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Host associations and turnover of haemosporidian parasites in manakins (Aves: Pipridae)


Parasites of the genera Plasmodium and Haemoproteus (Apicomplexa: Haemosporida) are a diverse group of pathogens that infect birds nearly worldwide. Despite their ubiquity, the ecological and evolutionary factors that shape the diversity and distribution of these protozoan parasites among avian communities and geographic regions are poorly understood. Based on a survey throughout the Neotropics of the haemosporidian parasites infecting manakins (Pipridae), a family of Passerine birds endemic to this region, we asked whether host relatedness, ecological similarity and geographic proximity structure parasite turnover between manakin species and local manakin assemblages. We used molecular methods to screen 1343 individuals of 30 manakin species for the presence of parasites. We found no significant correlations between manakin parasite lineage turnover and both manakin species turnover and geographic distance. Climate differences, species turnover in the larger bird community and parasite lineage turnover in non-manakin hosts did not correlate with manakin parasite lineage turnover. We also found no evidence that manakin parasite lineage turnover among host species correlates with range overlap and genetic divergence among hosts. Our analyses indicate that host switching (turnover among host species) and dispersal (turnover among locations) of haemosporidian parasites in manakins are not constrained at this scale.

Corresponding author
*Corresponding author: Laboratório de Evolução e Biogeografia, Universidade Federal da Bahia, Rua Barão de Jeremoabo, 147, Salvador, BA 40170115, Brazil. E-mail:
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This list contains references from the content that can be linked to their source. For a full set of references and notes please see the PDF or HTML where available.

C. A. Abella-Medrano , S. Ibáñez-Bernal , I. MacGregor-Fors and D. Santiago-Alarcon (2015). Spatiotemporal variation of mosquito diversity (Diptera: Culicidae) at places with different land-use types within a neotropical montane cloud forest matrix. Parasites & Vectors 8, 487.

M. Anciães and A. T. Peterson (2009). Ecological niches and their evolution among Neotropical manakins (Aves: Pipridae). Journal of Avian Biology 40, 591604.

H.-J. Bandelt , P. Forster and A. Röhl (1999). Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 3748.

J. A. Bell , J. D. Weckstein , A. Fecchio and V. V. Tkach (2015). A new real-time PCR protocol for detection of avian haemosporidians. Parasites & Vectors 8, 383.

J. Borner , C. Pick , J. Thiede , O. M. Kolawole , M. T. Kingsley , J. Schulze , V. M. Cottontail , N. Wellinghausen , J. Schmidt-Chanasit , I. Bruchhaus and T. Burmester (2016). Phylogeny of haemosporidian blood parasites revealed by a multi-gene approach. Molecular Phylogenetics and Evolution 94, 221231.

T. J. Davies and A. B. Pedersen (2008). Phylogeny and geography predict pathogen community similarity in wild primates and humans. Proceedings of the Royal Society B: Biological Sciences 275, 16951701.

S. V. Drovetski , S. A. Aghayan , V. A. Mata , R. J. Lopes , N. A. Mode , J. A. Harvey and G. Voelker (2014). Does the niche breadth or trade-off hypothesis explain the abundance–occupancy relationship in avian Haemosporidia? Molecular Ecology 23, 33223329.

V. A. Ellis , M. D. Collins , M. C. I. Medeiros , E. H. R. Sari , E. D. Coffey , R. C. Dickerson , C. Lugarini , J. A. Stratford , D. R. Henry , L. Merrill , A. E. Matthews , A. A. Hanson , J. R. Roberts , M. Joyce , M. R. Kunkel and R. E. Ricklefs (2015). Local host specialization, host-switching, and dispersal shape the regional distributions of avian haemosporidian parasites. Proceedings of the National Academy of Sciences of the United States of America 112, 1129411299.

G. W. Esch , A. O. Bush and J. M. Aho (1990). Parasite Communities: Patterns and Processes. Chapman and Hall, London.

K. L. Evans , K. J. Gaston , S. P. Sharp , A. McGowan , M. Simeoni and B. J. Hatchwell (2009). Effects of urbanisation on disease prevalence and age structure in blackbird Turdus merula populations. Oikos 118, 774782.

A. Fecchio , M. R. Lima , P. Silveira , É. M. Braga and M. Â. Marini (2011). High prevalence of blood parasites in social birds from a neotropical savanna in Brazil. Emu 111, 132138.

A. Fecchio , M. R. Lima , M. Svensson-Coelho , M. Â. Marini and R. E. Ricklefs (2013). Structure and organization of an avian haemosporidian assemblage in a Neotropical savanna in Brazil. Parasitology 140, 181192.

F. C. Ferreira Jr., R. A. Rodrigues , Y. Sato , M. A. Z. Borges and É. M. Braga (2016). Searching for putative avian malaria vectors in a seasonally dry tropical forest in Brazil. Parasites & Vectors 9, 587.

S. C. Galen and C. C. Witt (2014). Diverse avian malaria and other haemosporidian parasites in Andean house wrens: evidence for regional co-diversification by host-switching. Journal of Avian Biology 45, 374386.

C. Gonzalez-Quevedo , R. G. Davies and D. S. Richardson (2014). Predictors of malaria infection in a wild bird population: landscape-level analyses reveal climatic and anthropogenic factors. Journal of Animal Ecology 83, 10911102.

W. D. Hamilton and M. Zuk (1982). Heritable true fitness and bright birds: a role for parasites? Science 218, 384387.

O. Hellgren , J. Waldenström and S. Bensch (2004). A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium and Haemoproteus from avian blood. Journal of Parasitology 90, 797802.

R. J. Hijmans , S. E. Cameron , J. L. Parra , P. G. Jones and A. Jarvis (2005). Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25, 19651978.

F. Ishtiaq , L. Guillaumot , S. M. Clegg , A. B. Phillimore , R. A. Black , I. P. F. Owens , N. I. Mundy and B. C. Sheldon (2008). Avian haematozoan parasites and their associations with mosquitoes across Southwest Pacific Islands. Molecular Ecology 17, 45454555.

F. Ishtiaq , S. M. Clegg , A. B. Phillimore , R. A. Black , I. P. F. Owens and B. C. Sheldon (2010). Biogeographical patterns of blood parasite lineage diversity in avian hosts from southern Melanesian islands. Journal of Biogeography 37, 120132.

P. Jaccard (1912). The distribution of the flora in the alpine zone. 1. New phytologist 11, 3750.

T. Kamiya , K. O'Dwyer , S. Nakagawa and P. Poulin (2014). What determines species richness of parasitic organisms? A meta-analysis across animal, plant and fungal hosts. Biological Reviews 89, 123134.

E. J. Lauron , C. Loiseau , R. C. K. Bowie , G. S. Spicer , T. B. Smith , M. Melo and R. N. M. Sehgal (2015). Coevolutionary patterns and diversification of avian malaria parasites in African sunbirds (Family Nectariniidae). Parasitology 142, 635647.

C. Loiseau , T. Iezhova , G. Valkiūnas , A. Chasar , A. Hutchinson , W. Buermann , T. B. Smith and R. N. M. Sehgal (2010). Spatial variation of haemosporidian parasite infection in African rainforest bird species. Journal of Parasitology 96, 2129.

C. Loiseau , R. J. Harrigan , A. Robert , R. C. K. Bowie , H. A. Thomassen , T. B. Smith and R. N. M. Sehgal (2012). Host and habitat specialization of avian malaria in Africa. Molecular Ecology 21, 431441.

H. L. Lutz , W. M. Hochachka , J. I. Engel , J. A. Bell , V. V. Tkach , J. M. Bates , S. J. Hackett and J. D. Weckstein (2015). Parasite prevalence corresponds to host life history in a diverse assemblage of Afrotropical birds and haemosporidian parasites. PLoS ONE 10(4), e0121254.

A. E. Matthews , V. A. Ellis , A. A. Hanson , J. R. Roberts , R. E. Ricklefs and M. D. Collins (2016). Avian haemosporidian prevalence and its relationship to host life histories in eastern Tennessee. Journal of Ornithology 157, 533548.

M. C. I. Medeiros , G. L. Hamer and R. E. Ricklefs (2013). Host compatibility rather than vector-host encounter rate determines the host range of avian Plasmodium parasites. Proceedings of the Royal Society of London B: Biological Sciences 280, 20122947.

L. Mendes , T. Piersma , M. Lecoq , B. Spaans and R. E. Ricklefs (2005). Disease-limited distributions? Contrasts in the prevalence of avian malaria in shorebird species using marine and freshwater habitats. Oikos 109, 396404.

J. C. Nekola and P. S. White (1999). The distance decay of similarity in biogeography and ecology. Journal of Biogeography 26, 867878.

J. I. Ohlson , J. Fjeldså and P. G. P. Ericson (2013). Molecular phylogeny of the manakins (Aves: Passeriformes: Pipridae), with a new classification and the description of a new genus. Molecular Phylogenetics and Evolution 69, 796804.

S. Olsson-Pons , N. J. Clark , F. Ishtiaq and S. M. Clegg (2015). Differences in host species relationships and biogeographic influences produce contrasting patterns of prevalence, community composition and genetic structure in two genera of avian malaria parasites in southern Melanesia. Journal of Animal Ecology 84, 985998.

E. Paradis , J. Claude and K. Strimmer (2004). APE: analyses of phylogenetics and evolution in R-language. Bioinformatics 20, 289290.

J. Pérez-Tris , O. Hellgren , A. Križanauskienė , J. Waldenström , J. Secondi , C. Bonneaud , J. Fjeldså , D. Hasselquist and S. Bensch (2007). Within-host speciation of malaria parasites. PLoS ONE 2, e235.

R. Poulin (1997). Species richness of parasite assemblages: evolution and patterns. Annual Review of Ecology and Systematics 28, 341358.

R. Poulin (2003). The decay of similarity with geographical distance in parasite communities of vertebrate hosts. Journal of Biogeography 30, 16091615.

R. E. Ricklefs , S. M. Fallon and E. Bermingham (2004). Evolutionary relationships, cospeciation and host switching in avian malaria parasites. Systematic Biology 53, 111119.

R. E. Ricklefs , D. C. Outlaw , M. Svensson-Coelho , M. C. I. Medeiros , V. A. Ellis and S. Latta (2014). Species formation by host shifting in avian malaria parasites. Proceedings of the National Academy of Sciences of the United States of America 111, 1481614821.

D. Santiago-Alarcon , P. Havelka , H. M. Schaefer and G. Segelbacher (2012 b). Bloodmeal Analysis Reveals Avian Plasmodium Infections and Broad Host Preferences of Culicoides (Diptera: Ceratopogonidae) Vectors. PLoS ONE 7, e31098.

D. Santiago-Alarcon , V. Palinauskas and H. M. Schaefer (2012 a). Diptera vectors of avian Haemosporidian parasites: untangling parasite life cycles and their taxonomy. Biological Reviews 87, 928964.

D. Santiago-Alarcon , A. Rodríguez-Ferraro , P. G. Parker and R. E. Ricklefs (2014). Different meal, same flavor: cospeciation and host switching of haemosporidian parasites in some non-passerine birds. Parasites & Vectors 7, 286.

E. S. Scordato and M. R. Kardish (2014). Prevalence and beta diversity in avian malaria communities: host species is a better predictor than geography. Journal of Animal Ecology 83, 13871397.

J. Soininen , R. McDonald and H. Hillebrand (2007). The distance decay of similarity in ecological communities. Ecography 30, 312.

A. Stamatakis , P. Hoover and J. Rougemont (2008). A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology 57, 758771.

M. Svensson-Coelho and R. E. Ricklefs (2011). Host phylogeography and beta diversity in avian haemosporidian (Plasmodiidae) assemblages of the Lesser Antilles. Journal of Animal Ecology 80, 938946.

M. Svensson-Coelho , J. G. Blake , B. A. Loiselle , A. S. Penrose , P. G. Parker and R. E. Ricklefs (2013). Diversity, prevalence, and host specificity of avian Plasmodium and Haemoproteus in a Western Amazon assemblage. Ornithological Monographs 76, 147.

J. L. Tella (2002). The evolutionary transition to coloniality promotes higher blood parasitism in birds. Journal of Evolutionary Biology 15, 3241.

D. W. Thieltges , M. A. D. Ferguson , C. S. Jones , M. Krakau , X. Montaudouin , R. L. Noble , K. Reise and R. Poulin (2009). Distance decay of similarity among parasite communities of three marine invertebrate hosts. Oecologia 160, 163173.

M. V. Vinarski , N. P. Korallo , B. R. Krasnov , G. I. Shenbrot and R. Poulin (2007). Decay of similarity of gamasid mite assemblages parasitic on Palaearctic small mammals: geographic distance, host-species composition or environment. Journal of Biogeography 34, 16911700.

J. Waldenström , S. Bensch , S. Kiboi , D. Hasselquist and U. Ottoson (2002). Cross-species infection of blood parasites between resident and migratory songbirds in Africa. Molecular Ecology 11, 15451554.

J. J. Wiens (2003). Missing data, incomplete taxa, and phylogenetic accuracy. Systematic Biology 52, 528538.

J. J. Wiens and M. C. Morrill (2011). Missing data in phylogenetic analysis: reconciling results from simulations and empirical data. Systematic Biology 60, 719731.

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