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      Phylogenetic analyses reveal that Schellackia parasites (Apicomplexa) detected in American lizards are closely related to the genus Lankesterella: is the range of Schellackia restricted to the Old World?

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          Abstract

          Background

          Species of Schellackia Reichenow, 1919 have been described from the blood of reptiles distributed worldwide. Recently, Schellackia spp. detected in European and Asian lizards have been molecularly characterised. However, parasites detected in American lizard hosts remain uncharacterised. Thus, phylogenetic affinities between the Old and New World parasite species are unknown.

          Methods

          In the present study, we characterised morphologically and molecularly the hemococcidian parasites (sporozoites) that infect three lizard hosts from North America and two from South America.

          Results

          In total, we generated 12 new 18S rRNA gene sequences of hemococcidian parasites infecting New World lizard hosts. By the microscopic examination of the smears we identified Schellackia golvani Rogier & Landau, 1975 (ex Anolis carolinensis Voigt) and Schellackia occidentalis Bonorris & Ball, 1955 (ex Uta stansburiana Baird & Girard and Sceloporus occidentalis Baird & Girard) in some samples, but the phylogenetic analysis indicated that all 18S rDNA sequences are distant from Schellackia species found in Old World lizards. In fact, the hemococcidian parasites detected in the New World lizards (including S. occidentalis and S. golvani) were closely related to the genus Lankesterella Labbé, 1899. Consequently, we suggest these two species to be included within the genus Lankesterella.

          Conclusions

          Life history traits of hemococcidian parasites such as the type of host blood cells infected, host species or number of refractile bodies are not valid diagnostic characteristics to differentiate the parasites between the genera Schellackia and Lankesterella. Indeed, lankesterellid parasites with a different number of refractile bodies had a close phylogenetic origin. Based on the phylogenetic results we provide a systematic revision of the North American hemococcidians. Our recommendation is to include the species formerly described in the genus Schellackia that infect American lizards into Lankesterella (Lankesterellidae) as Lankesterella golvani (Rogier & Landau, 1975) n. comb and L. occidentalis (Bonorris & Ball, 1955) n. comb.

          Electronic supplementary material

          The online version of this article (10.1186/s13071-017-2405-0) contains supplementary material, which is available to authorized users.

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          Most cited references36

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          Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: multiple cases of cryptic speciation?

          Analyses of mitochondrial cytochrome b diversity among avian blood parasites of the genera Haemoproteus and Plasmodium suggest that there might be as many lineages of parasites as there are species of birds. This is in sharp contrast to the approximately 175 parasite species described by traditional methods based on morphology using light microscopy. Until now it has not been clear to what extent parasite mitochondrial DNA lineage diversity reflects intra- or interspecific variation. We have sequenced part of a fast-evolving nuclear gene, dihydrofolate reductase-thymidylate synthase (DHFR-TS), and demonstrate that most of the parasite mitochondrial DNA lineages are associated with unique gene copies at this locus. Although these parasite lineages sometimes coexist in the same host individual, they apparently do not recombine and could therefore be considered as functionally distinct evolutionary entities, with independent evolutionary potential. Studies examining parasite virulence and host immune systems must consider this remarkable diversity of avian malaria parasites.
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            A guideline for the preparation of species descriptions in the Eimeriidae.

            Members of the suborder Eimeriina (phylum Apicomplexa: class Sporozoea: order Eucoccidiorida) have complex 1 or 2 host life cycles that involve endogenous development in the tissues of vertebrates or invertebrates and exogenous development in an oocyst, usually outside the host(s). Because tissue stages are logistically difficult or even impossible to obtain in natural (wild) host-parasite systems, the vast majority (> 98%) of species in this parasite complex are known only from the structure of their sporulated oocyst. Unfortunately, the quality of these species descriptions is uneven because no guidelines are available for workers in the field to follow. Here we propose a specific set of guidelines for the preparation of species descriptions of coccidia based predominently on the structure of the sporulated oocyst, because the oocyst is the most readily available stage in the life cycle. In addition, we emphasize that ancillary data be incorporated whenever possible with the species description; these data may include, but are not limited to, ecological parameters, prevalence, seasonal data, and the deposition of both host symbiotypes and parasite hepantotypes (= phototypes) into accredited musecums so that accurate identification of both host and parasite material can be assured in perpetuity. And finally, if oocysts are collected in pure suspension, that is, if only one coccidian species (morphotype) is present in the sample, then some oocysts should be saved in 70% ethanol and archived in an accredited museum in the event that future workers might wish to amplify and, later, sequence the parasite's DNA.
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              On the specificity of avian blood parasites: revealing specific and generalist relationships between haemosporidians and biting midges.

              The study of host-parasite relationships involving vector-borne parasites requires understanding interactions between parasites and vectors. The capacity of haemosporidians to infect insects has clear evolutionary consequences for the transmission of diseases. Here, we investigated (i) the associations between blood parasites, biting midges and birds and (ii) the potential specificity between biting midge and haemosporidian haplotypes. A total of 629 parous biting midges Culicoides and 224 wild birds (belonging to seven species) from a locality of central Spain were individually examined for the presence of Haemoproteus and Plasmodium parasites by sequencing a fragment of cytochrome B. Biting midges were identified morphologically and characterized on the basis of a fragment of the cytochrome c oxidase (COI) gene. Overall, 12 Haemoproteus and three Plasmodium haplotypes were isolated and sequenced. Among them, 10 haplotypes were exclusively isolated from biting midges, three haplotypes only from birds and two haplotypes from both biting midges and birds. Biting midge haplotypes showed both specific and generalist relationships with Haemoproteus haplotypes but only generalist relationships with Plasmodium haplotypes. Several C. festivipennis and C. kibunesis haplotypes established significant coevolutionary links with Haemoproteus haplotypes. These results shed light on the specificity of interactions between vectors and blood parasites. © 2011 Blackwell Publishing Ltd.
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                Author and article information

                Contributors
                rodrigo.megia@mncn.csic.es
                auroch.f@gmail.com
                dhana4shree@gmail.com
                veronicalauradamico@gmail.com
                r.aguilar@unimelb.edu.au
                m.gabriela.palacios12@gmail.com
                rdcooper408@gmail.com
                francisco.martinez@uah.es
                lizardrps@gmail.com
                santiagom@mncn.csic.es
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                10 October 2017
                10 October 2017
                2017
                : 10
                : 470
                Affiliations
                [1 ]ISNI 0000 0004 1768 463X, GRID grid.420025.1, Departamento de Ecología Evolutiva, Museo Nacional de Ciencias Naturales-CSIC, ; Madrid, Spain
                [2 ]ISNI 0000 0004 1937 0239, GRID grid.7159.a, Departamento de Biomedicina y Biotecnología, Área de Parasitología, , Universidad de Alcalá de Henares, ; Alcalá de Henares, Spain
                [3 ]ISNI 0000 0001 0740 6917, GRID grid.205975.c, Department of Ecology and Evolutionary Biology, , University of California, ; Santa Cruz, California 95064 USA
                [4 ]ISNI 0000 0004 1775 6904, GRID grid.417569.8, Department of Biodiversity, Abasaheb Garware College, ; Pune, India
                [5 ]Grupo de Ecofisiología Aplicada al Manejo y Conservación de la Fauna Silvestre, Centro para el Estudio de Sistemas Marinos, Centro Nacional Patagónico, Puerto Madryn, Chubut Argentina
                [6 ]Instituto Argentino de Zonas Áridas, Grupo de Investigaciones de la Biodiversidad CONICET MENDOZA, Mendoza, Argentina
                [7 ]ISNI 0000 0001 2179 088X, GRID grid.1008.9, School of Biosciences, , The University of Melbourne, ; Melbourne, VIC Australia
                [8 ]ISNI 0000 0004 1768 463X, GRID grid.420025.1, Departamento de Biogeografía y Cambio Global, Museo Nacional de Ciencias Naturales-CSIC, ; Madrid, Spain
                Article
                2405
                10.1186/s13071-017-2405-0
                5633878
                29017602
                5174fbff-7337-4533-94ac-aefc3ad01ef3
                © The Author(s). 2017

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 13 February 2017
                : 26 September 2017
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100007136, Secretaría de Estado de Investigación, Desarrollo e Innovación;
                Award ID: CGL2012-40026-C02-01
                Award ID: CGL2012-40026-C02-02
                Award ID: EEBB-I-14-08326
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: EF-1241848
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100007829, Fundación San Ignacio del Huinay;
                Award ID: 2013CL0001
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2017

                Parasitology
                haemococcidia,lankesterellidae,lankesterella,schellackiidae,schellackia,reptile
                Parasitology
                haemococcidia, lankesterellidae, lankesterella, schellackiidae, schellackia, reptile

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