Wolbachia is a common intracellular bacterial genus that infects numerous arthropods and filarial nematodes. In arthropods, it typically acts as a reproductive parasite, leading to various phenotypic effects such as cytoplasmic incompatibility, parthenogenesis, feminization, or male-killing. Quill mites (Acariformes: Syringophilidae) are a group of bird parasites that have recently attracted increasing interest due to the detection of unique phylogenetic lineages of endosymbiotic bacteria and potentially pathogenic taxa. Our study used an unbiased 16S rRNA gene amplicon sequencing approach to examine several populations of Namibian quill mites for the presence of bacteria that could affect their biology. We detected Wolbachia in two mite populations collected from two species of larks. However, we did not find any other endosymbiotic bacteria or any that could be of epidemiological importance. Since the mite taxa we tested were previously unknown to science, we conducted comprehensive morphological and molecular systematic analyses on them. Our research revealed two new quill mite species of the genus Syringophilopsis Kethley, 1970 which parasitize three sub-Saharan alaudids, i.e., Syringophilopsis erythrochlamys sp. n. from the dune lark Calendulauda erythrochlamys (Strickland, HE) and S. christinae sp. n. from the Karoo long-billed lark Certhilauda subcoronata (Smith) and spike-heeled lark Chersomanes albofasciata (de Lafresnaye, NFAA). In addition, we provided the African reed warbler Acrocephalus baeticatus (Vieillot, LJP) as a new host for S. acrocephali Skoracki, 1999. Our study expands the knowledge on parasite diversity and provides new insights into Wolbachia infection among quill mites in Africa.

Crop Research Institute Drnovska 507 73 6 Ruzyne CZ 16106 Prague Czech Republic

Department of Animal Morphology Faculty of Biology Adam Mickiewicz University in Poznań Uniwersytetu Poznańskiego 6 61 614 Poznań Poland

Division of Birds Smithsonian Institution P O Box 37012 MRC 116 Washington DC 20013 7012 USA

Molecular Biology Techniques Laboratory Faculty of Biology Adam Mickiewicz University in Poznań Uniwersytetu Poznańskiego 6 61 614 Poznań Poland

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Werren J.H. Biology of Wolbachia. Annu. Rev. Entomol. 1997;42:587–609. doi: 10.1146/annurev.ento.42.1.587. PubMed DOI

Sharon G., Segal D., Ringo J., Hefetz A., Zilber-Rosenberg I., Rosenberg E. Commensal bacteria play a role in mating preference of Drosophila melanogaster. Proc. Natl. Acad. Sci. USA. 2010;107:20051–20056. doi: 10.1073/pnas.1009906107. PubMed DOI PMC

Zug R., Hammerstein P. Still a host of hosts for Wolbachia: Analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PLoS ONE. 2012;7:e38544. doi: 10.1371/journal.pone.0038544. PubMed DOI PMC

Glowska E., Dragun-Damian A., Dabert M., Gerth M. New Wolbachia supergroups detected in quill mites (Acari: Syringophilidae) Infect. Genet. Evol. 2015;30:140–146. doi: 10.1016/j.meegid.2014.12.019. PubMed DOI

Glowska E., Filutowska Z.K., Dabert M., Gerth M. Microbial composition of enigmatic bird parasites: Wolbachia and Spiroplasma are the most important bacterial associates of quill mites (Acariformes: Syringophilidae) MicrobiologyOpen. 2020;9:e964. doi: 10.1002/mbo3.964. PubMed DOI PMC

Johnston D.E., Kethley J.B. A numerical phenetic study of the quill mites of the family Syringophilidae (Acari) J. Parasitol. 1973;59:520–530. doi: 10.2307/3278787. DOI

Glowska E., Chrzanowski M., Kaszewska K. Checklist of the quill mites (Acariformes: Syringophilidae) of the World. Zootaxa. 2015;3968:001–081. doi: 10.11646/zootaxa.3968.1.1. PubMed DOI

Zmudzinski M., Skoracki M., Sikora B. An Updated Checklist of Quill Mites of the Family Syringophilidae (Acariformes: Prostigmata) 2021. [(accessed on 4 November 2024)]. Available online: https://figshare.com/articles/dataset/An_updated_checklist_of_quill_mites_of_the_family_Syringophilidae_Acariformes_Prostigmata_/16529574/1.

Skoracki M., Sikora B., Unsoeld M., Hromada M. Mite Fauna of the Family Syringophilidae (Acariformes: Prostigmata) Parasitizing Darwin’s Finches in Galápagos Archipelago. Diversity. 2022;14:585. doi: 10.3390/d14080585. DOI

Sikora B., Mahamoud-Issa M., Unsoeld M., Hromada M., Skoracki M. Species Composition of Parasitic Mites of the Subfamily Picobiinae (Acariformes: Syringophilidae) Associated with African Barbets (Piciformes: Lybiidae) Animals. 2023;13:2007. doi: 10.3390/ani13122007. PubMed DOI PMC

Skoracki M., Michalik J., Sikora B. Prevalence and habitat preference of quill mites (Acari, Syringophilidae) parasitizing forest passerine birds in Poland. Acta Parasitol. 2010;55:188–193. doi: 10.2478/s11686-010-0021-7. DOI

Glowska E., Dragun-Damian A., Dabert J. DNA-barcoding contradicts morphology in quill mite species Torotrogla merulae and T. rubeculi (Prostigmata: Syringophilidae) Folia Parasitol. 2013;60:51–60. doi: 10.14411/fp.2013.007. PubMed DOI

Glowska E., Dragun-Damian A., Broda L., Dabert J., Dabert M. DNA barcodes reveal female dimorphism in syringophilid mites (Actinotrichida: Prostigmata: Cheyletoidea): Stibarokris phoeniconaias and Ciconichenophilus phoeniconaias are conspecific. Folia Parasitol. 2014;61:272–276. doi: 10.14411/fp.2014.030. PubMed DOI

Glowska E., Broda L., Dabert M. Insight into the species diversity of the quill mite genus Betasyringophiloidus Skoracki, 2011 (Prostigmata: Syringophilidae) on the basis of the DNA barcodes. Folia Parasitol. 2019;66:009. doi: 10.14411/fp.2019.009. PubMed DOI

Skoracki M., Michalik J., Skotarczak B., Rymaszewska A., Sikora B., Hofman T., Wodecka B., Sawczuk M. First detection of Anaplasma phagocytophilum in quill mites (Acari: Syringophi-lidae) parasitizing passerine birds. Microbes Infect. 2006;8:303–307. doi: 10.1016/j.micinf.2005.06.029. PubMed DOI

Dabert J., Ehrnsberger R., Dabert M. Glaucalges tytonis sp. n. (Analgoidea, Xolalgidae) from the barn owl Tyto alba (Strigiformes, Tytonidae): Compiling morphology with DNA barcode data for taxon descriptions in mites (Acari) Zootaxa. 2008;1719:41–52. doi: 10.11646/zootaxa.1719.1.2. DOI

Therese K.L., Anand A.R., Madhavan H.N. Polymerase chain reaction in the diagnosis of bacterial endophthalmitis. BJO. 1998;82:1078–1082. doi: 10.1136/bjo.82.9.1078. PubMed DOI PMC

Hannon G.J. FASTX-Toolkit. 2014. [(accessed on 20 October 2024)]. Available online: http://hannonlab.cshl.edu.

Bolyen E., Rideout J.R., Dillon M.R., Bokulich N.A., Abnet C.C., Al-Ghalith G.A., Alexander H., Alm E.J., Arumugam M., Asnicar F., et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat. Biotechnol. 2019;37:852–857. doi: 10.1038/s41587-019-0209-9. PubMed DOI PMC

Callahan B.J., McMurdie P.J., Rosen M.J., Han A.W., Johnson A.J.A., Holmes S.P. DADA2: High-resolution sample inference from Illumina amplicon data. Nat. Methods. 2016;13:581–583. doi: 10.1038/nmeth.3869. PubMed DOI PMC

Edgar R.C. UNCROSS2: Identification of cross-talk in 16S rRNA OTU tables. bioRxiv. 2018:400762. doi: 10.1101/400762. DOI

Glöckner F.O., Yilmaz P., Quast C., Gerken J., Beccati A., Ciuprina A., Bruns G., Yarza P., Peplies J., Westram R., et al. 25 years of serving the community with ribosomal RNA gene reference databases and tools. J. Biotechnol. 2017;261:169–176. doi: 10.1016/j.jbiotec.2017.06.1198. PubMed DOI

Quast C., Pruesse E., Yilmaz P., Gerken J., Schweer T., Yarza P., Peplies J., Glöckner F.O. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 2013;41:590–596. doi: 10.1093/nar/gks1219. PubMed DOI PMC

Yilmaz P., Parfrey L.W., Yarza P., Gerken J., Pruesse E., Quast C., Schweer T., Peplies J., Ludwig W., Glöckner F.O. The SILVA and ‘all-species Living Tree Project (LTP)’ taxonomic frameworks. Nucleic Acids Res. 2014;42:643–648. doi: 10.1093/nar/gkt1209. PubMed DOI PMC

Kimura M. A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 1980;16:111–120. doi: 10.1007/BF01731581. PubMed DOI

Kumar S., Stecher G., Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol. Biol. Evol. 2016;33:1870–1874. doi: 10.1093/molbev/msw054. PubMed DOI PMC

Grandjean F. Les segments postlarvaires de l’hysterosoma chez les oribates (Acariens) Bull. Soc. Zool. Fr. 1939;64:273–284.

Kethley J.B. Acarina: Prostigmata (Actinedida) In: Dindal D.L., editor. Soil Biology Guide. Wiley and Sons; New York, NY, USA: 1990. pp. 667–754.

Grandjean F. Observations sur les acariens de la famille Stigmaeidae. Arch. Sci. Phys. Nat. 1944;26:103–131.

Bochkov A.V., OConnor B.M., Wauthy G. Phylogenetic position of the family Myobiidae within the Prostigmata (Acari: Acariformes) Zool. Anz. 2008;247:15–45. doi: 10.1016/j.jcz.2006.12.003. DOI

Skoracki M. Quill mites (Acari: Syringophilidae) of the Palaearctic region. Zootaxa. 2011;2840:1–414. doi: 10.11646/zootaxa.2840.1.1. DOI

Clements J.F., Schulenberg T.S., Iliff M.J., Roberson D., Fredericks T.A., Sullivan B.L., Wood C.L. The eBird/Clements Checklist of Birds of the World: v2022. [(accessed on 14 October 2024)]. Available online: http://www.birds.cornell.edu/clementschecklist/download/

Skoracki M., Flannery M.E., Spicer G.S. Quill mites of the genus Syringophilopsis Kethley, 1970 (Acari: Syringophilidae) from North American birds. Folia Parasitol. 2008;55:291–300. doi: 10.14411/fp.2008.037. PubMed DOI

Skoracki M. New genus and species of Syringophilidae from Eurasian Reed Warbler, Acrocephalus scirpaceus (Sylviidae: Passeriformes) Genus. 1999;10:155–162.

Glowska E., Dragun-Damian A., Dabert J. A new quill mite Syringophiloidus pseudonigritae sp. nov. (Prostigmata, Syringophilidae) parasitizing Pseudonigrita arnaudi (Passeriformes, Ploceidae)—A combined description using morphology and DNA barcode data. Zootaxa. 2012;3532:64–68. doi: 10.11646/zootaxa.3532.1.5. DOI

Glowska E., Broda L., Dabert M. A new quill mite Syringophiloidus plocei sp. nov. (Prostigmata: Syringophilidae) parasitizing ploceid birds (Passeriformes) in Gabon—A combined description using morphology and DNA barcode data. Acta Parasitol. 2016;61:562–566. doi: 10.1515/ap-2016-0075. PubMed DOI

Glowska E., Romanowska K., Schmidt B.K., Dabert M. Combined description (morphology with DNA barcode data) of a new quill mite Torotrogla paenae n. sp. (Acariformes: Syringophilidae) parasitising the Kalahari scrub-robin Cercotrichas paena (Smith) (Passeriformes: Muscicapidae) in Namibia. Syst. Parasitol. 2018;95:863–869. doi: 10.1007/s11230-018-9815-z. PubMed DOI PMC

Skoracki M.K., Dabert J., Schmäschke R. Observations on the quill mites (Acari: Syringophilidae) from charadriiform birds. Zootaxa. 2006;1156:51–64. doi: 10.11646/zootaxa.1156.1.2. DOI

Hosokawa T., Koga R., Kikuchi Y., Meng X.-Y., Fukatsu T. Wolbachia as a bacteriocyte-associated nutritional mutualist. Proc. Natl. Acad. Sci. USA. 2010;107:769–774. doi: 10.1073/pnas.0911476107. PubMed DOI PMC

Duron O., Morel O., Noël V., Buysse M., Binetruy F., Lancelot R., Loire E., Ménard C., Bouchez O., Vavre F., et al. Tick-bacteria mutualism depends on B vitamin synthesis pathways. Curr. Biol. 2018;28:1896–1902.e5. doi: 10.1016/j.cub.2018.04.038. PubMed DOI

Dille J.W., Rogers C.M., Schneegurt M.A. Isolation and characterization of bacteria from the feathers of wild Dark-eyed Juncos (Junco hyemalis) Auk. 2016;133:155–167. doi: 10.1642/AUK-15-126.1. DOI

Engel K., Sauer J., Jünemann S., Winkler A., Wibberg D., Kalinowski J., Tauch A., Caspers B.A. Individual- and species-specific skin microbiomes in three different estrildid finch species revealed by 16S amplicon sequencing. Microb. Ecol. 2018;76:518–529. doi: 10.1007/s00248-017-1130-8. PubMed DOI

Pearce D.S., Hoover B.A., Jennings S., Nevitt G.A., Docherty K.M. Morphological and genetic factors shape the microbiome of a seabird species (Oceanodroma leucorhoa) more than environmental and social factors. Microbiome. 2017;5:146. doi: 10.1186/s40168-017-0365-4. PubMed DOI PMC

Kethley J.B. A revision of the family Syringophilidae (Prostigmata: Acarina) Contrib. Am. Entomol. Inst. 1970;6:1–76.

Skoracki M., Dabert J. Syringophilopsis albicollisi sp. n., a new species of the quill mite of the family Syringophilidae (Acari: Prostigmata) Acarina. 2000;8:59–63.

Skoracki M., Hromada M., Wamiti W. A new species and new host records of syringophilid mites (Acari: Syringophilidae) from passerines from Kenya. Zootaxa. 2011;2922:34–40. doi: 10.11646/zootaxa.2922.1.4. DOI

Skoracki M.K., Hromada M., Kaszewska K., Sikora B. Females of the quill mite genera Peristerophila and Castosyringophilus (Acariformes: Syringophilidae) are two morphological forms: Ontogenetic and population evidences. SAA. 2020;25:1803–1820. doi: 10.11158/saa.25.10.6. DOI

Hebert P.D., Ratnasingham S., deWaard J.R. Barcoding animal life: Cytochrome c oxidase subunit 1 divergences among closely related species. Proc. Biol. Sci. 2003;270((Suppl. S1)):S96–S99. doi: 10.1098/rsbl.2003.0025. PubMed DOI PMC

Hebert P.D., Penton E.H., Burns J.M., Janzen D.H., Hallwachs W. Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc. Natl. Acad. Sci. USA. 2004;101:14812–14817. doi: 10.1073/pnas.0406166101. PubMed DOI PMC

Broda L., Dabert M., Glowska E. Aulonastus similis n. sp.—Combined description (morphology with DNA barcode data) of a new quill mite species (Syringophilidae) parasitising passeriform birds (Tyrannidae, Cardinalidae) in Mexico. Syst. Parasitol. 2016;93:715–719. doi: 10.1007/s11230-016-9653-9. PubMed DOI PMC