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A paradise for parasites? Seven new haemogregarine species infecting lizards from the Canary Islands

Published online by Cambridge University Press:  15 March 2019

Beatriz Tomé Open the ORCID record for Beatriz Tomé [Opens in a new window] ,
Ana Pereira ,
D. James Harris ,
Miguel A. Carretero  and
Ana Perera
Beatriz Tomé*
Affiliation:
CIBIO, InBIO – Research Network in Biodiversity and Evolutionary Biology, 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
Ana Pereira
Affiliation:
CIBIO, InBIO – Research Network in Biodiversity and Evolutionary Biology, 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
D. James Harris
Affiliation:
CIBIO, InBIO – Research Network in Biodiversity and Evolutionary Biology, Universidade do Porto, Campus de Vairão, Rua Padre Armando Quintas, 4485-661 Vairão, Portugal
Miguel A. Carretero
Affiliation:
CIBIO, InBIO – Research Network in Biodiversity and Evolutionary Biology, Universidade do Porto, Campus de Vairão, Rua Padre Armando Quintas, 4485-661 Vairão, Portugal
Ana Perera
Affiliation:
CIBIO, InBIO – Research Network in Biodiversity and Evolutionary Biology, Universidade do Porto, Campus de Vairão, Rua Padre Armando Quintas, 4485-661 Vairão, Portugal
*
Author for correspondence: Beatriz Tomé, E-mail: [email protected]
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Abstract

Oceanic islands are hotspots of biodiversity due to their high levels of endemism, with the Canary Islands being a notable example. A previous molecular study on the biogeography and host associations of haemogregarines (Apicomplexa: Adeleorina) infecting lizards from this archipelago detected seven parasite haplogroups. These haplogroups exhibited high host-specificity and geographical structure, suggesting that they might correspond to distinct biological identities. In this study, along with sequencing a longer fragment of the 18S rRNA, we further explore the distinctiveness of these parasites by analysing their morphology, effects on host erythrocytes and parasitaemia levels. These lines of evidence together with their genetics, host associations, frequency of occurrence and geographical distribution support them as different biological entities. As such, we describe seven new species: Karyolysus canariensis sp. nov., Karyolysus galloti sp. nov., Karyolysus stehlini sp. nov., Karyolysus gomerensis sp. nov., Karyolysus atlanticus sp. nov., Karyolysus tinerfensis sp. nov. and Karyolysus makariogeckonis sp. nov. These new taxa are further examples of endemic diversity in the Canarian archipelago. They also contribute to clarify the taxonomy within the Apicomplexa, a phylum estimated to have one of the lowest percentages of described species.

Keywords

ApicomplexaChalcidesdescriptionGallotiahaemoparasitesKaryolysusreptilesTarentolataxonomy
Type
Research Article
Information
Parasitology , Volume 146 , Issue 6 , May 2019 , pp. 728 - 739
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Copyright © Cambridge University Press 2019 

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References

Abràmoff, MD, Magalhães, PJ and Ram, SJ (2004) Image processing with ImageJ. Biophotonics International 11, 36–41.Google Scholar
Amo, L, López, P and Martín, J (2005) Prevalence and intensity of haemogregarine blood parasites and their mite vectors in the common wall lizard, Podarcis muralis. Parasitology Research 96, 378–381.Google Scholar
Ancochea, E, Hernán, F, Huertas, MJ, Brändle, JL and Herrera, R (2006) A new chronostratigraphical and evolutionary model for La Gomera: implications for the overall evolution of the Canarian Archipelago. Journal of Volcanology and Geothermal Research 157, 271–293.Google Scholar
Anderson, MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecology 26, 32–46.Google Scholar
Arbizu, PM (2017) pairwiseAdonis: Pairwise multilevel comparison using adonis. Version 0.0.1. Retrieved from: https://github.com/pmartinezarbizu/pairwiseAdonis (accessed 1 March 2018).Google Scholar
Bannert, B (1992) Sarcocystis simonyi sp. nov. (Apicomplexa: Sarcocystidae) from the endangered Hierro giant lizard Gallotia simonyi (Reptilia: Lacertidae). Parasitology Research 78, 142–145.Google Scholar
Bannert, B, Lux, E and Sedlaczek, J (1995) Studies on endo- and ectoparasites of Canarian Lizards. Scientia Herpetologica 1995, 293–296.Google Scholar
Bannert, B, Karaca, HY and Wohltmann, A (2000) Life cycle and parasitic interaction of the lizard-parasitizing mite Ophionyssus galloticolus (Acari: Gamasida: Macronyssidae), with remarks about the evolutionary consequences of parasitism in mites. Experimental and Applied Acarology 24, 597–613.Google Scholar
Barry, M, Peirce, MA, Heath, ACG, Brunton, DH and Barraclough, RK (2011) A new blood parasite within the relict endemic New Zealand gecko Hoplodactylus duvaucelii. Veterinary Parasitology 179, 199–202.Google Scholar
Bertrand, M, Pfliegler, WP and Sciberras, A (2012) Does the African native host explain the African origin of the parasite? The Maltese Geckobia estherae n. sp. parasitic on Tarentola mauritanica (Acari: Raphignathoidea: Pterygosomatidae). Acarologia 52, 353–366.Google Scholar
Carranza, S, Arnold, EN, Mateo, JA and Geniez, P (2002) Relationships and evolution of the North African geckos, Geckonia and Tarentola (reptilia: Gekkonidae), based on mitochondrial and nuclear DNA sequences. Molecular Phylogenetics and Evolution 23, 244–256.Google Scholar
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, 1071–1094.Google Scholar
Caudell, JN, Whittier, J and Conover, MR (2002) The effects of haemogregarine-like parasites on brown tree snakes (Boiga irregularis) and slatey-grey snakes (Stegonotus cucullatus) in Queensland, Australia. International Biodeterioration and Biodegradation 49, 113–119.Google Scholar
Clement, M, Posada, D and Crandall, KA (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.Google Scholar
Cook, CA, Netherlands, EC and Smit, NJ (2016) Redescription, molecular characterisation and taxonomic re-evaluation of a unique African monitor lizard haemogregarine Karyolysus paradoxa (Dias, 1954) n. comb. (Karyolysidae). Parasites & Vectors 9, 347.Google Scholar
Cox, SC, Carranza, S and Brown, RP (2010) Divergence times and colonization of the Canary Islands by Gallotia lizards. Molecular Phylogenetics and Evolution 56, 747–757.Google Scholar
Criado-Fornelio, A, Ruas, JL, Casado, N, Farias, NAR, Soares, MP, Müller, G, Brumt, JGW, Berne, MEA, Buling-Saraña, A and Barba-Carretero, JC (2006) New molecular data on mammalian Hepatozoon species (Apicomplexa: Adeleorina) from Brazil and Spain. Journal of Parasitology 92, 93–99.Google Scholar
Damas-Moreira, I, Harris, DJ, Rosado, D, Tavares, I, Maia, JP, Salvi, D and Perera, A (2014) Consequences of haemogregarine infection on the escape distance in the lacertid lizard. Podarcis vaucheri. Acta Herpetologica 9, 119–123.Google Scholar
Fain, A and Bannert, B (2000) Two new species of Ophionyssus megnin (Acari: Macronyssidae) parasitic on lizards of the genus Gallotia boulenger (Reptilia: Lacertidae) from the Canary Islands. International Journal of Acarology 26, 41–50.Google Scholar
Fain, A and Bannert, B (2002) New observations on species of the genus Ophionyssus Mégnin (Acari: Macronyssidae) parasitic on lizards of the genus Gallotia boulenger (Reptilia: Lacertidae) from the Canary Islands, Spain with description of a new species. International Journal of Acarology 28, 361–366.Google Scholar
Fajfer, M (2012) Acari (Chelicerata) – parasites of reptiles. Acarina 20, 108–129.Google Scholar
Feliu, C, López, M, Gómez, MS, Torres, J, Sánchez, S, Miquel, J, Abreu-Acosta, N, Segovia, JM, Martín-Alonso, A, Montoliu, I, Villa, M, Fernández-Álvarez, Á, Bakhoum, AJS, Valladares, B, Orós, J and Foronda, P (2012) Parasite fauna of rodents (Murinae) from El Hierro (Canary Islands, Spain): a multidisciplinary approach. Acta Parasitologica 57, 171–178.Google Scholar
Foronda, PR, Figueruelo, EO, Ortego, AR, Abreu, NA and Casanova, JC (2005) Parasites (viruses, coccidia and helminths) of the wild rabbit (Oryctolagus cuniculus) introduced to Canary Islands from Iberian Peninsula. Acta Parasitologica 50, 80–84.Google Scholar
Foronda, P, Santana-Morales, MA, Orós, J, Abreu-Acosta, N, Ortega-Rivas, A, Lorenzo-Morales, J and Valladares, B (2007) Clinical efficacy of antiparasite treatments against intestinal helminths and haematic protozoa in Gallotia caesaris (lizards). Experimental Parasitology 116, 361–365.Google Scholar
Foronda, P, López-González, M, Hernández, M, Haukisalmi, V and Feliu, C (2011) Distribution and genetic variation of hymenolepidid cestodes in murid rodents on the Canary Islands (Spain). Parasites & Vectors 4, 185.Google Scholar
García-Ramírez, A, Delgado-García, JD, Foronda-Rodríguez, P and Abreu-Acosta, N (2005) Haematozoans, mites and body condition in the oceanic island lizard Gallotia atlantica (Peters and Doria, 1882) (Reptilia: Lacertidae). Journal of Natural History 39, 1299–1305.Google Scholar
Haklová-Kočíková, B, Hižňanová, A, Majláth, I, Račka, K, Harris, DJ, Földvári, G, Tryjanowski, P, Kokošová, N, Malčeková, B and Majláthová, V (2014) Morphological and molecular characterization of Karyolysus – a neglected but common parasite infecting some European lizards. Parasites & vectors 7, 555.Google Scholar
Hassl, A (2012) Blood parasitism by hemogregarines in Central European lizards. Herpetozoa 25, 83–86.Google Scholar
Hatcher, MJ, Dick, JTA and Dunn, AM (2012) Diverse effects of parasites in ecosystems: linking interdependent processes. Frontiers in Ecology and the Environment 10, 186–194.Google Scholar
Hudson, PJ, Dobson, AP and Lafferty, KD (2006) Is a healthy ecosystem one that is rich in parasites? Trends in Ecology and Evolution 21, 381–385.Google Scholar
Illera, JC, Fernández-Álvarez, Á, Hernández-Flores, CN and Foronda, P (2015) Unforeseen biogeographical patterns in a multiple parasite system in Macaronesia. Journal of Biogeography 42, 1858–1870.Google Scholar
Illera, JC, Spurgin, LG, Rodriguez-Exposito, E, Nogales, M and Rando, JC (2016) What are we learning about speciation and extinction from the Canary Islands? Ardeola 63, 5–23.Google Scholar
Johnson, EM, Allen, KE, Panciera, RJ, Ewing, SA and Little, SE (2009) Experimental transmission of Hepatozoon americanum to New Zealand White rabbits (Oryctolagus cuniculus) and infectivity of cystozoites for a dog. Veterinary Parasitology 164, 162–166.Google Scholar
Jorge, F, Perera, A, Carretero, MA, Harris, DJ and Roca, V (2013) Cryptic species unveiled: the case of the nematode Spauligodon atlanticus. Journal of Zoological Systematics and Evolutionary Research 51, 187–202.Google Scholar
Jorge, F, Perera, A, Poulin, R, Roca, V and Carretero, MA (2018) Getting there and around: host range oscillations during colonization of the Canary Islands by the parasitic nematode Spauligodon. Molecular Ecology 27, 533–549.Google Scholar
Juan, C, Emerson, BC, Oromí, P and Hewitt, GM (2000) Colonization and diversification: towards a phylogeographic synthesis for the Canary Islands. Trends in Ecology and Evolution 15, 104–109.Google 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.Google Scholar
Katoh, K and Standley, DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772–780.Google Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.Google Scholar
Kvičerová, J, Hypša, V, Dvořáková, N, Mikulíček, P, Jandzik, D, Gardner, MG, Javanbakht, H, Tiar, G and Široký, P (2014) Hemolivia and Hepatozoon: haemogregarines with tangled evolutionary relationships. Protist 165, 688–700.Google Scholar
Maia, JPMC, Harris, DJ and Perera, A (2011) Molecular survey of Hepatozoon species in lizards from North Africa. Journal of Parasitology 97, 513–517.Google Scholar
Maia, JPMC, Perera, A and Harris, DJ (2012) Molecular survey and microscopic examination of Hepatozoon miller, 1908 (Apicomplexa: Adeleorina) in lacertid lizards from the western Mediterranean. Folia Parasitologica 59, 241–248.Google Scholar
Maia, JP, Álvares, F, Boratyński, Z, Brito, JC, Leite, JV and Harris, DJ (2014) Molecular assessment of Hepatozoon (Apicomplexa: Adeleorina) infections in wild canids and rodents from North Africa, with implications for transmission dynamics across taxonomic groups. Journal of Wildlife Diseases 50, 837–848.Google Scholar
Maia, JP, Carranza, S and Harris, DJ (2016 a) Comments on the systematic revision of adeleid haemogregarines: is more data needed? Journal of Parasitology 102, 549–552.Google Scholar
Maia, JP, Harris, DJ, Carranza, S and Goméz-Díaz, E (2016 b) Assessing the diversity, host-specificity and infection patterns of apicomplexan parasites in reptiles from Oman, Arabia. Parasitology 143, 1730–1747.Google Scholar
Mangiafico, S (2018) rcompanion: Functions to Support Extension Education Program Evaluation. Version 1.13.0. https://CRAN.R-project.org/package=rcompanion (accessed 1 March 2018).Google Scholar
Martínez-Silvestre, A, Mateo, JA, Silveira, L and Bannert, B (2001) Presencia de protozoos intraeritrocitarios en el lagarto gigante de La Gomera. Boletin de la Asociacion Herpetologica Española 12, 90–92.Google Scholar
Matuschka, FR and Bannert, B (1987) Cannibalism and autotomy as predator-prey relationship for monoxenous sarcosporidia. Parasitology Research 74, 88–93.Google Scholar
Matuschka, FR and Bannert, B (1989) Recognition of cyclic transmission of Sarcocystis stehlinii n. sp. in the Gran Canarian giant lizard. Journal of Parasitology 75, 383–387.Google Scholar
Medlin, L, Elwood, HJ, Stickel, S and Sogin, ML (1988) The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71, 491–499.Google Scholar
Megía-Palma, R, Martínez, J and Merino, S (2016) A structural colour ornament correlates positively with parasite load and body condition in an insular lizard species. The Science of Nature 103, 52.Google Scholar
Modrý, D, Beck, R, Hrazdilová, K and Baneth, G (2017) A review of methods for detection of Hepatozoon infection in carnivores and arthropod vectors. Vector-Borne and Zoonotic Diseases 17, 66–72.Google Scholar
Morrison, DA (2009) Evolution of the Apicomplexa: where are we now? Trends in Parasitology 25, 375–382.Google Scholar
Múrias Dos Santos, A, Cabezas, MP, Tavares, AI, Xavier, R and Branco, M (2015) TcsBU: a tool to extend TCS network layout and visualization. Bioinformatics (Oxford, England) 32, 627–628.Google Scholar
Myers, N, Mittermeier, RA, Mittermeier, CG, Da Fonseca, GAB and Kent, J (2000) Biodiversity hotspots for conservation priorities. Nature 403, 853.Google Scholar
Netherlands, EC, Cook, CA, Du Preez, LH, Vanhove, MPM, Brendonck, L and Smit, NJ (2018) 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, 1039–1050.Google Scholar
O'Dwyer, LH, Moço, TC, Paduan, KDS, Spenassatto, C, da Silva, RJ and Ribolla, PEM (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.Google Scholar
Oppliger, A, Vernet, R and Baez, M (1999) Parasite local maladaptation in the Canarian lizard Gallotia galloti (Reptilia: Lacertidae) parasitized by haemogregarian blood parasite. Journal of Evolutionary Biology 12, 951–955.Google Scholar
Padilla, DP, Illera, JC, Gonzalez-Quevedo, C, Villalba, M and Richardson, DS (2017) Factors affecting the distribution of haemosporidian parasites within an oceanic island. International Journal for Parasitology 47, 225–235.Google Scholar
Pérez-Rodríguez, A, Ramírez, Á, Richardson, DS and Pérez-Tris, J (2013) Evolution of parasite island syndromes without long-term host population isolation: parasite dynamics in Macaronesian blackcaps Sylvia atricapilla. Global Ecology and Biogeography 22, 1272–1281.Google Scholar
Prenter, J, MacNeil, C, Dick, JTA and Dunn, AM (2004) Roles of parasites in animal invasions. Trends in Ecology and Evolution 19, 385–390.Google Scholar
Rabie, SAH and Hussein, ANA (2014) A description of haemogregarina species naturally infecting white-spotted gecko (Tarentola annularis) in Qena, Egypt. Journal of the Egyptian Society of Parasitology 44, 351–358.Google Scholar
R Core Team (2017) R: A language and environment for statistical computing. Version 3.4.3. Retrieved from: https://www.R-project.org/ (accessed 1 March 2018).Google Scholar
Reyes-Betancort, JA, Santos Guerra, A, Guma, IR, Humphries, CJ and Carine, MA (2008) Diversity, rarity and the evolution and conservation of the Canary Islands endemic flora. Anales del Jardín Botánico de Madrid 65, 25–45.Google Scholar
Roca, V, Carretero, M, Llorente, G, Montori, A and Martin, J (2005) Helminth communities of two lizard populations (Lacertidae) from Canary Islands (Spain): host diet-parasite relationships. Amphibia-Reptilia 26, 535–542. doi: 10.1163/156853805774806160.Google Scholar
Roca, V, Jorge, F and Carretero, MA (2012) Synopsis of the helminth communities of the lacertid lizards from the Balearic and Canary Islands. Basic and Applied Herpetology 26, 107–116.Google Scholar
Sanmartín, I, Van Der Mark, P and Ronquist, F (2008) Inferring dispersal: a Bayesian approach to phylogeny-based island biogeography, with special reference to the Canary Islands. Journal of Biogeography 35, 428–449.Google Scholar
Saoud, MFA, Ramadan, NF, Mohammed, SH and Fawzi, SM (1995) Haemogregarines of geckos in Egypt, together with a description of Haemogregarina helmymohammedi n. sp. Qatar University Science Journal 15, 131–146.Google Scholar
Sloboda, M, Kamler, M, Bulantová, J, Votýpka, J and Modrý, D (2008) Rodents as intermediate hosts of Hepatozoon ayorgbor (Apicomplexa: Adeleina: Hepatozoidae) from the African ball python, Python regius? Folia parasitologica 55, 13–16.Google Scholar
Smith, TG (1996) The genus Hepatozoon (apicomplexa: Adeleina). Journal of Parasitology 82, 565–585.Google Scholar
Svahn, K (1975) Blood parasites of the genus Karyolysus (coccidia, Adeleidae) in Scandinavian lizards. Description and life cycle. Norwegian Journal of Zoology 23, 277–295.Google Scholar
Telford, SR (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, 883–887.Google Scholar
Tomé, B, Maia, JP, Salvi, D, Brito, JC, Carretero, MA, Perera, A, Meimberg, H and Harris, DJ (2014) Patterns of genetic diversity in Hepatozoon spp. infecting snakes from North Africa and the Mediterranean Basin. Systematic Parasitology 87, 249–258.Google Scholar
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, 476–480.Google Scholar
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, 1–13.Google Scholar
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.Google Scholar
Van As, J, Davies, AJ and Smit, NJ (2013) Hepatozoon langii n. sp. and Hepatozoon vacuolatus n. sp. (Apicomplexa: Adeleorina: Hepatozoidae) from the crag lizard (Sauria: Cordylidae) Pseudocordylus langi from the North Eastern Drakensberg escarpment, Eastern Free State, South Africa. Zootaxa 3608, 345–356.Google Scholar
Venables, WN and Ripley, BD (2002) Random and mixed effects. In Venables, WN and Ripley, BD (eds), Modern Applied Statistics with S. New York, USA: Springer, pp. 271–300.Google Scholar
Votýpka, J, Modrý, D, Oborník, M, Šlapeta, J and Lukeš, J (2017) Apicomplexa. In Archibald, JM, Simpson, AGB and Slamovits, CH (eds), Handbook of the Protists. New York, USA: Springer, pp. 567–624.Google Scholar
Wheeler, B and Torchiano, M (2016) lmPerm: Permutation Tests for Linear Models. Version 2.1.0. Retrieved from: https://CRAN.R-project.org/package=lmPerm (accessed 1 March 2018).Google Scholar
Zapatero-Ramos, LM, Gonzalez-Santiago, PM, Solera-Puertas, MA and Carvajal-Gallardo, MM (1989) Estudio de nuevas especies de Pterigosomidae (Acari: Antinedida) sobre Gekkonidos de las Islas Canarias. Descripción de Geckobia canariensis n. sp. y de Geckobia tinerfensis n. sp. Revista Iberica de Parasitologia 49, 51–64.Google Scholar
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