figure S1

Download Lauron Supplementary Material(Image)
Image 13.5 KB
Supplementary material: Image

Lauron Supplementary Material

Figure S2

Download Lauron Supplementary Material(Image)
Image 28.1 KB
Supplementary material: Image

Lauron Supplementary Material

Figure S3

Download Lauron Supplementary Material(Image)
Image 17.8 KB
Supplementary material: Image

Lauron Supplementary Material

Figure S4A-B

Download Lauron Supplementary Material(Image)
Image 628.7 KB
Supplementary material: Image

Lauron Supplementary Material

Figure S4C-D

Download Lauron Supplementary Material(Image)
Image 644.5 KB
Supplementary material: Image

Lauron Supplementary Material

Figure S4E-F

Download Lauron Supplementary Material(Image)
Image 702.7 KB
Supplementary material: Image

Lauron Supplementary Material

Table S1a

Download Lauron Supplementary Material(Image)
Image 25.2 KB
Supplementary material: Image

Lauron Supplementary Material

Table S1b

Download Lauron Supplementary Material(Image)
Image 21.4 KB
Supplementary material: Image

Lauron Supplementary Material

Table S2

Download Lauron Supplementary Material(Image)
Image 127.6 KB
Supplementary material: Image

Lauron Supplementary Material

Table S2 (continued)

Download Lauron Supplementary Material(Image)
Image 96.6 KB
Supplementary material: Image

Lauron Supplementary Material

Table S3

Download Lauron Supplementary Material(Image)
Image 133.8 KB
Supplementary material: Image

Lauron Supplementary Material

Table S3 (continued)

Download Lauron Supplementary Material(Image)
Image 5.8 KB
Supplementary material: Image

Lauron Supplementary Material

Table S4

Download Lauron Supplementary Material(Image)
Image 152.6 KB
Supplementary material: Image

Lauron Supplementary Material

Table S4 (continued)

Download Lauron Supplementary Material(Image)
Image 88.6 KB