Geographical and host species barriers differentially affect generalist and specialist parasite community structure in a tropical sky-island archipelago

Gupta, Pooja; Vishnudas, C. K.; Ramakrishnan, Uma; Robin, V. V.; Dharmarajan, Guha

doi:10.1098/rspb.2019.0439

Title: Geographical and host species barriers differentially affect generalist and specialist parasite community structure in a tropical sky-island archipelago

Journal Article · 05 June 2019 · Proceedings of the Royal Society B: Biological Sciences

DOI: https://doi.org/10.1098/rspb.2019.0439 · OSTI ID:1819706

^[1]; Vishnudas, C. K. ^[2]; Ramakrishnan, Uma ^[3];

^[2];

^[4]

Univ. of Georgia, Aiken, SC (United States); Univ. of Georgia, Athens, GA (United States)
Indian Inst. of Science Education and Research Tirupati (India)
National Centre for Biological Sciences, Bangalore (India)
Univ. of Georgia, Aiken, SC (United States

Understanding why some parasites emerge in novel host communities while others do not has broad implications for human and wildlife health. In the case of haemosporidian blood parasites, epidemic wild bird mortalities on oceanic islands have been linked to Plasmodium spp., but not genera like Haemoproteus. Indeed, Haemoproteus is absent from many oceanic islands. By contrast, birds on continental islands share long coevolutionary histories with both Plasmodium and Haemoproteus, and are thus ideal model systems to elucidate eco-evolutionary endpoints associated with these parasites in oceanic islands. Here, we examine eco-evolutionary dynamics of avian haemosporidian in the Shola sky-island archipelago of the Western Ghats, India. Our analyses reveal that compared to Plasmodium, Haemoproteus lineages were highly host-specific and diversified via co-speciation with their hosts. We show that community structure of host-generalist Plasmodium was primarily driven by geographical factors (e.g. biogeographic barriers), while that of host-specialist Haemoproteus was driven by host species barriers (e.g. phylogenetic distance). Consequently, a few host species can harbour a high diversity of Plasmodium lineages which, in turn, are capable of infecting multiple host species. Furthermore, these two mechanisms can act in concert to increase the risk of introduction, establishment, and emergence of novel Plasmodium lineages in island systems.

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Research Organization:: Savannah River Site (SRS), Aiken, SC (United States). Savannah River Ecology Lab. (SREL)

Sponsoring Organization:: USDOE

Grant/Contract Number:: FC09-07SR22506

OSTI ID:: 1819706

Journal Information:: Proceedings of the Royal Society B: Biological Sciences, Vol. 286, Issue 1904; ISSN 0962-8452

Publisher:: The Royal Society PublishingCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 22 works

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References (61)

hierfstat, a package for r to compute and test hierarchical F-statistics Goudet, Jerome Molecular Ecology Notes, Vol. 5, Issue 1 https://doi.org/10.1111/j.1471-8286.2004.00828.x	journal	March 2005
Avian host composition, local speciation and dispersal drive the regional assembly of avian malaria parasites in South American birds Fecchio, Alan; Bell, Jeffrey A.; Pinheiro, Rafael B. P. Molecular Ecology, Vol. 28, Issue 10 https://doi.org/10.1111/mec.15094	journal	May 2019
Invasive avian malaria as an emerging parasitic disease in native birds of Peru Marzal, Alfonso; García-Longoria, Luz; Cárdenas Callirgos, Jorge M. Biological Invasions, Vol. 17, Issue 1 https://doi.org/10.1007/s10530-014-0718-x	journal	May 2014
From The Cover: Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community Lips, K. R.; Brem, F.; Brenes, R. Proceedings of the National Academy of Sciences, Vol. 103, Issue 9 https://doi.org/10.1073/pnas.0506889103	journal	February 2006
Evolutionary Relationships, Cospeciation, and Host Switching in Avian Malaria Parasites Ricklefs, Robert E.; Fallon, Sylvia M.; Bermingham, Eldredge Systematic Biology, Vol. 53, Issue 1 https://doi.org/10.1080/10635150490264987	journal	February 2004
Is Avian Malaria Playing a Role in Native Bird Declines in New Zealand? Testing Hypotheses along an Elevational Gradient Niebuhr, Chris N.; Poulin, Robert; Tompkins, Daniel M. PLOS ONE, Vol. 11, Issue 11 https://doi.org/10.1371/journal.pone.0165918	journal	November 2016
Biodiversity hotspots for conservation priorities Myers, Norman; Mittermeier, Russell A.; Mittermeier, Cristina G. Nature, Vol. 403, Issue 6772 https://doi.org/10.1038/35002501	journal	February 2000
Impact of the repurposed drug thonzonium bromide on host oral-gut microbiomes Simon-Soro, Aurea; Kim, Dongyeop; Li, Yong npj Biofilms and Microbiomes, Vol. 7, Issue 1 https://doi.org/10.1038/s41522-020-00181-5	journal	January 2021
Ecological replacement of native red squirrels by invasive greys driven by disease Tompkins, D. M.; White, A. R.; Boots, M. Ecology Letters, Vol. 6, Issue 3 https://doi.org/10.1046/j.1461-0248.2003.00417.x	journal	March 2003
Climate variation influences host specificity in avian malaria parasites Fecchio, Alan; Wells, Konstans; Bell, Jeffrey A. Ecology Letters, Vol. 22, Issue 3 https://doi.org/10.1111/ele.13215	journal	January 2019
A General Coefficient of Similarity and Some of Its Properties Gower, J. C. Biometrics, Vol. 27, Issue 4 https://doi.org/10.2307/2528823	journal	December 1971
Host associations and evolutionary relationships of avian blood parasites from West Africa Beadell, Jon S.; Covas, Rita; Gebhard, Christina International Journal for Parasitology, Vol. 39, Issue 2 https://doi.org/10.1016/j.ijpara.2008.06.005	journal	January 2009
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 Olsson-Pons, Sophie; Clark, Nicholas J.; Ishtiaq, Farah Journal of Animal Ecology, Vol. 84, Issue 4 https://doi.org/10.1111/1365-2656.12354	journal	March 2015
Host specificity in phylogenetic and geographic space Poulin, Robert; Krasnov, Boris R.; Mouillot, David Trends in Parasitology, Vol. 27, Issue 8 https://doi.org/10.1016/j.pt.2011.05.003	journal	August 2011
Latitudinal gradients in niche breadth: empirical evidence from haematophagous ectoparasites Krasnov, Boris R.; Shenbrot, Georgy I.; Khokhlova, Irina S. Journal of Biogeography, Vol. 35, Issue 4 https://doi.org/10.1111/j.1365-2699.2007.01800.x	journal	April 2008
A review of global diversity in avian haemosporidians (Plasmodium and Haemoproteus: Haemosporida): new insights from molecular data Clark, Nicholas J.; Clegg, Sonya M.; Lima, Marcos R. International Journal for Parasitology, Vol. 44, Issue 5 https://doi.org/10.1016/j.ijpara.2014.01.004	journal	April 2014
The global biogeography of avian haemosporidian parasites is characterized by local diversification and intercontinental dispersal Ellis, Vincenzo A.; Sari, Eloisa H. R.; Rubenstein, Dustin R. Parasitology, Vol. 146, Issue 2 https://doi.org/10.1017/S0031182018001130	journal	July 2018
Disease Ecology Meets Ecosystem Science Preston, Daniel L.; Mischler, John A.; Townsend, Alan R. Ecosystems, Vol. 19, Issue 4 https://doi.org/10.1007/s10021-016-9965-2	journal	February 2016
Low Haemosporidian Diversity and one Key-Host Species in a bird Malaria Community on a Mid-Atlantic Island (sÃo Miguel, Azores) Hellgren, Olof; Križanauskienė, Asta; Hasselquist, Dennis Journal of Wildlife Diseases, Vol. 47, Issue 4 https://doi.org/10.7589/0090-3558-47.4.849	journal	October 2011
Diversity, Prevalence, and Host Specificity of Avian Plasmodium and Haemoproteus in a Western Amazon Assemblage Svensson-Coelho, Maria; Blake, John G.; Loiselle, Bette A. Ornithological Monographs, Vol. 76, Issue 1 https://doi.org/10.1525/om.2013.76.1.1	journal	June 2013
Multiple regression on distance matrices: a multivariate spatial analysis tool Lichstein, Jeremy W. Plant Ecology, Vol. 188, Issue 2 https://doi.org/10.1007/s11258-006-9126-3	journal	March 2006
EltonTraits 1.0: Species-level foraging attributes of the world's birds and mammals Wilman, Hamish; Belmaker, Jonathan; Simpson, Jennifer Ecology, Vol. 95, Issue 7 https://doi.org/10.1890/13-1917.1	journal	July 2014
The mean and variance of phylogenetic diversity under rarefaction Nipperess, David A.; Matsen, Frederick A. Methods in Ecology and Evolution, Vol. 4, Issue 6 https://doi.org/10.1111/2041-210X.12042	journal	April 2013
MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages Bensch, Staffan; Hellgren, Olof; PÉRez-Tris, Javier Molecular Ecology Resources, Vol. 9, Issue 5 https://doi.org/10.1111/j.1755-0998.2009.02692.x	journal	September 2009
Plasmodium relictum (lineage P-SGS1): Effects on experimentally infected passerine birds Palinauskas, Vaidas; Valkiūnas, Gediminas; Bolshakov, Casimir V. Experimental Parasitology, Vol. 120, Issue 4 https://doi.org/10.1016/j.exppara.2008.09.001	journal	December 2008
Species formation by host shifting in avian malaria parasites Ricklefs, R. E.; Outlaw, D. C.; Svensson-Coelho, M. Proceedings of the National Academy of Sciences, Vol. 111, Issue 41 https://doi.org/10.1073/pnas.1416356111	journal	September 2014
Niche breadth predicts geographical range size: a general ecological pattern Slatyer, Rachel A.; Hirst, Megan; Sexton, Jason P. Ecology Letters, Vol. 16, Issue 8 https://doi.org/10.1111/ele.12140	journal	June 2013
PACo: A Novel Procrustes Application to Cophylogenetic Analysis Balbuena, Juan Antonio; Míguez-Lozano, Raúl; Blasco-Costa, Isabel PLoS ONE, Vol. 8, Issue 4 https://doi.org/10.1371/journal.pone.0061048	journal	April 2013
Phylogenetic uniqueness, not latitude, explains the diversity of avian blood parasite communities worldwide Clark, Nicholas J. Global Ecology and Biogeography, Vol. 27, Issue 6 https://doi.org/10.1111/geb.12741	journal	April 2018
What do Interaction Network Metrics tell us About Specialization and Biological Traits Blüthgen, Nico; Fründ, Jochen; Vázquez, Diego P. Ecology, Vol. 89, Issue 12 https://doi.org/10.1890/07-2121.1	journal	December 2008
Prevalence and Diversity of Avian Hematozoan Parasites in Asia: a Regional Survey Ishtiaq, Farah; Gering, Eben; Rappole, Jon H. Journal of Wildlife Diseases, Vol. 43, Issue 3 https://doi.org/10.7589/0090-3558-43.3.382	journal	July 2007
ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R Paradis, Emmanuel; Schliep, Klaus Bioinformatics, Vol. 35, Issue 3 https://doi.org/10.1093/bioinformatics/bty633	journal	July 2018
Deep and wide valleys drive nested phylogeographic patterns across a montane bird community Robin, V. V.; Vishnudas, C. K.; Gupta, Pooja Proceedings of the Royal Society B: Biological Sciences, Vol. 282, Issue 1810 https://doi.org/10.1098/rspb.2015.0861	journal	July 2015
Complexity of multitrophic interactions in a grassland ecosystem depends on plant species diversity: Plant diversity and multitrophic interactions Rzanny, Michael; Voigt, Winfried Journal of Animal Ecology, Vol. 81, Issue 3 https://doi.org/10.1111/j.1365-2656.2012.01951.x	journal	January 2012
Haemoproteus minutus is highly virulent for Australasian and South American parrots Ortiz-Catedral, Luis; Brunton, Dianne; Stidworthy, Mark F. Parasites & Vectors, Vol. 12, Issue 1 https://doi.org/10.1186/s13071-018-3255-0	journal	January 2019
Exploring the Phylogenetic Structure of Ecological Communities: An Example for Rain Forest Trees Webb, Campbell O. The American Naturalist, Vol. 156, Issue 2 https://doi.org/10.1086/303378	journal	August 2000
Seasonal dynamics in mosquito abundance and temperature do not influence avian malaria prevalence in the Himalayan foothills Ishtiaq, Farah; Bowden, Christopher G. R.; Jhala, Yadvendradev V. Ecology and Evolution, Vol. 7, Issue 19 https://doi.org/10.1002/ece3.3319	journal	September 2017
Ancient Geographical Gaps and Paleo-Climate Shape the Phylogeography of an Endemic Bird in the Sky Islands of Southern India Robin, V. V.; Sinha, Anindya; Ramakrishnan, Uma PLoS ONE, Vol. 5, Issue 10 https://doi.org/10.1371/journal.pone.0013321	journal	October 2010
Molecular characterisation of haemoparasites in forest birds from Robinson Crusoe Island: Is the Austral Thrush a potential threat to endemic birds? MartÍNez, Javier; VÁSquez, Rodrigo A.; Venegas, Cristobal Bird Conservation International, Vol. 25, Issue 2 https://doi.org/10.1017/S0959270914000227	journal	August 2014
Human drivers of ecological and evolutionary dynamics in emerging and disappearing infectious disease systems Rogalski, Mary A.; Gowler, Camden D.; Shaw, Clara L. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 372, Issue 1712 https://doi.org/10.1098/rstb.2016.0043	journal	January 2017
Host Specialization and Geographic Localization of Avian Malaria Parasites: A Regional Analysis in the Lesser Antilles Fallon, Sylvia M.; Bermingham, Eldredge; Ricklefs, Robert E. The American Naturalist, Vol. 165, Issue 4 https://doi.org/10.1086/428430	journal	April 2005
Two new genera of songbirds represent endemic radiations from the Shola Sky Islands of the Western Ghats, India Robin, V. V.; Vishnudas, C. K.; Gupta, Pooja BMC Evolutionary Biology, Vol. 17, Issue 1 https://doi.org/10.1186/s12862-017-0882-6	journal	January 2017
Host community similarity and geography shape the diversity and distribution of haemosporidian parasites in Amazonian birds Fecchio, A.; Pinheiro, R.; Felix, G. Ecography, Vol. 41, Issue 3 https://doi.org/10.1111/ecog.03058	journal	May 2017
Description, molecular characterisation, diagnostics and life cycle of Plasmodium elongatum (lineage pERIRUB01), the virulent avian malaria parasite Palinauskas, Vaidas; Žiegytė, Rita; Iezhova, Tatjana A. International Journal for Parasitology, Vol. 46, Issue 11 https://doi.org/10.1016/j.ijpara.2016.05.005	journal	October 2016
Jane: a new tool for the cophylogeny reconstruction problem Conow, Chris; Fielder, Daniel; Ovadia, Yaniv Algorithms for Molecular Biology, Vol. 5, Issue 1 https://doi.org/10.1186/1748-7188-5-16	journal	January 2010
The mean and variance of phylogenetic diversity under rarefaction Nipperess, David A.; Matsen, Frederick A. arXiv https://doi.org/10.48550/arxiv.1208.6552	preprint	January 2012
Human-modified landscapes narrow the isotopic niche of neotropical birds Navarro, Ana Beatriz; Magioli, Marcelo; Bogoni, Juliano André Oecologia, Vol. 196, Issue 1 https://doi.org/10.1007/s00442-021-04908-9	journal	April 2021
The Role of Introduced Diseases in the Extinction of the Endemic Hawaiian Avifauna Warner, Richard E. The Condor, Vol. 70, Issue 2 https://doi.org/10.2307/1365954	journal	April 1968
Haemoproteus minutus is highly virulent for Australasian and South American parrots. Ortiz-Catedral, Luis; Brunton, Dianne; Stidworthy, Mark F. BioMed Central https://doi.org/10.7892/boris.140644	text	January 2019
MrBayes 3: Bayesian phylogenetic inference under mixed models Ronquist, Fredrik; Huelsenbeck, John P. Bioinformatics, Vol. 19, Issue 12, p. 1572-1574 https://doi.org/10.1093/bioinformatics/btg180	journal	August 2003
Parasites and biological invasions: parallels, interactions, and control Dunn, Alison M.; Hatcher, Melanie J. Trends in Parasitology, Vol. 31, Issue 5 https://doi.org/10.1016/j.pt.2014.12.003	journal	May 2015
Establishment of exotic parasites: the origins and characteristics of an avian malaria community in an isolated island avifauna Ewen, John G.; Bensch, Staffan; Blackburn, Tim M. Ecology Letters, Vol. 15, Issue 10 https://doi.org/10.1111/j.1461-0248.2012.01833.x	journal	July 2012
Avian malaria in New Zealand Schoener, Er; Banda, M.; Howe, L. New Zealand Veterinary Journal, Vol. 62, Issue 4 https://doi.org/10.1080/00480169.2013.871195	journal	February 2014
Diversification by host switching and dispersal shaped the diversity and distribution of avian malaria parasites in Amazonia Fecchio, Alan; Bell, Jeffrey Andrew; Collins, Michael David Oikos, Vol. 127, Issue 9 https://doi.org/10.1111/oik.05115	journal	March 2018
Host shift and cospeciation rate estimation from co-phylogenies Alcala, Nicolas; Jenkins, Tania; Christe, Philippe Ecology Letters, Vol. 20, Issue 8 https://doi.org/10.1111/ele.12799	journal	June 2017
Picante: R tools for integrating phylogenies and ecology Kembel, S. W.; Cowan, P. D.; Helmus, M. R. Bioinformatics, Vol. 26, Issue 11 https://doi.org/10.1093/bioinformatics/btq166	journal	April 2010
Preferential Host Switching by Primate Lentiviruses Can Account for Phylogenetic Similarity with the Primate Phylogeny Charleston, M. A.; Robertson, D. L. Systematic Biology, Vol. 51, Issue 3 https://doi.org/10.1080/10635150290069940	journal	May 2002
Hosts as Islands Kuris, Armand M.; Blaustein, Andrew R.; Alio, Jose Javier The American Naturalist, Vol. 116, Issue 4 https://doi.org/10.1086/283647	journal	October 1980
A parameter-adaptive dynamic programming approach for inferring cophylogenies Merkle, Daniel; Middendorf, Martin; Wieseke, Nicolas BMC Bioinformatics, Vol. 11, Issue S1 https://doi.org/10.1186/1471-2105-11-S1-S60	journal	January 2010
Discovering potential sources of emerging pathogens: South America is a reservoir of generalist avian blood parasites Moens, Michaël A. J.; Pérez-Tris, Javier International Journal for Parasitology, Vol. 46, Issue 1 https://doi.org/10.1016/j.ijpara.2015.08.001	journal	January 2016
Host phylogeography and beta diversity in avian haemosporidian (Plasmodiidae) assemblages of the Lesser Antilles: Haemospordian beta diversity and host phylogeography Svensson-Coelho, Maria; Ricklefs, Robert E. Journal of Animal Ecology, Vol. 80, Issue 5 https://doi.org/10.1111/j.1365-2656.2011.01837.x	journal	March 2011

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59 BASIC BIOLOGICAL SCIENCES
avian
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India

Supplementary material from "Geographical and host species barriers differentially affect generalist and specialist parasite community structure in a tropical sky-island archipelago" Gupta, Pooja; Vishnudas, C. K.; Ramakrishnan, Uma https://doi.org/10.6084/m9.figshare.c.4509134.v2 The current record is supplemented by this collection	collection	January 2019
Supplementary material from "Geographical and host species barriers differentially affect generalist and specialist parasite community structure in a tropical sky-island archipelago" Gupta, Pooja; Vishnudas, C. K.; Ramakrishnan, Uma https://doi.org/10.6084/m9.figshare.c.4509134.v1 The current record is supplemented by this collection	collection	January 2019
Laboratory and statistical methods from Geographical and host species barriers differentially affect generalist and specialist parasite community structure in a tropical sky-island archipelago. Gupta, Pooja; Vishnudas, C. K.; Ramakrishnan, Uma https://doi.org/10.6084/m9.figshare.8144465.v2 The current record is supplemented by this text	text	January 2019
Laboratory and statistical methods from Geographical and host species barriers differentially affect generalist and specialist parasite community structure in a tropical sky-island archipelago Gupta, Pooja; Vishnudas, C. K.; Ramakrishnan, Uma https://doi.org/10.6084/m9.figshare.8144465.v1 The current record is supplemented by this text	text	January 2019
Parasite Lineage data from Geographical and host species barriers differentially affect generalist and specialist parasite community structure in a tropical sky-island archipelago. Gupta, Pooja; Vishnudas, C. K.; Ramakrishnan, Uma https://doi.org/10.6084/m9.figshare.8144462.v2 The current record is supplemented by this dataset	dataset	January 2019
Parasite Lineage data from Geographical and host species barriers differentially affect generalist and specialist parasite community structure in a tropical sky-island archipelago. Gupta, Pooja; Vishnudas, C. K.; Ramakrishnan, Uma https://doi.org/10.6084/m9.figshare.8144462 The current record is supplemented by this dataset	dataset	January 2019
Laboratory and statistical methods from Geographical and host species barriers differentially affect generalist and specialist parasite community structure in a tropical sky-island archipelago. Gupta, Pooja; Vishnudas, C. K.; Ramakrishnan, Uma https://doi.org/10.6084/m9.figshare.8144465 The current record is supplemented by this text	text	January 2019
Tables and Figures from Geographical and host species barriers differentially affect generalist and specialist parasite community structure in a tropical sky-island archipelago. Gupta, Pooja; Vishnudas, C. K.; Ramakrishnan, Uma https://doi.org/10.6084/m9.figshare.8144459 The current record is supplemented by this text	text	January 2019
Tables and Figures from Geographical and host species barriers differentially affect generalist and specialist parasite community structure in a tropical sky-island archipelago. Gupta, Pooja; Vishnudas, C. K.; Ramakrishnan, Uma https://doi.org/10.6084/m9.figshare.8144459.v2 The current record is supplemented by this text	text	January 2019
Tables and Figures from Geographical and host species barriers differentially affect generalist and specialist parasite community structure in a tropical sky-island archipelago Gupta, Pooja; Vishnudas, C. K.; Ramakrishnan, Uma https://doi.org/10.6084/m9.figshare.8144459.v1 The current record is supplemented by this text	text	January 2019

Title: Geographical and host species barriers differentially affect generalist and specialist parasite community structure in a tropical sky-island archipelago

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