Hostname: page-component-7479d7b7d-qlrfm Total loading time: 0 Render date: 2024-07-15T18:36:29.414Z Has data issue: false hasContentIssue false

Parasites in a hotspot: diversity and specificity patterns of apicomplexans infecting reptiles from the Socotra Archipelago

Published online by Cambridge University Press:  19 October 2020

Beatriz Tomé
Affiliation:
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório Associado, Universidade do Porto, Campus de Vairão, Rua Padre Armando Quintas 4485-661, Vairão, Portugal Departamento de Biologia, Faculdade de Ciências da Universidade do Porto, Rua do Campo Alegre 4169-007, Porto, Portugal
João Maia
Affiliation:
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório Associado, Universidade do Porto, Campus de Vairão, Rua Padre Armando Quintas 4485-661, Vairão, Portugal Departamento de Biologia, Faculdade de Ciências da Universidade do Porto, Rua do Campo Alegre 4169-007, Porto, Portugal IBE, Institute of Evolutionary Biology (CSIC-Universitat Pompeu Fabra), Passeig Marítim de la Barceloneta, Barcelona, Spain
Ana Perera
Affiliation:
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório Associado, Universidade do Porto, Campus de Vairão, Rua Padre Armando Quintas 4485-661, Vairão, Portugal
Salvador Carranza
Affiliation:
IBE, Institute of Evolutionary Biology (CSIC-Universitat Pompeu Fabra), Passeig Marítim de la Barceloneta, Barcelona, Spain
Raquel Vasconcelos*
Affiliation:
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório Associado, Universidade do Porto, Campus de Vairão, Rua Padre Armando Quintas 4485-661, Vairão, Portugal IBE, Institute of Evolutionary Biology (CSIC-Universitat Pompeu Fabra), Passeig Marítim de la Barceloneta, Barcelona, Spain
*
Author for correspondence: Raquel Vasconcelos, E-mail: raquel.vasconcelos@cibio.up.pt

Abstract

Although parasites represent a major component of biodiversity, they remain poorly assessed, especially in remote regions. In this study, we screened 461 reptiles from Socotra, the largest and most biologically diverse archipelago in Arabia. Using 18S rRNA primers, we detected various apicomplexan parasites, namely haemogregarines, sarcocystids and eimeriids. Haemogregarines were the most common and genetically diverse, followed by sarcocystids (genus Sarcocystis) and eimeriids (genera Isospora and Lankesterella). All were related to parasites of other reptiles, including species from Arabia, Northern Africa and Asia. Like their 29 endemic reptile hosts, almost all Socotran parasites presented high genetic divergence and ecological differences from those found elsewhere, and probably represent undescribed endemic species. Among hosts, skinks were the most parasitized, which contrasted with similar studies from other areas, probably due to their more generalist diet and habitat use. As expected due to its high species richness, geckos harboured the highest parasite diversity in the archipelago. Parasite diversity also seemed to be correlated to island size, as the largest island harboured most haplotypes. This study emphasizes the importance of screening parasites in wild hosts from remote regions and of considering host ecology to understand disease transmission across taxa.

Type
Research Article
Copyright
Copyright © The Author(s) 2020. Published by Cambridge University Press

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

Autin, J, Bellahsen, N, Leroy, S, Husson, L, Beslier, M-O and d'Acremont, E (2013) The role of structural inheritance in oblique rifting: insights from analogue models and application to the Gulf of Aden. Tectonophysics 607, 5164.CrossRefGoogle Scholar
Badiane, A, Garcia-Porta, J, Červenka, J, Kratochvíl, L, Sindaco, R, Robinson, MD, Morales, H, Mazuch, T, Price, T and Amat, F (2014) Phylogenetic relationships of Semaphore geckos (Squamata: Sphaerodactylidae: Pristurus) with an assessment of the taxonomy of Pristurus rupestris. Zootaxa 3835, 3358.CrossRefGoogle ScholarPubMed
Barta, JR, Ogedengbe, JD, Martin, DS and Smith, TG (2012) Phylogenetic position of the adeleorinid coccidia (Myzozoa, Apicomplexa, Coccidia, Eucoccidiorida, Adeleorina) inferred using 18S rDNA sequences. Journal of Eukaryotic Microbiology 59, 171180.CrossRefGoogle ScholarPubMed
Carranza, S, Arnold, EN, Geniez, P, Roca, J and Mateo, JA (2008) Radiation, multiple dispersal and parallelism in the skinks, Chalcides and Sphenops (Squamata: Scincidae), with comments on Scincus and Scincopus and the age of the Sahara Desert. Molecular Phylogenetics and Evolution 46, 10711094.CrossRefGoogle Scholar
Combes, C (2001) Parasitism: The Ecology and Evolution of Intimate Interactions. Chicago, USA: University of Chicago Press.Google Scholar
Cornuault, J, Bataillard, A, Warren, BH, Lootvoet, A, Mirleau, P, Duval, T, Mila, B, Thebaud, C and Heeb, P (2012) The role of immigration and in-situ radiation in explaining blood parasite assemblages in an island bird clade. Molecular Ecology 21, 14381452.CrossRefGoogle Scholar
Darriba, D, Taboada, GL, Doallo, R and Posada, D (2012) Jmodeltest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.CrossRefGoogle ScholarPubMed
Duszynski, DW and Upton, SJ (2009) The Biology of the Coccidia (Apicomplexa) of Snakes of the World: A Scholarly Handbook for Identification and Treatment. North Charleston, USA: CreateSpace publishing.Google Scholar
Felsenstein, J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783791.CrossRefGoogle ScholarPubMed
Gjerde, B (2013) Phylogenetic relationships among Sarcocystis species in cervids, cattle and sheep inferred from the mitochondrial cytochrome c oxidase subunit I gene. International Journal for Parasitology 43, 579591.CrossRefGoogle ScholarPubMed
Gómez-Díaz, E, Sindaco, R, Pupin, F, Fasola, M and Carranza, S (2012) Origin and in situ diversification in Hemidactylus geckos of the Socotra Archipelago. Molecular Ecology 21, 40744092.CrossRefGoogle ScholarPubMed
Guindon, S, Dufayard, JF, Lefort, V, Anisimova, M, Hordijk, W and Gascuel, O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307321.CrossRefGoogle ScholarPubMed
Harris, DJ, Maia, JPMC and Perera, A (2011) Molecular characterization of Hepatozoon species in reptiles from the Seychelles. Journal of Parasitology 97, 106110.CrossRefGoogle ScholarPubMed
Harris, DJ, Maia, JPMC and Perera, A (2012) Molecular survey of Apicomplexa in Podarcis wall lizards detects Hepatozoon, Sarcocystis, and Eimeria species. Journal of Parasitology 98, 592597.CrossRefGoogle ScholarPubMed
Huelsenbeck, JP and Ronquist, F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754755.CrossRefGoogle ScholarPubMed
Jacobson, ER (2007) Infectious Diseases and Pathology of Reptiles: Color Atlas and Text. Boca Raton, USA: CRC Press.CrossRefGoogle Scholar
Jean, K, Burnside, WR, Carlson, L, Smith, K and Guégan, JF (2016) An equilibrium theory signature in the island biogeography of human parasites and pathogens. Global Ecology and Biogeography 25, 107116.CrossRefGoogle Scholar
Karadjian, G, Chavatte, JM and Landau, I (2015) Systematic revision of the adeleid haemogregarines, with creation of Bartazoon N. g., reassignment of Hepatozoon Argantis Garnham, 1954 to Hemolivia, and molecular data on Hemolivia stellata. Parasite 22, 31.CrossRefGoogle Scholar
Katoh, K and Standley, DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772780.CrossRefGoogle ScholarPubMed
Librado, P and Rozas, J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 14511452.CrossRefGoogle ScholarPubMed
Maia, JPMC, Harris, DJ and Perera, A (2011) Molecular survey of Hepatozoon species in lizards from North Africa. Journal of Parasitology 97, 513517.CrossRefGoogle ScholarPubMed
Maia, JP, Crottini, A and Harris, DJ (2014) Microscopic and molecular characterization of Hepatozoon domerguei (Apicomplexa) and Foleyella furcata (Nematoda) in wild endemic reptiles from Madagascar. Parasite 21, 47.CrossRefGoogle ScholarPubMed
Maia, JP, Harris, DJ, Carranza, S and Goméz-Díaz, E (2016) Assessing the diversity, host-specificity and infection patterns of apicomplexan parasites in reptiles from Oman, Arabia. Parasitology 143, 17301747.CrossRefGoogle ScholarPubMed
Martín, N, Martínez, S, Pujol-Buxó, E, Vinolas, A, Llorente, GA, Sanpera, C, Vasconcelos, R, Carranza, S and Santos, X (2017) Stable isotopes and diet uncover trophic-niche divergence and ecological diversification processes of endemic reptiles on Socotra Island. Zoologischer Anzeiger 267, 6981.CrossRefGoogle Scholar
McAllister, CT, Duszynski, CW, Austin, CC and Fisher, RN (2017) Four new species of Eimeria (Apicomplexa: Eimeriidae) from Emoia spp. skinks (Sauria: Scincidae), from Papua New Guinea and the Insular Pacific. Journal of Parasitology 103, 103110.CrossRefGoogle Scholar
Megía-Palma, R, Martínez, J, Nasri, I, Cuervo, JJ, Martín, J, Acevedo, I, Belliure, J, Ortega, J, García-Roa, R and Selmi, S (2016) Phylogenetic relationships of Isospora, Lankesterella, and Caryospora species (Apicomplexa: Eimeriidae) infecting lizards. Organisms Diversity & Evolution 16, 275288.CrossRefGoogle Scholar
Mittermeier, RA, Turner, WR, Larsen, FW, Brooks, TM and Gascon, C (2011) Global biodiversity conservation: the critical role of hotspots. In Zachos, FE and Habel, JC (eds), Biodiversity Hotspots: Distribution and Protection of Conservation Priority Areas. Berlin, DE: Springer, pp. 322.CrossRefGoogle Scholar
Morrison, DA (2009) Evolution of the Apicomplexa: where are we now? Trends in Parasitology 25, 375382.CrossRefGoogle ScholarPubMed
Netherlands, EC, Cook, CA, Du Preez, LH, Vanhove, MPM, Brendonck, L and Smit, NJ (2017) Monophyly of the species of Hepatozoon (Adeleorina: Hepatozoidae) parasitizing (African) anurans, with the description of three new species from hyperoliid frogs in South Africa. Parasitology 145, 112.Google ScholarPubMed
Nieberding, C, Morand, S, Libois, R and Michaux, JR (2006) Parasites and the island syndrome: the colonization of the western Mediterranean islands by Heligmosomoides polygyrus (Dujardin, 1845). Journal of Biogeography 33, 12121222.CrossRefGoogle Scholar
O'Shea, M (2018) The Book of Snakes: A Life-size Guide to Six Hundred Species from Around the World. Chicago, USA: University of Chicago Press.CrossRefGoogle Scholar
Perkins, SL and Keller, AK (2001) Phylogeny of nuclear small subunit rRNA genes of hemogregarines amplified with specific primers. Journal of Parasitology 87, 870876.CrossRefGoogle ScholarPubMed
Poulin, R (2011) The many roads to parasitism: a tale of convergence. Advances in Parasitology 74, 140.CrossRefGoogle ScholarPubMed
Poulin, R and Mouillot, D (2005) Combining phylogenetic and ecological information into a new index of host specificity. Journal of Parasitology 91, 511514.CrossRefGoogle ScholarPubMed
Razzetti, E, Sindaco, R, Grieco, C, Pella, F, Ziliani, U, Pupin, F, Riservato, E, Pellitteri-Rosa, D, Butikofer, L and Suleiman, AS (2011) Annotated checklist and distribution of the Socotran Archipelago Herpetofauna (Reptilia). Zootaxa 2826, 144.CrossRefGoogle Scholar
Sambrook, J, Fritsch, EF and Maniatis, T (1989) Molecular Cloning: A Laboratory Manual. New York, USA: Cold Spring Harbor Press.Google Scholar
Simó-Riudalbas, M, Tamar, K, Šmíd, J, Mitsi, P, Sindaco, R, Chirio, L and Carranza, S (2019) Biogeography of Mesalina (Reptilia: Lacertidae), with special emphasis on the Mesalina adramitana group from Arabia and the Socotra Archipelago. Molecular Phylogenetics and Evolution 137, 300312.CrossRefGoogle Scholar
Sindaco, R, Metallinou, M, Pupin, F, Fasola, M and Carranza, S (2012) Forgotten in the ocean: systematics, biogeography and evolution of the Trachylepis skinks of the Socotra Archipelago. Zoologica Scripta 41, 346362.CrossRefGoogle Scholar
Smith, TG (1996) The genus Hepatozoon (Apicomplexa: Adeleina). Journal of Parasitology 82, 565585.CrossRefGoogle Scholar
Tamar, K, Carranza, S, Sindaco, R, Moravec, J, Trape, JF and Meiri, S (2016) Out of Africa: phylogeny and biogeography of the widespread genus Acanthodactylus (Reptilia: Lacertidae). Molecular Phylogenetics and Evolution 103, 618.CrossRefGoogle Scholar
Tamar, K, Simó-Riudalbas, M, Garcia-Porta, J, Santos, X, Llorente, G, Vasconcelos, R and Carranza, S (2019) An integrative study of island diversification: insights from the endemic Haemodracon geckos of the Socotra Archipelago. Molecular Phylogenetics and Evolution 133, 166175.CrossRefGoogle ScholarPubMed
Tamura, K, Nei, M and Kumar, S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proceedings of the National Academy of Sciences 101, 1103011035.CrossRefGoogle ScholarPubMed
Telford, SR Jr (2009) Hemoparasites of the Reptilia. Color Atlas and Text. Boca Raton, USA: CRC Press.Google Scholar
Tomé, B, Maia, JPMC and Harris, DJ (2013) Molecular assessment of apicomplexan parasites in the snake Psammophis from North Africa: do multiple parasite lineages reflect the final vertebrate host diet? Journal of Parasitology 99, 883887.CrossRefGoogle ScholarPubMed
Tomé, B, Rato, C, Perera, A and Harris, DJ (2016) High diversity of Hepatozoon spp. in geckos of the genus Tarentola. Journal of Parasitology 102, 476480.CrossRefGoogle ScholarPubMed
Tomé, B, Pereira, A, Jorge, F, Carretero, MA, Harris, DJ and Perera, A (2018) Along for the ride or missing it altogether: exploring the host specificity and diversity of haemogregarines in the Canary Islands. Parasites & Vectors 11, 113.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, 670672.CrossRefGoogle ScholarPubMed
Upton, SJ (2000) Suborder Eimeriorina Léger, 1911. In Lee, JJ, Leedale, GF and Bradbury, P (eds), The Illustrated Guide to the Protozoa, 2nd Edn, vol. 1. Lawrence, USA: Allen Press, Inc., pp. 318339.Google Scholar
Van Damme, K (2009) Socotra archipelago. In Gillespie, RG and Clague, DA (eds), Encyclopedia of Islands. Berkeley and Los Angeles, USA: University of California Press, pp. 846851.Google 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, 501527.CrossRefGoogle Scholar
Vasconcelos, R, Montero-Mendieta, S, Simó-Riudalbas, M, Sindaco, R, Santos, X, Fasola, M, Llorente, G, Razzetti, E and Carranza, S (2016) Unexpectedly high levels of cryptic diversity uncovered by a complete DNA barcoding of reptiles of the Socotra Archipelago. PLoS ONE 11, e0149985.CrossRefGoogle ScholarPubMed
Wassermann, M, Raisch, L, Lyons, JA, Natusch, DJD, Richter, S, Wirth, M, Preeprem, P, Khoprasert, Y, Ginting, S, Mackenstedt, U and Jäkel, T (2017) Examination of Sarcocystis spp. of giant snakes from Australia and Southeast Asia confirms presence of a known pathogen–Sarcocystis nesbitti. PLoS ONE 12, e0187984.CrossRefGoogle ScholarPubMed
Zhu, BY, Hartigan, A, Reppas, G, Higgins, DP, Canfield, PJ and Šlapeta, J (2009) Looks can deceive: molecular identity of an intraerythrocytic apicomplexan parasite in Australian gliders. Veterinary Parasitology 159, 105111.CrossRefGoogle ScholarPubMed
Supplementary material: File

Tomé et al. supplementary material

Tables S1-S5

Download Tomé et al. supplementary material(File)
File 60.4 KB