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

  • ALAN FECCHIO (a1), MARIA SVENSSON-COELHO (a2), JEFFREY BELL (a3), VINCENZO A. ELLIS (a4), MATTHEW C. MEDEIROS (a5), CHRISTOPHER H. TRISOS (a6), JOHN G. BLAKE (a7), BETTE A. LOISELLE (a8), JOSEPH A. TOBIAS (a9), REBEKA FANTI (a10), ELYSE D. COFFEY (a10), IUBATÃ P. DE FARIA (a11), JOÃO B. PINHO (a12), GABRIEL FELIX (a13), ERIKA M. BRAGA (a13), MARINA ANCIÃES (a14), VASYL TKACH (a3), JOHN BATES (a15), CHRISTOPHER WITT (a16), JASON D. WECKSTEIN (a1) (a17), ROBERT E. RICKLEFS (a10) and IZENI P. FARIAS (a18)...
Summary
SUMMARY

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.

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Corresponding author
*Corresponding author: Laboratório de Evolução e Biogeografia, Universidade Federal da Bahia, Rua Barão de Jeremoabo, 147, Salvador, BA 40170115, Brazil. E-mail: alanfecchio@gmail.com
References
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Abella-MedranoC. A., Ibáñez-BernalS., MacGregor-ForsI. and Santiago-AlarconD. (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.
AnciãesM. and PetersonA. T. (2009). Ecological niches and their evolution among Neotropical manakins (Aves: Pipridae). Journal of Avian Biology 40, 591604.
BandeltH.-J., ForsterP. and RöhlA. (1999). Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 3748.
BellJ. A., WecksteinJ. D., FecchioA. and TkachV. V. (2015). A new real-time PCR protocol for detection of avian haemosporidians. Parasites & Vectors 8, 383.
BivandR., KeittT., RowlingsonB., PebesmaE., SumnerM., HijmansR. and RouaultE. (2014). rgdal: Bindings for the Geospatial Data Abstraction Library. version 0.9-1.http://www.gdal.org, https://r-forge.r-project.org/projects/rgdal/
BivandR., Lewin-KohN., PebesmaE., ArcherE., BaddeleyA., BibikoH.-J., BreyS., CallahanJ., CarrilloG., DrayS., ForrestD., FriendlyM., GiraudouxP., GolicherD., Gómez-RubioV., HausmannP., HufthammerK. O., JaggerT., LuqueS., MacQueenD., NiccolaiA., Perpiñán-LamigueiroO., ShortT., SnowG., StablerB., StokelyM. and TurnerR. (2015). maptools: Tools for Reading and Handling Spatial Objects. version 0.8-34. http://r-forge.r-project.org/projects/maptools/
BornerJ., PickC., ThiedeJ., KolawoleO. M., KingsleyM. T., SchulzeJ., CottontailV. M., WellinghausenN., Schmidt-ChanasitJ., BruchhausI. and BurmesterT. (2016). Phylogeny of haemosporidian blood parasites revealed by a multi-gene approach. Molecular Phylogenetics and Evolution 94, 221231.
DaviesT. J. and PedersenA. B. (2008). Phylogeny and geography predict pathogen community similarity in wild primates and humans. Proceedings of the Royal Society B: Biological Sciences 275, 16951701.
DrovetskiS. V., AghayanS. A., MataV. A., LopesR. J., ModeN. A., HarveyJ. A. and VoelkerG. (2014). Does the niche breadth or trade-off hypothesis explain the abundance–occupancy relationship in avian Haemosporidia? Molecular Ecology 23, 33223329.
EllisV. A., CollinsM. D., MedeirosM. C. I., SariE. H. R., CoffeyE. D., DickersonR. C., LugariniC., StratfordJ. A., HenryD. R., MerrillL., MatthewsA. E., HansonA. A., RobertsJ. R., JoyceM., KunkelM. R. and RicklefsR. E. (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.
EschG. W., BushA. O. and AhoJ. M. (1990). Parasite Communities: Patterns and Processes. Chapman and Hall, London.
EvansK. L., GastonK. J., SharpS. P., McGowanA., SimeoniM. and HatchwellB. J. (2009). Effects of urbanisation on disease prevalence and age structure in blackbird Turdus merula populations. Oikos 118, 774782.
FallonS. M., RicklefsR. E., SwansonB. L. and BerminghamE. (2003). Detecting avian malaria: an improved polymerase chain reaction diagnostic. Journal of Parasitology 85, 10441047.
FecchioA., LimaM. R., SilveiraP., BragaÉ. M. and MariniM. Â. (2011). High prevalence of blood parasites in social birds from a neotropical savanna in Brazil. Emu 111, 132138.
FecchioA., LimaM. R., Svensson-CoelhoM., MariniM. Â. and RicklefsR. E. (2013). Structure and organization of an avian haemosporidian assemblage in a Neotropical savanna in Brazil. Parasitology 140, 181192.
FentonA. and PedersenA. B. (2005). Community epidemiology in theory and practice: a conceptual framework for classifying disease threats in human and wild populations. Emerging Infectious Diseases 11, 18151821.
FerreiraF. C.Jr., RodriguesR. A., SatoY., BorgesM. A. Z. and BragaÉ. M. (2016). Searching for putative avian malaria vectors in a seasonally dry tropical forest in Brazil. Parasites & Vectors 9, 587.
GalenS. C. and WittC. C. (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.
GonzálezA. D., MattaN. E., EllisV. A., MillerE. T., RicklefsR. E. and GutiérrezH. R. (2014). Mixed species flock, nest height, and elevation partially explain avian haemoparasite prevalence in Colombia. PLoS ONE 9, e100695.
Gonzalez-QuevedoC., DaviesR. G. and RichardsonD. S. (2014). Predictors of malaria infection in a wild bird population: landscape-level analyses reveal climatic and anthropogenic factors. Journal of Animal Ecology 83, 10911102.
GosleeS. C. and UrbanD. L. (2007). The ecodist package for dissimilarity-based analysis of ecological data. Journal of Statistical Software 22, 119.
HamiltonW. D. and ZukM. (1982). Heritable true fitness and bright birds: a role for parasites? Science 218, 384387.
HellgrenO., WaldenströmJ. and BenschS. (2004). A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium and Haemoproteus from avian blood. Journal of Parasitology 90, 797802.
Hernández-LaraC., González-GarcíaF. and Santiago-AlarconD. (2017). Spatial and seasonal variation of avian malaria infections in five different land use types within a Neotropical montane forest matrix. Landscape and Urban Planning 157, 151160.
HijmansR. J., CameronS. E., ParraJ. L., JonesP. G. and JarvisA. (2005). Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25, 19651978.
IshtiaqF., GuillaumotL., CleggS. M., PhillimoreA. B., BlackR. A., OwensI. P. F., MundyN. I. and SheldonB. C. (2008). Avian haematozoan parasites and their associations with mosquitoes across Southwest Pacific Islands. Molecular Ecology 17, 45454555.
IshtiaqF., CleggS. M., PhillimoreA. B., BlackR. A., OwensI. P. F. and SheldonB. C. (2010). Biogeographical patterns of blood parasite lineage diversity in avian hosts from southern Melanesian islands. Journal of Biogeography 37, 120132.
JaccardP. (1912). The distribution of the flora in the alpine zone. 1. New phytologist 11, 3750.
KamiyaT., O'DwyerK., NakagawaS. and PoulinP. (2014). What determines species richness of parasitic organisms? A meta-analysis across animal, plant and fungal hosts. Biological Reviews 89, 123134.
KrasnovB. R., ShenbrotG. I., MouillotD., KhokhlovaI. S. and PoulinR. (2005). Spatial variation in species diversity and composition of flea assemblages in small mammalian hosts: geographical distance or faunal similarity? Journal of Biogeography 32, 633644.
LauronE. J., LoiseauC., BowieR. C. K., SpicerG. S., SmithT. B., MeloM. and SehgalR. N. M. (2015). Coevolutionary patterns and diversification of avian malaria parasites in African sunbirds (Family Nectariniidae). Parasitology 142, 635647.
LoiseauC., IezhovaT., ValkiūnasG., ChasarA., HutchinsonA., BuermannW., SmithT. B. and SehgalR. N. M. (2010). Spatial variation of haemosporidian parasite infection in African rainforest bird species. Journal of Parasitology 96, 2129.
LoiseauC., HarriganR. J., RobertA., BowieR. C. K., ThomassenH. A., SmithT. B. and SehgalR. N. M. (2012). Host and habitat specialization of avian malaria in Africa. Molecular Ecology 21, 431441.
LutzH. L., HochachkaW. M., EngelJ. I., BellJ. A., TkachV. V., BatesJ. M., HackettS. J. and WecksteinJ. D. (2015). Parasite prevalence corresponds to host life history in a diverse assemblage of Afrotropical birds and haemosporidian parasites. PLoS ONE 10(4), e0121254.
MagurranA. E. (2004). Measuring Biological Diversity. Blackwell Science Ltd, Malden, MA, USA.
ManlyB. F. J. (2007). Randomization, Bootstrap and Monte Carlo Methods in Biology. Chapman & Hall/CRC, Boca Raton, FL, USA.
MantelN. (1967). The detection of disease clustering and a generalized regression approach. Cancer Research 27, 209220.
MatthewsA. E., EllisV. A., HansonA. A., RobertsJ. R., RicklefsR. E. and CollinsM. D. (2016). Avian haemosporidian prevalence and its relationship to host life histories in eastern Tennessee. Journal of Ornithology 157, 533548.
MedeirosM. C. I., HamerG. L. and RicklefsR. E. (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.
MedeirosM. C. I., RicklefsR. E., BrawnJ. D. and HamerG. L. (2015). Plasmodium prevalence across avian host species is positively associated with exposure to mosquito vectors. Parasitology 142, 16121620.
MendesL., PiersmaT., LecoqM., SpaansB. and RicklefsR. E. (2005). Disease-limited distributions? Contrasts in the prevalence of avian malaria in shorebird species using marine and freshwater habitats. Oikos 109, 396404.
NekolaJ. C. and WhiteP. S. (1999). The distance decay of similarity in biogeography and ecology. Journal of Biogeography 26, 867878.
OakgroveK. S., HarriganR. J., LoiseauC., GuersS., SeppiB. and SehgalR. N. M. (2014). Distribution, diversity and drivers of blood-borne parasite co-infections in Alaskan bird populations. International Journal for Parasitology 44, 717727.
OhlsonJ. I., FjeldsåJ. and EricsonP. G. P. (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.
OksanenJ., BlanchetF. G., KindtR., LegendreP., MinchinP. R., O'HaraR. B., SimpsonG. L., SolymosP., StevensM. H. H. and WagnerH. (2010). vegan: Community Ecology Package. R package version 1.17–0. https://CRAN.R-project.org/package=vegan
Olsson-PonsS., ClarkN. J., IshtiaqF. and CleggS. M. (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.
ParadisE., ClaudeJ. and StrimmerK. (2004). APE: analyses of phylogenetics and evolution in R-language. Bioinformatics 20, 289290.
Pérez-TrisJ., HellgrenO., KrižanauskienėA., WaldenströmJ., SecondiJ., BonneaudC., FjeldsåJ., HasselquistD. and BenschS. (2007). Within-host speciation of malaria parasites. PLoS ONE 2, e235.
PoulinR. (1997). Species richness of parasite assemblages: evolution and patterns. Annual Review of Ecology and Systematics 28, 341358.
PoulinR. (2003). The decay of similarity with geographical distance in parasite communities of vertebrate hosts. Journal of Biogeography 30, 16091615.
PoulinR. (2007). Evolutionary Ecology of Parasites. Princeton University Press, Princeton, NJ, USA.
R Core Team. (2016). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
RicklefsR. E., FallonS. M. and BerminghamE. (2004). Evolutionary relationships, cospeciation and host switching in avian malaria parasites. Systematic Biology 53, 111119.
RicklefsR. E., OutlawD. C., Svensson-CoelhoM., MedeirosM. C. I., EllisV. A. and LattaS. (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.
Santiago-AlarconD., HavelkaP., SchaeferH. M. and SegelbacherG. (2012 b). Bloodmeal Analysis Reveals Avian Plasmodium Infections and Broad Host Preferences of Culicoides (Diptera: Ceratopogonidae) Vectors. PLoS ONE 7, e31098.
Santiago-AlarconD., PalinauskasV. and SchaeferH. M. (2012 a). Diptera vectors of avian Haemosporidian parasites: untangling parasite life cycles and their taxonomy. Biological Reviews 87, 928964.
Santiago-AlarconD., Rodríguez-FerraroA., ParkerP. G. and RicklefsR. E. (2014). Different meal, same flavor: cospeciation and host switching of haemosporidian parasites in some non-passerine birds. Parasites & Vectors 7, 286.
SchnuteJ. T., BoersN., HaighR., GrandinC., ChabotD., JohnsonA., WesselP., AntonioF., Lewin-KohN. J. and BivandR. (2015). PBSmapping: Mapping Fisheries Data and Spatial Analysis Tools. version 2.68.68. https://cran.r-project.org/web/packages/PBSmapping/index.html
ScordatoE. S. and KardishM. R. (2014). Prevalence and beta diversity in avian malaria communities: host species is a better predictor than geography. Journal of Animal Ecology 83, 13871397.
SoininenJ., McDonaldR. and HillebrandH. (2007). The distance decay of similarity in ecological communities. Ecography 30, 312.
StamatakisA., HooverP. and RougemontJ. (2008). A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology 57, 758771.
Svensson-CoelhoM. and RicklefsR. E. (2011). Host phylogeography and beta diversity in avian haemosporidian (Plasmodiidae) assemblages of the Lesser Antilles. Journal of Animal Ecology 80, 938946.
Svensson-CoelhoM., BlakeJ. G., LoiselleB. A., PenroseA. S., ParkerP. G. and RicklefsR. E. (2013). Diversity, prevalence, and host specificity of avian Plasmodium and Haemoproteus in a Western Amazon assemblage. Ornithological Monographs 76, 147.
TellaJ. L. (2002). The evolutionary transition to coloniality promotes higher blood parasitism in birds. Journal of Evolutionary Biology 15, 3241.
ThieltgesD. W., FergusonM. A. D., JonesC. S., KrakauM., MontaudouinX., NobleR. L., ReiseK. and PoulinR. (2009). Distance decay of similarity among parasite communities of three marine invertebrate hosts. Oecologia 160, 163173.
ValkiūnasG. (2005). Avian Malaria Parasites and other Haemosporidian. CRC Press, Boca Raton, FL, USA.
VinarskiM. V., KoralloN. P., KrasnovB. R., ShenbrotG. I. and PoulinR. (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.
WaldenströmJ., BenschS., KiboiS., HasselquistD. and OttosonU. (2002). Cross-species infection of blood parasites between resident and migratory songbirds in Africa. Molecular Ecology 11, 15451554.
WiensJ. J. (2003). Missing data, incomplete taxa, and phylogenetic accuracy. Systematic Biology 52, 528538.
WiensJ. J. and MorrillM. C. (2011). Missing data in phylogenetic analysis: reconciling results from simulations and empirical data. Systematic Biology 60, 719731.
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Parasitology
  • ISSN: 0031-1820
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