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Molecular Characterization and Genetic Diversity of Ornithonyssus

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Molecular Characterization and Genetic Diversity of Ornithonyssus Bhowmick et al. Parasites Vectors (2019) 12:553 https://doi.org/10.1186/s13071-019-3809-9 Parasites & Vectors RESEARCH Open Access Molecular characterization and genetic diversity of Ornithonyssus sylviarum in chickens (Gallus gallus) from Hainan Island, China Biswajit Bhowmick1, Jianguo Zhao1, Øivind Øines2, Tianlin Bi1, Chenghong Liao1, Lei Zhang1 and Qian Han1* Abstract Background: The northern fowl mite (NFM), Ornithonyssus sylviarum, is an obligatory hematophagous ectoparasite of birds and one of the most important pests in the poultry industry on several continents. Although NFM poses a serious problem, it remains a neglected pest of poultry in China and other Asian countries. Therefore, a molecular analysis was conducted to provide baseline information on the occurrence, genetic diversity and emergence of NFM in poultry farms from China. Methods: This study focused on morphological description and identifcation of adults based on electron micros- copy, molecular sequencing of the mitochondrial cox1 gene and phylogenetic analysis. We have also used the DNA sequences of the cox1 gene to study the genetic diversity, population structure and demographic history. The neutral- ity tests were used to analyze signatures of historical demographic events. Results: The mites collected were identifed as the northern fowl mite Ornithonyssus sylviarum based on external morphological characterization using electron microscopy. Molecular analysis using a 756-bp long partial fragment of the cox1 gene revealed 99–100% sequence identity with NFM and phylogenetic inferences showed a bootstrap value of 99% indicating a well-supported monophyletic relationship. Molecular diversity indices showed high levels of hap- lotype diversity dominated by private haplotypes, but low nucleotide divergence between haplotypes. The Tajima’s D test and Fu’s Fs test showed negative value, indicating deviations from neutrality and both suggested recent popu- lation expansion of mite populations supported by a star-like topology of the isolates in the network analysis. Our genetic data are consistent with a single introduction of NFM infestations and the spread of NFM infestation in Hainan poultry farms and a private haplotype dominance, which suggest that infestations are recycled within the farms and transmission routes are limited between farms. Conclusions: To our knowledge, this is the frst time a molecular report of NFM in chicken from China including other Asian countries using DNA barcoding. The fndings have potential implications with respect to understanding the transmission patterns, emergence and populations trends of parasitic infestations of poultry farms that will help for setting the parameters for integrated pest management (IPM) tactics against mite infestations. Keywords: Ornithonyssus sylviarum, cox1 gene, Identifcation, Genetic diversity, Chicken *Correspondence: [email protected] 1 Key Laboratory of Tropical Biological Resources of Ministry of Education and Laboratory of Tropical Veterinary Medicine and Vector Biology, School of Life and Pharmaceutical Sciences, Hainan University, Haikou, Hainan 570228, China Full list of author information is available at the end of the article © The Author(s) 2019. This 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. Bhowmick et al. Parasites Vectors (2019) 12:553 Page 2 of 15 Background levels, NFM can cause up to 6% blood loss per day per Te northern fowl mite (NFM), Ornithonyssus sylvi- hen, in addition to an activation of the of host’s immune arum, (Canestrini & Fanzago, 1877) (Mesostigmata: responses. Signs of NFM infestation include restless- Macronyssidae), was frst discovered in Pisa, Italy, in ness, feather pecking, cannibalism, and anaemia that in 1877 [1], but was frst described in substantial detail severe infestations can cause death [22]. and under controlled conditions by Sikes & Chamber- Although exact species identifcation is an important lain [2]. It is one of the primary blood-feeding ectopar- frst step in any biological study, species that are closely asites in poultry. Many North American records found related can be difcult to distinguish by the use of mor- that 72 species of wild birds from 26 bird families can phological characters alone because of similar gross serve as hosts for NFM [3]. Although NFM and another morphology, unclear or inconsistent diagnostic morpho- two species of mites, i.e. the tropical fowl mite (TFM) logical characters and high levels of morphological plas- Ornithonyssus bursa and the poultry red mite (PRM) ticity [23–25]. More than 40,000 species of mites have Dermanyssus gallinae, are largely considered as avian- been described, and up to 1 million may grace our planet. specifc ectoparasites, when natural host is absent, Tese eight-legged arthropods (arachnids) represent one hungry mites will occasionally feed on a range of mam- of the most successful animal radiations on land [26]. mals, i.e. dogs [4], cats [5], horses [6], and humans par- Tis calls for a need for specialists to be able to diferenti- ticularly in people living or working in close proximity ate these from thousands of other mite species. Morpho- to poultry [7–10]. Te poultry red mite D. gallinae logical identifcation may also be very labour-intensive if (Mesostigmata: Dermanyssidae) was frst identifed by several specimens need to be identifed. Some key charac- De Geer in 1778 and the tropical fowl mite, O. bursa ters may also only be present in certain life stages or only (Berlese, 1888) (Mesostigmata: Macronyssidae) was in females or males, limiting their usefulness across a frst recognized as a potentially serious poultry pest by variety of sample and sample types. Terefore, the use of Wood [11]. Tropical fowl mite (TFM) and poultry red sex- and life-stage independent approaches, such as using mite (PRM) both are also common blood-sucking avian DNA-based methods could be key for successful identi- ectoparasites found in the poultry industry [12, 13]. fcation at the species level. Tis approach can also pro- Superfcially, NFM resembles PRM in gross appear- vide additional information such as distribution patterns, ance; however, there are morphological keys present to origin, epidemiological and systematic investigations data diferentiate these species [14]. Unlike other mites of for a particular species. Among diferent DNA regions poultry, D. gallinae feeds mainly at night and for short used in molecular systematics, mitochondrial DNA is a periods of time. Te rest of the time, mites reside in suitable tool as a molecular marker for both intraspecifc multi-stage colonies in cracks, crevices and hide away variation and species identifcation due to higher evo- from the birds for the remainder of the time [15]. In lution rate of genes compared to those in nuclear DNA contrast, NFM and TFM are permanent ectoparasites and their strictly maternal inheritance has been par- and complete their entire life-cycle on avian hosts [16, ticularly useful at the intraspecifc level [27, 28]. As the 17]. Te nymphs and adults of TFM take blood meals, mitochondrial genome has a high copy number in most as opposed to only the protonymph and adult stages cells, molecular diagnostic tools targeting mitochondrial in NFM and PRM [2, 18]. NFM can cause severe dam- sequences may have the additional advantage of higher age and loss for chicken and turkey breeders, as well as detection sensitivity than those targeting nuclear genes egg degradation, and is considered a key pest for lay- [27]. Among diferent mitochondrial DNA regions, the ers in North America, Brazil, China and Australia [19]. mitochondrial protein-coding gene cytochrome c oxi- Although widespread, NFM is not a major problem in dase subunit 1 (cox1) has been used as successful genetic commercial poultry uniformly across the world [19]. marker in barcoding of mites. Many studies have demon- PRM has a global distribution and is now at epidemic strated that cox1 can provide a powerful tool for phyloge- levels in many parts of the world [15]. Te tropical fowl netics at the deepest levels within the Acari [29–31], and mite is widely distributed throughout subtropical and for description of more shallow genetic relatedness, such tropical countries [13]. However, there are some areas as the movement of mites between farms and to describe like Brazil where all three mite species have been col- industrial routes in larger geographical areas [32]. cox1 lected from birds [20]. In China, Wang et al. [21] found has been known as the ‘barcoding gene’ and it has proven that NFM prevalence was 47% in parent hens, whilst for successful for its use for species identifcation and dis- the commercial layers the prevalence was 64% for PRM covery across a variety of animal organisms [33]. Te [21]. Tis suggests that these mites succeed diferently usefulness of the marker is justifed by the availability of depending on the production systems due to difer- abundant cox1 data generated for a variety of organisms ences in their behavior and biology. At high
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