Evaluation of Genetic Diversity in Quill Mites of the Genus Syringophiloidus Kethley, 1970 (Prostigmata: Syringophilidae) with Six New-to-Science Species.

Quill mites (Acariformes: Syringophilidae) are poorly explored bird parasites. Syringophiloidus Kethley, 1970, is the most specious and widespread genus in this family. It is believed to contain mono-, steno- and poly-xenous parasites and thus seems to be an exemplary for studies on biodiversity and host associations. In this work, we applied the DNA barcode marker (mitochondrial cytochrome c oxidase subunit I gene fragment, COI) to analyze the species composition and host specificity of representatives of fifteen Syringophiloidus populations parasitizing fifteen bird species. The neighbor joining analyses distinguished thirteen monophyletic lineages, almost completely corresponding to seven previously known species recognized based on morphological features, and six new-to-science species. The only exception is S. amazilia Skoracki, 2017, which is most likely conspecific with Syringophiloidus stawarczyki Skoracki, 2004. The intraspecific distances of all species were not higher than 0.9%, whilst the interspecific diversity ranged from 5.9% to 19.2% and 6.3-22.4%, inferred as the distances p and K2P, respectively. Although all putative species (except S. amazilia) are highly supported, the relationships between them have not been fully resolved and only faintly indicate that both host phylogeny and distributions influence the phylogenetic structure of quill mite taxa.

Draft genome sequence of a Wolbachia endosymbiont from Syringophilopsis turdi (Fritsch, 1958) (Acari, Syringophilidae).

We present the draft genome of a Wolbachia endosymbiont from quill mites. This is the first representative of a recently discovered distinct Wolbachia lineage (supergroup P). We hope the genome will be a useful resource for comparative evolutionary and genomic studies across the globally distributed symbiont Wolbachia.

Microbial composition of enigmatic bird parasites: Wolbachia and Spiroplasma are the most important bacterial associates of quill mites (Acariformes: Syringophilidae).

BACKGROUND: The microbiome is an integral component of many animal species, potentially affecting behavior, physiology, and other biological properties. Despite this importance, bacterial communities remain vastly understudied in many groups of invertebrates, including mites. Quill mites (Acariformes: Syringophilidae) are a poorly known group of permanent bird ectoparasites that occupy quills of feathers and feed on bird subcutaneous tissue and fluids. Most of the known species have strongly female-biased sex ratio, and it was hypothesized that this is caused by endosymbiotic bacteria. Previously, Anaplasma phagocytophilum (Foggie) and a high diversity of Wolbachia strains were detected in quill mites via targeted PCR screens. Here, we use an unbiased 16S rRNA gene amplicon sequencing approach to determine other bacteria that potentially impact quill mite biology. RESULTS: We performed 16S rRNA gene amplicon sequencing of 126 quill mite individuals from eleven species parasitizing twelve species (four families) of passeriform birds. In addition to Wolbachia, we found Spiroplasma as potential symbiont of quill mites. Consistently, high Spiroplasma titers were only found in individuals of two mite species associated with finches of the genus Carduelis, suggesting a history of horizontal transfers of Spiroplasma via the bird host. Furthermore, there was evidence for Spiroplasma negatively affecting Wolbachia titers. We found no evidence for the previously reported Anaplasma in quill mites, but detected sequences of high similarity to the potential pathogens Brucella and Bartonella at low abundances. Other amplicon sequence variants (ASVs) could be assigned to a diverse number of bacterial taxa, including several that were previously isolated from bird skin. Further, many frequently found ASVs were assigned to taxa that show a very broad distribution with no strong prior evidence for symbiotic association with animals. We interpret these findings as evidence for a scarcity of resident microbial associates (other than inherited symbionts) in quill mites.

Insight into the species diversity of the quill mite genus Betasyringophiloidus Skoracki, 2011 (Prostigmata: Syringophilidae) on the basis of the DNA barcodes.

Betasyringophiloidus Skoracki, 2011 is a genus of quill mites (Prostigmata: Syringophilidae) that is believed to contain mono-, steno- and polyxenous parasites associated with a wide range of passerine birds (Passeriformes) across the world. In this work we applied the DNA-barcode marker (mitochondrial cytochrome c oxidase subunit I gene fragment, COI) to verify whether Betasyringophiloidus schoeniclus (Skoracki, 2002) and Betasyringophiloidus seiuri (Clark, 1964) are actual steno- and polyxenous species associated with the currently recognised host ranges, or their populations are highly host-specific, cryptic species. Our results revealed that a population living on the Tristram's bunting Emberiza tristrami Swinhoe (Emberizidae) in Russia, so far classified as B. schoeniclus, is a new cryptic species Betasyringophiloidus emberizae sp. nov. Both topologies of the neighbor-joining and maximum likelihood phylogenetic trees as well as genetic distance (11.9% Kimura 2-parameter distance) (K2P) support species status of the mite population from E. tristrami. The same data support previously established conspecific status of B. seiuri found on the ovenbird Seiurus aurocapilla (Linnaeus) (Parulidae) (type host) and the northern waterthrush Parkesia noveboracensis (Gmelin) (Parulidae) and expand its range with a population found on a new host species Icterus pustulatus (Wagler) (Icteridae) with intraspecific K2P distance up to 1.9% and interpopulation distances ranging from 1.3 to 3.1%.

A new quill mite Torotrogla emberizae sp. nov. (Acariformes: Syringophilidae) from the Chestnut-eared Bunting (Passeriformes: Emberizidae) in Japan (morphology and DNA barcode data).

A new quill mite Torotrogla emberizae sp. nov. (Acariformes: Syringophilidae) parasitizing the Chestnut-eared Bunting Emberiza fucata Pallas, 1776 (Passeriformes: Emberizidae) in Japan is described based on the external morphology and DNA barcode data (mitochondrial cytochrome c oxidase subunit I sequences, COI). Females of T. emberizae sp. nov. differ from T. volgini Skoracki and Mironov, 2013 by having the short, wide and blunt-ended hypostomal protuberances (vs long, thin and sharp-ended), setae h1 ca. twice shorter than f1 (vs h1 longer than f1), the fan-like setae p' and p" of legs III-IV provided with ca. 10 tines (vs 7-8 tines) and lengths of setae vi 70-105 (vs 55-65), ve 105-135 (vs 85-90) and h1 55-60 (vs 95-120).

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.

A new quill mite species Torotrogla paenae n. sp. (Acariformes: Syringophilidae) parasitising the Kalahari scrub-robin Cercotrichas paena (Smith) (Passeriformes: Muscicapidae) in Namibia is described based on the external morphology and DNA barcode data (the mitochondrial cytochrome c oxidase subunit 1 sequences, cox1). Females of T. paenae n. sp. morphologically differ from the most similar species T. lusciniae Skoracki, 2004 by the total body length (780-830 vs 645-715 µm in T. lusciniae) and the presence of hysteronotal shields (vs absence), apunctate propodonotal and pygidial shields (vs punctate), apunctate coxal fields (vs punctate), the fan-like setae p' and p" of legs III-IV provided with c.10 tines (vs 14-15) and the length of setae si (140-180 vs 190-210 µm) and se (160-185 vs 210-225 µm). The male of T. paenae n. sp. morphologically differs from T. lusciniae by the lateral branch of peritremes composed of 4 chambers (vs 7-8 chambers) and lengths of setae ve (45 vs 70-75 µm) and se (120 vs 165 µm).

Aulonastus similis n. sp., a new quill mite species (Syringophilidae) parasitising passeriform birds (Tyrannidae and Cardinalidae) in Mexico.

A new quill mite species, Aulonastus similis n. sp. (Acariformes: Syringophilidae), parasitising Myiozetetes similis (Spix) (Tyrannidae) and Habia fuscicauda (Cabanis) (Cardinalidae) in Mexico is described and DNA barcode sequences of the mitochondrial cytochrome c oxidase subunit I (cox1) and D1-D3 region of the nuclear 28S rRNA gene are provided. Morphologically, females of A. similis are close to A. euphagus Skoracki, Hendricks & Spicer, 2010 but differ from this species in the length ratios of the idiosomal setae: ve:si (2-2.3:1 vs 1:1) and f2:f1 (4.7-6.3:1 vs 3.3:1).

A new quill mite Syringophiloidus plocei sp. nov. (Prostigmata: Syringophilidae) parasitizing ploceid birds (Passeriformes) in Gabon - a combined description using morphology and DNA barcoding.

A new species of quill mites (Syringophilidae) Syringophiloidus plocei sp. nov. parasitizing Ploceus cucullatus (St. Muller) (type host), P. aurantius (Vieillot) and P. nigerrimus (Vieillot) (Ploceidae: Passeriformes) in Gabon is described using external morphology and DNA barcode data (the mitochondrial cytochrome c oxidase subunit I sequences (COI) and D1-D3 region of the nuclear 28S rRNA gene). Females of S. plocei sp. nov. differ from S. pseudonigritae Glowska, Dragun-Damian and Dabert, 2012 by the length of setae ag3 190-230 (vs 145-160). The genetic distances (K2P) between COI haplotypes of S. plocei sp. nov. individuals (from P. cucullatus, P. nigerrimus and P. aurantius) and S. pseudonigritae ranges from 13.1-13.7%.

Stibarokris mariasi sp. nov. - a new quill mite species (Acariformes: Syringophilidae) parasitizing Puffinus pacificus (Gmelin) (Procellariidae) on Johnston Atoll.

A new quill mite species Stibarokris mariasi sp. nov. (Acariformes: Syringophilidae) is described from the Wedge-tailed Shearwater Puffinus pacificus (Gmelin) (Procellariiformes: Procellariidae) from Johnston Atoll. Females of S. mariasi sp. nov. differ from most similar species S. phoeniconaias Skoracki and OConnor, 2010 by the longitudinal branch of the peritremes consisting of 11-14 chambers (vs 15-17 chambers in S. phoeniconaias), the movable cheliceral digit 145 long (vs 170), setal bases c1 situated distinctly anterior to the level of setae se (vs setal bases c1 and se situated at the same transverse level), the propodonotal shield punctate on the whole surface (vs propodonotal shield punctate at the lateral margins), the small, balloonlike hysteronotal shield, bearing bases of setae d1 and densely punctate on the whole surface (vs hysteronotal shield bearing setal bases d1 and e2 and punctate at the anterior part), the pseudanal setae ps1 1.8 times longer than setae ps2 (vs setae ps1 and ps2 subequal in length), subequal lengths of setae h1 and f1 (vs setae h1 twice longer than f1) and the lengths of setae ag1, ag2, and ag3 145-170, 105-125, 120-165, respectively (vs ag1, ag2 and ag3 245-285, 245-270, 330-340, respectively). A key to all known species of the genus Stibarokris Kethley, 1970 is proposed.

Checklist of the Quill mites (Acariformes: Syringophilidae) of the World.

Mites of the family Syringophilidae (Acariformes: Cheyletoidea) are ectoparasites inhabiting the quills of various feather types in many groups of birds. Until now, 334 valid species and 60 genera of quill mites have been described and recorded from 482 bird species (95 families and 24 orders). Currently, the family is divided into 2 subfamilies: Syringophilinae Lavoipierre, 1953 with 260 species grouped in 49 genera, and Picobinae Johnston and Kethley, 1973 with 74 species grouped in 11 genera. Mites of the subfamily Syringophilinae inhabit quills of primaries, secondaries, tertials, rectrices and wing coverts and just occasionally the body feathers; representatives of the subfamily Picobinae live predominantly inside the body feathers. The rapid increase of the knowledge on biodiversity and systematics of quill mites started in end of the 1990s; numerous new descriptions appeared since that time and taxonomic rearrangements make an urgent need to summarize all previous data. We present a complete checklist of the family Syringophilidae of the world including the following data: a species name, author(s), references, a number of first page of description, figure numbers in descriptions, depository of type and non-type materials, host spectrum and geographical distribution. The checklist is additionally provided with the table including bird hosts and associated quill mite species.

Stibarokris annae n. sp. from Ciconia maguari (Gmelin) (Ciconiiformes: Ciconiidae), a new species of quill mites (Acariformes: Syringophilidae) exhibiting dimorphism of females.

A new quill mite species having dimorphic females Stibarokris annae n. sp. (Acariformes: Syringophilidae) is described from the maguari stork Ciconia maguari (Gmelin) (Ciconiiformes: Ciconiidae) from Uruguay. "S-form" females of S. annae differ from S. phoeniconaias Skoracki & OConnor, 2010 by the hysteronotal shield not reaching setal bases d1 (vs hysteronotal shield bearing setal bases d2 and d1 in S. phoeniconaias), the length ratio of setae ag1:ag2:ag3 1:1-1.4:2-2.4 (vs 1:1:1.2-1.3), the genital setae g1 2-2.5 times as long as g2 (vs g1 1.4-1.8× as long as g2), the fan-like setae of legs III-IV with 15-17 tines (vs with 6-8 tines) and the length of setae f2 (230-255 vs 295-370 µm), h1 (25-30 vs 45-55 µm), ag1 (125-165 vs 245-285 µm) and ag2 (145-180 vs 245-270 µm). "C-form" females of S. annae are distinguishable from S. phoeniconaias ("C-form") by the longitudinal branch of the peritremes with 14-16 chambers (vs 12-13 chambers in S. phoeniconaias), the propodonotal shield weakly sclerotised and punctate along its lateral borders (vs well sclerotised and apunctate), the hysteronotal shield represented by an oval area covered by delicate striations (vs distinct hysteronotal shield), genital setae g1 1.5-1.8 times as long as g2 (vs g1 and g2 subequal in length), the fan-like setae p' and p" with 10 tines (vs with 5 tines) and the length of setae ve (120-130 vs 185-195 µm), si (120-130 vs 220 µm), se (180-200 vs 245-295 µm), c1 (180-195 vs 270-285 µm), d2 (180-205 vs 265-270 µm), d1 (195-205 vs 255-285 µm) and e2 (195-215 vs 285-320 µm).

Two new picobiin mite species (Acari: Cheyletoidea: Syringophilidae) parasitizing passerine birds in Guyana.

Two new picobiin mite species (Cheyletoidea: Syringophilidae) are described from passeriform birds in Guyana, Rafapicobia automoli sp. nov. parasitizing two furnariid species Automolus ochrolaemus (Tschudi) (type host) and Automolus rufipileatus (Pelzeln) (Passeriformes: Furnariidae) and Neopicobia herbicolae sp. nov. from Emberizoides herbicola (Vieillot) (Thraupidae). Additionally, Picumnus exilis (Lichtenstein) (Piciformes: Picidae) is recorded as a new host species for Neopicobia hepburni Glowska et Laniecka, 2014.

New Wolbachia supergroups detected in quill mites (Acari: Syringophilidae).

Wolbachia is the most abundant intracellular bacterial genus infecting a wide range of arthropods and filarial nematodes. Wolbachia have evolved parasitic, mutualistic and commensal relationships with their hosts but in arthropods generally act as reproductive parasites, inducing a wide range of phenotypic effects such as cytoplasmic incompatibility, parthenogenesis, feminization and male-killing. Up to now, the genus has been divided into 14 supergroups successively named A-O. Here, we describe two new Wolbachia supergroups from syringophilid mites (Acari: Cheyletoidea). These obligatory ectoparasites of birds inhabit the quills of feathers in many avian groups. The species of this family reproduce in a haplodiploid mode sensu arrhenotoky and are usually strongly female-biased. Based on the sequences of four protein-coding genes (ftsZ, gltA and groEL and coxA) and the 16S rRNA we identified strains of three Wolbachia supergroups (F and two distinct, yet undescribed ones) in five quill mite species. Our results suggest that in some cases the distribution of the bacteria can be better correlated with the mite's bird host rather than with mite taxonomy as such. The discovery of two new Wolbachia supergroups not only broadens the knowledge of the diversity of this bacterium but also raises questions about potential effects induced in quill mites and transmission mechanisms of the endosymbionts in this peculiar bacteria-quill mite-bird system.

New taxa of the subfamily Picobiinae (Cheyletoidea: Syringophilidae) parasitizing antbirds and gnateaters (Passeriformes: Thamnophilidae, Conopophagidae) in Guyana.

A new genus and three new species of the picobiin quill mites (Cheyletoidea: Syringophilidae) are described from passeriform birds in Guyana, Phipicobia pygiptilae gen. nov. and sp. nov. parasitizing Pygiptila stellaris (Spix) (Thamnophilidae), Rafapicobia thamnophili sp. nov. from Thamnophilus insignis Salvin et Godman (type host), Myrmoborus leucophrys (Tschudi), Myrmeciza ferruginea (St. Müller), Myrmotherula longipennis Pelzeln, and Hypocnemis cantator (Boddaert) (Thamnophilidae), and Rafapicobia milenskyi sp. nov. from Conopophaga aurita (Gmelin) (Conopophagidae).

A new quill mite species Neopicobia hepburni sp. nov. (Cheyletoidea: Syringophilidae) parasitizing picid birds (Piciformes: Picidae) in Peru.

A new quill mite species Neopicobia hepburni sp. nov. is described from the Ecuadorian Piculet Picumnus sclateri Taczanowski (type host) and the Olivaceous Piculet Picumnus olivaceus Lafresnaye (Piciformes: Picidae) from Peru. Females of N. hepburni are distinguishable from most similar species N. ea Skoracki et Unsoeld by the propodonotal shield divided into 3 sclerites, the pygidial shield with a vertical furrow and wing-like appendages, the presence of the genital lobes, setae f2 2.7 times longer than f1 and length ratio of ag1:ag2:ag3 equals 2:1:2. In females of N. ea, the propodonotal shield is entire, the pygidial shield is oval, without vertical furrow and appendages, the genital lobes are absent, setae f2 are 4.5-5.5 times longer than f1 and length ratios of ag1:ag2:ag3 are 2.2-2.7:1:3-3.2.

New species of the genus Picobia (Cheyletoidea: Syringophilidae) parasitizing tyrannid birds (Passeriformes: Tyrannidae).

Three new quill mite species of the genus Picobia Haller (Cheyletoidea: Syringophilidae) are described from 6 host species of the family Tyrannidae (Passeriformes), P. ochoi sp. nov. from Tolmomyias sulphurescens (Spix) (Guyana), P. schmidti sp. nov. from Lophotriccus pileatus (Tschudi) (type host) (Peru) and Hemitriccus margaritaceiventer (Orbigny & Lafresnaye) (Guyana), and P. myiopagi sp. nov. from Myiopagis gaimardii (Orbigny) (type host) (Guyana), M. subplacens (Sclater) (Peru) and Elaenia ruficeps Pelzeln (Guyana).

DNA barcodes reveal female dimorphism in syringophilid mites (Actinotrichida: Prostigmata: Cheyletoidea): Stibarokris phoeniconaias and Ciconichenophilus phoeniconaias are conspecific.

Here we present the first evidence of female dimorphism in ectoparasitic quill mites of the family Syringophilidae (Actinotrichida: Prostigmata: Cheyletoidea). Stibarokris phoeniconaias Skoracki et OConnor, 2010 and Ciconichenophilus phoeniconaias Skoracki et OConnor, 2010 so far have been treated as two distinct species cohabiting inside the quills of feathers of the lesser flamingo Phoeniconaias minor (Geoffroy Saint-Hilaire) and the American flamingo Phoenicopterus ruber Linnaeus. Although females of these species differ morphologically by the extent of body sclerotisation, presence/absence of lateral hypostomal teeth, and shape of dorsal setae, their important common features are the lack of leg setae vs II, and both stylophore and peritremes shape. Here, we apply the DNA barcode markers to test whether the differences between S. phoeniconaias and C. phoeniconaias have a genetic basis, indicating that they really are distinct taxa, or whether they just represent two morphs of a single species. All analysed sequences (616 bp for COI and 1159 bp for 28S rDNA) obtained for specimens representing females of both studied taxa as well as male, tritonymph, protonymph and larva of S. phoeniconaias were identical, which indicates that S. phoeniconaias and C. phoeniconaias are conspecific. The formal taxonomic consequence of our results is denial of the genus status of Ciconichenophilus Skoracki et OConnor, 2010 and species status of C. phoeniconaias, and recommendation that they should be treated as junior synonyms of Stibarokris Kethley, 1970 and S. phoeniconaias, respectively.

New quill mites (Cheyletoidea: Syringophilidae) parasitizing tyrannid birds (Passeriformes: Tyrannidae) in Peru.

Two new quill mite species (Cheyletoidea: Syringophilidae) are described from tyrannid birds (Passeriformes: Tyrannidae) in Peru: Picobia sayornis sp. nov. from the black phoebe Sayornis nigricans (Swainson) (first record of Picobia Haller species on tyrannid host) and Syringophilopsis szeffleri sp. nov. from the scale-crested pygmy-tyrant Lophotriccus pileatus (Tschudi). The Pacific elaenia Myiopagis subplacens (Sclater) is recorded as a new host for Syringophilopsis tyranni Bochkov and Galloway.

New quill mites (Cheyletoidea: Syringophilidae) parasitizing the black-headed paradise-flycatcher Terpsiphone rufiventer (Passeriformes: Monarchidae) in Gabon.

A new genus of quill mites (Cheyletoidea: Syringophilidae) and two new species Pipicobia terpsiphoni gen. nov. and sp. nov. and Syringophiloidus furthi sp. nov. parasitizing the black-headed paradise-flycatcher Terpsiphone rufiventer (Swainson) (Passeriformes: Monarchidae) in Gabon are described. Three species of the Neopicobia Skoracki, 2011 are moved to the newly established genus: Pipicobia locustella (Skoracki, Bochkov and Wauthy, 2004) comb. nov., Pipicobia pyrrholaemus (Skoracki and Glowska, 2008) comb.nov., and Pipicobia glossopsitta (Skoracki, Glowska and Sikora, 2008) comb.nov. Syringophilids are recorded on hosts of the family Monarchidae and in Gabon for the first time. A key to the genera of the subfamily Picobiinae is proposed.

DNA-barcoding contradicts morphology in quill mite species Torotrogla merulae and T. rubeculi (Prostigmata: Syringophilidae).

Torotrogla merulae Skoracki, Dabert et Ehrnsberger, 2000 and T. rubeculi Skoracki, 2004 have been considered as distinct steno- and monoxenous quill mite species (Acari: Prostigmata: Syringophilidae) parasitizing the thrushes of the genus Turdus Linnaeus and the European robin Erithacus rubecula (Linnaeus), respectively. Morphological and molecular studies on the taxonomical status of these two species provided contradictory results. Well defined differences in morphology were not supported by substantial genetic distance in nucleotide sequences of the DNA barcode (mitochondrial cytochrome c oxidase subunit I, COI, and D2 domain of the nuclear 28S rRNA gene), by the topology of the phylogenetic trees (neighbor-joining, maximum parsimony, maximum likelihood) and the network analyses of the COI haplotype genealogy (median-joining, statistical parsimony) that reveal rubeculi populations nested within merulae haplotypes. Since detected differences between T. merulae and T. rubeculi populations (1.6-2.4% for COI and 0.1% for D2) are comparable to the intraspecific level observed in majority of currently recognized European Torotrogla species and are much lower than the interspecific distances observed in the genus, we postulate their conspecificity. Because main morphological distinctions concern the structures used for feeding, we hypothesize that they are the result of phenotypic plasticity evoked by specific and different environmental conditions prevailing on the host bodies (thickness of the feather quill wall).