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      Identifying avian malaria vectors: sampling methods influence outcomes

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          Abstract

          Background

          The role of vectors in the transmission of avian malaria parasites is currently understudied. Many studies that investigate parasite-vector relationships use limited trapping techniques and/or identify potential competent vectors in the field in such ways that cannot distinguish between an infected or infectious vector. Without the use of multiple trapping techniques that address the specific biology of diverse mosquito species, and without looking at the infection status of individual mosquitoes, it is not possible to make dependable conclusions on the role of mosquitoes in the transmission of avian malaria parasites.

          Methods

          We conducted two years of mosquito collections at a riparian preserve in California where a wide diversity of species were collected with multiple trap types. We hypothesized that competent mosquito species can influence the distribution and diversity of avian malaria parasites by acting as a compatibility filter for specific Plasmodium species. To determine the infection status of all individual mosquitoes for Plasmodium species/lineages, amplification within the cytochrome b gene was carried out on over 3000 individual mosquito thoraxes, and for those that tested positive we then repeated the same process for abdomens and salivary glands.

          Results

          Our data show heterogeneity in the transmissibility of Plasmodium among ornithophillic mosquito species . More specifically, Culex stigmatosoma appears to not be a vector of Plasmodium homopolare, a parasite that is prevalent in the avian population, but is a vector of multiple other Plasmodium species/lineages.

          Conclusions

          Our results suggest that conclusions made on the role of vectors from studies that do not use different mosquito trapping methods should be re-evaluated with caution, as we documented the potential for trapping biases, which may cause studies to miss important roles of specific mosquito species in the transmission of avian malaria. Moreover, we document heterogeneity in the transmission of Plasmodium spp. by mosquitoes can influence Plasmodium diversity and prevalence in specific locations to Plasmodium-vector incompatibilities.

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          Most cited references51

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          R: A language and environment for statistical computing

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            A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood.

            Recently, several polymerase chain reaction (PCR)-based methods for detection and genetic identification of haemosporidian parasites in avian blood have been developed. Most of these have considerably higher sensitivity compared with traditional microscope-based examinations of blood smears. These new methods have already had a strong impact on several aspects of research on avian blood parasites. In this study, we present a new nested PCR approach, building on a previously published PCR method, which has significantly improved performance. We compare the new method with some existing assays and show, by sequence-based data, that the higher detection rate is mainly due to superior detection of Plasmodium spp. infections, which often are of low intensity and, therefore, hard to detect with other methods.
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              A three-genome phylogeny of malaria parasites (Plasmodium and closely related genera): evolution of life-history traits and host switches.

              Phylogenetic analysis of genomic data allows insights into the evolutionary history of pathogens, especially the events leading to host switching and diversification, as well as alterations of the life cycle (life-history traits). Hundreds, perhaps thousands, of malaria parasite species exploit squamate reptiles, birds, and mammals as vertebrate hosts as well as many genera of dipteran vectors, but the evolutionary and ecological events that led to this diversification and success remain unresolved. For a century, systematic parasitologists classified malaria parasites into genera based on morphology, life cycle, and vertebrate and insect host taxa. Molecular systematic studies based on single genes challenged the phylogenetic significance of these characters, but several significant nodes were not well supported. We recovered the first well resolved large phylogeny of Plasmodium and related haemosporidian parasites using sequence data for four genes from the parasites' three genomes by combining all data, correcting for variable rates of substitution by gene and site, and using both Bayesian and maximum parsimony analyses. Major clades are associated with vector shifts into different dipteran families, with other characters used in traditional parasitological studies, such as morphology and life-history traits, having variable phylogenetic significance. The common parasites of birds now placed into the genus Haemoproteus are found in two divergent clades, and the genus Plasmodium is paraphyletic with respect to Hepatocystis, a group of species with very different life history and morphology. The Plasmodium of mammal hosts form a well supported clade (including Plasmodium falciparum, the most important human malaria parasite), and this clade is associated with specialization to Anopheles mosquito vectors. The Plasmodium of birds and squamate reptiles all fall within a single clade, with evidence for repeated switching between birds and squamate hosts.
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                Author and article information

                Contributors
                jennysaracarlson@gmail.com
                mocker21@gmail.com
                RFryxell@utk.edu
                zagal92@gmail.com
                latell@ucdavis.edu
                sehgal@sfsu.edu
                cmbarker@ucdavis.edu
                ajcornel@ucanr.edu
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                11 July 2015
                11 July 2015
                2015
                : 8
                : 365
                Affiliations
                [ ]Department of Entomology, University of California, Davis, CA USA
                [ ]Department of Biology, San Francisco State University, San Francisco, CA USA
                [ ]Department of Entomology and Plant Pathology, The University of Tennessee, Knoxville, TN USA
                [ ]Department of Medicine and Epidemiology, University of California, Davis, CA USA
                [ ]Department of Pathology, Microbiology, and Immunology, University of California, Davis, CA USA
                Article
                969
                10.1186/s13071-015-0969-0
                4702297
                26160384
                f02d52d0-6b9e-47e0-a838-d6cd6a87876b
                © Carlson et al. 2015

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. 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 2015
                : 30 June 2015
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100007707, University of California, Davis;
                Award ID: 201224501
                Award Recipient :
                Funded by: FundRef , Mosquito Research Foundation;
                Award ID: 201224501
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2015

                Parasitology
                avian malaria,culex spp.,plasmodium spp.,vector competence,vector compatibility filter,trapping bias

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