Hostname: page-component-8448b6f56d-42gr6 Total loading time: 0 Render date: 2024-04-18T22:54:49.943Z Has data issue: false hasContentIssue false
  • English
  • Français

Assessing the diversity, host-specificity and infection patterns of apicomplexan parasites in reptiles from Oman, Arabia

Published online by Cambridge University Press:  09 September 2016

JOÃO P. MAIA Open the ORCID record for JOÃO P. MAIA [Opens in a new window] ,
D. JAMES HARRIS ,
SALVADOR CARRANZA  and
ELENA GOMÉZ-DÍAZ
JOÃO P. MAIA*
Affiliation:
CIBIO Research Centre in Biodiversity and Genetic Resources, InBIO, Universidade do Porto, Campus Agrário de Vairão, Rua Padre Armando Quintas, N°7, 4485-661 Vairão, Vila do Conde, Portugal Departamento de Biologia, Faculdade de Ciências, Universidade do Porto, Rua do Campo Alegre FC4 4169-007 Porto, Portugal Institute of Evolutionary Biology (CSIC-Universitat Pompeu Fabra). Passeig Maritim de la Barceloneta, 37-49. 08003 Barcelona, Spain
D. JAMES HARRIS
Affiliation:
CIBIO Research Centre in Biodiversity and Genetic Resources, InBIO, Universidade do Porto, Campus Agrário de Vairão, Rua Padre Armando Quintas, N°7, 4485-661 Vairão, Vila do Conde, Portugal Departamento de Biologia, Faculdade de Ciências, Universidade do Porto, Rua do Campo Alegre FC4 4169-007 Porto, Portugal
SALVADOR CARRANZA
Affiliation:
Institute of Evolutionary Biology (CSIC-Universitat Pompeu Fabra). Passeig Maritim de la Barceloneta, 37-49. 08003 Barcelona, Spain
ELENA GOMÉZ-DÍAZ*
Affiliation:
Department of Wetland Ecology, Estación Biológica de Doñana (EBD-CSIC), 41080 Sevilla, Spain
*
*Corresponding authors: Department of Wetland Ecology, Estación Biológica de Doñana (EBD-CSIC), 41080 Sevilla, Spain. E-mail: elena.gomez@ebd.csic.es and CIBIO Research Centre in Biodiversity and Genetic Resources, InBIO, Universidade do Porto, Campus Agrário de Vairão, Rua Padre Armando Quintas, N°7, 4485-661 Vairão, Vila do Conde, Portugal. E-mail: jpmaiapt@gmail.com
*Corresponding authors: Department of Wetland Ecology, Estación Biológica de Doñana (EBD-CSIC), 41080 Sevilla, Spain. E-mail: elena.gomez@ebd.csic.es and CIBIO Research Centre in Biodiversity and Genetic Resources, InBIO, Universidade do Porto, Campus Agrário de Vairão, Rua Padre Armando Quintas, N°7, 4485-661 Vairão, Vila do Conde, Portugal. E-mail: jpmaiapt@gmail.com
Get access Rights & Permissions [Opens in a new window]

Summary

Understanding the processes that shape parasite diversification, their distribution and abundance provides valuable information on the dynamics and evolution of disease. In this study, we assessed the diversity, distribution, host-specificity and infection patterns of apicomplexan parasites in amphibians and reptiles from Oman, Arabia. Using a quantitative PCR approach we detected three apicomplexan parasites (haemogregarines, lankesterellids and sarcocystids). A total of 13 haemogregarine haplotypes were identified, which fell into four main clades in a phylogenetic framework. Phylogenetic analysis of six new lankesterellid haplotypes revealed that these parasites were distinct from, but phylogenetically related to, known Lankesterella species and might represent new taxa. The percentage of infected hosts (prevalence) and the number of haemogregarines in the blood (parasitaemia) varied significantly between gecko species. We also found significant differences in parasitaemia between haemogregarine parasite lineages (defined by phylogenetic clustering of haplotypes), suggesting differences in host–parasite compatibility between these lineages. For Pristurus rupestris, we found significant differences in haemogregarine prevalence between geographical areas. Our results suggest that host ecology and host relatedness may influence haemogregarine distributions and, more generally, highlight the importance of screening wild hosts from remote regions to provide new insights into parasite diversity.

Keywords

Haemogregarineeimeriorinaamphibianhost–parasite associationsecologyaltitudehost relatednessprevalenceintensityparasitaemia
Type
Research Article
Information
Parasitology , Volume 143 , Issue 13 , November 2016 , pp. 1730 - 1747
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

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

Abd-Al-Aal, Z. (1998). Light and electron microscopic studies on gamogony of Sarcocystis sp.(Apicomplexa: Sarcocystidae) infecting the snake Lytorhynchus diadema . Egyptian German Society of Zoology 26, 231–238.Google Scholar
Abdel-Baki, A. S., Abdel-Haleem, H. M. and Al-Quraishy, S. (2012). A new Sarcocystis species (Apicomplexa: Sarcocystidae) from the rock gecko Bunopus tuberculatus in Saudi Arabia. Journal of Parasitology 98, 951–953.CrossRefGoogle ScholarPubMed
Abdel-Baki, A.-A. S., Al-Quraishy, S. and Zhang, J. Y. (2014). Redescription of Haemogregarina garnhami (Apicomplexa: Adeleorina) from the blood of Psammophis schokari (Serpentes: Colubridae) as Hepatozoon garnhami n. comb. based on molecular, morphometric and morphologic characters. Acta parasitologica, 59, 294–300.CrossRefGoogle ScholarPubMed
Abdel-Ghaffar, F., Bashtar, A.-R., Al-Quraishy, S., Al Nasr, I. and Mehlhorn, H. (2009). Sarcocystis infecting reptiles in Saudi Arabia: 1--Light and electron microscopic study on Sarcocysts of Sarcocystis turcicii sp. nov. infecting the gecko Hemidactylus turcicus Linnaeus. Parasitology Research 104, 503–508.CrossRefGoogle ScholarPubMed
Al-Farraj, S. (2008). Light and electron microscopic study on a haemogregarine species infecting the viper Cerastes cerastes gasperitti from Saudi Arabia. Pakistan Journal of Biological Sciences 11, 1414–1421.CrossRefGoogle ScholarPubMed
Atkinson, C. T., Utzurrum, R. B., Lapointe, D. A., Camp, R. J., Crampton, L. H., Foster, J. T. and Giambelluca, T. W. (2014). Changing climate and the altitudinal range of avian malaria in the Hawaiian Islands – an ongoing conservation crisis on the island of Kaua'i. Global Change Biology 20, 2426–2436.CrossRefGoogle ScholarPubMed
Badiane, A., Garcia-Porta, J., Červenka, J., Kratochvíl, L., Sindaco, R., Robinson, M. D., Morales, H., Mazuch, T., Price, T., Amat, F., Shobrak, M. Y., Wilms, T., Simó-Riudalbas, M., Ahmadzadeh, F., Papenfuss, T. J., Cluchier, A., Viglione, J. and Carranza, S. (2014). Phylogenetic relationships of Semaphore geckos (Squamata: Sphaerodactylidae: Pristurus) with an assessment of the taxonomy of Pristurus rupestris . Zootaxa 3835, 33–58.CrossRefGoogle ScholarPubMed
Barta, J. R., Ogedengbe, J. D., Martin, D. S. and Smith, T. G. (2012). Phylogenetic position of the adeleorinid coccidia (Myzozoa, Apicomplexa, Coccidia, Eucoccidiorida, Adeleorina) inferred using 18S rDNA sequences. Journal of Eukaryotic Microbiology 59, 171–180.CrossRefGoogle ScholarPubMed
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 of London B: Biological Sciences 267, 1583–1589.CrossRefGoogle ScholarPubMed
Bødker, R., Akida, J., Shayo, D., Kisinza, W., Msangeni, H. A., Pedersen, E. M. and Lindsay, S. W. (2003). Relationship between altitude and intensity of Malaria transmission in the Usambara Mountains, Tanzania. Journal of Medical Entomology 40, 706–717.CrossRefGoogle ScholarPubMed
Camargo, A., Sinervo, B. and Sites, J. W. (2010). Lizards as model organisms for linking phylogeographic and speciation studies. Molecular Ecology 19, 3250–3270.CrossRefGoogle ScholarPubMed
Carranza, S. and Arnold, E. N. (2012). A review of the geckos of the genus Hemidactylus (Squamata: Gekkonidae) from Oman based on morphology, mitochondrial and nuclear data, with descriptions of eight new species. Zootaxa 3378, 1–95.CrossRefGoogle Scholar
Clayton, D. H., Tamimi, S. A. and Johnson, K. P. (2003). The ecological basis of coevolutionary history. In Tangled Trees: Phylogeny, Cospeciation and Coevolution (ed. Page, R. D. M.), pp. 310–341. University of Chicago Press, Chicago, London.Google Scholar
Cox, N. A., Mallon, D., Bowles, P., Els, J. and Tognelli, M. F. (2012). The Conservation Status and Distribution of Reptiles of the Arabian Peninsula. IUCN, Cambridge, UK/Gland, Switzerland and Environment and Protected Areas Authority, Sharjah, UAE.Google Scholar
De León, G. P.-P. and Choudhury, A. (2005). Biogeography of helminth parasites of freshwater fishes in Mexico: the search for patterns and processes. Journal of Biogeography 32, 645–659.CrossRefGoogle Scholar
de Pous, P., Machado, L., Metallinou, M., Červenka, J., Kratochvíl, L., Paschou, N., Mazuch, T., Šmíd, J., Simó-Riudalbas, M., Sanuy, D. and Carranza, S. (2016). Taxonomy and biogeography of Bunopus spatalurus (Reptilia; Gekkonidae) from the Arabian Peninsula. Journal of Zoological Systematics and Evolutionary Research 54, 67–81.CrossRefGoogle Scholar
du Toit, N., van Vuuren, B. J., Matthee, S. and Matthee, C. A. (2013). Biogeography and host-related factors trump parasite life history: limited congruence among the genetic structures of specific ectoparasitic lice and their rodent hosts. Molecular Ecology 22, 5185–5204.CrossRefGoogle ScholarPubMed
Eisen, R. J. and Wright, N. M. (2001). Landscape features associated with infection by a malaria parasite (Plasmodium mexicanum) and the importance of multiple scale studies. Parasitology 122, 507–513.CrossRefGoogle ScholarPubMed
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. The American Naturalist 165, 466–480.CrossRefGoogle ScholarPubMed
Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783–791.CrossRefGoogle ScholarPubMed
Gardner, A. S. (2009). Mapping the terrestrial reptile distributions in Oman and the United Arab Emirates. ZooKeys 31, 165–177.CrossRefGoogle Scholar
Gardner, A. S. (2013). The Amphibians and Reptiles of Oman and the UAE. Edition Chimaira, Frankfurt am Main. 480 p.Google Scholar
Harris, D. J., Borges-Nojosa, D. M. and Maia, J. P. (2015). Prevalence and diversity of Hepatozoon in Native and Exotic Geckos from Brazil. Journal of Parasitology 101, 80–85.CrossRefGoogle ScholarPubMed
Huelsenbeck, J. P., Rannala, B. (2004). Frequentist properties of Bayesian posterior probabilities of phylogenetic trees under simple and complex substitution models. Systematic Biology 53, 904–913.CrossRefGoogle ScholarPubMed
Huelsenbeck, J. P. and Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.CrossRefGoogle ScholarPubMed
Ishtiaq, F., Guillaumot, L., Clegg, S. M., Phillimore, A. B., Black, R. A., Owens, I. P. F., Mundy, N. I. and Sheldon, B. C. (2008). Avian haematozoan parasites and their associations with mosquitoes across Southwest Pacific Islands. Molecular Ecology 17, 4545–4555.CrossRefGoogle ScholarPubMed
Kamiya, T., O'Dwyer, K., Nakagawa, S. and Poulin, R. (2014). Host diversity drives parasite diversity: meta-analytical insights into patterns and causal mechanisms. Ecography 37, 689–697.CrossRefGoogle Scholar
Klein, S. L. (2004). Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunology 26, 247–264.CrossRefGoogle ScholarPubMed
Krasnov, B. R., Shenbrot, G. I., Mouillot, D., Khokhlova, I. S. and Poulin, R. (2006). Ecological characteristics of flea species relate to their suitability as plague vectors. Oecologia 149, 474–481.CrossRefGoogle ScholarPubMed
Lafferty, K. D. (2012). Biodiversity loss decreases parasite diversity: theory and patterns. Philosophical Transactions of the Royal Society B: Biological Sciences 367, 2814–2827.CrossRefGoogle ScholarPubMed
Librado, P. and Rozas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics (Oxford, England) 25, 1451–1452.Google ScholarPubMed
Lindström, K. M., Foufopoulos, J., Pärn, H. and Wikelski, M. (2004). Immunological investments reflect parasite abundance in island populations of Darwin's finches. Proceedings of the Royal Society of London B: Biological Sciences 271, 1513–1519.CrossRefGoogle ScholarPubMed
Maia, J. P., Harris, D. J., Carranza, S. and Gómez-Díaz, E. (2014). A comparison of multiple methods for estimating parasitemia of Hemogregarine Hemoparasites (Apicomplexa: Adeleorina) and its application for studying infection in natural populations. PLoS ONE 9, e95010.CrossRefGoogle ScholarPubMed
Mallon, D. P. (2011). Global hotspots in the Arabian Peninsula. Zoology in the Middle East 54, 13–20.CrossRefGoogle Scholar
Megía-Palma, R., Martínez, J. and Merino, S. (2013). Phylogenetic analysis based on 18S rRNA gene sequences of Schellackia parasites (Apicomplexa: Lankesterellidae) reveals their close relationship to the genus Eimeria . Parasitology 140, 1149–1157.CrossRefGoogle Scholar
Megía-Palma, R., Martínez, J. and Merino, S. (2014). Molecular characterization of haemococcidia genus Schellackia (Apicomplexa) reveals the polyphyletic origin of the family Lankesterellidae. Zoologica Scripta 43, 304–312.CrossRefGoogle Scholar
Metallinou, M. and Carranza, S. (2013). New species of Stenodactylus (Squamata: Gekkonidae) from the Sharqiyah Sands in northeastern Oman. Zootaxa 3745, 449–468.Google ScholarPubMed
Metallinou, M., Červenka, J., Crochet, P.-A., Kratochvíl, L., Wilms, T., Geniez, P., Shobrak, M. Y., Brito, J. C. and Carranza, S. (2015). Species on the rocks: systematics and biogeography of the rock-dwelling Ptyodactylus geckos (Squamata: Phyllodactylidae) in North Africa and Arabia. Molecular Phylogenetics and Evolution 85, 208–220.CrossRefGoogle ScholarPubMed
Morand, S. and Poulin, R. (2003). Phylogenies, the comparative method and parasite evolutionary ecology. Advances in Parasitology 54, 281–302.CrossRefGoogle ScholarPubMed
Morrison, D. A. (2009). Evolution of the Apicomplexa: where are we now? Trends in Parasitology 25, 375–382.CrossRefGoogle ScholarPubMed
Nieberding, C. M., Durette-Desset, M. C., Vanderpoorten, A., Casanova, J. C., Ribas, A., Deffontaine, V., Feliu, C., Morand, S., Libois, R. and Michaux, J. R. (2008). Geography and host biogeography matter for understanding the phylogeography of a parasite. Molecular Phylogenetics and Evolution 47, 538–554.CrossRefGoogle ScholarPubMed
O'Dwyer, L. H., Moço, T. C., Barrella, T. H., Vilela, F. C. and Silva, R. J. (2003). Prevalence of Hepatozoon spp. (Apicomplexa, Hepatozoidae) among recently captured Brazilian snakes. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 55, 309–314.CrossRefGoogle Scholar
O'Dwyer, L. H., Moço, T. C., Paduan, K. D. S., Spenassatto, C., da Silva, R. J. and Ribolla, P. E. M. (2013). Description of three new species of Hepatozoon (Apicomplexa, Hepatozoidae) from Rattlesnakes (Crotalus durissus terrificus) based on molecular, morphometric and morphologic characters. Experimental Parasitology 135, 200–207.CrossRefGoogle ScholarPubMed
Posada, D. (2008). jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.CrossRefGoogle ScholarPubMed
Poulin, R. (2005). Relative infection levels and taxonomic distances among the host species used by a parasite: insights into parasite specialization. Parasitology 130, 109–115.CrossRefGoogle ScholarPubMed
Poulin, R. (2006). Variation in infection parameters among populations within parasite species: intrinsic properties versus local factors. International Journal for Parasitology 36, 877–885.CrossRefGoogle ScholarPubMed
Poulin, R. (2011). The many roads to parasitism: a tale of convergence. Advances in Parasitology 74, 1–40.CrossRefGoogle ScholarPubMed
Poulin, R. and Mouillot, D. (2005). Combining phylogenetic and ecological information into a new index of host specificity. Journal of Parasitology 91, 511–514.CrossRefGoogle ScholarPubMed
Poulin, R., Krasnov, B. R. and Mouillot, D. (2011). Host specificity in phylogenetic and geographic space. Trends in Parasitology 27, 355–361.CrossRefGoogle ScholarPubMed
Ricklefs, R., Fallon, S. and Bermingham, E. (2004). Evolutionary relationships, cospeciation, and host switching in Avian Malaria Parasites. Systematic Biology 53, 111–119.CrossRefGoogle ScholarPubMed
Ricklefs, R. E., Outlaw, D. C., Svensson-Coelho, M., Medeiros, M. C. I., Ellis, V. A., and Latta, S. (2014). Species formation by host shifting in avian malaria parasites. Proceedings of the National Academy of Sciences of the United States of America 111, 14816–14821.CrossRefGoogle ScholarPubMed
Ruijter, J. M., Ramakers, C., Hoogaars, W. M. H., Karlen, Y., Bakker, O., van den Hoff, M. J. B. and Moorman, A. F. M. (2009). Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Research 37, e45.CrossRefGoogle ScholarPubMed
Sambrook, J., Fritsch, E. F. and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Press, New York, 545 p.Google Scholar
Schall, J. J. (1992). Parasite-mediated competition in Anolis lizards. Oecologia 92, 58–64.CrossRefGoogle ScholarPubMed
Schall, J. J. and Vogt, S. P. (1993). Distribution of malaria in Anolis lizards of the Luquillo Forest, Puerto Rico: implications for host community ecology. Biotropica 25, 229–235.CrossRefGoogle Scholar
Šmíd, J., Martínez, G., Gebhart, J., Aznar, J., Gállego, J., Göçmen, B., De Pous, P., Tamar, K. and Carranza, S. (2015). Phylogeny of the genus Rhynchocalamus (Reptilia; Colubridae) with a first record from the Sultanate of Oman. Zootaxa 4033, 380–392.CrossRefGoogle ScholarPubMed
Smith, T. G. (1996). The genus Hepatozoon (Apicomplexa: Adeleina). Journal of Parasitology 82, 565–585.CrossRefGoogle ScholarPubMed
Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690.CrossRefGoogle ScholarPubMed
Stekolnikov, A. A., Carranza, S. and Gomez-diaz, E. (2012). A new genus and species of Apoloniinae (Acari: Trombiculidae) from Oman. Zootaxa 3499, 74–80.CrossRefGoogle Scholar
Tamar, K., Scholz, S., Crochet, P. A., Geniez, P., Meiri, S., Schmitz, A., Wilms, T. and Carranza, S. (2016). Evolution around the red sea: systematics and biogeography of the agamid genus Pseudotrapelus (Squamata: Agamidae) from North Africa and Arabia. Molecular Phylogenetics and Evolution 97, 55–68.CrossRefGoogle ScholarPubMed
Tamura, K., Stecher, G., Peterson, D., Filipski, A. and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.CrossRefGoogle ScholarPubMed
Tanga, M. C., Ngundu, W. I., Judith, N., Mbuh, J., Tendongfor, N., Simard, F. and Wanji, S. (2010). Climate change and altitudinal structuring of malaria vectors in south-western Cameroon: their relation to malaria transmission. Transactions of the Royal Society of Tropical Medicine and Hygiene 104, 453–460.CrossRefGoogle ScholarPubMed
Tomé, B., Rato, C., Perera, A. and Harris, D. J. (2016). High diversity of Hepatozoon spp. in geckos of the genus Tarentola . Journal of Parasitology 102, 476–480.CrossRefGoogle ScholarPubMed
Ujvari, B., Madsen, T. and Olsson, M. (2004). High prevalence of Hepatozoon spp. (Apicomplexa, Hepatozoidae) infection in water pythons (Liasis fuscus) from tropical Australia. Journal of Parasitology 90, 670–672.CrossRefGoogle ScholarPubMed
Van Rooyen, J., Lalubin, F., Glaizot, O. and Christe, P. (2013). Altitudinal variation in haemosporidian parasite distribution in great tit populations. Parasites & Vectors 6, 139.CrossRefGoogle Scholar
Vasconcelos, R. and Carranza, S. (2014). Systematics and biogeography of Hemidactylus homoeolepis Blanford, 1881 (Squamata: Gekkonidae), with the description of a new species from Arabia. Zootaxa 3835, 501–527.CrossRefGoogle ScholarPubMed
Wells, K., O'Hara, R. B., Morand, S., Lessard, J.-P. and Ribas, A. (2015). The importance of parasite geography and spillover effects for global patterns of host–parasite associations in two invasive species. Diversity and Distributions 21, 477–486.CrossRefGoogle Scholar
Whiteman, N. K. and Parker, P. G. (2005). Using parasites to infer host population history: a new rationale for parasite conservation. Animal Conservation 8, 175–181.CrossRefGoogle Scholar
Wolinska, J. and King, K. C. (2009). Environment can alter selection in host-parasite interactions. Trends in Parasitology 25, 236–244.CrossRefGoogle ScholarPubMed
Supplementary material: File

Maia supplementary material

Supplementary Tables

Download Maia supplementary material(File)
File 82 KB