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Article

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

by
Eliza Glowska
1,*,
Izabella Laniecka
1,
Kamila Ostrowska
1,
Christina A. Gebhard
2,
Julia Olechnowicz
3 and
Miroslawa Dabert
3
1
Department of Animal Morphology, Faculty of Biology, Adam Mickiewicz University in Poznań, Uniwersytetu Poznańskiego 6, 61-614 Poznan, Poland
2
Division of Birds, Smithsonian Institution, MRC 116, P.O. Box 37012, Washington, DC 20013-7012, USA
3
Molecular Biology Techniques Laboratory, Faculty of Biology, Adam Mickiewicz University in Poznań, Uniwersytetu Poznańskiego 6, 61-614 Poznan, Poland
*
Author to whom correspondence should be addressed.
Animals 2023, 13(24), 3877; https://doi.org/10.3390/ani13243877
Submission received: 28 October 2023 / Revised: 25 November 2023 / Accepted: 6 December 2023 / Published: 16 December 2023
(This article belongs to the Special Issue The Ecology, Evolution, Systematics and Behaviour of Mites)
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Abstract

:

Simple Summary

Morphology and barcode data were used to estimate the diversity and genetic variability of fourteen putative species of the genus Syringophiloidus Kethley, 1970. In most cases, both sources of information were consistent. The only exception was S. amazilia Skoracki, 2017, which according to our results is most likely a population of S. stawarczyki Skoracki, 2004, and probably should be treated as its junior synonym. The further findings of our study are six new-to-science species described herein. We indicate that both the host phylogeny and distribution can drive the evolution of quill mites. Our results increase the knowledge of quill mite diversity and provide some premises to formulate and further test evolutionary, ecological, and epidemiological inquiries.

Abstract

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.

1. Introduction

Quill mites (Acariformes: Syringophilidae) are widespread permanent bird ectoparasites. To date, 417 species have been described [1,2], although their actual number is estimated to be several times higher, probably reaching up to 5000 species [3]. Although the knowledge about syringophilid diversity and host associations has been growing recently [4,5,6], they remain one of the least understood bird parasites. This is due to their small body size, poorly accessible habitats (bird’s feather quill), and low prevalence [7]. Further difficulties are caused by weakly informative morphology and relatively few diagnostic characters [8,9]. Moreover, the vast majority of species were described only on the basis of female features, and the consequence is that males, nymphs, and larvae are virtually unidentifiable. To overcome the limitations of morphology, molecular methods have recently come into use in mite taxonomic studies [9,10,11]. DNA barcoding is an approach employing a short fragment of the mitochondrial cytochrome c oxidase subunit I (COI) sequence. It is commonly used as an effective marker in the process of species identification in many groups of animals (Hebert 2003, 2004) [12,13], including quill mites [14]. Although only a very small fraction of those parasites have been barcoded so far, this approach has proven reliable in such systematic inquiries as female dimorphism or phenotypic plasticity [8,9]. It has also been successfully used for the estimation of host spectrum [15] and cryptic species detection [16].
Precise and unambiguous species diagnosis is crucial for any other research, including that on quill mites’ parasitological and epidemiological importance. This is particularly important in the context of recent reports that mites are the host of unique phylogenetic lineages of bacteria of the genera Wolbachia and Spiroplasma. In addition, the presence of Bartonella and Brucella taxa has been detected in syringophilids, which makes them potentially important in the process of circulation of pathogens among birds [17].
The Syringophiloidus Kethley, 1970, is the most specious and widely distributed genus of quill mites with 48 known species widespread around the world. This taxon has been recorded from 80 avian host species, belonging to 29 families and five orders [1,2]. Since the species of this genus are known to have various (mono-, steno- and poly-xenous) associations with hosts, they seem to be a representative material for research on diversity and host associations.
In this paper, we supplement the morphology with DNA barcode coverage to evaluate the species composition and host specificity of representatives of fifteen Syringophiloidus populations parasitizing fifteen selected bird species.

2. Materials and Methods

2.1. Animal Material and Morphological Analysis

Mite material used in the study (Table 1) was acquired from several sources: (i) the collection of feathers deposited in the Smithsonian Institution, National Museum of Natural History, Department of Vertebrate Zoology, Division of Birds, Washington, DC, USA (USNM) (September 2014), and bird specimens originally collected in Gabon (2009), Namibia (2009), and Peru (2009); (ii) the Biocenter Grindel and Zoological Museum (University of Hamburg), and bird specimens originally collected in Tanzania; (iii) mite samples collected in Mexico (field no. SVM 08-0506-1/4) (2008) and Brazil (2010); (iv) mites obtained from dead birds (due to probable collisions with the window glass) found at the AMU campus, Poznań, Poland (2009).
Drawings were made with an Olympus BH2/BX41/BX53 microscopes with differential interference contrast (DIC) optics and a camera lucida. All measurements are in micrometers (µm). Idiosomal setation follows that of [18] with modifications adapted for Prostigmata by [19]. The nomenclature of leg chaetotaxy follows that proposed by [20]. The application of this chaetotaxy to Syringophilidae was recently provided by [21] with a few changes by [22]. Latin and common names of the birds follow [23].
Material depositories and abbreviations: AMU—Adam Mickiewicz University, Poznań, Poland; USNM—Smithsonian Institution, National Museum of Natural History, Washington, DC, USA. The voucher slides and corresponding DNA samples are deposited in the collection of the AMU and USNM under the identification numbers indicated below. The sequences are deposited in GenBank under accession nos. specified in Table 1.

2.2. Molecular Data and Analysis

Total genomic DNA was extracted from single specimens using DNeasy Blood & Tissue Kit (Qiagen GmbH, Hilden, Germany) as described by [24]. The COI gene fragment was amplified via PCR with degenerate primers: Aseq01F (GGAACRATATAYTTTATTTTTAGA) and Aseq03R (GGATCTCCWCCTCCWGATGGATT) [9]. PCR amplifications were carried out in 10 µL reaction volumes containing 5 µL of Type-it Microsatellite Kit (Qiagen), 0.5 µM of each primer, and 4 µL of DNA template using a thermocycling profile of one cycle of 5 min at 95 °C followed by 35 steps of 30 s at 95 °C, 1 min at 50 °C, and 1 min at 72 °C, with a final step of 5 min at 72 °C. After amplification, PCR products were diluted two-fold with water, and 5 µL of the sample was analyzed via electrophoresis on 1.0% agarose gel. Samples containing visible bands were purified with thermosensitive Exonuclease I and FastAP Alkaline Phosphatase (Fermentas, Thermo Scientific, Waltham, MA, USA). The amplicons (585 bp) were sequenced in one direction using the Aseq01F primer. Sequencing was performed with BigDye Terminator v3.1 on ABI Prism 3130XL Analyzer (Applied Biosystems, Foster City, CA, USA). Sequence chromatograms were checked for accuracy and edited using Geneious R11 (Biomatters Ltd., Auckland, New Zealand).
Phylogenetic associations between the studied taxa were estimated with the neighbor joining (NJ) method implemented in MEGA7 [25]. Support for the recovered trees was evaluated with 1000 (NJ) non-parametric bootstrap replicates [26]. Pairwise distances between nucleotide COI sequences were calculated using Kimura’s two-parameter (K2P) and distance p models [27] for all codon positions with MEGA7. Stibarokris phoeniconaias Skoracki and OConnor, 2010, was chosen as an outgroup to root the tree. Tree visualizations were prepared using tree editing tools in MEGA7 and Figtree v.1.4.2—[28] (http://tree.bio.ed.ac.uk/) URL (accessed on 15 October 2023).

3. Results

3.1. Systematics

  • Family Syringophilidae Lavoipierre
  • Subfamily Syringophilinae Lavoipierre
  • Genus Syringophiloidus Kethley

3.2. Molecular Analysis

We provided DNA barcode coverage for the representation of fifteen populations of Syringophiloidus ssp. recorded from fifteen bird species. The COI alignment was 552 bp long and comprised 43 sequences of Syringophiloidus mites (ingroup) and one sequence of Stibarokris phoeniconaias Skoracki & OConnor, 2010 (outgroup). The number of sequences obtained from each mite population varied from 1 to 10. The alignment contained 242 variable sites, 196 of which were parsimony informative.
The neighbor joining phylogenetic analyses (K2P and distance p) distinguished thirteen monophyletic lineages, among which seven lineages exactly correspond to seven previously known and species that are morphologically distinguished here. The only exception in the obtained pattern is presented by S. amazilia, which is very close to that of S. stawarczyki and most likely represents a population or subspecies of this species (Figure 1 and Figure A1).
This assumption is also supported by the genetic distance between the two populations (1.4 and 1.5% of distance p and K2P) (Table 2), which is lower than that between bihost S. plocei populations (2.1%) and comparable to the previously reported intraspecific values within other quill mites [8]. Although all putative species are highly supported with bootstrap values (100%) and, as they predictably delineate the morphospecies, the relationships between them have not been fully resolved and only weakly suggest various evolutionary scenarios.
The genetic distances were compared at intra- and inter-specific levels according to both the distance p and the K2P model. The integrity and separateness of particular taxa were proven for almost all populations resulting in the recognition of seven previously known species and six species new to science. 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% for genetic distances p and K2P, respectively (Table 2).

3.3. Morphological Systematics

3.3.1. Descriptions

Syringophiloidus atlapetes sp. n. (Figure 2 and Figure 3)

For females (holotype and three paratypes; range in parentheses) (Figure 2A–E), the total body length is 605 (600–620). For Gnathosoma, the infracapitulum is punctate. Each medial and lateral branch of peritremes has 2–3 and 9–11 chambers, respectively (Figure 2C). The stylophore is punctate and has a body length of 165 (150–155). For Idiosoma, the propodonotal shield is rounded anteriorly and sparsely punctate on the entire surface. The length ratio of setae vi:ve:si is 1:1:3.3–4.6. The hysteronotal shield is clearly visible and punctate in anterior and posterior parts. The pygidial shield is punctate and distinctly sclerotized in the area bearing bases of setae f1 and f2. Setae f1 and h1 are subequal in length. The length ratio of setae ag1:ag2:ag3 is 1.1:1:1.2. For Legs, Coxal fields I–IV are sparsely punctate. Setae 3c is 3.4–3.6 times longer than 3b. Fan-like setae p’ and p” of legs III–IV have seven tines (Figure 2E). Setae tc” is 1.3–1.6 times longer than tc’. Lengths of setae are as follows: vi 15 (20); ve 15 (20); si 70 (65–75); c2 160 (185); se 205 (195–225); c1 215; d2 175 (165); d1 145 (145); e2 125 (140–170); f1 20 (25); f2 180 (205); h1 25 (20); h2 295 (285); ag1 125; ag2 115 (125–135); ag3 160; g1, g2 25 (25); ps1 12 (12); ps2 17 (17), tc’ (30–40); tc” (50); l’RIII 35 (40–45); l’RIV (25); 3b 25 (15); 3c 85 (55–75); 4b 20 (20); 4c 85 (55).
For males (paratype) (Figure 3A–E), the total body length is 400. For Gnathosoma, the infracapitulum is apunctate. The stylophore is apunctate and 130 long. Each medial branch of peritremes has four chambers, and each lateral branch has 10 chambers (Figure 3C). For Idiosoma, the propodonotal shield is weakly sclerotized, bearing bases of setae vi, ve, si, se, and c1, and sparsely punctate near bases of setae vi, ve and si. Striation is clearly visible on the entire surface. The length ratio of setae ve:si is 1:1. The hysteronotal shield is weakly sclerotized, and the striae are visible, not fused to a pygidial shield, and apunctate. Setae d1, d2, and e2 are subequal in length. The pygidial is shield small, restricted to bases of setae f2 and h2, and to the genito-anal region or only to the genito-anal region; it is apunctate. Genital setae g1 is situated anterior to the level of setae g2, and both pairs are subequal in length. Pseudanal setae ps1 and ps2 are subequal in length. Length ratios of setae ag1:ag2 and f2:h2 are 1.3:1 and 1:11.5, respectively. Coxal fields I–IV are punctate. Setae 3c is four times longer than 3b. For legs, fan-like setae p’ and p” of legs III and IV have 6 tines (Figure 3E). The length ratio of setae tc’III–IV:tc”III–IV is 1:1.7. The lengths of setae are as follows: ve 15, si 15, se 100, c1 100, c2 55, d1 13, d2 13, e2 13, f2 10, h2 115, ag1 45, ag2 35, 3b 10, 3c 40, l’RIII 13, l’RIV 15 tc’III–IV 15, and tc”III–IV 25.
  • Host and Distribution
Birds of the family Passerellidae: the white-headed brushfinch, Atlapetes albiceps (Taczanowski) from Peru.
  • Type Material
The type material included a female holotype, and seven female and one male paratypes from the quill of the white-headed brushfinch, Atlapetes albiceps (Taczanowski) (Passeriformes: Passerellidae), PERU, Tumbes, Parque Nacional Cerros de Amotape, El Platano, 4 07 46 S, 80 37 13 W, 11, 13 July 2009, coll. Milensky, C. M, (USNM 643973). Mites were sampled by Glowska E.; the vouchers and DNA codes are as follows: EG974–977. DNA barcode GenBank accession numbers as specified in Table 1.
  • Type Material Deposition
The female holotype (USNMENT acc. number: USNMENT01967000) and four paratypes (three females and one male) (USNMENT01967001–USNMENT01967004) are deposited in the USNM, and four female paratypes are deposited in the AMU (EG23-0628-003.01-04).
  • Differential Diagnosis
Syringophiloidus atlapetes sp. n. is morphologically most similar to S. stawarczyki Skoracki, 2004, described from the golden-rumped euphonia Euphonia cyanocephala (Vieillot) (Passeriformes: Fringillidae) and additionally recorded from the white-lined tanager, Tachyphonus rufus (Boddaert), and the blue dacnis, Dacnis cayana (L.) (Passeriformes: Thraupidae) [29,30]. Females of both species have a similar number of peritremal chambers, punctate dorsal shields, and Coxal fields I–IV, as well as similar or nearly coinciding lengths of most setae. Females of S. atlapetes sp. n. differ from those of S. stawarczyki in terms of a stylophore length of 150–165 (vs. that of 170–195 in S. stawarczyki), lengths of the setae se of 200–225 (vs. 165–170) and d2 165–175 (vs. 115–125), and the sparse punctation of the dorsal and Coxal shields (vs. dense punctation). The genetic distance between both species is 6.3% of K2P and 5.9% of distance p. S. atlapetes sp. n. is also very similar to S. coccothraustes Skoracki, 2011, described from the hawfinch Coccothraustes coccothraustes (L.) (Passeriformes: Fringillidae) [22]. Females of both species have a similar number of peritremal chambers, punctate dorsal shields, and Coxal fields I-IV, as well as coinciding lengths of most setae. Females of S. atlapetes sp. n. differ from those of S. coccothraustes in terms of the lengths of setae vi of 15–20 (vs. 25–35), ve of 15–20 (vs. 25–35), h2 of 285–295 (vs. 305–330), g1 and g2 of 25 (vs. 35–40), and tc” of 50 (vs. 70).
  • Etymology
The name is taken from the generic name of the host and is a noun in apposition.

Syringophiloidus calamonastes sp. n. (Figure 4A–E)

Female (holotype and 7 paratypes; range in parentheses). Total body length 715 (645). Gnathosoma. Infracapitulum apunctate. Each medial and lateral branch of peritremes with 6–8 and 8–10 chambers, respectively (Figure 4D). Stylophore apunctate, 155 (155) long. Idiosoma. Propodonotal shield rounded anteriorly and apunctate. Length ratio of setae vi:ve:si 1:1.4–2.3:2.2–3.5. Hysteronotal shield strongly sclerotized and apunctate, fused to pygidial shield. Pygidial shield punctate, distinctly sclerotized in the area bearing bases of setae f1 and f2. Setae h1 1.2–1.5 longer than f1. Length ratio of setae ag1:ag2:ag3 1–1.2:1:1.3–1.6. Genital plate present, bearing bases of setae ag2 and ag3. Legs. Coxal fields I–IV apunctate. Setae 3c 2.6–3.2 times longer than 3b. Fan-like setae p’ and p” of legs III–IV with 6–7 tines (Figure 4E). Setae tc” 2–2.8 times longer than tc’. Lengths of setae: vi 25 (20–25); ve 35 (35–45); si 55 (55–70); c2 155 (130–170); se 170 (165–205); c1 200 (170–180); d2 145 (130–180); d1 105 (105–145); e2 155 (145–155); f1 20 (25); f2 145 (160); h1 30 (30–35); h2 340 (260–295); ag1 125 (115–130); ag2 110 (95–130); ag3 160 (150–165); g1, g2 30 (30–35); ps1,2 15 (15–20); tc’ 20 (20–25); tc” 55 (45–60); l’RIII 35 (25); l’RIV 35 (35); 3b 25 (20–25); 3c 65 (65–75); 4b 35 (25–30); 4c 60 (70–80).
Male: not found.
  • Host and Distribution
Birds of the family Cisticolidae: southern barred warbler Calamonastes fasciolatus (Smith) from Namibia.
  • Type Material
Female holotype and 10 female paratypes from the quill of the Southern Barred Warbler Calamonastes fasciolatus (Smith) (Passeriformes: Cisticolidae), NAMIBIA, Erongo, Tubusis, 21 39 46 S, 15 23 44 E, 4 Sep 2009, bird specimen coll. Gebhard, C. A. (USNM 642616), mites sampled by Glowska E. (15 Sep 2013); vouchers and DNA codes: KR043, KR045; DNA barcode GenBank accession numbers as specified in Table 1.
  • Type Material Deposition
Female holotype (USNMENT acc. number: USNMENT01967005) and 5 paratypes (USNMENT01967006–USNMENT01967010) are deposited in the USNM and 5 female paratypes in the AMU (EG23-0628-001.01–05).
  • Differential Diagnosis
Syringophiloidus calamonastes sp. n. is morphologically most similar to S. picidus Skoracki, Klimovičová, Muchai and Hromada, 2014 described from the cardinal woodpecker Dendropicos fuscescens (Vieillot) (Piciformes: Picidae) and recorded in Kenya, Tanzania and Uganda [31]. Females of both species have a similar number of peritremal chambers, all propodonotal setae serrated, fused, posteriorly punctate hystero-pygidial shield, and pseudanal setae ps1 and ps2 subequal in length. Females of S. calamonastes sp. n. differ from S. picidus by apunctate infracapitulum, propodonotal shield and coxal fields (vs. punctate in S. picidus), length ratio of setae vi:ve:si 1:1.4–2.3:2.2–3.5 (vs. 1:1.2–1.3:1.7–2.3) and equal genital setae (vs. g1 1.2 longer than g2). Our molecular analysis revealed that both species differ by 7.3% of K2P (and 6.9% of distance p). S. calamonastes sp. n. is also very similar to S. minor (Berlese, 1887) described from the house sparrow Passer domesticus (L.) (Passeriformes: Passeridae) from Europe and additionally recorded from several species and localities around the world [22]. Females of both species have a similar number of peritremal chambers, fused hysteronotal and pygidial shields, fan-like setae p’ and p” of legs III–IV with 6–7 tines and same lengths of most setae. Females of S. calamonastes sp. n. differ from S. minor by apunctate infracapitulum and propodonotal shield (vs. punctate in S. minor) and the lengths of setae se 165–205 (vs. 150–160), e2 145–155 (vs. 105–135), tc’ 20–25 (vs. 40), and tc” 45–60 (vs. 75–80).
  • Etymology
The name is taken from the generic name of the host and is a noun in apposition.

Syringophiloidus campephilus sp. n. (Figure 5A–E)

Female (holotype and 7 paratypes; range in parentheses). Total body length 665 (650–655). Gnathosoma. Infracapitulum apunctate or sparsely punctate. Each medial and lateral branch of peritremes with 2–3 and 8–10 chambers, respectively (Figure 5C). Stylophore apunctate, 150 (150) long. Idiosoma. Propodonotal shield weakly sclerotized punctate around bases of setae ve. Length ratio of setae vi:ve:si 1:1–1.6:1–1.6. Hysteronotal shield weakly sclerotized and apunctate, fused to pygidial shield. Pygidial shield sparsely punctate. Setae f1 and h1 subequal in length. Length ratio of setae ag1:ag2:ag3 1:1.1–1.9:1.5–1.9. Legs. Coxal fields I–II sparsely punctate, III–IV punctate. Setae 3c 3.3–5 times longer than 3b. Fan-like setae p’ and p” of legs III–IV with 6–7 tines (Figure 5E). Setae tc” 1.4–1.6 times longer than tc’. Lengths of setae: vi 15 (15); ve 25 (20–25); si 25 (15–20); c2 145 (145–170); se 180 (195); c1 180 (170–195); d2 15 (10–15); d1 70 (65–80); e2 (70–90); f1 15 (10–20); f2 205 (215–235); h1 15 (15–20); h2 285; ag1 65 (55–60); ag2 70 (75–105); ag3 100 (105); g1, g2 15 (15); ps1 15 (15); tc’ 25 (20–25); tc” 35 (30–40); l’RIII 25 (20–25); l’RIV 25 (15–20); 3b 10 (10–15); 3c 50 (35–50); 4b 10 (10–15); 4c 50 (35–50).
  • Host and Distribution
Birds of the family Picidae: guayaquil woodpecker Campephilus gayaquilensis (Lesson) from Peru.
  • Type Material
Female holotype and 7 female paratypes from the quill of the guayaquil woodpecker Campephilus gayaquilensis (Lesson) (Piciformes: Picidae) (USNM 643881), PERU, Tumbes, El Caucho Biological Station, 3 49 25 S, 80 15 37 W, 9 Jun 2009, bird coll. Vargas, W.; mites sampled by Glowska E.; vouchers and DNA codes: EG964, EG971; DNA barcode GenBank accession numbers as specified in Table 1.
  • Type Material Deposition
Female holotype (USNMENT acc. number: USNMENT01967011) and 3 paratypes (USNMENT01967012–USNMENT01967014) are deposited in the USNM and 4 female paratypes in the AMU (EG23-0628-004.01–04).
  • Differential Diagnosis
Syringophiloidus campephilus sp. n. is morphologically most similar to S. atlapetes sp. n. described from the white-headed brushfinch Atlapetes albiceps (Taczanowski) (Passeriformes: Passerellidae) from Peru. Females of both species have a similar number of peritremal chambers, punctate pygidial shields and fan-like setae with 6–7 tines. Females of S. campephilus sp. n. differ from S. atlapetes sp. n by the apunctate stylophore (vs. punctate in S. atlapetes) and lengths of setae si 15–25 (vs. 65–75), d2 10–15 (vs. 165–175), d1 65–80 (vs. 145), e2 70–90 (vs. 125–170), ag1 55–65 (vs. 125) and ag3 100–105 (vs. 160). The genetic distance between these species equals 17.3% of K2P (and 15.1% of distance p). S. campephilus sp. n. is also very similar to S. dendrocittae Fain, Bochkov and Mironov, 2000 described from the rufous treepie Dendrocitta rufa Baker (Passeriformes: Corvidae) from East Asia [32]. Females of both species have a similar number of peritremal chambers and fan-like setae p’ and p” of legs III–IV with 6–8 tines. Females of S. campephilus sp. n. differ from S. dendrocittae by the lengths of the setae vi 15 (vs. 24), ve 20–25 (vs. 45), d2 10–15 (vs. 94), d1 65–80 (vs. 157), e2 70–90 (vs. 132), ag1 55–65 (vs. 128–157), ag2 70–105 (vs. 135), ag3 (vs. 166), g1,2 15 (vs. 33), ps1,2 15 (vs. 27).
  • Etymology
The name is taken from the generic name of the host and is a noun in apposition.

Syringophiloidus mahali sp. n. (Figure 6A–E)

In terms of females (a holotype and six paratypes; range in parentheses), the total body length is 785 (715–785). For Gnathosoma, the infracapitulum is sparsely punctate. Each medial and lateral branch of peritremes has 5–6 and 10–11 chambers, respectively (Figure 6C). The stylophore is apunctate and 185 (170–180) long. For Idiosoma, the propodonotal shield is anteriorly concave and apunctate. The length ratio of setae vi:ve:si is 1:1.1–1.3:1.1–1.8. The hysteronotal shield is apunctate and fused to the pygidial shield. The pygidial shield is distinctly sclerotized and punctate in the area bearing bases of setae f1 and f2. Setae h1 is 1.2–1.3 times longer than f1. The length ratio of setae ag1:ag2:ag3 is 1–1.2:1–1.2:1.1–1.3. Setae ps2 is 1.3–1.4 longer than ps1. Setae g1 and g2 are subequal in length. For Legs, Coxal fields I–IV are sparsely punctate. Setae 3c is 3–3.6 times longer than 3b. Fan-like setae p’ and p” of legs III–IV have six to seven tines (Figure 6E). Setae tc” is 1.5–2 times longer than tc’. Lengths of setae are as follows: vi 30 (25–30); ve 40 (30–35); si 55 (35–45); c2 155 (135–160); se 185 (175–195); c1 170 (180); d2 150 (155–180); d1 130 (145–155); e2 150 (155–170); f1 20 (15–20); f2 120 (130–150); h1 25 (20–25); h2 285 (290–295); ag1 150 (110–130); ag2 120 (115–130); ag3 130 (145–150); g1, g2 25 (20); ps1 15 (10–15); ps2 20 (15–20); tc’ 35 (20–30); tc” 55 (40–45); l’RIII 30 (30–35); l’RIV 30 (25); 3b 25 (25); 3c 80 (75–90); 4b 25 (20–25); 4c 90 (85–65).
  • Host and Distribution
Birds of the family Ploceidae: the white-browed sparrow-weaver, Plocepasser mahali Smith from Namibia.
  • Type Material
The type material consisted of a female holotype and six female paratypes from the quill of the white-browed sparrow-weaver, Plocepasser mahali Smith (Passeriformes: Ploceidae) (USNM 642639), Namibia, Hardap, Aukens, 25 09 03 S, 16 32 00 E, 29 Aug 2009, coll. Mughongora, V. K. Mites were sampled by Glowska E.; vouchers and DNA codes are as follows: KR047-048 and KR052. DNA barcode GenBank accession numbers are specified in Table 1.
  • Type Material Deposition
A female holotype (USNMENT acc. number: USNMENT01967015) and three paratypes (USNMENT01967016–USNMENT01967018) are deposited in the USNM; three female paratypes are deposited in the AMU (EG23-0628-005.01–03).
  • Differential Diagnosis
Syringophiloidus mahali sp. n. is morphologically most similar to S. picidus Skoracki, Klimovičová, Muchai and Hromada, 2014, described from the cardinal woodpecker Dendropicos fuscescens and recorded in Kenya, Tanzania and Uganda [31]. Females of both species have a similar number of peritremal chambers, a hysteronotal shield fused to the pygidial shield, a punctate pygidial shield in the posterior part, and punctate Coxal fields I–IV. Females of S. mahali sp. n. differ from those of S. picidus in terms of the length of the stylophore, which is 170–185 (vs. 155–170 in S. picidus), the setae ps2, which is 1.3–1.4 longer than ps1 (vs. ps1,2 subequal in length), and the lengths of setae si, which are 35–55 (vs. 60–80), of c1, which are 170–180 (vs. 210–215), of f2, which are120–150 (vs. 150–180), and of h2, which are 285–295 (vs. 315–395). S. mahali sp. n. is also very similar to S. philomelosus Skoracki, 2011, described from the song thrush Turdus philomelos Brehm (Passeriformes: Turdidae) from Jordan [22]. Females of both species have a similar number of chambers in the lateral branches, fan-like setae p’ and p” of legs III–IV with six to seven tines and lengths of most setae. Females of S. mahali sp. n. differ from those of S. philomelosus in terms of the number of chambers of the medial branch of peritremes (5–6 and 8–10 in S. mahali sp. n. and S. philomelosus, respectively), fused hysteronotal and pygidial shields (vs. not fused) and lengths of setae c1 of 170–180 (vs. 220–225), c2 of 135–160 (vs. 175–180), f1 of 15–20 (vs. 30), f2 of 120–150 (vs. 190–200), h2 of 285–295 (vs. 345), tc’ of 20–35 (vs. 40–45), and tc” of 40–55 (vs. 65).
  • Etymology
The name is taken from the generic name of the host and is a noun in apposition.

Syringophiloidus paludicolae sp. n. (Figure 7A–E)

In terms of females (a holotype and seven paratypes; range in parentheses), the total body length is 800 (770–835). For Gnathosoma, the infracapitulum is sparsely punctate. Each medial and lateral branch of peritremes has one to two and seven to eight chambers, respectively (borders are poorly marked) (Figure 7C). The stylophore is apunctate and has a length of 160 (150–155). For Idiosoma, the propodonotal shield is weakly sclerotized and apunctate. The length ratio of setae vi:ve:si is 1:1.5–1.6:5.3–6. The hysteronotal shield is weakly sclerotized (striation is clearly visible on the entire surface) and apunctate. The pygidial shield is distinctly sclerotized and sparsely punctate in the area bearing bases of setae f1 and f2, while the upper part is weakly sclerotized. Setae h1 is 1.1 times longer than f1. The length ratio of setae ag1:ag2:ag3 ois 1.1–1.3:1:1.1–1.6. For Legs, Coxal fields I–IV are sparsely punctate. Setae 3c is 2.5–2.9 times longer than 3b. Fan-like setae p’ and p” of legs III–IV have seven to eight tines (Figure 7E). Setae tc” is 1.6–2.4 times longer than tc’. Lengths of setae are as follows: vi 30 (30); ve 50 (45); si (160–180); c2 230 (220–250); se 270 (255–265); c1 270 (270–285); d2 115 (105); d1 195 (170–180); e2 180 (160–180); f1 35 (35–40); f2 (305–330); h1 40 (40–45); h2 420 (400–410); ag1 175 (170–195); ag2 155 (130–175); ag3 205 (195–230); g1, g2 40 (40–50); ps1 20 (25); ps2 35 (40); tc’ 35 (25–35); tc” 50 (55–60); l’RIII 55 (40–55); l’RIV 30 (25–35); 3b 40 (40–50); 3c 110 (115–125); 4b 35 (30–45); 4c 120 (95–135).
Male: not found.
  • Host and Distribution
Birds of the family Hirundinidae: the plain martin, Riparia paludicola (Vieiilot) from Namibia.
  • Type Material
The type material consists of a female holotype and seven female paratypes from the quill of the plain martin, Riparia paludicola (Vieiilot) (Passeriformes: Hirundinidae) (USNM 642532), NAMIBIA, Karas, Sandfontein near Orange River, 28 51 45 S, 18 33 08 E, 17 Aug 2009, bird specimen coll. Gebhard C. A., mites are sampled by Glowska E.; vouchers and DNA codes are as follows: KR055-056. DNA barcode GenBank accession numbers are specified in Table 1.
  • Type Material Deposition
A female holotype (USNMENT acc. number: USNMENT01967019) and three paratypes (USNMENT01967020–USNMENT01967022) are deposited in the USNM, and four female paratypes are deposited in the AMU (EG23-0628-002.01–04).
  • Differential Diagnosis
Syringophiloidus paludicolae sp. n. is morphologically most similar to S. tarnii Skoracki and Sikora, 2002, described from the huet huet Pteroptochos tarni (King) (Passeriformes: Rhinocryptidae) from Argentina [33]. Females of both species have a punctate infracapitulum, a weakly sclerotized and apunctate hysteronotal shield, fan-like setae p’ and p” of legs III–IV with six to eight tines, and similar lengths of most setae. Females of S. paludicolae sp. n. differ from those of S. tarnii in terms of the number of peritremal chambers, i.e., one to two and seven to eight in medial and lateral branches (vs. three to four and nine), and lengths of setae c2 of 220–250 (vs. 155–205), se of 255–270 (vs. 165–225), c1 of 270–285 (vs. 190–240), d1 of 170–195 (vs. 125–145), e2 of 160–180 (vs. 115–155), and f2 of 305–330 (vs. 250–280). S. paludicolae sp. n. is also very similar to S. ripariae sp. n., described from the sand martin, Riparia riparia (L.) (Passeriformes: Hirundinidae) from Poland (p.p.). Females of both species are similar in length and weakly sclerotized, have a similar number of peritremal chambers, and setae g1 and g2 that are subequal in length. Females of S. paludicola sp. n. differ from those of S. ripariae sp. n. in terms of the lengths of setae ve of 45–50 (vs. 35 in S. paludicolae), d2 of 105–115 (vs. 180), h1 of 40–45 (vs. 30), and ps2 of 35–40 (vs. 25). The genetic distance between these species is 15.3% of K2P (and 13.7 of distance p).
  • Etymology
The name is taken from the specific name of the host and is a noun in the genitive case.

Syringophiloidus ripariae sp. n.

Female (holotype). Total body length 820. Gnathosoma. Infracapitulum punctate. Each medial and lateral branch of peritremes with 2 and 7 chambers, respectively. Stylophore apunctate, 180 long. Idiosoma. Propodonotal shield weakly sclerotized and apunctate. Length ratio of setae vi:ve 1:1.4. Hysteronotal shield weakly sclerotized (striation visible on the entire surface) and apunctate. Pygidial shield sparsely punctate, distinctly sclerotized in the area bearing bases of setae f1 and f2, upper part weakly sclerotized. Setae f1 1.1 longer than h1. Length ratio of setae ag1:ag2:ag3 1.3–1:1.7 Legs. Coxal fields I sparsely punctate, III–IV apunctate. Setae 3c 1.4 times longer than 3b. Fan-like setae p’ and p” of legs III–IV with 6 tines. Lengths of setae: vi 25; ve 35; c2 205; se 260; c1 275; d2 180; d1 180; e2 180; f1 32; f2 300; h1 28; h2 355; ag1 170; ag2 130; ag3 220; 40; ps1 20, ps2 25; l’RIII 45; l’RIV 40; 3b 55; 3c 80; 4b 35; 4c 100.
Male: not found.
  • Host and Distribution
Birds of the family Hirundinidae: the sand martin Riparia riparia (L.) from Poland.
  • Type Material
The type material was a female holotype from the quill of the sand martin, Riparia riparia (L.) (Passeriformes: Hirundinidae), Poznań, POLAND, 52.4672007265976, 16.924954974622207, April 2009, coll. Glowska E.; the voucher and DNA code are as follows: EG079 (holotype). DNA barcode GenBank accession numbers are specified in Table 1.
  • Type Material Deposition
The holotype was accidentally crushed after species diagnosis was carried out and before the specimen was drawn.
  • Differential Diagnosis
Syringophiloidus ripariae sp. n. is morphologically most similar to S. tarnii Skoracki and Sikora, 2002, described from the huet huet Pteroptochos tarnii (Passeriformes: Rhinocryptidae) from Argentina [33]. Females of both species have a punctate infracapitulum, a weakly sclerotized and apunctate hysteronotal shield, fan-like setae p’ and p” of legs III–IV with six tines, and similar lengths of most setae. Females of S. ripariae sp. n. differ from those of S. tarnii in terms of the number of peritremal chambers, i.e., two and seven in the medial and lateral branches (vs. 3–4 and 9), and lengths of setae se of 260 (vs. 165–225), c1 of 275 (vs. 190–240), d2 of 180 (vs. 130), d1 of 180 (vs. 125–145), e2 of 180 (vs. 115–155), and ag3 of 220 (vs. 145–185). Syringophiloidus ripariae sp. n. is also very similar to S. paludicolae sp. n. described from the plain martin, Riparia paludicola (Vieillot), from Namibia (p.p.). See the S. paludicolae sp. n. differential diagnosis that is given above.
  • Etymology
The name is taken from the specific name of the host and is a noun in the genitive case.

3.3.2. Other Species

Syringophiloidus amazilia Skoracki, 2017

Syringophiloidus amazilia Skoracki, 2017: 181.
Type host: Chlorestes candida (Bourcier and Mulsant) (Apodiformes: Trochilidae). Type locality: Mexico.
  • Host and Distribution
Birds of the family Trochilidae: the white-bellied emerald, Amazilia candida (Bourcier and Mulsant), from Mexico [34].
  • Material Examined
The material examined included one female from the quill of the white-bellied emerald, Amazilia candida (Bourcier and Mulsant) (Apodiformes: Trochilidae), Mexico, Veracruz, Los Tuxtlas, 9 May 2008, coll. S.V. Mironov (SVM 08-0509-8/4). Specimen vouchers and DNA codes are as follows: EG880. DNA barcode GenBank accession nos. are given in Table 1.
  • Material Deposition
Material deposited in the AMU (EG23-0628-008.01).
  • Remark
Our results revealed that S. stawarczyki and S. amazilia are conspecific, and as a consequence, S. amazilia could be treated as a junior synonym of S. stawarczyki. Although our results are precise, they are based on a relatively small sample. This is due to the limited availability of the mite material. For this reason, we do not formally synonymize these species, but only formulate a premise for further systematic research on the populations covering a more significant number of individuals.

Syringophiloidus glandarii (Fritsch,1958)

Syringophilus minor glandarii Fritsch, 1958: 235.
Syringophilus glandarii as incertae sedis Kethley 1970: 65.
Syringophiloidus glandarii Bochkov and Mironov 1998: 14.
Type host: Garrulus glandarius L. (Passeriformes: Corviidae)
Type locality: Germany.
  • Host and Distribution
Birds of the family Corvidae: the eurasian jay, Garrulus glandarius (L)., eurasian magpie, Pica pica (L.), eurasian jackdaw, Corvus monedula L., rook Corvus frugilegus L. [22], American crow, Corvus brachyrhynchos Brehm, steller’s jay, Cyanocitta stelleri (Gmelin) [35], and hooded crow, Corvus corone L. (p.p.) from Germany [36], Russia, Kazakhstan, Japan [22], USA [35], and Poland (p.p.).
  • Material Examined
Four females from the quill of the hooded crow Corvus corone cornix L. (Passeriformes: Corvidae) were used, and the material obtained from dead birds (due to probable collisions with a window) was found on the AMU campus, Poznań, Poland (8 May 2009), coll, Glowska E. Specimen vouchers and DNA codes are as follows: EG519 and EG522. DNA barcode GenBank accession nos. are given in Table 1.
  • Material Deposition
Material is deposited in the AMU (EG23-0628-13.01–04).

Syringophiloidus parapresentalis Skoracki, 2011

Syringophiloidus parapresentalis Skoracki, 2011: 63.
Type host: Turdus merula L. (Passeriformes: Turdidae)
Type locality: Poland.
  • Host Range and Distribution
Birds of the family Turdidae: the Eurasian blackbird, Turdus merula L., fieldfare, T. pilaris L., black-throated thrush, T. atrogularis Jarocki [22], and redwing T. iliacus L. ([22], p.p.) from Slovakia, Kazakhstan, Russia and Jordan [22], and Poland ([22], p.p.).
  • Material Examined
Five females from the quill of the redwing Turdus iliacus L. (Passeriformes: Turdidae) made up the material examined, and the material was obtained from dead birds (due probable collision with glass) found on the AMU campus, Poznań, Poland (16 July 2009), coll, Glowska E. Specimen vouchers and DNA codes are as follows: EG019, EG061-063. DNA barcode GenBank accession nos. are given in Table 1.
  • Material Deposition
Material is deposited in the AMU (EG23-0628-14.01–05).

Syringophiloidus picidus Skoracki, Klimovičová, Muchai and Hromada, 2014

Syringophiloidus picidus Skoracki, Klimovičová, Muchai and Hromada, 2014: 184.
Type host: Dendropicos fuscescens (Vieillot) (Piciformes: Picidae)
Type locality: Kenya.
  • Host and Distribution
Birds of the family Picidae: the cardinal woodpecker, Dendropicos fuscescens (Vieillot), from Kenya, Tanzania, Uganda [31], Namibia (p.p).
  • Material Examined
Two females from the quill of the cardinal woodpecker, Dendropicos fuscescens (Vieillot) (Piciformes: Picidae), NAMIBIA, 14 August 2009, Karas, Oas, 27 29 43 S, 19 13 14 E, bird coll. Gebhard C. A., mite coll. Glowska E (USNM 642511), were examined. Specimen vouchers and DNA codes are as follows: KR031; KR033. DNA barcode GenBank accession nos. are given in Table 1.
  • Material Deposition
One female deposited in the USNM (USNMENT acc. number: USNMENT01967023) and one female in the AMU (EG23-0628-009.01).

Syringophiloidus plocei Glowska, Broda, Gebhard and Dabert, 2016

Syringophiloidus plocei Glowska, Broda, Gebhard and Dabert, 2016: 563.
Type host: Ploceus cucullatus (St. Muller) (Passeriformes: Ploceidae).
Type locality: Gabon.
  • Host and Distribution
Birds of the family Ploceidae: the village weaver, Ploceus cucullatus (Müller), and Vieillot’s black weaver, Ploceus nigerrimus Vieillot [15].
  • Material Examined
Four females from the quill of the village weaver, Ploceus cucullatus (St. Muller) (Passeriformes: Ploceidae) GABON, Ogooue Maritime Province, Gamba Complex of Protected Areas, near the mouth of Nyanga River, 22 October 2009, bird host coll. C.A. Gebhard, were sampled; mites were sampled by E. Glowska (September 2014) (USNM 642906). Four females from the Vieillot’s black weaver, Ploceus nigerrimus Vieillot (Ploceidae), GABON, Estuaire Province, Cap Esterias, National Forestry School (ENEF), 3 November 2009, bird host coll. C.A. Gebhard, were also sampled; mites were sampled by E. Glowska (USNM 642955). Specimen vouchers and DNA codes are as follows: GE038-039; GE041-042. DNA barcode GenBank accession nos. are given in Table 1.
  • Material Deposition
Two females from each species (the village weaver and the Vieillot’s black weaver) are deposited in the USNM (USNMENT acc. number: USNMENT01967024–USNMENT01967027) and in the AMU (EG23-0628-011.01–04).

Syringophiloidus pseudonigritae Glowska, Dragun-Damian and Dabert, 2012

Syringophiloidus pseudonigritae Glowska, Dragun-Damian and Dabert, 2012.
Type host: Pseudonigrita arnaudi (Bonaparte) (Passeriformes: Ploceidae).
Type locality: Tanzania.
  • Host and Distribution
Birds of the family Ploceidae: the grey-headed social weaver, Pseudonigrita arnaudi (Bonaparte), from Tanzania (Glowska et al., 2012) [10].
  • Material Examined
Four females from the quill of the frozen specimen of the grey-headed social weaver, Pseudonigrita arnaudi (Bonaparte) (Passeriformes: Ploceidae), were examined; the bird host was initially collected from the wild in Tanzania and imported to Hamburg in 1990 where it was housed in the Biozentrum Grindel and Hamburg Zoological Museum in the University of Hamburg, Germany, coll. E. Glowska, November 2010.
Specimen vouchers and DNA codes are as follows: EG545-547. DNA barcode GenBank accession nos. are given in Table 1.
  • Material Deposition
Material is deposited in the AMU (EG23-0628-12.01–04).

Syringophiloidus sporophila Skoracki, 2017

Syringophiloidus sporophila Skoracki, 2017: 184.
Type host: Sporophila torqueola (Bonaparte) (Passeriformes: Thraupidae). Type locality: Mexico.
  • Host and Distribution
Birds of the family Thraupidae: the cinnamon-rumped seedeater, Sporophila torqueola (Bonaparte), from Mexico (Skoracki 2017) [34].
  • Material Examined
Ten females from the quill of the cinnamon-rumped seedeater, Sporophila torqueola (Bonaparte) (Passeriformes: Thraupidae), Mexico, Veracruz, Los Tuxtlas, 6 May 2008, coll. S.V. Mironov (SVM 08-0506-1/4), were used. Specimen vouchers and DNA codes are as follows: EG362–366, and EG688–692. DNA barcode GenBank accession nos. are given in Table 1.
  • Material Deposition
Material deposited in the AMU (EG23-0628-006.01–10).

Syringophiloidus stawarczyki Skoracki, 2004

Syringophiloidus stawarczyki Skoracki, 2004: 291.
Type host: Euphonia cyanocephala (Vieillot) (Passeriformes: Emberizidae). Type locality: Brazil.
  • Host and Distribution
Birds of the families Emberizidae and Thraupidae: the golden-rumped euphonia, Euphonia cyanocephala (Vieillot) (type host), white-lined tanager, Tachyphonus rufus (Boddaert) [29], and blue dacnis, Dacnis cayana (L.) [30].
  • Material Examined
Two females from the quill of the blue dacnis Dacnis cayana (Linnaeus) (Passeriformes: Thraupidae), Brazil, Minas Gerais, Nova Lima, APP do Condomínio Miguelão, 20°07′17.2″ S 43°58′03.1″ W, 8 September 2010, coll. S.V. Mironov, F.A. Hernandes & M.P. Valim (field no. SVM 10-0908-1–2), were examined. Specimen vouchers and DNA codes are as follows: EG854–855. DNA barcode GenBank accession nos. are given in Table 1.
  • Material Deposition
Materials are deposited in the AMU (EG23-0628-007.01–02).

4. Discussion

Both topologies of the phylogenetic trees and genetic distances revealed thirteen strongly supported monophyletic lineages which are in most cases in accordance with the morphological identifications. The only exception is S. amazilia, which very close to the S. stawarczyki clade and most likely represents a population of this species. This result is further supported by the genetic distance between the two lineages (1.4% and 1.5% of distances p and K2P, respectively), which is lower than that between bihost S. plocei populations (2.1%) and comparable to the previously reported intraspecific values within other quill mites [8,16]. Also, a morphological analysis of the type material of both species showed that they are almost indistinguishable and share most diagnostic characteristics (both qualitative and quantitative). The differences between the alleged “species” are very subtle and manifest only in the length of setae d2 (135–170 in females of S. amazilia vs. 115–125 in S stawarczyki), f2 (175 vs. 220), ag1 (105–120 vs. 130–135), and ag2 (100–110 vs. 125–135). It is very likely that the differences are caused by the fact that both species were described based on a few specimens only (seven and three females of S. amazilia and S. stawarczyki, respectively) [29,34]. This is a common practice when researchers work with hard-to-reach and low-prevalence material. It seems, however, that more individuals’ availability would fill the metric data gap between S. amazilia and S. stawarczyki and show the continuity of the divergent characters. The presence of the same mite species on two phylogenetically distant hosts (representatives of different orders, i.e., Apodiformes and Passeriformes) can be explained by horizontal transfer since the ranges of both hosts overlap in Central America. At the moment, we do not have sufficient data to point the direction of the transfer. To carry this out, more individuals representing more populations of both hosts should be analyzed The cases of the host switching of quill mites have already been reported and our result supports the earlier assumption that this phenomenon is not incidental but rather one of the possible scenarios for the dispersion and evolution of this group of parasites [16,37].
In all other cases, the analysis of molecular data (NJ and genetic distances) confirmed the morphological separateness of previously known and newly described species. The intraspecific distances of all tested taxa were not higher than 0.9% and were comparable to the interpopulation values, i.e., 1.5% between S. plocei from the vieillot’s black weaver and village weaver. All these values are similar to those previously observed in other stenoxenous quill mites (0.0–2.3) [8,14]. Also, interspecific diversity, which ranged from 5.9% to 19.2% and 6.3–22.4% based on distance p and K2P, respectively (Table 2), is comparable to that among the species in other previously barcoded syringophilid genera [16].
Although all putative species (except S. amazilia) are highly supported with bootstrap values (100%), the relationships between them have not been fully resolved and only faintly indicate that both the host phylogeny and distributions may influence the phylogenetic structure of mites. For example, S. ripariae sp. n. from Poland and S. paludicolae sp. n. from Namibia were both recorded from hirundinid birds. Their populations show clear intraspecific integrity as well as species separateness measured via genetic distance (16.3% and 14.5% of K2P and p, respectively). Even though both species come from geographically distant locations, they form a sister group on the phylogenetic tree. This may suggest a parallel evolution of mites with avian hosts. Another example of a co-phylogenetic relationship is shown by S. plocei found on two ploceid species in Namibia. This clade forms a sister group with S. pseudonigritae, a parasite of another ploceid bird, the grey-headed social weaver in Tanzania. This result confirmed our earlier observations for these taxa (Glowska et al. 2016) [15]. Another factor that may shape the phylogenetic structure of mites is geographical distribution. Two species, S. glandarii and S. parapresentalis, form a statistically well-supported sister group. Although they were obtained from birds from different families (Corvidae and Turdidae, respectively), they have a common location (Poland). Analogously, two species parasitize separate bird orders, S. calamonastes sp. n. and S. picidus form the “Namibian cluster”. The same can be observed with the clearly distinct clade represented by mites from Mexico and South America (S. atlapetes; S. Stawarczyki-S. amazilia).
In this work, we used morphological and barcode data to estimate the diversity and genetic variability of fifteen populations of the genus Syringophiloidus. In most cases, both sources of information were consistent. The only exception was S. amazilia, which seems to be a population of S. stawarczyki and formally should be treated as its junior synonym. The further findings of our study are six now-to-science species, described herein. We indicate that both host phylogeny and distribution can drive the evolution of quill mites. However, we treat our results as a starting point for further in-depth research on these issues. Our results increase the knowledge about mite diversity and demonstrate the usefulness of the parallel use of morphological and molecular methods in solving systematic puzzles in this group of parasites.

5. Conclusions

Even though there has been progress in understanding quill mite systematics, little is known about their global diversity and host associations. This is mainly due to the weakly informative morphology and relatively few diagnostic characters. To address this challenge, a combination of classical morphology and DNA barcodes is used to increase the efficiency of species identification. This approach has been proven to be a reliable tool for this purpose, regardless of sex or developmental stage. It is also helpful for estimating genetic diversity and host specificity issues or revealing phenomena resulting from the incorrect interpretation of morphological characters, such as phenotypic plasticity, polymorphisms, or cryptic species.
Accurate species diagnosis is essential for further research, particularly in understanding quill mites’ epidemiological importance. Recent reports suggest that mites host unique phylogenetic lineages of bacteria, such as Wolbachia and Spiroplasma. Additionally, they are believed to spread diseases by ingesting food (sucking the host’s bodily fluids), although their epidemiological significance has not yet been well studied. Our findings contribute to knowledge about mite diversity and provide a basis for further evolutionary, ecological, and epidemiological investigations.

Author Contributions

Conceptualization, E.G. and M.D.; data curation, E.G.; formal analysis, E.G.; funding acquisition, E.G.; investigation, E.G., I.L., K.O., J.O. and M.D.; methodology, E.G. and M.D.; project administration, E.G.; resources, E.G. and C.A.G.; software, E.G.; supervision, E.G.; validation, E.G.; visualization, E.G. and I.L.; writing—original draft, E.G.; writing—review and editing, E.G. and M.D. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by National Science Centre of Poland grant 2015/19/D/NZ8/00191 (EG).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Informed consent was obtained from all subjects involved in the study.

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Acknowledgments

We thank the reviewers for their valuable comments on the manuscript. We are very grateful to the late Andre V. Bochkov, Pavel Klimov, and Sergey V. Mironov, who collected the material and made it available for our research. The collection of mites in Mexico was conducted under the license no. FAUT-0209 issued by Dirección General de Vida Silvestre (Mexico); the field expedition was supported by a grant from the U.S. National Science Foundation (DEB-0613769) to Barry M. OConnor (Museum of Zoology, University of Michigan, Ann Arbor, USA). We also thank the staff of the Department of Vertebrate Zoology, Division of Birds, Smithsonian Institution, National Museum of Natural History, Washington, D.C., USA (USNM), for making the collection of feathers available for this study.

Conflicts of Interest

The authors declare no conflict of interest.

Appendix A

Animals 13 03877 g0a1
Figure A1. Neighbor-joining phylogenetic tree of the Syringophiloidus species based on the distance p model. The tree was constructed in Mega v.7. and rooted by Stibarokris phoeniconaias.
Figure A1. Neighbor-joining phylogenetic tree of the Syringophiloidus species based on the distance p model. The tree was constructed in Mega v.7. and rooted by Stibarokris phoeniconaias.
Animals 13 03877 g0a1

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Figure 1. Neighbor joining phylogenetic tree of the Syringophiloidus species based on the K2P model. The tree was constructed in Mega v.7. and rooted by Stibarokris phoeniconaias.
Figure 1. Neighbor joining phylogenetic tree of the Syringophiloidus species based on the K2P model. The tree was constructed in Mega v.7. and rooted by Stibarokris phoeniconaias.
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Animals 13 03877 g002
Figure 2. (A–E). Syringophiloidus atlapetes sp. n., female: (A) dorsal view, (B) ventral view, (C) peritremes, (D) hypostomal apex, and (E) fan-like setae p’ of leg III. Scale bars: (A,B) = 50 µm; (C–E) = 25 µm.
Figure 2. (A–E). Syringophiloidus atlapetes sp. n., female: (A) dorsal view, (B) ventral view, (C) peritremes, (D) hypostomal apex, and (E) fan-like setae p’ of leg III. Scale bars: (A,B) = 50 µm; (C–E) = 25 µm.
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Animals 13 03877 g003
Figure 3. (A–E). Syringophiloidus atlapetes sp. n., male: (A) dorsal view, (B) ventral view, (C) peritremes, (D) hypostomal apex, and (E) fan-like setae p’ of leg III. Scale bars: (A,B) = 50 µm; (C–E) = 25 µm.
Figure 3. (A–E). Syringophiloidus atlapetes sp. n., male: (A) dorsal view, (B) ventral view, (C) peritremes, (D) hypostomal apex, and (E) fan-like setae p’ of leg III. Scale bars: (A,B) = 50 µm; (C–E) = 25 µm.
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Animals 13 03877 g004
Figure 4. (A–E). Syringophiloidus calamonastes sp. n., female: (A)—dorsal view, (B)—ventral view, (C)—peritremes, (D)—hypostomal apex, (E)—fan-like setae p’ of leg III. Scale bars: (A,B) = 50 µm; (C–E) = 25 µm.
Figure 4. (A–E). Syringophiloidus calamonastes sp. n., female: (A)—dorsal view, (B)—ventral view, (C)—peritremes, (D)—hypostomal apex, (E)—fan-like setae p’ of leg III. Scale bars: (A,B) = 50 µm; (C–E) = 25 µm.
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Animals 13 03877 g005
Figure 5. (A–E). Syringophiloidus campephilus sp. n., female: (A)—dorsal view, (B)—ventral view, (C)—peritremes, (D)—hypostomal apex, (E)—fan-like setae p’ of leg III. Scale bars: (A,B) = 50 µm; (C–E) = 25 µm.
Figure 5. (A–E). Syringophiloidus campephilus sp. n., female: (A)—dorsal view, (B)—ventral view, (C)—peritremes, (D)—hypostomal apex, (E)—fan-like setae p’ of leg III. Scale bars: (A,B) = 50 µm; (C–E) = 25 µm.
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Animals 13 03877 g006
Figure 6. (A–E). Syringophiloidus mahali sp. n., female: (A) dorsal view, (B) ventral view, (C) peritremes, (D) hypostomal apex, and (E) fan-like setae p’ of leg III. Scale bars: (A,B) = 50 µm; (C–E) = 25 µm.
Figure 6. (A–E). Syringophiloidus mahali sp. n., female: (A) dorsal view, (B) ventral view, (C) peritremes, (D) hypostomal apex, and (E) fan-like setae p’ of leg III. Scale bars: (A,B) = 50 µm; (C–E) = 25 µm.
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Animals 13 03877 g007
Figure 7. (A–E). Syringophiloidus paludicolae sp. n., female: (A) dorsal view, (B) ventral view, (C) peritremes, (D) hypostomal apex, and (E) fan-like setae p’ of leg III. Scale bars: (A,B) = 50 µm; (C–E) = 25 µm.
Figure 7. (A–E). Syringophiloidus paludicolae sp. n., female: (A) dorsal view, (B) ventral view, (C) peritremes, (D) hypostomal apex, and (E) fan-like setae p’ of leg III. Scale bars: (A,B) = 50 µm; (C–E) = 25 µm.
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Table 1. Mites and sequences used in the molecular study.
Table 1. Mites and sequences used in the molecular study.
Mite SpeciesHost SpeciesHost Order and FamilyLocationSpecimen and DNA CodeGenBank Access No.
Syringophiloidus calamonastes sp. n.Barred Wren-Warbler
Calamonastes fasciolatus (Smith)		Passeriformes:
Cisticolidae		NamibiaKR043OR721880
KR045OR721881
S. paludicolae sp. n.Plain Martin
Riparia paludicola (Vieiilot)		Passeriformes:
Hirundinidae		NamibiaKR055OR723490
KR056OR723491
S. ripariae sp. n.Bank Swallow
Riparia riparia (L.)		Passeriformes:
Hirundinidae		PolandEG079OR723492
EG080OR723493
S. atlapetes sp. n.White-headed Brushfinch
Atlapetes albiceps (Taczanowski)		Passeriformes:
Passerellidae		PeruEG974OR827223
EG975OR827224
EG976OR827229
EG977OR827227
S. campephilus sp. n.Guayaquil Woodpecker
Campephilus gayaquilensis (Lesson)		Piciformes:
Picidae		PeruEG964OR723494
EG971OR723495
S. mahali sp. n.White-browed Sparrow-Weaver
Plocepasser mahali Smith		Passeriformes:
Ploceidae		NamibiaKR047OR827226
KR048OR827228
KR052OR827225
S. sporophila Skoracki, 2017Cinnamon-rumped Seedeater
Sporophila torqueola (Bonaparte)		Passeriformes:
Thraupidae		MexicoEG362OR829593
EG363OR829592
EG364OR829594
EG365OR829596
EG366OR829595
EG688OR829597
EG689OR829598
EG690OR829599
EG691OR829601
EG692OR829602
* S. stawarczyki Skoracki, 2004Blue Dacnis
Dacnis cayana (Linnaeus)		Passeriformes:
Thraupidae		BrazilEG854OR829600
EG855OR829606
* S. amazilia Skoracki, 2017White-bellied Emerald
Chlorestes candida (Bourcier and Mulsant)		Caprimulgiformes:
Trochilidae		MexicoEG880OR829607
S. picidus Skoracki, Klimovičová, Muchai and Hromada, 2014Cardinal Woodpecker
Chloropicus fuscescens (Vieillot)		Piciformes:
Picidae		NamibiaKR031OR730469
KR033OR730471
S. plocei Glowska, Broda, Gebhard and Dabert, 2016Village Weaver
Ploceus cucullatus (St. Muller)		Passeriformes:
Ploceidae		GabonGE041OR829603
GE042KU646845.1
Vieillot’s Black Weaver
Ploceus nigerrimus (Vieillot)		Passeriformes:
Ploceidae		GabonGE038OR829605
GE039OR829604
S. pseudonigritae Glowska, Dragun-Damian and Dabert, 2012Gray-headed Social-Weaver
Pseudonigrita arnaudi (Bonaparte)		Passeriformes:
Ploceidae		TanzaniaEG545OR829610
EG546OR829608
EG547OR829609
S. glandarii (Fritsch, 1958)Hooded Crow
Corvus corone cornix L.		Passeriformes:
Corvidae		PolandEG519OR829611
EG522OR829612
S. parapresentalis Skoracki, 2011Redwing Turdus iliacus L.Passeriformes:
Turdidae		PolandEG019OR829613
EG061OR829614
EG062OR829615
EG063OR829616
Stibarokris phoeniconaias Skoracki & OConnor, 2010 outgroupAmerican flamingo
Phoenicopterus ruber L.		Galliformes:
Phasianidae		GermanyEG642OR726320
* According to our results, S. amazilia and S. stawarczyki are conspecific.
Table 2. Estimates of evolutionary divergences between COI sequences of Syringophiloidus populations based on K2P (and p) distances.
Table 2. Estimates of evolutionary divergences between COI sequences of Syringophiloidus populations based on K2P (and p) distances.
Mite SpeciesDistance p (Lower Left) and K2P (Upper Right) (%)
Within GroupsBetween Groups
1.2.3.4.5.6.7.8.9.10.11.12.13.14.15.16.
1. S. ripariae sp. n.
ex_Bank_Swallow		0.0 16.216.014.416.916.315.415.814.216.317.716.017.217.416.239.9
2. S. sporophila
ex Cinnamon-rumped Seedeater		0.214.5 17.015.621.815.614.214.416.219.622.415.116.617.817.436.8
3. S. pseudonigritae
ex Gray-headed Social-Weaver		0.014.315.0 18.720.415.712.612.118.420.221.219.820.219.118.639.4
4. S. stawarczyki
ex Blue Dacnis		0.013.014.016.3 14.46.316.215.81.517.816.115.315.514.513.439.5
5. S. campephilus sp. n.
ex Guayaquil Woodpecker		0.015.018.717.612.9 17.320.521.014.619.019.519.019.019.617.543.0
6. S. atlapetes sp. n.
ex White-headed Brushfinch		0.714.514.014.05.915.1 17.817.26.320.218.716.416.615.015.241.2
7. S. plocei
ex Village Weaver		0.913.912.811.314.517.815.7 2.117.318.020.119.119.918.318.337.7
8. S. plocei
ex Vieillot’s Black Weaver		0.214.113.011.014.118.115.22.1 16.618.019.019.519.617.918.336.2
9. S. amazilia
ex White-bellied Emerald		n/a12.914.516.11.413.05.915.314.8 18.316.016.215.114.214.039.5
10. S. paludicolae sp. n.
ex Plain Martin		0.014.517.217.615.816.717.515.915.916.1 21.919.021.418.519.839.2
11. S. mahali sp. n.
ex White-browed Sparrow-Weaver		0.015.719.218.414.417.116.417.516.714.418.9 18.617.619.920.644.6
12. S. picidus
ex Cardinal Woodpecker		0.014.313.617.213.816.714.616.817.014.516.716.2 7.321.719.541.4
13. S. calamonastes sp. n.
ex Barred Wren-Warbler		0.015.214.817.613.916.714.817.417.113.618.515.56.9 19.919.238.6
14. S. parapresentalis
ex Redwing		0.015.415.816.713.017.013.516.115.812.916.317.518.717.4 12.141.2
15. S. glandarii
ex Hooded Crow		0.014.515.416.312.115.413.616.116.112.717.217.917.016.811.1 42.3
16. Stibarokris phoeniconaias (outgroup)-30.428.830.130.332.131.129.328.430.330.133.031.229.731.231.7
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Glowska, E.; Laniecka, I.; Ostrowska, K.; Gebhard, C.A.; Olechnowicz, J.; Dabert, M. Evaluation of Genetic Diversity in Quill Mites of the Genus Syringophiloidus Kethley, 1970 (Prostigmata: Syringophilidae) with Six New-to-Science Species. Animals 2023, 13, 3877. https://doi.org/10.3390/ani13243877

AMA Style

Glowska E, Laniecka I, Ostrowska K, Gebhard CA, Olechnowicz J, Dabert M. Evaluation of Genetic Diversity in Quill Mites of the Genus Syringophiloidus Kethley, 1970 (Prostigmata: Syringophilidae) with Six New-to-Science Species. Animals. 2023; 13(24):3877. https://doi.org/10.3390/ani13243877

Chicago/Turabian Style

Glowska, Eliza, Izabella Laniecka, Kamila Ostrowska, Christina A. Gebhard, Julia Olechnowicz, and Miroslawa Dabert. 2023. "Evaluation of Genetic Diversity in Quill Mites of the Genus Syringophiloidus Kethley, 1970 (Prostigmata: Syringophilidae) with Six New-to-Science Species" Animals 13, no. 24: 3877. https://doi.org/10.3390/ani13243877

APA Style

Glowska, E., Laniecka, I., Ostrowska, K., Gebhard, C. A., Olechnowicz, J., & Dabert, M. (2023). Evaluation of Genetic Diversity in Quill Mites of the Genus Syringophiloidus Kethley, 1970 (Prostigmata: Syringophilidae) with Six New-to-Science Species. Animals, 13(24), 3877. https://doi.org/10.3390/ani13243877

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