Urban emergence of Dermanyssus gallinae lineage L1 and Ornithonyssus sylviarum in Hungary: phylogenetic differentiation between the roles of migrating vs transported synanthropic birds

Abstract Background Among Dermanyssoidea, the chicken red mite (Dermanyssus gallinae) and the northern fowl mite (Ornithonyssus sylviarum) are considered to be the cause of high economic losses endured by the poultry industry in the Holarctic region, with O. sylviarum predominating in North America...

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Main Authors: Sándor Hornok, Nóra Takács, Gábor Sipos, Pál Morandini, Attila D. Sándor, Sándor Szekeres, Andrea Grima, Jenő Kontschán
Format: Article
Language:English
Published: BMC 2021-03-01
Series:Parasites & Vectors
Subjects:
Online Access:https://doi.org/10.1186/s13071-021-04643-3
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author Sándor Hornok
Nóra Takács
Gábor Sipos
Pál Morandini
Attila D. Sándor
Sándor Szekeres
Andrea Grima
Jenő Kontschán
author_facet Sándor Hornok
Nóra Takács
Gábor Sipos
Pál Morandini
Attila D. Sándor
Sándor Szekeres
Andrea Grima
Jenő Kontschán
author_sort Sándor Hornok
collection DOAJ
description Abstract Background Among Dermanyssoidea, the chicken red mite (Dermanyssus gallinae) and the northern fowl mite (Ornithonyssus sylviarum) are considered to be the cause of high economic losses endured by the poultry industry in the Holarctic region, with O. sylviarum predominating in North America and D. gallinae in Europe. Both species have a short life-cycle (thereby allowing a rapid build-up of massive infestations), a wide range of hosts, synanthropic presence and the ability to bite humans. The aim of this study was to analyze dermanyssoid mite specimens, collected in two human dwellings and two racing pigeon premises in different urban areas in Hungary, with molecular–phylogenetic methods. Methods Mite species were identified morphologically. This was followed by DNA extraction and molecular–phylogenetic analyses of selected mites, based on the cytochrome c oxidase subunit I (cox1) and 28S rRNA (28S) genes. Results Mites that had invaded a home from a pigeon nest and were linked to human dermatitis were morphologically and molecularly identified as D. gallinae special lineage L1. Specimens collected at all other sampling sites were identified as O. sylviarum, including mites that had invaded a home from a house martin (Delichon urbicum) nest, as well as those which were collected from racing pigeons. House martin- or pigeon-associated O. sylviarum specimens showed the highest sequence identity and closest phylogenetic relationship with conspecific mites reported in GenBank from Israel or Canada, respectively. Conclusions Detailed morphological and molecular–phylogenetic analyses of D. gallinae lineage L1 confirmed its status as a cryptic species within D. gallinae (s.l.). Taking into account the well-documented latitudinal migratory routes of house martins between Hungary and Africa, O. sylviarum associated with this bird species most likely arrived on its host from the eastern Mediterranean region. On the other hand, mites collected from pigeons in Hungary showed cox1 genetic homogeneity with North American O. sylviarum, which can only be explained by a long-distance (west-to-east intercontinental) connection of birds and their mites as part of human activity (e.g. transportation to exhibitions or trading). In summary, this is the first molecularly confirmed and phylogenetically analyzed case of O. sylviarum infestation of birds in Hungary, implicating urban environment and involving distant parts of the country. This is also the first report of D. gallinae lineage L1 in central Europe.
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spelling doaj.art-8ccd411546c6498cb4503922b14120b52022-12-21T20:00:49ZengBMCParasites & Vectors1756-33052021-03-011411910.1186/s13071-021-04643-3Urban emergence of Dermanyssus gallinae lineage L1 and Ornithonyssus sylviarum in Hungary: phylogenetic differentiation between the roles of migrating vs transported synanthropic birdsSándor Hornok0Nóra Takács1Gábor Sipos2Pál Morandini3Attila D. Sándor4Sándor Szekeres5Andrea Grima6Jenő Kontschán7Department of Parasitology and Zoology, University of Veterinary MedicineDepartment of Parasitology and Zoology, University of Veterinary MedicineDepartment of Parasitology and Zoology, University of Veterinary MedicineHungarian Ornithological and Nature Conservation SocietyDepartment of Parasitology and Zoology, University of Veterinary MedicineDepartment of Parasitology and Zoology, University of Veterinary MedicineAPH Veterinary HospitalPlant Protection Institute, Centre for Agricultural Research, ELKHAbstract Background Among Dermanyssoidea, the chicken red mite (Dermanyssus gallinae) and the northern fowl mite (Ornithonyssus sylviarum) are considered to be the cause of high economic losses endured by the poultry industry in the Holarctic region, with O. sylviarum predominating in North America and D. gallinae in Europe. Both species have a short life-cycle (thereby allowing a rapid build-up of massive infestations), a wide range of hosts, synanthropic presence and the ability to bite humans. The aim of this study was to analyze dermanyssoid mite specimens, collected in two human dwellings and two racing pigeon premises in different urban areas in Hungary, with molecular–phylogenetic methods. Methods Mite species were identified morphologically. This was followed by DNA extraction and molecular–phylogenetic analyses of selected mites, based on the cytochrome c oxidase subunit I (cox1) and 28S rRNA (28S) genes. Results Mites that had invaded a home from a pigeon nest and were linked to human dermatitis were morphologically and molecularly identified as D. gallinae special lineage L1. Specimens collected at all other sampling sites were identified as O. sylviarum, including mites that had invaded a home from a house martin (Delichon urbicum) nest, as well as those which were collected from racing pigeons. House martin- or pigeon-associated O. sylviarum specimens showed the highest sequence identity and closest phylogenetic relationship with conspecific mites reported in GenBank from Israel or Canada, respectively. Conclusions Detailed morphological and molecular–phylogenetic analyses of D. gallinae lineage L1 confirmed its status as a cryptic species within D. gallinae (s.l.). Taking into account the well-documented latitudinal migratory routes of house martins between Hungary and Africa, O. sylviarum associated with this bird species most likely arrived on its host from the eastern Mediterranean region. On the other hand, mites collected from pigeons in Hungary showed cox1 genetic homogeneity with North American O. sylviarum, which can only be explained by a long-distance (west-to-east intercontinental) connection of birds and their mites as part of human activity (e.g. transportation to exhibitions or trading). In summary, this is the first molecularly confirmed and phylogenetically analyzed case of O. sylviarum infestation of birds in Hungary, implicating urban environment and involving distant parts of the country. This is also the first report of D. gallinae lineage L1 in central Europe.https://doi.org/10.1186/s13071-021-04643-3DermanyssoideaChicken red miteNorthern fowl miteCox128S rRNA
spellingShingle Sándor Hornok
Nóra Takács
Gábor Sipos
Pál Morandini
Attila D. Sándor
Sándor Szekeres
Andrea Grima
Jenő Kontschán
Urban emergence of Dermanyssus gallinae lineage L1 and Ornithonyssus sylviarum in Hungary: phylogenetic differentiation between the roles of migrating vs transported synanthropic birds
Parasites & Vectors
Dermanyssoidea
Chicken red mite
Northern fowl mite
Cox1
28S rRNA
title Urban emergence of Dermanyssus gallinae lineage L1 and Ornithonyssus sylviarum in Hungary: phylogenetic differentiation between the roles of migrating vs transported synanthropic birds
title_full Urban emergence of Dermanyssus gallinae lineage L1 and Ornithonyssus sylviarum in Hungary: phylogenetic differentiation between the roles of migrating vs transported synanthropic birds
title_fullStr Urban emergence of Dermanyssus gallinae lineage L1 and Ornithonyssus sylviarum in Hungary: phylogenetic differentiation between the roles of migrating vs transported synanthropic birds
title_full_unstemmed Urban emergence of Dermanyssus gallinae lineage L1 and Ornithonyssus sylviarum in Hungary: phylogenetic differentiation between the roles of migrating vs transported synanthropic birds
title_short Urban emergence of Dermanyssus gallinae lineage L1 and Ornithonyssus sylviarum in Hungary: phylogenetic differentiation between the roles of migrating vs transported synanthropic birds
title_sort urban emergence of dermanyssus gallinae lineage l1 and ornithonyssus sylviarum in hungary phylogenetic differentiation between the roles of migrating vs transported synanthropic birds
topic Dermanyssoidea
Chicken red mite
Northern fowl mite
Cox1
28S rRNA
url https://doi.org/10.1186/s13071-021-04643-3
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