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The New Internal Transcribed Spacer 2 Diagnostic Tool Clarifies The Hodge et al. Malar J (2021) 20:141 https://doi.org/10.1186/s12936-021-03676-4 Malaria Journal RESEARCH Open Access The new Internal Transcribed Spacer 2 diagnostic tool clarifes the taxonomic position and geographic distribution of the North American malaria vector Anopheles punctipennis James M. Hodge1, Andrey A. Yurchenko1,2,3, Dmitriy A. Karagodin2, Reem A. Masri1, Ryan C. Smith4, Mikhail I. Gordeev5 and Maria V. Sharakhova1,2* Abstract Background: The malaria mosquito Anopheles punctipennis, a widely distributed species in North America, is capable of transmitting human malaria and is actively involved in the transmission of the ungulate malaria parasite Plasmo- dium odocoilei. However, molecular diagnostic tools based on Internal Transcribed Spacer 2 (ITS2) of ribosomal DNA are lacking for this species. Anopheles punctipennis is a former member of the Anopheles maculipennis complex but its systematic position remains unclear. Methods: In this study, ITS2 sequences were obtained from 276 An. punctipennis specimens collected in the eastern and midwestern United States and a simple and robust Restriction Fragment Length Polymorphism approach for species identifcation was developed. The maximum-likelihood phylogenetic tree was constructed based on ITS2 sequences available through this study and from GenBank for 20 species of Anopheles. Results: The analysis demonstrated a consistent ITS2 sequence length and showed no indications of intragenomic variation among the samples based on ITS2, suggesting that An. punctipennis represents a single species in the studied geographic locations. In this study, An. punctipennis was found in urban, rural, and forest settings, suggesting its potential broad role in pathogen transmission. Phylogeny based on ITS2 sequence comparison demonstrated the close relationship of this species with other members of the Maculipennis group. Conclusions: This study developed molecular tools based on ITS2 sequences for the malaria vector An. punctipennis and clarifed the phylogenetic position of the species within the Maculipennis group. Keywords: Anopheles punctipennis, Mosquito, Molecular diagnostics, Internal transcribed spacer, Restriction fragment length polymorphism Background Malaria is one of the most dangerous infectious dis- eases transmitted by mosquitoes [1]. In 2018, the World Health Organization (WHO) reported 228 million cases of malaria occurring worldwide. However, in contrast *Correspondence: [email protected] to the African region, where the WHO reports a steady 1 Department of Entomology and the Fralin Life Sciences Institute, declining of the disease, the rise in malaria cases has Virginia Polytechnic Institute and State University, Blacksburg, VA, USA Full list of author information is available at the end of the article been recorded in the American region [2]. Malaria had © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Hodge et al. Malar J (2021) 20:141 Page 2 of 11 been a signifcant problem in North America where it utilized for species diagnostics in the Anopheles gambiae was introduced in the seventeenth century during the complex [17], the Anopheles funestus group [18], and the slave trade and, because of the presence of native com- Anopheles bancroftii group [19]. One nucleotide difer- petent malaria vectors, it rapidly spread through the ence in ITS2 led to the discovery of the M and S forms entire continent [3]. In the USA, numerous outbreaks of of An. gambiae, which have now been elevated to spe- malaria occurred from as far north as Massachusetts to cies status as An. gambiae (former S form) and Anopheles subtropical southern states in the eighteenth and nine- coluzzii (former M form) [20]. Tree new Eurasian spe- teenth centuries. Starting in the 1930s, intensive eforts cies—Anopheles artemievi [21], Anopheles persiensis [22], to control malaria were undertaken and, in 1954, malaria and Anopheles daciae [23]—were described based on dif- was declared eliminated from the USA [3]. Nevertheless, ferences in their ITS2 sequences. ITS2 sequences have each year, the Center for Disease Control and Prevention been successfully used for the identifcation of North (CDC) reports between 1,000 and 1,500 cases of malaria American mosquitoes, including a newly identifed spe- in the USA [4], with 63 outbreaks of locally transmitted cies, Anopheles hermsi [24], and four new species in the malaria occurring since 1957 [5]. Climate change, human Quadrimaculatus complex [25]. More recently ITS2- migration, political instability, and the presence of com- based diagnostic tools were developed for species from petent malaria vectors increase the risk of malaria and the Anopheles crucians complex [26]. Despite the wide other tropical diseases being imported and transmitted in distribution in North America and its obvious role in regions where they were eradicated [5]. pathogen transmission, a molecular diagnostic tool using Tree species are considered dominant malaria vec- ITS2 of the rDNA from An. punctipennis has not been tors in North America—Anopheles freeborni, Anopheles developed yet. pseudopunctipennis, and Anopheles quadrimaculatus [6]. In the past, An. punctipennis was a member of the for- In addition to these species, Anopheles punctipennis, the mer Anopheles maculipennis complex, which included 7 most common and widely distributed anopheline mos- Eurasian and 6 North American species [27]. Although, quito species in North America [7], was an important considered distance by the classical morphological contributor to malaria transmission in the USA in the approach, An. punctipennis was still placed within the past [8]. Similar to An. quadrimaculatus, this species is An. maculipennis complex based on interspecies hybridi- capable of transmitting two major human malaria para- zation with other members of the complex and the struc- sites, Plasmodium vivax and Plasmodium falciparum [9]. ture of its polytene chromosomes [28]. In 2004, Harbach Moreover, An. punctipennis can also transmit Plasmo- proposed a new classifcation for the genus Anopheles dium odocoilei, which infects wild hooved animals, such that was largely based on morphological characteristics as deer. A recent study conducted in 17 states across the and ITS2 sequence analyses [29]. According to this classi- USA estimated a 25% P. odocoilei infection rate in white- fcation, the An. maculipennis complex was transformed tailed deer [10]. Malaria in wildlife populations may to the Maculipennis group, which was subdivided into also have an impact on biodiversity, as infection reduces two North American subgroups, Freeborni and Quad- the deer population by killing fawns [11]. Tis can also rimaculatus, and one Eurasian Maculipennis subgroup. present problems for humans due to the possibility of Anopheles punctipennis was excluded from the Macu- zoonotic transmission to livestock ungulates vectored lipennis group and placed into a separate Punctipennis from wild ungulates [11]. Te ability of An. punctipen- group that included An. punctipennis, Anopheles perplex- nis to transmit arboviruses, such as Cache Valley [12] ens, and the An. crucians complex. and eastern equine encephalomyelitis [13] viruses, as In this study, malaria mosquitoes were collected from well as a nematode Diroflaria immitis [14] has also been 10 sites in eastern (Virginia and Florida) and midwestern reported. states (Iowa and Minnesota) and 2 assays based on the Continuous study of mosquitoes in the feld requires sequencing of ITS2 of the rDNA and Restriction Frag- rapid and robust identifcation of the species. Te avail- ment Length Polymorphism (RFLP) of ITS2 for molecu- ability of PCR-based molecular technologies enable the lar diagnostics of An. punctipennis were developed. In use of ribosomal DNA (rDNA) for species diagnostics addition, ITS2 sequences were used to clarify the phylo- [15]. rDNA genes are organized in arrays of multiple genetic relationships of An. punctipennis. copies in eukaryotic genomes and undergo “concerted evolution” which leads to unifcation of gene and inter- Methods genic sequences [16]. Unlike Intragenic Spacer and Mosquito collection Intergenic Transcribed Spacer 1, Intergenic Transcribed A collection of approximately 500 Anopheles mosqui- Spacer 2 (ITS2) is a reliable tool for species diagnostics toes were sampled from multiple locations across four in the Anopheles genus [15]. ITS2 sequences have been states during the summers of 2017 and 2018 as shown Hodge et al. Malar J (2021) 20:141 Page 3 of 11 in Table 1. Te
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